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Strong pollinator-mediated selection for increased flower brightness and contrast in a deceptive orchid
Abstract
Contrasting flower color patterns that putatively attract or direct pollinators towards a reward are common among angiosperms. In the deceptive orchid Anacamptis morio, the lower petal, which makes up most of the floral display, has a light central patch with dark markings. Within populations, there is pronounced variation in petal brightness, patch size, amount of dark markings, and contrast between patch and petal margin. We tested whether pollinators mediate selection on these color traits and on morphology (plant height, number of flowers, corolla size, spur length), and whether selection is consistent with facilitated or negative frequency-dependent pollination. Pollinators mediated strong selection for increased petal brightness (Δβpoll = 0.42) and contrast (Δβpoll = 0.51). Pollinators also tended to mediate stabilizing selection on brightness (Δγpoll = -0.27, n.s.) favoring the most common phenotype in the population. Selection for reduced petal brightness among hand-pollinated plants indicated a fitness cost associated with brightness. The results demonstrate that flower color traits influence pollination success and seed production in A. morio, indicating that they affect attractiveness to pollinators, efficiency of pollen transfer, or both. The documented selection is consistent with facilitated pollination and selection for color convergence towards co-occurring rewarding species. This article is protected by copyright. All rights reserved.
... While the food-deception strategy in Orchidaceae has been the subject of extensive examination in numerous studies, it remains still poorly understood phenomenon. The relationships between the floral display traits of orchids, rewarding plants, and reproduction output have been typically described using two-factor interactions, that is, correlation between fruit set and spur length (Johnson & Steiner, 1997;O'Connel & Johnston, 1998), plant height and flower number (Sabat & Ackerman, 1996;Sletvold et al., 2010), flower brightness (Sletvold et al., 2016) and flower position (Vallius, 2000). ...
... Two-year studies were performed from May to July in three D. majalis populations (KA, 2014(KA, -2015SKI, 2015-2016and SKII, 2016, three D. incarnata var. incarnata populations (ZB, 2014(ZB, -2015RO andMR, 2015-2016), and three D. fuchsii populations (CM, 2015(CM, -2016BR, andGR, 2014-2015) located in northeastern Poland (Table S1, Figure S1). ...
... The studies of relationships between the morphological and/or phenological traits and female and male success in food-deceptive orchids are well-documented (Mattila & Kuitunen, 2000;Sletvold & Ågren, 2014;Sletvold et al., 2010;Trunschke et al., 2017;Vallius et al., 2007). However, these studies encompass only single-year data sets and reveal associations such as the impact of floral display on fruit set in Anacamptis longicornu (Capó et al., 2019), the density of co-flowering rewarding plants in Orchis militaris (Henneresse et al., 2017), floral display in Caladenia valida and Tolumnia variegata (Tremblay et al., 2010), inflorescence traits in the environmental context in Anacamptis laxiflora (Scopece et al., 2021), as well as flower brightness (Sletvold et al., 2016), flower color (Trunschke et al., 2021), and flowering time (Sabat & Ackerman, 1996). gued that the frequency of pollinaria removal, which is higher than fruit set, is the rule rather than the exception in deceptive plants because the flowers act as males but not females. ...
A large suite of floral signals, and environmental and biotic characteristics influence the behavior of pollinators, affecting the female success of food‐deceptive orchids. In this study, we examined the many factors shaping the reproductive output of three orchid taxa: Dactylorhiza majalis , D. incarnata var. incarnata , and D. fuchsii . We applied a statistical model to correlate female success (number of fruit sets) with individual characteristics (plant and inflorescence height, number of flowers, and spur length), number of pollinaria removed, flowering time, and density of floral units of co‐flowering rewarding plants. Our findings suggested that the broad spectrum of variations in Dactylorhiza's morphological traits, floral display, and flowering phenology within different environmental contexts has a significant impact on their reproductive success. The number of fruits increased with an increase in the number of pollinaria removed in the studied Dactylorhiza taxa. In contrast, a higher number of flowers per inflorescence and higher inflorescences in relation to individual height always decreased fruit set. We observed that low number of co‐flowering rewarding plants in populations could affect the Dactylorhiza reproductive output as magnets and competitor plants. The synchronization of flowering, or lack thereof, between Dactylorhiza and rewarding plants can limit reproductive success. This demonstrates that the food deception strategy is multidirectional, and reproductive output can vary considerably both spatially and temporally within the context of this strategy.
... A recent study by van der Kooi and Kelber (2022) has shown that for nocturnal and diurnal hawkmoths the intensity of target stimuli plays a role for its visibility. Intensity has been considered as a potentially important factor for flower evolution (Hopkins and Rausher 2012;Renoult et al. 2014;Sletvold et al. 2016), and an experimental approach by Hempel de Ibarra et al. (2000) demonstrated that high brightness contrast between a stimulus and its background can impact the choice behaviour of bees. In bees, achromatic perception of targets is driven by green contrast (modulation of green receptor against the background) and this factor is considered to play an important role in shape processing and motion perception in these insects (von Hess 1913;Kaiser and Liske 1974;Lehrer and Bischof 1995;Hempel de Ibarra and Giurfa 2003;Stach et al. 2004;Stojcev et al. 2011;Morawetz et al. 2013). ...
... We additionally considered in hypothesis (iii) if honey bees show evidence of being able to learn changes in stimuli intensity and, hypothesis (iv) if T. carbonaria bees show evidence of being able to learn changes in stimuli intensity. This question was assessed with fine-tuned changes in stimuli given that several recent ecology studies have assumed intensity may be an important factor in flower evolution (Hopkins and Rausher 2012;Renoult et al. 2014;Sletvold et al. 2016). We discuss our findings with respect to how pollinator perception may influence flower colour evolution. ...
... A second main research question considered in the current study was whether either species of bees tested might prefer stimulus intensity when colour hue and spectral purity was controlled. This question is important as several recent ecology studies on flower signalling have suggested that in some cases the brightness or intensity of a flower may be a factor in attracting pollinators (Hopkins and Rausher 2012;Renoult et al. 2014;Sletvold et al. 2016;van der Kooi and Kelber 2022). In honey bees we thus tested hypothesis (iii) and the results show that variations in stimulus intensity do significantly influence preferences when bees were conditioned towards the most intense colour (Fig. 5), however, when independent honey bees were conditioned towards the least intense colour then no significant preference was evidenced for any stimulus in resulting tests (Fig. 4). ...
Bees play a vital role as pollinators worldwide and have influenced how flower colour signals have evolved. The Western honey bee, Apis mellifera (Apini), and the Buff-tailed bumble bee, Bombus terrestris (Bombini) are well-studied model species with regard to their sensory physiology and pollination capacity, although currently far less is known about stingless bees (Meliponini) that are common in pantropical regions. We conducted comparative experiments with two highly eusocial bee species, the Western honey bee, A. mellifera, and the Australian stingless bee, Tetragonula carbonaria, to understand their colour preferences considering fine-scaled stimuli specifically designed for testing bee colour vision. We employed stimuli made of pigment powders to allow manipulation of single colour parameters including spectral purity (saturation) or colour intensity (brightness) of a blue colour (hue) for which both species have previously shown innate preferences. Both A. mel-lifera and T. carbonaria demonstrated a significant preference for spectrally purer colour stimuli, although this preference is more pronounced in honey bees than in stingless bees. When all other colour cues were tightly controlled, honey bees receiving absolute conditioning demonstrated a capacity to learn a high-intensity stimulus significant from chance expectation demonstrating some capacity of plasticity for this dimension of colour perception. However, honey bees failed to learn low-intensity stimuli, and T. carbonaria was insensitive to stimulus intensity as a cue. These comparative findings suggest that there may be some common roots underpinning colour perception in bee pollinators and how they interact with flowers, although species-specific differences do exist.
... Yet, we are aware of only 18 studies that aimed to quantify selection on continuous variation in petal coloration in the context of pollination (Tables 1, 2). Moreover, of these studies, only six used a hand-pollination treatment to estimate selection gradients associated with pollinator interactions (Caruso et al., 2010;Parachnowitsch and Kessler, 2010;Lavi and Sapir, 2015;Sletvold et al., 2016;Zhang et al., 2017;Souto-Vilarósa et al., 2018;Supplementary Table 3). Some other studies used modeling approaches linking the flower color phenotype -fitness relationship to pollinator visitation data to determine the contribution of pollinators to observed total selection (e.g., Veiga et al., 2015;Rodriguez-Castañeda et al., 2020;Brunet et al., 2021;Supplementary Table 3). ...
... It is striking that studies have rarely detected significant evidence for directional net selection (which includes all possible causes of selection) on achromatic color parameters. In two studies, natural selection was found to act in a linear manner favoring less bright flowers in Lobelia siphilitica in one of these studies (Caruso et al., 2010), and brighter and contrastrich petal colorization in the deceptive orchid Anacamptis morio in the other (Sletvold et al., 2016). In addition, the study by Sletvold et al. (2016) confirmed that pollinators accounted for 100% of observed net selection among openpollinated plants. ...
... In two studies, natural selection was found to act in a linear manner favoring less bright flowers in Lobelia siphilitica in one of these studies (Caruso et al., 2010), and brighter and contrastrich petal colorization in the deceptive orchid Anacamptis morio in the other (Sletvold et al., 2016). In addition, the study by Sletvold et al. (2016) confirmed that pollinators accounted for 100% of observed net selection among openpollinated plants. In addition, Brunet et al. (2021) found, in a population of Medicago sativa, that bumblebees (Bombus impatiens) preferred darker flowers but this was due to correlational selection with flower number. ...
The evolution of floral traits in animal-pollinated plants involves the interaction between flowers as signal senders and pollinators as signal receivers. Flower colors are very diverse, effect pollinator attraction and flower foraging behavior, and are hypothesized to be shaped through pollinator-mediated selection. However, most of our current understanding of flower color evolution arises from variation between discrete color morphs and completed color shifts accompanying pollinator shifts, while evidence for pollinator-mediated selection on continuous variation in flower colors within populations is still scarce. In this review, we summarize experiments quantifying selection on continuous flower color variation in natural plant populations in the context of pollinator interactions. We found that evidence for significant pollinator-mediated selection is surprisingly limited among existing studies. We propose several possible explanations related to the complexity in the interaction between the colors of flowers and the sensory and cognitive abilities of pollinators as well as pollinator behavioral responses, on the one hand, and the distribution of variation in color phenotypes and fitness, on the other hand. We emphasize currently persisting weaknesses in experimental procedures, and provide some suggestions for how to improve methodology. In conclusion, we encourage future research to bring together plant and animal scientists to jointly forward our understanding of the mechanisms and circumstances of pollinator-mediated selection on flower color.
... This variation is particularly noticeable in deceptive orchid species, i.e. orchids that offer no reward to their pollinators, and can range from continuous variation (e.g. Sletvold et al., 2016) to more extreme cases of discrete variation, where two or more floral morphs can be discerned among (e.g. Delle-Vedove et al., 2011) or even within populations (Gigord et al., 2001;Kellenberger et al., 2019). ...
... For each flower, we also determined the number of marked spots on the labellum. Achromatic brightness of the central part of the labellum and the spots on the labellum (Fig. 1) was assessed by calculating the mean RGB value of both flower parts as I = 1/3 [R + B + G] (Lambert and Carron, 1999;Sletvold et al., 2016). Brightness values vary between 0 (no light, black) and 1 (full light, white). ...
... This is not unusual and most studies investigating selection gradients in orchids report significant selection on floral display size, and the selection gradients obtained here are largely congruent with values reported elsewhere. For example, in the food-deceptive orchid Anacamptis morio, the selection gradient for the number of flowers was 0.59 (Sletvold et al., 2016), which is similar to the values reported here. However, in contrast to their study, no significant selection on labellum contrast was found here. ...
Background and aims:
Angiosperms vary remarkably in traits such as colour, size and shape of flowers, yet such variation generally tends to be low within species. In deceptive orchids, however, large variation in floral traits has been described, not only between, but also within populations. Nonetheless, the factors driving variation in floral traits in deceptive orchids remain largely unclear.
Methods:
To identify determinants of variation in floral traits, we investigated patterns of fruit set and selection gradients in the food-deceptive orchid Orchis purpurea, which typically presents large within-population variation in the colour and size of the flowers. Using long-term data, fruit set was quantified in two populations during sixteen consecutive years (2004-2019). Artificial hand pollination was performed to test the hypothesis that fruit set was pollinator limited and that selfing led to decreased seed set and viability. Annual variation (2016-2019) in selection gradients was calculated for three colour traits (brightness, contrast and the number of spots on the labellum), flower size (spur length, labellum length and width) and plant size (number of flowers, plant height).
Key results:
Fruit set was, on average, low (~12%) and severely pollinator limited. Opportunities for selection varied strongly across years, but we found only weak evidence for selection on floral traits. In contrast, there was strong and consistent positive selection on floral display. Selfing led to reduced production of viable seeds and hence severe inbreeding depression (δ = 0.38).
Conclusion:
Overall, these results demonstrate that the large variation in flower colour and size that is regularly observed in natural O. purpurea populations is maintained by the consistent lack of strong selection pressures on these traits through time.
... orchids with similar colouration to the model have higher pollination). Instead, our findings are in line with a former study on A. morio where pollinators mediated strong selection for increased petal brightness and contrast, promoting the most common phenotype in the population (Sletvold et al. 2016). Furthermore, orchids with lower reflectance than P. nicaeensis had lower pollination, i.e. those orchids with exaggerated colour signals to the rewarding plants have higher pollination success (Scaccabarozzi et al. 2023). ...
... Bumble bees innately use flower brightness and contrast as cues for visiting an inflorescence or for close-up orientation and positively select for these traits (Renoult et al. 2013). We argue that the presence/absence of differently coloured rewarding plants may influence the strength and direction of this selection, contributing to the maintenance of colour variation typically observed among A. morio populations (Sletvold et al. 2016). ...
... In the laboratory, the falls positioned beneath the style branches with pollinated stigmas, as well as the arbitrarily chosen falls (one per flower) from non-pollinated flowers, were cut at their bases and scanned using an optical scanner (CanoScan 5600F; Canon Inc., Tokyo, Japan; 600 dpi resolution). Digital images of fresh falls were used for analyses of achromatic brightness, which is defined as the mean RGB value and can vary between zero (black, no light) and one (white, full light intensity) [43,44]. For morphometric analyses, the complete sample of flowers, including the detached falls, was conserved in 70% ethanol at room temperature until dissection. ...
... In the present study, the flower color was characterized in an alternative way-as achromatic brightness, determined as RGB mean score. Higher brightness implies that a particular flower reflects more light, increasing its visibility over long distances and attractiveness to pollinators, so selection for higher flower brightness could occur [44]. Pollinated I. pumila flowers generally exhibited higher brightness values than non-pollinated flowers. ...
To gain insight into the evolution of flower traits in the generalized food-deceptive plant Iris pumila, we assessed the color, size, shape, and fluctuating asymmetry (FA) of three functionally distinct floral organs—outer perianths (‘falls’), inner perianths (‘standards’), and style branches—and estimated pollinator-mediated selection on these traits. We evaluated the perianth color as the achromatic brightness of the fall, measured the flower stem height, and analyzed the floral organ size, shape, and FA using geometric morphometrics. Pollinated flowers had significantly higher brightness, longer flower stems, and larger floral organs compared to non-pollinated flowers. The shape and FA of the floral organs did not differ, except for the fall FA, where higher values were found for falls of pollinated flowers. Pollinator-mediated selection was confirmed for flower stem height and for subtle changes in the shape of the fall and style branch—organs that form the pollination tunnel. This study provides evidence that, although all analyzed flower traits play significant roles in pollinator attraction, flower stem height and pollination tunnel shape evolved under the pollinator-mediated selection, whereas achromatic brightness, size, and symmetry of floral organs did not directly affect pollination success.
... Under such circumstances, flowers can adapt their properties according to pollinator types to achieve reproductive success, because pollination success depends on the mutual match between the structure of flowers and pollinators [35][36][37]. Numerous studies document the pollinator-mediated selection of flower traits in orchids [37][38][39][40][41][42][43][44][45][46]. The better mechanical fit between the flower and the pollinator increases the precision of pollen transfer, affecting the effectiveness of plant reproduction [35,47]. ...
... Therefore, an important determinant of RS is the mutual match between flower and pollinator structures, which is one of the crucial evolutionary mechanisms in shaping plant-pollinator interactions and one of the essential prerequisites for successful pollination [35,89]. Pollinators act as selection agents on flower morphology and influence plant fitness [37,41,45,90,91]. Our results show the weak importance of flower traits in shaping pollinaria removal and fruit set in E. helleborine populations. ...
The purpose of our study was to determine the role of flower structure and nectar composition in shaping the reproductive success (RS) of the generalist orchid Epipactis helleborine in natural and anthropogenic populations. We supposed that the distinct character of two groups of habitats creates different conditions for plant–pollinator relationships, thus influencing reproductive success in E. helleborine populations. Both pollinaria removal (PR) and fruiting (FRS) were differentiated between the populations. On average, FRS was almost two times higher in the anthropogenic than in the natural populations. The difference between the two population groups in PR was smaller but still statistically significant. RS parameters were correlated with some floral display and flower traits. Floral display influenced RS only in three anthropogenic populations. Flower traits had a weak influence on RS (10 of the 192 cases analyzed). The more important trait in shaping RS was nectar chemistry. The nectar of E. helleborine is relatively diluted with a lower sugar concentration in the anthropogenic than in the natural populations. In the natural populations, domination of sucrose over hexoses was found, while in the anthropogenic populations, hexoses were more abundant and the participation of sugars was balanced. In some populations, sugars influenced RS. In E. helleborine nectar, 20 proteogenic and 7 non-proteogenic amino acids (AAs) were found with a clear domination of glutamic acid. We noted relationships between some AAs and RS, but distinct AAs shaped RS in different populations, and their impact was independent of their participation. Our results indicate that the flower structure and nectar composition of E. helleborine reflect its generalistic character and meet the requirements of a wide range of pollinators. Simultaneously, the differentiation of flower traits suggests a variation in pollinator assemblages in particular populations. Knowledge about the factors influencing RS in distinct habitats helps to understand the evolutionary potential of species and to understand mechanisms and processes crucial for shaping interactions between plants and pollinators.
... Studies on such species show that increasing the mechanical fit between flower and pollinator increases the precision of pollen transfer, thus affecting plant fitness [51]. Pollinator-mediated selection on flower traits is also documented by studies on deceptive orchids [52][53][54][55][56]. ...
... For example, rewarded species achieve higher RS than deceptive ones, and among rewarding species, those which produce nectar have the best effectiveness of pollination [7,11,13]. Many data document that reproductive success in orchids is strictly related to an important component of reproductive strategies-the flower's properties [42,46,49,56]. Generally, orchids are known as a group with a relatively low fruit set, especially non-autogamous species, mainly due to their limited pollinators [11,13,57]. ...
The aim of this study was to determine the level of reproductive success (RS) in natural and anthropogenic populations of generalist orchid Epipactis palustris and its dependence on flower structure and nectar composition, i.e., amino acids and sugars. We found that both pollinaria removal and female reproductive success were high and similar in all populations, despite differences in flower traits and nectar chemistry. Flower structures were weakly correlated with parameters of RS. Nectar traits were more important in shaping RS; although, we noted differentiated selection on nectar components in distinct populations. Individuals in natural populations produced nectar with a larger amount of sugars and amino acids. The sucrose to (fructose and glucose) ratio in natural populations was close to 1, while in anthropogenic ones, a clear domination of fructose and glucose was noted. Our results indicate that the flower traits and nectar composition of E. palustris reflect its generalist character and meet the requirements of a wide range of pollinators, differing according to body sizes, mouth apparatus, and dietary needs. Simultaneously, differentiation of nectar chemistry suggests a variation of pollinator assemblages in particular populations or domination of their some groups. To our knowledge, a comparison of nectar chemistry between natural and anthropogenic populations of orchids is reported for the first time in this paper.
... First, the flower pigmentation of numerous species exhibits considerable intraspecific variation [reviewed by Sapir et al. (2021)]. Intraspecific flower color variation can be discrete (Schemske and Bierzychudek, 2007;Streinzer et al., 2019;von Witt et al., 2020;Buide et al., 2021) or continuous, e.g., covering the spectrum of white, pink and purple in Trifolium pratense (Figure 1), orchids (Sletvold et al., 2016;Dormont et al., 2019) and the Iris atropurpurea complex (Roguz et al., 2020). The amount of pigment that is synthesized is a quantitative trait, and therefore small changes in the pigment synthesis pathway can yield appreciable changes in color (Shrestha et al., 2014;. ...
... Of these types of pigments, anthocyanins are most commonly associated with flower color polymorphisms (Sapir et al., 2021). Indeed, many species for which flower color variation was reported (Frey, 2004;Rakosy et al., 2012;Renoult et al., 2013;Sletvold et al., 2016;Dormont et al., 2019;Paine et al., 2019;Streinzer et al., 2019;Gómez et al., 2020;Whitney et al., 2020) have blue, pink or purple colors that are commonly due to anthocyanin pigments. It would be interesting to know, for these species, how standing variation in pigmentation relates to the flower's conspicuousness to their pollinators. ...
Floral pigments are a core component of flower colors, but how much pigment a flower should have to yield a strong visual signal to pollinators is unknown. Using an optical model and taking white, blue, yellow and red flowers as case studies, I investigate how the amount of pigment determines a flower’s color contrast. Modeled reflectance spectra are interpreted using established insect color vision models. Contrast as a function of the amount of pigment shows a pattern of diminishing return. Low pigment amounts yield pale colors, intermediate amounts yield high contrast, and extreme amounts of pigment do not further increase, and sometimes even decrease, a flower’s color contrast. An intermediate amount of floral pigment thus yields the highest visibility, a finding that is corroborated by previous behavioral experiments on bees. The implications for studies on plant-pollinator signaling, intraspecific flower color variation and the costs of flower color are discussed.
... For example, increasing display size, as observed by Torices et al. (2018), may compromise investment towards attractiveness such as colour. However, there remains disagreement over the extent to which producing flower colour pigments is costly (Archetti, 2009;Del Valle et al., 2019), and thus over whether such trade-offs should be expected (but see Sletvold et al., 2016). Moreover, the combination of size and colour may affect attractiveness to pollinators in non-additive ways, and may strongly depend on pollinator identity (Wertlen et al., 2008;de Ibarra et al., 2015;Stewart et al., 2015). ...
... The visitation rate and foraging decisions of many pollinators are influenced by floral colour (Ômura and Honda, 2005;Schaefer and Ruxton, 2011;Dötterl et al., 2014;de Ibarra et al., 2015;Fattorini and Glover, 2020). As such, floral colour influences pollination success, seed production, and siring success (Jones and Reithel, 2001;Caruso et al., 2010;Shang et al., 2011;Veiga et al., 2015;Sletvold et al., 2016), although selection intensity on floral colour frequently depends on environmental conditions (Caruso et al., 2019;Sletvold, 2019). Importantly, the effect of floral colour on pollinator behaviour and plant reproductive success may also depend on the distribution of rewards offered by other competing flowers in the pollination market (Chittka and Schürkens, 2001;Benitez-Vieyra et al., 2014). ...
The reproductive success of plants depends both on their phenotype and the local neighbourhood in which they grow. Animal-pollinated plants may benefit from increased visitation when surrounded by attractive conspecific individuals, via a “magnet effect.” Group attractiveness is thus potentially a public good that can be exploited by individuals, with selfish exploitation predicted to depend on genetic relatedness within the group. Petal colour is a potentially costly trait involved in floral signalling and advertising to pollinators. Here, we assessed whether petal colour was plastically sensitive to the relatedness of neighbours in the annual herb Moricandia moricandioides, which produces purple petals through anthocyanin pigment accumulation. We also tested whether petal colour intensity was related to nectar volume and sugar content in a context-dependent manner. Although both petal colour and petal anthocyanin concentration did not significantly vary with the neighbourhood configuration, plants growing with kin made a significantly higher investment in petal anthocyanin pigments as a result of the greater number and larger size of their flowers. Moreover the genetic relatedness of neighbours significantly modified the relationship between floral signalling and reward quantity: while focal plants growing with non-kin showed a positive relationship between petal colour and nectar production, plants growing with kin showed a positive relationship between number of flowers and nectar volume, and sugar content. The observed plastic response to group relatedness might have important effects on pollinator behaviour and visitation, with direct and indirect effects on plant reproductive success and mating patterns, at least in those plant species with patchy and genetically structured populations.
... When close relatives within a lineage occur in sympatry and are adapted to similar functional groups of pollinators, competition for pollinators can occur and negatively impact fitness of one or both plant species, particularly when pollinators are scarce and pollen limitation can occur (Caruso, 2000;Grossenbacher & Stanton, 2014;Muchhala et al., 2014;Sletvold et al., 2016). In such instances, selection for floral divergence in sympatry can arise, which has been documented in numerous groups of flowering plants, especially in temperate angiosperms (Sletvold et al., 2016). ...
... When close relatives within a lineage occur in sympatry and are adapted to similar functional groups of pollinators, competition for pollinators can occur and negatively impact fitness of one or both plant species, particularly when pollinators are scarce and pollen limitation can occur (Caruso, 2000;Grossenbacher & Stanton, 2014;Muchhala et al., 2014;Sletvold et al., 2016). In such instances, selection for floral divergence in sympatry can arise, which has been documented in numerous groups of flowering plants, especially in temperate angiosperms (Sletvold et al., 2016). Competition for pollinators can thus lead to greater floral divergence in sympatry compared to allopatry, or reproductive character displacement (RCD; Grossenbacher & Stanton, 2014), which represents an important mode of ecological character displacement sensu the classical definition (MacArthur & Levins, 1967). ...
Reproductive character displacement is a pattern whereby sympatric lineages diverge more in reproductive character morphology than allopatric lineages. This pattern has been observed in many plant species, but comparably few have sought to disentangle underlying mechanisms. Here, in a diverse lineage of Neotropical plants (Ruellia; Acanthaceae), we present evidence of reproductive character displacement in a macroevolutionary framework (i.e., among species) and document mechanistic underpinnings. In a series of interspecific hand pollinations in a controlled glasshouse environment, we found that crosses between species that differed more in overall flower size, particularly in style length, were significantly less likely to produce viable seeds. Further, species pairs that failed to set seed were more likely to have sympatric distributions in nature. Competition for pollinators and reinforcement to avoid costly interspecific mating could both result in these patterns and are not mutually exclusive processes. Our results add to growing evidence that reproductive character displacement contributes to exceptional floral diversity of angiosperms. Our study yields evidence of reproductive character displacement (RCD) in a diverse and widespread lineage of tropical plants. It is set apart from other studies in that we investigate RCD from a macroevolutionary perspective, by comparing data from experimental crosses among 33 different species pairs. We additionally generate and review evidence to help distinguish two primary drivers of RCD in animal‐pollinated plants: pollinator competition and reinforcement. Using this approach, we find evidence that more strongly supports a hypothesis of reinforcement over pollinator competition. Our study builds on prior macroevolutionary studies of RCD and underlying drivers, including landmark research in Drosophila.
... Floral color has been mostly viewed by evolutionary biologists as a qualitative trait (Harder and Johnson, 2009), and studies assessing selection on that floral feature as a continuous trait are not frequent (but see Renoult et al., 2013;Sletvold et al., 2016). In shore campion (Silene littorea Brot.), flower color shows a genetically determined continuous variation from dark pink to white, which so far has been analyzed considering the dark pink, light pink, and white categories for simplicity, with frequency distribution of colors differing drastically among populations (Casimiro-Soriguer et al., 2016;Del Valle et al., 2019). ...
... Herrera, 1993;Gómez, 2000;Harder and Johnson, 2009); however, the impact of flower production on male fitness has been more rarely reported (but see Maad, 2000). Total flower production and floral display showed a strong correlation in both populations, a fact that is usual (Worley and Barrett, 2000;Sletvold et al., 2016), although floral display may be more constant among species than the total flower number (Kudo and Harder, 2005). Floral display is one of the most important determinants of a plant's visual display and pollinators usually select plants with large floral displays (e.g., Eckhart, 1991;Thompson, 2001;Mitchell et al., 2004;Carlson and Holsinger, 2013). ...
Flower color, as other floral traits, may suffer conflicting selective pressures mediated by both mutualists and antagonists. The maintenance of intraspecific flower color variability has been usually explained as a result of direct selection by biotic agents. However, flower color might also be under indirect selection through correlated traits, since correlations among flower traits are frequent. In this study, we aimed to find out how flower color variability is maintained in two nearby populations of Silene littorea that consistently differ in the proportions of white-flowered plants. To do that, we assessed natural selection on floral color and correlated traits by means of phenotypic selection analysis and path analysis. Strong directional selection on floral display and flower production was found in both populations through either male or female fitness. Flower color had a negative indirect effect on the total male and female fitness in Melide population, as plants with lighter corollas produced more flowers. In contrast, in Barra population, plants with darker corollas produced more flowers and have darker calices, which in turn were selected. Our results suggest that the prevalence of white-flowered plants in Melide and pink-flowered plants in Barra is a result of indirect selection through correlated flower traits and not a result of direct selection of either pollinators or herbivores on color.
... Of these, nectar is perhaps the most important in an evolutionary sense (Simpson and Neff, 1983;Canto et al., 2011). Although it is a strong attractant, producing nectar is physiologically costly, and thus in several cases, the ability of flowers to produce nectar has been lost (Little, 1983;Dafni, 1984;Sletvold et al., 2016). In some plant families, e.g., Orchidaceae, the presence or absence of a nectar reward may be correlated with flower color. ...
... In any case, it is surprising that more taxa in these subgenera did not regain nectar production. Comparative studies have shown that nectarless taxa in general (Aragon and Ackerman, 2004;Sletvold et al., 2016), and Iris taxa specifically (Lavi and Sapir, 2015;Souto-Vilarós et al., 2018), are much more pollen limited than nectar producing taxa. ...
Floral color plays a key role as visual signaling and is therefore of great importance in shaping plant-pollinator interactions. Iris (Iridaceae), a genus comprising over 300 species and named after the Greek goddess of the colorful rainbow, is famous for its dazzling palette of flower colors and patterns, which vary considerably both within and among species. Despite the large variation of flower color in Iris, little is known about the phylogenetic and ecological contexts of floral color. Here, we seek to resolve the evolution of flower color in the genus Iris in a macroevolutionary framework. We used a phylogenetic analysis to reconstruct the ancestral state of flower color and other pollination-related traits (e.g., the presence of nectar and mating system), and also tracked the evolution of color variation. We further explored weather floral trait transitions are better explained by environmental or pollinator-mediated selection. Our study revealed that the most recent common ancestor likely had monomorphic, purple flowers, with a crest and a spot on the fall. The flowers were likely insect-pollinated, nectar-rewarding, and self-compatible. The diversity of floral traits we see in modern irises, likely represents a trade-off between conflicting selection pressures. Whether shifts in these flower traits result from abiotic or biotic selective agents or are maintained by neutral processes without any selection remains an open question. Our analysis serves as a starting point for future work exploring the genetic and physiological mechanisms controlling flower coloration in the most color-diverse genus Iris.
... Co-evolutionary dynamics between plants and pollinators drive reciprocal adaptations: plants modulate floral traits (e.g., morphology, pigmentation, scent profiles, and nectar chemistry) to optimize pollinator attraction, while insects evolve behaviours that enhance pollen transfer efficiency [6]. For instance, floral displays with larger corollas or high-contrast pigmentation attract greater pollinator diversity and visitation rates [7,8], whereas scent preferences vary taxonomically. Hymenoptera (e.g., bees) favor aromatic volatiles, whereas Diptera (e.g., flies) respond to sulfuraceous compounds [9,10]. ...
Camellia oleifera is an important woody oil plant in southern China, and developing its industry can enhance forest resource uses and increase edible oil supply. This study investigated the floral characteristics of different C. oleifera varieties, analysed the species and diversity of flower-visiting insects in different habitats, identified the main pollinators and their flower-visiting behaviours, and explored the relationship between pollinating insects and their floral characteristics. The floral lifespan of individual C. oleifera flowers was 5–8 d across cultivars, which is essentially the same. However, floral traits and nectar sugar composition exhibited distinct differences. There were 22 species of insect pollinators from 14 genera and 8 families, including Hymenoptera and Diptera, in 3 habitats. High-potential pollinators varied by habitat, with Apis cerana and Phytomia zonata being the most frequent. A comparison showed that A. cerana was the best pollinator, whereas P. zonata had a larger population, was not affected by oil tea nectar poisoning, and could still pollinate. Therefore, the contribution of P. zonata cannot be overlooked. Redundancy analysis revealed the response relationship between the floral traits of C. oleifera and three insect population characteristics. Stamen length was the main floral trait affecting insect populations.
... Moreover, across related taxa in Solonaceae in which floral divergence is driven by pollinator shifts, petal anthocyanin chemistry is unassociated with leaf flavonoid chemistry (Berardi et al., 2016b). While pollinator-mediated selection on pigments produced by the flavonoid pathway in petals is important (e.g., Sletvold et al., 2016), a recent meta-analysis shows that abiotic selection on floral traits is as strong as selection by pollinators (Caruso et al., 2019). Floral flavonoids and anthocyanins protect pollen from abiotic stress (Llorens et al., 2015;Koski and Ashman, 2015;Muhlemann et al., 2018;Koski and Galloway, 2018) and modify floral temperature with downstream impacts on seed production (Lacey et al., 2012). ...
... We used an experimental design in which we compared plants subjected to open (natural) versus hand pollination, performing path analysis to explore how floral traits (corolla shape, corolla size, spur length, nectar guide size, reproductive stalk length) and plant size affect plant fitness. Corolla size and nectar guide size are expected to increase flower attractiveness (De Jager et al., 2017;Sletvold et al., 2016;Van der Kooi et al., 2019;Zhang et al., 2017), whereas corolla shape variation could facilitate landing or flower handling by pollinators (De Ibarra et al., 2015;G omez & Perfectti, 2010). Stalk length is related to fitness either as a trait that increases flower visibility or by reducing the prey-pollinator conflict (Cross et al., 2018;El-Sayed et al., 2016;Jürgens et al., 2012). ...
In carnivorous plants, the fitness impacts of phenotypic variation in traits involved in prey attraction and capture have been well documented. However, floral traits could also contribute to the fitness of carnivorous plants. Pinguicula moranensis is a carnivorous plant that presents colorful zygomorphic flowers, which suggests some degree of specialization in its interactions with pollinators. We first tested pollen limitation experimentally by comparing the fruit set in plants that were manually cross‐pollinated with those that were pollinated naturally. Then, using a path analysis approach, we explored the effects of plant size and floral traits (corolla shape, corolla size, spur length, nectar guide size, and stalk length) on fitness (seed number per fruit). We performed two independent path analyses—one with the naturally pollinated plants and the other with the hand pollinated plants—to consider the impacts of these variables with and without the pressure of pollinator attraction. We expected stronger selection on floral traits in naturally pollinated plants. We found evidence of pollen limitation in the fruit set of the naturally pollinated group, suggesting that pollinator availability could impose selective pressures. The path analyses showed a marked direct positive effect of rosette size on plant fitness in both groups. The direct effects of all floral traits had similar magnitudes between the naturally pollinated and hand pollinated plants, except for corolla shape that showed higher coefficients in the first group. Thus, although we evidenced pollen limitation, our prediction about the role of pollinators as selective agents of floral traits in P. moranensis was barely supported.
... Natural intraspecific floral colour variations that also vary in their frequencies within and between populations are surprisingly widespread in nature (Sapir et al., 2021;Trunschke et al., 2021). In some deceptive orchids, white or pale-flowered variants of brightly-coloured species often coexist as polymorphic colours -for example, Dactylorhiza sambucina (Gigord et al., 2001) and continuous gradients -for example, Anacamptis morio (Sletvold et al., 2016) within natural population at relatively high frequencies. Instances where they occur at very low frequencies (ca. ...
Visual cues are of critical importance for the attraction of animal pollinators, however, little is known about the molecular mechanisms underpinning intraspecific floral colour variation. Here, we combined comparative spectral analysis, targeted metabolite profiling, multi‐tissue transcriptomics, differential gene expression, sequence analysis and functional analysis to investigate a bee‐pollinated orchid species, Glossodia major with common purple‐ and infrequent white‐flowered morphs. We found uncommon and previously unreported delphinidin‐based anthocyanins responsible for the conspicuous and pollinator‐perceivable colour of the purple morph and three genetic changes underpinning the loss of colour in the white morph – (1) a loss‐of‐function (LOF; frameshift) mutation affecting dihydroflavonol 4‐reductase ( DFR1 ) coding sequence due to a unique 4‐bp insertion, (2) specific downregulation of functional DFR1 expression and (3) the unexpected discovery of chimeric Gypsy transposable element (TE)‐gene ( DFR ) transcripts with potential consequences to the genomic stability and post‐transcriptional or epigenetic regulation of DFR . This is one of few known cases where regulatory changes and LOF mutation in an anthocyanin structural gene, rather than transcription factors, are important. Furthermore, if TEs prove to be a frequent source of mutation, the interplay between environmental stress‐induced TE evolution and pollinator‐mediated selection for adaptive colour variation may be an overlooked mechanism maintaining floral colour polymorphism in nature.
... Plant mutualists and antagonists such as pollinators and herbivores are important agents of selection on plant traits (Strauss 1997;Strauss & Whittall 2006;Caruso et al. 2019). Pollinatormediated selection can favor floral traits that increase pollinator attraction such as large floral displays, bright colours, or particular compounds of the floral scent (Parachnowitsch & Kessler 2010;Sletvold et al. 2016;Caruso et al. 2019;Chapurlat et al. 2019). However, more apparent floral signals J Poll Ecol 36(6) Manson et al. 2012). ...
Considering both pollinator and herbivore pressures on plant reproductive and defensive traits is key to understanding patterns of selection for plants. However, phenotypic selection studies connecting floral traits and plant defenses with pollinator activity and herbivore damage remain rare. We used the common milkweed, Asclepias syriaca (Apocynaceae), to study phenotypic selection on attractive and defensive traits, and nectar rewards. We measured herbivore (leaf damage) and pollinator activity (pollinia movement) and quantified selection via female (pollinia insertions and fruit number) and male fitness (pollinia removals). We found selection to increase plant and inflorescence size and to decrease floral size (i.e. petal width) via female fitness. We also detected selection to increase floral but not leaf latex. The lack of selection on leaf latex was congruent with the low herbivory observed, however we also did not observe florivory in the population that would explain the advantage of more floral latex. Interestingly, we found selection on attractive traits differed via pollinia insertions and fruits initiated, suggesting that something other than pollinators was driving selection via fruit production. In contrast to female fitness, we did not find selection on any trait through male fitness, suggesting no sexual conflicting selection, at least through these proxies. Our findings reinforce the importance of the direct assessment of pollinator pressures in phenotypic selection studies before assuming pollinators as drivers of floral evolution by natural selection. Further work in southern populations closer to the centre of the species range, where herbivory and plant defense investment are higher, may help elucidate selection on attractive and defensive traits.
... In fact, a study on bumble bees has shown that the contrast of flowers against their background is more critical for identifying their targets than color patterns within the flower (Whitney et al. 2013). Alternatively, within-flower contrast helps in guiding pollinators towards the nectar (Goldblatt et al. 1998;Hempel de Ibarra and Vorobyev 2009;Sletvold et al. 2016). Additionally, factors such as scent and nectar composition also play a major role in female attractivity (Bawa and Opler 1975;Ashman 2009). ...
Identifying plant sexual dimorphic traits is critical in advancing our knowledge on plant–pollinator interactions. For example, dimorphism in floral colors, or sexual dichromatism, is a crucial mediator of pollinator choice on foraging decisions. We studied Cylindropuntia wolfii, a model system, with diverse flower colors and a functionally dioecious sexual system. However, evidence suggests that sexual reproduction is limited in this species as it has a low seed set especially in naturally pollinated fruits. Thus, it is critical to this native species’ conservation to investigate its relationship with pollinators. Our goals were to: (a) investigate the sexual dimorphism including the sexual dichromatism in the flowers of the cactus, and (b) determine whether sexually dimorphic traits affect the pollinator attraction of both the sexes. We measured several quantitative and qualitative traits and compared them between male and female flowers. Then we recorded the pollinator visitation rate in nature for both sexes and tracked pollinator color preference using fluorescent dyes as pollen analogues. Our study showed that male flowers of C. wolfii are bigger and brighter, and they attract more potential pollinators than females, supporting the hypothesis that sexual dimorphism influences pollinator visitation preference. Fluorescence dichromatism, in which female flowers’ anthers fluoresce more than male flower anthers suggest this could be female flowers’ strategy to compensate for their dark colors and small size. The results from this study showed that C. wolfii exhibits sexual dichromatism and fluorescence dichromatism, which is a novel finding in plant research.
... Furthermore, the reproductive success of a plant may depend on its ability to attract flower visitors. These visitors that aid in pollination may exert selection on specific floral traits that are attractive to them [7][8][9]. The genus Barleria has approximately 300 species of shrubs and herbs that are distributed in the subtropical and tropical regions of the world [10][11][12][13]. ...
Barleria albostellata C.B. Clarke (grey barleria, Acanthaceae) is an indigenous shrub to South Africa and has been relatively understudied. This shrub is a valuable medicinal plant with a wide spectrum of antibacterial and anti-inflammatory activities. Detailed studies on the floral and pollen morphology on B. albostellata are rare. This study was conducted to observe the morphology of the flower and pollen grains using stereomicroscopy and scanning electron microscopy (SEM). Morphological observations showed numerous non-glandular trichomes on the bracteoles and bracts of B. albostellata. Three types of trichomes were identified on these structures: I—unicellular, II—multangulate-dendritic branched non-glandular trichomes, and III—capitate glandular trichomes. A taxonomical description of the floral structures using stereo and SEM micrographs is provided. SEM micrographs revealed the pollen grains as globose tricolporate with a rough honeycomb exine, and small granules inside the lumina. The diameter of the pollen grains was 77.53 ± 5.63 μm, whereas the aperture of these grains was 14.31 ± 0.59 µm. This study provides insight into the floral biology of B. albostellata, and the results presented here will add to the body of knowledge and encourage further research on this species.
... balearica), the phenotype weakly contributed to reproductive success traits, probably because they invest resources to promote other traits to attract pollinators by sexual deception, such as the shape of the labellum or floral scents rather than tall flower stalks or the number of flowers. Overall, pollen transfer is highly variable depending on spatiotemporal fluctuations and the individual and floral phenotypic traits and reproductive strategies that modulate pollinator attraction (Sletvold and Ågren, 2010;Sletvold et al., 2016). ...
Premise:
Deceptive pollination, a fascinating mechanism that independently originated in several plant families for benefiting from pollinators without providing any reward, is particularly widespread among orchids. Pollination efficiency is crucial in orchids due to the aggregated pollen in a pollinarium, which facilitates pollen transfer and promotes cross-pollination as pollinators leave after being deceived.
Methods:
In this study, we compiled data on reproductive ecology from five orchid species with different pollination strategies: three deceptive-strategy species (shelter imitation, food deception, sexual deception), one nectar-rewarding species, and one shelter-imitation but spontaneously selfing species. We aimed to compare the reproductive success (female fitness: fruit set; male fitness: pollinarium removal) and pollination efficiency of species representing these strategies. We also investigated pollen limitation and inbreeding depression among the pollination strategies.
Results:
Male and female fitness were strongly correlated in all species but the spontaneously selfing species, which had high fruit set and low pollinarium removal. As expected, pollination efficiency was highest for the rewarding species and the sexually deceptive species. Rewarding species had no pollen limitation but did have high cumulative inbreeding depression; deceptive species had high pollen limitation and moderate inbreeding depression; and spontaneously selfing species did not have pollen limitation or inbreeding depression.
Conclusions:
Pollinator response to deception is critical to maintain reproductive success and avoid inbreeding in orchid species with non-rewarding pollination strategies. Our findings contribute to a better understanding of the trade-offs associated with different pollination strategies in orchids and highlight the importance of pollination efficiency in orchids due to the pollinarium.
... In some systems, experimental studies could be designed that manipulate both individual phenotypes and their local selective environments simultaneously, that is "double-level" manipulations (Sinervo & Basolo, 1996;Svensson & Sinervo, 2000). Experimental manipulations of selective agents such as removing plant herbivores (Mauricio & Rausher, 1997), plant pollinators (Sletvold et al., 2016), or changing the density or frequency of intra-or inter-specific competitors or predators (Calsbeek & Cox, 2010;Schluter, 1994Schluter, , 2003Svensson & Sinervo, 2000) can sometimes be carried out. In many cases, however, experimental manipulations of selective agents are practically impossible. ...
In 1983, Russell Lande and Stevan Arnold published "The measurement of selection on correlated characters" which became a highly influential citation classic in evolutionary biology. This paper stimulated a cottage industry of field studies of natural and sexual selection in nature and resulted in several large-scale meta-analyses, statistical developments and method papers. The statistical tools they suggested contributed to a breakdown of the traditional dichotomy between ecological and evolutionary time scales and stimulated later developments such as "eco-evolutionary dynamics". However, regression-based selection analyses also became criticized from philosophical, methodological and statistical viewpoints and stimulated some still ongoing debates about causality in evolutionary biology. Here I return to this landmark paper by Lande and Arnold, analyse the controversies and debates it gave rise to and discuss the past, present and future of selection analyses in natural populations. A remaining legacy of Lande and Arnold (1983) are that studies of selection and inheritance can fruitfully be decoupled and be studied separately, since selection acts on phenotypes regardless of their genetic basis, and hence selection and evolutionary responses to selection are distinct processes.
... Flower color, especially petal color, is indispensable to plant reproduction and plays vital role in pollinator attraction and seed production (Abid et al. 2022;Sletvold et al. 2016). More importantly, floral color is a key determinant of the quality and commercial value of ornamental plants (Zhao and Tao 2015). ...
Key message
Yellow PetallocusGaYPis located on chromosome 11 and encodes a Sg6 R2R3-MYB transcription factor, which promotes flavonol biosynthesis and yellow coloration in Asiatic cotton petals.
Abstract
Petal color is pivotal to ornamental value and reproduction of plants. Yellow coloration in plant petals is mainly attributed to colorants including carotenoids, aurones and some flavonols. To date, the genetic regulatory mechanism of flavonol biosynthesis in petals is still to be elucidated. Here, we employed Asiatic cottons with or without deep yellow coloration in petals to address this question. Multi-omic and biochemical analysis revealed significantly up-regulated transcription of flavonol structural genes and increased levels of flavonols, especially gossypetin and 6-hydroxykaempferol, in yellow petals of Asiatic cotton. Furthermore, the Yellow Petal gene (GaYP) was mapped on chromosome 11 by using a recombinant inbred line population. It was found that GaYP encoded a transcriptional factor belonging to Sg6 R2R3-MYB proteins. GaYP could bind to the promoter of flavonol synthase gene (GaFLS) and activate the transcription of downstream genes. Knocking out of GaYP or GaFLS homologs in upland cotton largely eliminated flavonol accumulation and pale yellow coloration in petals. Our results indicated that flavonol synthesis, up-regulated by the R2R3-MYB transcription activator GaYP, was the causative factor for yellow coloration of Asiatic cotton petals. In addition, knocking out of GaYP homologs also led to decrease in anthocyanin accumulation and petal size in upland cotton, suggesting that GaYP and its homologs might modulate developmental or physiological processes beyond flavonol biosynthesis.
... Colour transitions in plant species may represent an adaptation to different, sometimes new, suites of pollinators (Thomson & Wilson 2008;Fenster et al. 2015;Sobral et al. 2015;Johnson et al. 2020;Mor e et al. 2020). Unless preferences differ among visitor species, phenotypic selection mediated by a specific functional group of pollinators is expected to constrain floral colour variation within plant populations (Sletvold et al. 2016;Brunet et al. 2021), since alternate colours arising through mutation are selected against (Eckhart et al. 2006). Importantly, however, pollinator-imposed constraints may only be obvious within the visual space of the pollinator, meaning that floral colour variation is in the eye of the beholder, while colour variation may be less constrained in the visual spaces of non-pollinators (Paine et al. 2019). ...
Cyclopia intermedia (honeybush) is a plant species endemic to the fynbos biome. Wild harvested populations are used commercially to produce tea. The species is a resprouter, regrowing from underground rootstock after fires, and as such resprouts once it has been cut. However, there is concern that premature cutting may be compromising rootstock recovery. We report on an initial 400 wild plants measured and monitored under different harvest regimes, including control plants. Plants were harvested once in 2018 and regrowth and survival monitored until 2021. Here, an allometric calculation is provided based on height and stem number to estimate the harvest yield. Plants in valleys or with high surrounding vegetation had the highest yield values and potential fecundity. After harvest, an increase in mortality was correlated with plant size, being higher for smaller plants, but after two years of drought high mortality was not explained by any harvesting category nor any of the site variables, suggesting drought results in high plant mortality regardless of harvest history. The study clarifies several speculative components of harvest method, demonstrates that a complete cut rather than half cut results in better potential yield, and that an ash admixture post-harvest had no measurable impact on regrowth.
... Colour transitions in plant species may represent an adaptation to different, sometimes new, suites of pollinators (Thomson & Wilson 2008;Fenster et al. 2015;Sobral et al. 2015;Johnson et al. 2020;Mor e et al. 2020). Unless preferences differ among visitor species, phenotypic selection mediated by a specific functional group of pollinators is expected to constrain floral colour variation within plant populations (Sletvold et al. 2016;Brunet et al. 2021), since alternate colours arising through mutation are selected against (Eckhart et al. 2006). Importantly, however, pollinator-imposed constraints may only be obvious within the visual space of the pollinator, meaning that floral colour variation is in the eye of the beholder, while colour variation may be less constrained in the visual spaces of non-pollinators (Paine et al. 2019). ...
Invasive plants displaying disparate pollination environments and abiotic conditions in native and non‐native ranges provide ideal systems to test the role of different ecological factors driving flower colour variation.
We quantified corolla reflectance of the ornithophilous South American Nicotiana glauca in native populations, where plants are pollinated by hummingbirds, and in populations from two invaded regions: South Africa, where plants are pollinated by sunbirds, and the Balearic island of Mallorca, where plants reproduce by selfing. Using visual modelling we examined how corolla reflectance could be perceived by floral visitors present in each region. Through Mantel tests we assessed a possible association between flower colour and different abiotic factors.
Corolla reflectance variation (mainly along medium to long wavelengths, i.e. human green‐yellow to red colours) was greater among studied regions than within them. Flower colour was more similar between South America and South Africa, which share birds as pollinators. Within invaded regions, corolla reflectance variation was lower in South Africa, where populations could not be distinguished from each other by sunbirds, than in Spain, where populations could be distinguished from each other by their occasional visitors. Differences in corolla colour among populations were partially associated with differences in temperature.
Our findings suggest that shifts in flower colour of N. glauca across native and invaded ranges could be shaped by changes in both pollination environment and climatic factors. This is the first study on plant invasions considering visual perception of different pollinators and abiotic drivers of flower colour variation.
... Field margins or bunds sown with a range of different annual and perennial flowering species result in variable improvements in the diversity and abundance of bees and other pollinators, depending on plant composition, seasonal flowering patterns and bee forage preferences (Carvell et al., 2007). There is also a long-standing theory that coflowering plants may facilitate pollination rather than competing for it (Sletvold et al., 2016). ...
Ecosystems are rapidly urbanizing at the global and regional scales, particularly in the tropics, which has deleterious effect on hymenopteran pollinators. Based on the literature spanning multiple disciplines including ecology, pollination, agriculture, agroecology and entomology, this review deliberates on the pollinators and their global decline. Also, it turns the focus on honey bees and their role in agroecosystem. Relevant information from melissopalynology is brought together and the gaps and directions of future research on conservation and management of honey bees in tropical peninsular India are discussed. Focus is on the two species of the hived native Apis cerana indica F., and Tetragonula iridipennis Smith (Hymenoptera: Apidae), as these play a major role in transforming existing agricultural landscapes into agroecosystems, benefitting the farmers and maintaining ecological balance in tropical peninsular India. This review brings to the fore the fact that there is a tangible gap in reports and long-term studies of many native pollinators and in particular the two hived honey bees. Most studies present in a thorough manner visual observations of pollinators (bees) on plants but rarely combine them with quantifying the resources gathered from the plants, especially pollen. This combined approach is especially important to understand the hymenopteran pollinators from the purview of the pollination service they provide. It can be concluded that there is a pressing requirement for long-term observations along these lines with quantifiable pollen and vegetation data to arrive at meaningful plant-pollinator networks that are essential for conservation and management of the native Asiatic honey bees as pollinators.
... It is also generally unclear what role brightness and chroma may play in pollinator attraction. Brightness is not thought to be used in the context of feeding by flies, wasps or bees (Chittka, 1992;Kevan et al., 1996;Troje, 1993) but has nonetheless been found to be under pollinator-mediated selection in multiple experimental studies (Caruso et al., 2010;Sletvold et al., 2016). Therefore, it is unclear if brightness is an important cue that Floral volatile compounds found in 11 Ferraria species. ...
One of the most compelling explanations for floral trait diversification and speciation in angiosperms is the process of pollinator shifts. The African genus, Ferraria, is a relatively small and understudied group of irises which interacts with many distinct pollinator groups and exhibits large variation in floral scent and colour. We built a phylogeny for the genus using three chloroplast gene regions and reconstructed the joint evolutionary history of pollination systems and floral traits. We found evidence for several historical shifts amongst pollinator functional groups and associations between pollinators and certain floral visual cues and mechanical fit traits. We also found evidence that colour divergence in Ferraria flowers evolved through non-random evolution. This indicates that pollinators may have played an important role in the diversification of visual floral traits within the genus. On the other hand, we found no association between pollinators and the overall scent chemistry of the flowers that they visited. This indicates that various olfactory cue combinations may attract similar pollinator assemblages, or that chemical compounds involved in pollinator attraction comprise only a small subset of all emitted compounds. Overall, these results suggest that adaptations to pollinators have influenced floral trait evolution within Ferraria.
... Fitness in orchids has been correlated with other phenotypic traits, such as the inflorescence size, as reported for Cephalanthera falcata by Suetsugu et al. (2015) and A. longicornu by Capó et al. (2020b), the spur length as seen in A. morio by Zitari et al. (2011), the number of flowers (Johnson and Nilsson 1999) or the brightness of the corolla (Sletvold et al. 2016). In the case of A. coriophora, no correlations were observed between fitness and any plant features, height, inflorescence length or flower number even considering correlations within populations (Fig. 3). ...
Pollination of deceptive orchids has enabled scientists to understand how these species avoid inbreeding depression by reducing the number of pollinator visits per inflorescence. In rewarding species, which receive a higher rate of visits per plant, geitonogamy is usually higher and therefore the risk of inbreeding increases. In this study, we assess the breeding system of the rewarding orchid A. corio-phora, and the spatio-temporal changes in its fitness as well as variation in nectar content after pollination. We found that the species partially selects allogamous pollen if pollinia from the same stalk and other plants arrive to the stigma. Furthermore, when self-pollination occurs, despite successful fructification, seed viability is significantly lower than that of cross-pollinated plants. A. coriophora exhibits spatio-temporal variation in fitness that does not correlate with any plant feature. Moreover, nectar volume is reduced after pollination, but the sugar concentration is maintained. This study emphasizes how essential the pre-zygotic and post-zygotic reproductive barriers are for rewarding orchids to avoid inbreeding depression.
... Each species was characterised by a phenological and a morphological distribution, both modelled by Gaussian curves. A Gaussian allows to represent a bell shape that often fits well the phenologies of flowering and pollinator activities (Malo, 2002;Rabinowitz et al., 1981;Stewart et al., 2020) or morphological trait distributions (Sletvold et al., 2016). Gaussian parameters have direct biological meaning that corresponds to the phenology peak or average morphological trait value and the variance to the phenology duration or morphological variation within species. ...
Morphological and phenological traits are key determinants of the structure of mutualistic networks. Both traits create forbidden links, but phenological traits can also decouple interaction in time. While such difference likely affects the indirect effects among species and consequently network persistence, it remains overlooked. Here, using a dynamic model, we show that networks structured by phenology favour facilitation over competition within guilds of pollinators and plants, thereby increasing network persistence, while the contrary holds for networks structured by morphology. We further show that such buffering of competition by phenological traits mostly beneficiate to specialists, the most vulnerable species otherwise, which propagate the most positive effects within guilds and promote nestedness. Our results indicate that beyond trophic mismatch, phenological shifts such as those induced by climate change are likely to affect indirect effects within mutualistic assemblages, with consequences for biodiversity. By developing a theoretical model including phenological and morphological structures in interactions, we show that mutualistic communities structured by phenological traits exhibit higher viability, species coexistence and nestedness than communities structured by morphological traits. We find that these contrasting effects on viability and coexistence arise from a shift in the balance between positive and negative indirect interactions among species, with phenological traits favouring within guild facilitation over competition contrary to morphological traits.
... As flower color is a trait highly affected by evolutionary constraints due to the influence of pollinator and non-pollinator agents of selection (Schiestl and Johnson, 2013;Sletvold et al., 2016), plasticity in flower color is expected to be low in comparison with other floral and vegetative traits (Del Valle et al., 2018; but see Gómez et al., 2020). However, flower color may show some degree of plasticity in response to abiotic as well as to biotic stressors, such as herbivores or pathogens (Wang et al., 2017;Rusman et al., 2019b;Koski and Galloway, 2020). ...
Variation in flower color due to transgenerational plasticity could stem directly from abiotic or biotic environmental conditions. Finding a link between biotic ecological interactions across generations and plasticity in flower color would indicate that transgenerational effects of ecological interactions, such as herbivory, might be involved in flower color evolution. We conducted controlled experiments across four generations of wild radish (Raphanus sativus, Brassicaceae) plants to explore whether flower color is influenced by herbivory, and to determine whether flower color is associated with transgenerational chromatin modifications. We found transgenerational effects of herbivory on flower color, partly related to chromatin modifications. Given the presence of herbivory in plant populations worldwide, our results are of broad significance and contribute to our understanding of flower color evolution.
... Although macroevolutionary studies have established broad correlations between floral traits and particular groups of flowers visitors (Van der Niet and Johnson 2012; Johnson and Wester 2017), experiments involving responses of animals to natural manipulated or artificial flowers are the most powerful way to determine the function of floral traits (Schemske and Bradshaw 1999;Campbell 2009). Studies of phenotypic selection involving standing trait variation (Sletvold and Ågren 2010;Sletvold et al. 2016;Caruso et al. 2019) and experimental evolution (Gervasi and Schiestl 2017) are also valuable, but in some cases, it is necessary by means of techniques such as hybridisation, to reintroduce phenotypic variation that may have been eliminated by selection (Schemske and Bradshaw 1999), or to use artificial or manipulated natural flowers to gain insights into floral function (Campbell 2009;Campbell et al. 2016;Policha et al. 2016). The advantage of using artificial flowers or manipulations of natural flowers is that this allows precise identification of traits that influence behaviour (Bell 1985;Mitchell-Olds and Shaw 1987;Fulton and Hodges 1999). ...
Experimental studies of the use of visual and olfactory cues by flower-visiting animals can shed light on the evolution of floral signalling traits. We examined the functional significance of floral traits in Clivia miniata (Amaryllidaceae). This forest lily with large orange trumpet-shaped flowers is pollinated mainly by swallowtail butterflies and belongs to a lineage with ancestral bird pollination. We used C. miniata flowers varying in colour, orientation and scent, and arrays of artificial flowers varying in colour, pattern, orientation, size, shape, and scent to assess foraging preferences of the butterflies that pollinate C. miniata. Butterflies preferred orange over yellow colour morphs of C. miniata and preferred red and orange model flowers over yellow ones. Orange models with a central yellow target ‘nectar guide’ were favoured over plain orange models. Butterflies also favoured large over small model flowers and preferred to alight on upward-facing flowers. Addition of scent compounds emitted by C. miniata flowers increased butterfly visitation to model and natural flowers. These results identify the importance of particular combinations of visual and olfactory signals for attraction of swallowtail butterflies and shed light on the floral modifications associated with a shift from bird to butterfly pollination.
... The broad associations between flower color and different pollinator groups offer indirect evidence that pollinators may have played a crucial role in floral color evolution (Faegri and van der Pijl, 1966;Fenster et al., 2004), while selection studies demonstrate more directly that pollinators can select on flower color (Harder and Johnson, 2009;Sletvold et al., 2016). Furthermore, geographically structured color forms of the same species (floral ecotypes), or closely related species, are frequently visited by different pollinators, providing additional evidence that pollinators are important drivers of flower color divergence (e.g., van der Niet et al., 2014;Newman et al., 2015;. ...
The striking variation in flower color across and within Angiosperm species is often attributed to divergent selection resulting from geographic mosaics of pollinators with different color preferences. Despite the importance of pollinator mosaics in driving floral divergence, the distributions of pollinators and their color preferences are seldom quantified. The extensive mass-flowering displays of annual daisy species in Namaqualand, South Africa, are characterized by striking color convergence within communities, but also color turnover within species and genera across large geographic scales. We aimed to determine whether shifts between orange and white-flowered daisy communities are driven by the innate color preferences of different pollinators or by soil color, which can potentially affect the detectability of different colored flowers. Different bee-fly pollinators dominated in both community types so that largely non-overlapping pollinator distributions were strongly associated with different flower colors. Visual modeling demonstrated that orange and white-flowered species are distinguishable in fly vision, and choice experiments demonstrated strongly divergent color preferences. We found that the dominant pollinator in orange communities has a strong spontaneous preference for orange flowers, which was not altered by conditioning. Similarly, the dominant pollinator in white communities exhibited an innate preference for white flowers. Although detectability of white flowers varied across soil types, background contrast did not alter color preferences. These findings demonstrate that landscape-level flower color turnover across Namaqua daisy communities is likely shaped by a strong qualitative geographic mosaic of bee-fly pollinators with divergent color preferences. This is an unexpected result given the classically generalist pollination phenotype of daisies. However, because of the dominance of single fly pollinator species within communities, and the virtual absence of bees as pollinators, we suggest that Namaqua daisies function as pollination specialists despite their generalist phenotypes, thus facilitating differentiation of flower color by pollinator shifts across the fly pollinator mosaic.
... In orchids, floral color often shows intraspecific polymorphism and many orchids present nectar guides and differences in color between floral parts (Darwin, 1877;Aguiar et al., 2012;Sletvold et al., 2016;Pansarin et al., 2018). Furthermore, orchid flowers present a specialized structure, the labellum, a modified petal which is usually distinct from petals and sepals regarding both color and morphology (Darwin, 1877;van der Pijl and Dodson, 1966;Fay and Chase, 2009). ...
Flower color has been studied in different ecological levels of organization, from individuals to communities. However, it is unclear how color is structured at the intrafloral level. In bee-pollinated flowers, the unidirectional gradient in color purity and pollen mimicry are two common processes to explain intrafloral color patterns. Considering that floral traits are often integrated, usually reflecting evolutionary modules under pollinator-mediated selection, we hypothesize that such intrafloral color patterns are structured by intrafloral color modules as perceived by bee color vision system. Here, we studied the tropical bee-pollinated orchid Cattleya walkeriana, given its intrafloral color complexity and variation among individuals. Considering bee color vision, we investigated if intrafloral color modules arose among intrafloral patches (tip or base of the sepals, petals, and labellum). We expected a separate color module between the labellum patches (the main attractive structure in orchids) and petals and sepals. We measured the color reflectance and calculated the photoreceptor excitation, spectral purity, hue, and the chromatic contrast of the floral structures in the hexagon color model. Spectral purity (saturation) was higher in the labellum tip in comparison to petals and sepals, generating a unidirectional gradient. Labellum base presented a less saturated yellow UV-absorbing color, which may reflect a pollen mimicry strategy. C. walkeriana presented three intrafloral color modules corresponding to the color of petals and sepals, the color of the labellum tip, and the color of labellum base. These color modules were unrelated to the development of floral structures. Given the importance of intrafloral color patterns in bee attraction and guidance, our results suggest that intrafloral patterns could be the outcome of evolutionary color modularization under pollinator-mediated selection.
... We are still lacking observational and experimental evidence of the link between individual variation in odour bouquet and reproductive success in a spatially explicit context, that is by considering Ophrys densities, habitat geometry and nearest-neighbour distance within local populations, and the intensity of gene flow within metapopulations (see Sletvold, Grindeland, & Ågren, 2010;Sletvold et al., 2016). Such research should also investigate the additive or interactive effects of potential explanatory variables influencing pollination success, such as pollinator abundances and weather conditions. ...
Adaptive radiations occur mostly in response to environmental variation through the evolution of key innovations that allow emerging species to occupy new ecological niches. Such biological innovations may play a major role in niche divergence when emerging species are engaged in reciprocal ecological interactions. To demonstrate coevolution is a difficult task; only a few studies have confirmed coevolution as driver of speciation and diversification. Herein we review current knowledge about bee orchid (Ophrys spp.) reproductive biology. We propose that the adaptive radiation of the Mediterranean orchid genus Ophrys, comprising several hundred species, is due to coevolutionary dynamics between these plants and their pollinators. We suggest that pollination by sexual swindling used by Ophrys orchids is the main driver of this coevolution. Flowers of each Ophrys species mimic a sexually receptive female of one particular insect species, mainly bees. Male bees are first attracted by pseudo-pheromones emitted by Ophrys flowers that are similar to the sexual pheromones of their females. Males then are lured by the flower shape, colour and hairiness, and attempt to copulate with the flower, which glues pollen onto their bodies. Pollen is later transferred to the stigma of another flower of the same Ophrys species during similar copulation attempts. In contrast to rewarding pollination strategies, Ophrys pollinators appear to be parasitized. Here we propose that this apparent parasitism is in fact a coevolutionary relationship between Ophrys and their pollinators. For plants, pollination by sexual swindling could ensure pollination efficiency and specificity, and gene flow among populations. For pollinators, pollination by sexual swindling could allow habitat matching and inbreeding avoidance. Pollinators might use the pseudo-pheromones emitted by Ophrys to locate suitable habitats from a distance within complex landscapes. In small populations, male pollinators would disperse once they have memorized the local diversity of sexual pseudo-pheromone bouquets or if all Ophrys flowers are fertilized and thus repel pollinators via production of repulsive pheromones that mimic those produced by fertilized female bees. We propose the following evolutionary scenario: Ophrys radiation is driven by strong intra-specific competition among Ophrys individuals for the attraction of species-specific pollinators, which is a consequence of the high cognitive abilities of pollinators. Male bees record the pheromone signatures of kin or of previously courted partners to avoid further copulation attempts, thereby inducing strong selection on Ophrys for variation in odour bouquets emitted by individual flowers. The resulting odour bouquets could by chance correspond to pseudo-pheromones of the females of another bee species, and thus attract a new pollinator. If such pollinator shifts occur simultaneously in several indivuals, pollen exchanges might occur and initiate speciation. To reinforce the attraction of the new pollinator and secure prezygotic isolation, the following step is directional selection on flower phenotypes (shape, colour and hairiness) towards a better match with the body of the pollinator's female. Pollinator shift and the resulting prezygotic isolation is adaptive for new Ophrys species because they may benefit from competitor-free space for limited pollinators. We end our review by proritizing several critical research avenues.
... Pollinators select on flower color attributes such as brightness and hue (Caruso et al., 2010;Sletvold et al., 2016), so the most commonly tested driver of geographic variation in floral coloration is the pollination community. Pollinator guilds often differ in their sensory biases for flower color (Schiestl and Johnson, 2013) and if pollinator communities differ between populations they can drive geographically divergent selection. ...
Petal color variation within species is common and may be molded by abiotic or biotic selection pressures, or neutral population structure. For example, darker flowers may be favored in cooler environments because they absorb more solar radiation, elevating the temperature of reproductive structures. Additionally, flower color may evolve to attract the dominant or most efficient pollinator type in a given population. Here, we evaluate geographic variation in petal coloration across the range of Campanula americana in Eastern North America and test whether color covaries with abiotic factors, the pollination community, and genetic structure established through post-glacial expansion. Consistent with other studies, flowers from cooler, higher latitude populations were less reflective across the UV-NIR spectrum than those from warmer populations. Local temperature explained variation in petal reflectance better than the pollinator community or colonization history. Petal color perceived by trichromatic bee pollinators displayed a strong longitudinal pattern but was unassociated with climatic factors and the pollinator community. Instead, pollinator-perceived color was tightly correlated with the geographic distance from C. americana's glacial refugium. In total, abiotic conditions appear to shape large-scale geographic variation in the intensity of petal reflectance while genetic structure is the strongest driver of pollinator-perceived petal coloration. This study highlights the importance of abiotic factors and historical processes associated with range expansion as major evolutionary forces shaping diversity of flower coloration on large geographic scales.
... Many recent studies that manipulated pollinators as the agents of natural selection found display size [27][28][29], flower color [30,31] and floral phenology [32,33] under strong selection, suggesting that phenotypic plasticity in those traits can affect pollinator behavior and, in consequence, the fitness outcome for a plant. Leaf herbivory has indeed been found to induce reductions in the number of flowers as well as corolla size, which is usually associated with a reduced seed set per flower [18,34]. ...
Plant induced responses to herbivory have long been found to function as plant direct and indirect defenses and to be major drivers of herbivore community and population dynamics. While induced defenses are generally understood as cost-saving strategies that allow plants to allocate valuable resources into defense expression, it recently became clear that, in particular, induced metabolic changes can come with significant ecological costs. In particular, interactions with mutualist pollinators can be significantly compromised by herbivore-induced changes in floral morphology and metabolism. We review recent findings on the evidence for ecological conflict between defending against herbivores and attracting pollinators while using similar modes of information transfer (e.g. visual, olfactory, tactile). Specifically, we discuss plant traits and mechanisms through which plants mediate interactions between antagonists and mutualist and present functional hypotheses for how plants can overcome the resulting conflicts.
... The three studied subspecies were characterized by different floral colours, yet no phenotypic selection was found on this trait, contrary to what has been reported in other orchids (Gross et al., 2016;Sletvold, Trunschke, Smit, Verbeek, & Ågren, 2016). ...
Current divergent selection may promote floral trait differentiation among conspecific populations in flowering plants. However, whether this applies to complex traits such as colour or scents has been little studied, even though these traits often vary within species. In this study, we compared floral colour and odour as well as selective pressures imposed upon these traits among seven populations belonging to three subspecies of the widespread, generalist orchid Anacamptis coriophora . Colour was characterised using calibrated photographs and scents were sampled using dynamic headspace extraction and analysed using gas chromatography‐mass spectrometry. We then quantified phenotypic selection exerted on these traits by regressing fruit set values on floral trait values. We showed that the three studied subspecies were characterised by different floral colour and odour, with one of the two predominant floral volatiles emitted by each subspecies being taxon‐specific. Plant size was positively correlated with fruit set in most populations, while we found no apparent link between floral colour and female reproductive success. We detected positive selection on several taxon‐specific compounds in A. coriophora subsp. fragrans , whereas no selection was found on floral volatiles of A. coriophora subsp. coriophora and A. coriophora subsp. martrinii . This study is one of the first to document variation in phenotypic selection exerted on floral scents among conspecific populations. Our results suggest that selection could contribute to ongoing chemical divergence among A. coriophora subspecies.
... Our analysis revealed an overall trend for the transformation of petal color in Cucurbitaceae from yellow to white (Supplemental Figure 26). The transition to white petals reduces the visibility of plants to bees (Sletvold et al., 2016), implying a change of or decrease in the demand for pollinators. The reduction of stamen number (Supplemental Figure 22) and the enlargement of pollen size (Supplemental Figure 23) seem to simplify the structure of flowers, allowing the plants to reallocate the energy and resources to other purposes, such as increasing ovule production (Sicard and Lenhard, 2011). ...
The ability of climbing plants to grow upward along others to reach canopy for photosynthesis is hypothesized as a key innovation in flowering plants. Cucurbitaceae, a family containing ∼1000 species and many important crops, are mostly climbers and have characteristic tendrils and pepo fruits. Here, we present 127 newly sequenced transcriptomes and genomes along with other datasets for a total of 136 cucurbits representing all tribes to establish a robust Cucurbitaceae phylogeny containing eight highly resolved major clades. We analyzed whole genome duplication (WGD), diversification dynamics and ancestral morphologies, and found that after early genome duplication event(s), a burst of diversification and morphological innovations in flower, fruit and root characters occurred under the climate optimum in the Early Eocene. Species radiation under Mid-Eocene Climatic Optimum also coincided with several morphological changes shared by 80% of cucurbits. We found that the cucurbit-specific tendril identity gene TEN originated from a paleo-polyploidization at the origin of the family. Our results support the hypothesis that cucurbit diversifications were probably driven by increased genetic diversity following polyploidizations and novel state of traits under paleo-climate upheavals. This study provides a phylogenetic framework and new insights into morphological and genomic changes facilitating the adaptive evolution of Cucurbitaceae.
Pollinators navigate complex and heterogeneous “flower markets”, where floral resources vary in quality, availability, and distribution. Bumblebees, as generalist foragers, visit numerous flowers during their foraging bouts. Yet, the factors influencing their flower choices and the notable individual differences in foraging behaviour among bees are still not well understood. We hypothesised that early foraging experiences influence bees’ subsequent flower choices. To test this, we observed individual Bombus terrestris workers forage for three consecutive bouts in two artificial flower arrays. One array simulated a favourable environment with patches alternating high- and low-quality flowers (40% vs. 20% w/w sucrose solution), while the other array presented a more challenging environment with patches of high-quality flowers alongside unrewarded flowers (40% w/w sucrose solution vs. plain water). In both arrays, bees rapidly improved their foraging efficiency, increasing sucrose intake per unit time across bouts. In the favourable array, most bees became highly selective for high-quality flowers, while some continued visiting both flower types. Their degree of pickiness was influenced by early experiences: bees initially exposed to high-quality flowers became more selective, whereas those encountering low-quality flowers first were less selective in subsequent foraging. Despite differences in pickiness and array conditions, bees achieved comparable sucrose intake rates within three bouts. This study highlights the adaptability of bee foraging behaviour and emphasizes the role of early foraging experiences in driving individual differences.
Significance statement
To forage efficiently, pollinators must navigate complex “flower markets”, where floral resources vary in quality and availability. We observed Bombus terrestris workers forage across three bouts in two artificial flower arrays: a favourable array with flower patches alternating high- and low-quality flowers (40% vs. 20% w/w sucrose solution), and an extreme array with high-quality and non-rewarding flowers (40% w/w sucrose solution vs. plain water). We found that bees initially exposed to high-quality flowers became highly selective, whereas those encountering low-quality flowers first were less picky, collecting both flower types. Despite these differences, bees rapidly improved foraging efficiency over successive bouts, achieving similar sucrose intake rates within three bouts. This study highlights the foraging flexibility of bumblebees and suggests that early experiences can have lasting effects, influencing flower choices dozens of visits later.
Premise
While some studies have found leaf variegation to reduce photosynthetic capacity, others showed that it can increase photosynthesis. Thus, what maintains variegation remains an open question. Two primary hypotheses—the anti‐herbivory and abiotic heterogeneity hypotheses—have been posited, yet little empirical research explicitly investigates the maintenance of naturally occurring variegation.
Methods
We used field surveys, image analysis, and climatic associations to explore the anti‐herbivory and abiotic heterogeneity hypotheses in 21 populations of Hexastylis heterophylla and H. shuttleworthii , both polymorphic for leaf variegation. We measured the frequency of variegated individuals, variegation intensity, and herbivory for each morph, assessed abiotic correlates with variegation, and measured photosynthetic efficiency.
Results
We found a strong elevational cline in leaf variegation strongly linked with abiotic heterogeneity; variegation was more common in lower‐elevation populations characterized by higher temperatures, UV‐B exposure, seasonal light change, and drier, more basic soils. Variegated and nonvariegated individuals experienced similar levels of herbivory. Morphs had similar photosynthetic quantum yields. However, nonvariegated leaves experienced more nonphotochemical quenching, an indication of photoinhibition, and had higher surface temperatures under high light.
Conclusions
Our results suggest that variegation may serve as an adaptation to high temperatures and light conditions and can reduce photoinhibition in certain environmental contexts. Thus, abiotic factors can maintain variegation in wild populations and shape geographic clines in variegation.
Premise
The family Annonaceae possesses a broad array of floral phenotypes and pollination specialisations, and are important in the plant-pollinator interactions of tropical rainforests. Although there has been considerable effort to assess their interactions with pollinators, attempts to characterise their visual and olfactory communication channels are scarce.
Methods
Here, we investigated the pollination biology of 12 Annonaceae species from five genera, viz. Meiogyne , Monoon , Polyalthia , Pseuduvaria , and Uvaria . Furthermore, their floral colour was characterised by reflectance spectroscopy and floral odour chemistry was assessed using gas chromatography-mass spectrometry. Floral scent was further compared across the whole family using non-metric dimensional scaling plots to identify specialisation in floral odour.
Results
The Meiogyne species are likely pollinated by small beetles; the Polyalthia and Pseuduvaria species are likely pollinated by beetles and flies; and the Uvaria species is likely pollinated by beetles and bees. Flowers of most species are UV non-reflective, and have various spectral reflectance profile across the remaining visible spectra. Multiple species produce floral odour resembling ripe fruits. The flowers of Meiogyne species and Polyalthia xanthocarpa emitted mostly branched-chain esters, while flowers of Uvaria released mainly straight-chain esters. The Pseuduvaria species instead emitted scent reminiscent of rotten fruits, largely consisting of 2,3-butanediol. The inner petal corrugation in Meiogyne functions as a food reward, and the inner petal growth serves as a nectary gland for Pseuduvaria .
Conclusions
Our study identifies the visual and olfactory cues of multiple Annonaceae species and provides insights into how Annonaceae flowers attract different guilds of pollinators.
In this review, we tried to summarize the results of all more or less noticeable works carried out in recent years and devoted to the search for ecological factors influencing the corolla color in flowering plants. The influence of various factors on corolla color has been established, including temperature, precipitation, soil characteristics, geographic latitude and longitude, distance from the place of species origin, interaction with pollinators, and in some cases the nature of such influence has been analyzed. However, it should be noted that the results obtained are rather scattered and relate to particular species, groups or phytocenoses. Significant efforts remain to be done to summarize the particular results into an overall picture, and we offer and justify our proposals for the direction of future research.
Background
Pollinators impose strong selection on floral traits. Indeed, pollinator syndromes are the result of these strong selective forces, but other abiotic and biotic agents also drive the evolution of floral traits and influence plant reproduction. Global change is expected to have widespread effects on biotic and abiotic systems resulting in novel selection on floral traits under future conditions.
Scope
Global change has depressed pollinator abundance and altered abiotic conditions, thereby exposing flowering plant species to novel suites of selective pressures. Here we consider how biotic and abiotic factors interact to shape the expression and evolution of various floral characteristics (the targets of selection), including floral size, color, physiology, reward quantity and quality, and longevity amongst other traits. We examine cases in which selection imposed by climatic factors conflicts with pollinator-mediated selection. Additionally, we explore how floral traits respond to environmental changes through phenotypic plasticity and how that can alter plant fecundity. In this review, we evaluate how global change may shift the expression and evolution of floral phenotypes.
Conclusions
Floral traits evolve in response to multiple interacting agents of selection. Different agents can sometimes exert conflicting selection. For example, pollinators often prefer large flowers, but drought stress can favor the evolution of smaller flowers, and the size of floral organs can evolve as a trade-off between selection mediated by these opposing actors. Nevertheless, few studies have factorially manipulated abiotic and biotic agents of selection to disentangle their relative strengths and directions of selection. The literature has more often evaluated plastic responses of floral traits to stressors than it has considered how abiotic factors alter selection on these traits. Furthermore, global change will likely alter the selective landscape through changes in the abundance and community compositions of mutualists and antagonists and novel abiotic conditions. We encourage future work to consider a more holistic model of floral evolution, which will enable more robust predictions about floral evolution and plant reproduction as global change progresses.
Human‐mediated environmental change, by reducing mean fitness, is hypothesized to strengthen selection on traits that mediate interactions among species. For example, human‐mediated declines in pollinator populations are hypothesized to reduce mean seed production by increasing the magnitude of pollen limitation and thus strengthen pollinator‐mediated selection on floral traits that increase pollinator attraction or pollen transfer efficiency. To test this hypothesis, we measured two female fitness components and six floral traits of Lobelia siphilitica plants exposed to supplemental hand‐pollination, ambient open‐pollination, or reduced open‐pollination treatments. The reduced treatment simulated pollinator decline, while the supplemental treatment was used to estimate pollen limitation and pollinator‐mediated selection. We found that plants in the reduced pollination treatment were significantly pollen limited, resulting in pollinator‐mediated selection for taller inflorescences and more vibrant petals, both traits that could increase pollinator attraction. This contrasts with plants in the ambient pollination treatment, where reproduction was not pollen limited and there was not significant pollinator‐mediated selection on any floral trait. Our results support the hypothesis that human‐mediated environmental change can strengthen selection on traits of interacting species and suggest that these traits have the potential to evolve in response to changing environments.
Understanding whether and how resource limitation alters phenotypic selection on floral traits is key to predict the evolution of plant-pollinator interactions under climate change. Two important resources predicted to decline with our changing climate are pollinators and water in the form of increased droughts. Most work, however, has studied these selective agents separately and in the case of water deficit, studies are rare. Here, we use the common morning glory (Ipomoea purpurea) to investigate the effects of experimental reduction in pollinator access and water availability on floral signals and nectar rewards and their effects on phenotypic selection on these traits. We conducted a manipulative experiment in a common garden, where we grew plants in three treatments: 1) pollinator restriction, 2) water reduction, and 3) unmanipulated control. Plants in pollinator restriction and control treatments were well-watered compared to water deficit. We found that in contrast to pollinator restriction, water deficit had strong effects altering floral signals and nectar rewards but also differed in the direction and strength of selection on these traits compared to control plants. Water deficit increased the opportunity for selection, and selection in this treatment favored lower nectar volumes and larger floral sizes, which might further alter pollinator visitation. In addition, well-watered plants, both in control and pollinator deficit, showed similar patterns of selection to increase nectar volume suggesting non-pollinator-mediated selection on nectar. Our study shows that floral traits may evolve in response to reduction in water access faster than to declines in pollinators and reinforces that abiotic factors can be important agents of selection on floral traits. Although only few experimental selection studies have manipulated access to biotic and abiotic resources, our results suggest that this approach is key for understanding how pollination systems may evolve under climate change.
Identifying plant sexual dimorphic traits is critical in advancing our knowledge on plant-pollinator interactions. For example, dimorphism in floral colors, or sexual dichromatism, is a crucial mediator of pollinator choice on foraging decisions. We studied Cylindropuntia wolfii, an exemplary model system, with diverse flower colors and a functionally dioecious sexual system. However, it is struggling to reproduce sexually as it has a low seed set especially in naturally pollinated fruits. Thus, it is critical to this native species’ conservation to investigate its relationship with pollinators. Our goals were to: a) investigate the sexual dimorphism including the sexual dichromatism in the flowers of the cactus, and b) determine whether sexually dimorphic traits affect the pollinator attraction of both the sexes. We measured several quantitative and qualitative traits for sexual dimorphism and compared them using statistical analyses. Then we recorded the pollinator visitation rate in nature for both sexes and tracked pollinator color preference using fluorescent dyes as pollen analogues. Our study showed that male flowers of C. wolfii are bigger and brighter, and they attract more potential pollinators than females, supporting that sexual dimorphism influences pollinator visitation preference. Fluorescence dichromatism plays a role on pollinator visitation in this species, in which female flowers’ anthers fluoresce more than male flower anthers suggesting this could be female flowers’ strategy to compensate for their dark colors and small size. The results from this study showed that C. wolfii exhibits sexual dichromatism and fluorescence dichromatism, which is a novel finding in plant research.
Premise:
Floral traits are frequently under pollinator-mediated selection, especially in taxa subject to strong pollen limitation, such as those reliant on pollinators. However, antagonists can be agents of selection on floral traits as well. The causes of selection acting on spring ephemerals are understudied though these species can experience particularly strong pollen limitation. I examined pollinator- and antagonist-mediated selection in a narrowly endemic spring ephemeral, Trillium discolor.
Methods:
I measured pollen limitation in T. discolor across two years, and evaluated its breeding system. I compared selection on floral traits (display height, petal size, petal color, flowering time) between open-pollinated, and pollen-supplemented plants to measure the strength and mode of pollinator-mediated selection. I assessed whether natural levels of antagonism impacted selection on floral traits.
Results:
Trillium discolor was self-incompatible and experienced pollen limitation in both years of the study. Pollinators exerted negative disruptive selection on display height and petals size. In one year, pollinator-mediated selection favored lighter petals but in the second year pollinators favored darker petals. Antagonist damage did not alter selection on floral traits.
Conclusions:
Results demonstrate that pollinators mediate the strength and mode of selection on floral traits in T. discolor. Interannual variation in the strength, mode, and direction of pollinator-mediated selection on floral traits could be important for maintaining of floral diversity in this system. Observed levels of antagonism were weak agents of selection on floral traits. This article is protected by copyright. All rights reserved.
Reduced water availability can cause physiological stress in plants that affects floral development leading to changes in floral morphology and traits that mediate interactions with pollinators. As pollinators can detect small changes in trait expressions, drought-induced changes in floral traits could affect pollinator visitations. However, the linkage between changes in floral traits and pollinator visitations under drought conditions is not well explored. We therefore tested whether drought-induced changes in floral morphology and abundance of flowers are linked to changes in pollinator visitations. We conducted flight cage experiments with a radio frequency identification system for automated visitation recordings with bumble bees (Bombus terrestris) and common charlock (Sinapis arvensis) as the model system. In total, we recorded interactions for 31 foraging bumble bees and 6,569 flower visitations. We found that decreasing soil moisture content correlated with decreasing size of all measured morphological traits except stamen length and nectar tube width. The reductions in floral size, petal width and length, nectar tube depth and number of flowers resulted in decreasing visitation rates by bumble bees. These decreasing visitations under lower soil moisture availability might be explained by lower numbers of flowers and thus a reduced attractiveness and/or by increased difficulties experienced by bumble bees in handling smaller flowers. Whether these effects act additively or synergistically on pollinator behaviour and whether this leads to changes in pollen transfer and to different selection pressures require further investigation.
In Japan, Camellia japonica and Camellia rusticana are naturally distributed. Despite differences in their habitats and morphologies, they have been classified by various researchers as either varieties, subspecies, or species. The taxonomic position of C. japonica and C. rusticana remain unclear because morphological comparisons have been restricted to limited areas and quantitative data are scarce. C. rusticana grows in snowy places, unlike C. japonica. While C. japonica displays ornithophily, C. rusticana displays entomophily. Both species have adapted to different growing environments and pollinators, which have altered the morphology of flowers and leaves. We therefore quantitatively estimated the differentiation between these two taxa by comparing the morphologies of leaf hypodermis, flower form, petal color, and filament color in twenty populations. Our findings allowed us to differentiate these two species by the presence or absence of a leaf hypodermis. We also discovered an intermediate type of leaf hypodermis, which might also be caused by hybridization. Principal component analysis (PCA) indicated that the flower morphologies between these species were significantly different. The petal and filament colors were also significantly different. Our quantitative analysis suggests that speciation caused by differences in both pollinators and environment is one of the factors involved in this group. These findings in C. japonica and C. rusticana help to explain speciation processes for other species as well.
Background
Genetic pathways involved with flower color and shape are thought to play an important role in the development of flowers associated with different pollination syndromes, such as those associated with bee, butterfly, or hummingbird pollination. Because pollination syndromes are complex traits that are orchestrated by multiple genes and pathways, the gene regulatory networks have not been explored. Gene co-expression networks provide a systems level approach to identify important contributors to floral diversification.
Methods
RNA-sequencing was used to assay gene expression across two stages of flower development (an early bud and an intermediate stage) in 10 species of Achimenes (Gesneriaceae). Two stage-specific co-expression networks were created from 9,503 orthologs and analyzed to identify module hubs and the network periphery. Module association with bee, butterfly, and hummingbird pollination syndromes was tested using phylogenetic mixed models. The relationship between network connectivity and evolutionary rates ( dN / dS ) was tested using linear models.
Results
Networks contained 65 and 62 modules that were largely preserved between developmental stages and contained few stage-specific modules. Over a third of the modules in both networks were associated with flower color, shape, and pollination syndrome. Within these modules, several hub nodes were identified that related to the production of anthocyanin and carotenoid pigments and the development of flower shape. Evolutionary rates were decreased in highly connected genes and elevated in peripheral genes.
Discussion
This study aids in the understanding of the genetic architecture and network properties underlying the development of floral form and provides valuable candidate modules and genes for future studies.
The hypothesis that the understory herbs Costus allenii and C. laevis (Zingiberaceae) have converged in floral characteristics to use the same pollinator was investigated in central Panama. Observations and experiments indicated that these species (1) occupy the same habitats, (2) flower synchronously, (3) are identical in flower color, morphology, and nectar secretion patterns, (4) share the same pollinator, the bee Euglossa imperialis, (5) are self-compatible, but not autogamous, and (6) have strong barriers to hybridization. Both grow in low density along streamsides and produce a single flower per day for an extended period (up to 4 mo). Flower density is depressed through extensive predation by the weevil Cholus cinctus, which damaged 31% of all C. allenii and 60% of all C. laevis inflorescences. Direct observation of foraging bees indicated that individuals regularly visit both plant species. An experimental analysis of interspecific pollen transfer using powered paint as a marker verified these results; 97% of the flowers checked had received heterospecific visits. The high probability of interspecific pollination did not affect fruiting success. I suggest that low flower density, exaggerated by extreme floral predation, has selected for floral similarity and pollinator sharing in these species. Floral convergence increases effective flower density and nectar supplies, and probably increases the regularity and rate of pollinator visitation.
•
When coflowering plant species share pollinators, pollinator-mediated competition may favor divergent floral characters associated with pollinator attraction. One potential outcome of this process is that sympatric populations will display increased divergence in floral traits compared with allopatric populations. We developed a new system to study the pattern and process of character displacement. In the central Sierra Nevada of California, USA, Mimulus bicolor is a spring wildflower with two flower-color morphs, one of which resembles coflowering M. guttatus.•
We documented a fine-scale geographic pattern of character displacement in sympatric and allopatric patches and, using experimental arrays, measured seed set in M. bicolor color morphs in the presence versus absence of M. guttatus.•
In sympatric arrays yellow, guttatus-like M. bicolor morphs had lower relative fitness (0.35 ± 0.05) and reduced conspecific pollen deposition compared with the distinct alternative morph, whereas in allopatric arrays yellow, guttatus-like morphs were occasionally strongly favored.•
Pollinator-mediated competition with M. guttatus is consistent with ecological character displacement in M. bicolor and likely contributes to a geographic pattern of character displacement.
© 2014 Botanical Society of America, Inc.
Significance
A prominent floral display may increase attractiveness to pollinators but also the risk of damage from herbivores. Here, we show experimentally that differences in the relative strength of interactions with grazers and pollinators could explain variation in selection on floral display among natural populations of an insect-pollinated primrose. In addition, we demonstrate that differences in selection translate into rather rapid changes in the genetic composition of local plant populations. The results indicate that interactions with mutualists and antagonists can drive adaptive differentiation not only across broad geographic scales but also among populations across relatively short distances.
Despite the dominating role of pollinators in floral evolution, mounting evidence reveals significant additional, often antagonistic, influences of abiotic and biotic non-pollinator agents. Even when pollinators and other agents impose selection on floral traits in the same direction, the role of other agents is fre- quently overlooked. Maintenance of genetic variation in floral traits and divergence from trait optima for pollination can result from both indirect selection on correlated traits and direct selection on floral traits. For example, in numerous species, periods of heat or drought favour pink- or purple-flowered individuals over white-flowered ones, because associated anthocyanins in vegetative tissues enhance stress tolerance. Conflicting selection on floral traits may also occur directly when floral antagonists and mutualists share the same preferences. We review the evidence for influences of abiotic and biotic non-pollinator agents of selection on several floral traits: petal colour, flower and display size, flower shape, nectar composition, flowering phenology, and breeding system. Despite growing evidence of the importance of non-pollinator selection, few studies have explored the relative strength of selection from pollinators versus other sources. In several cases, pollinators are not the strongest current source of selection on floral traits, despite perhaps being the driving factor shaping floral traits historically. Future studies will benefit from a synthetic approach that recognizes the entire ecological context of floral adaptation and combines field experiments with genetic studies to determine the relative roles of pollinators and non-pollinator agents in floral evolution. The study of floral evolution will be enhanced by approaches that incorporate a broader context that includes both abiotic and biotic agents of selection.
Spatial variation in plant-pollinator interactions may cause variation in pollinator-mediated selection on floral traits, but to establish this link conclusively experimental studies are needed. We quantified pollinator-mediated selection on flowering phenology and morphology in four populations of the fragrant orchid Gymnadenia conopsea, and compared selection mediated by diurnal and nocturnal pollinators in two of the populations. Variation in pollinator-mediated selection explained most of the among-population variation in the strength of directional and correlational selection. Pollinators mediated correlational selection on pairs of display traits, and on one display trait and spur length, a trait affecting pollination efficiency. Only nocturnal pollinators selected for longer spurs, and mediated stronger selection on the number of flowers compared with diurnal pollinators in one population. The two types of pollinators caused correlational selection on different pairs of traits and selected for different combinations of spur length and number of flowers. The results demonstrate that spatial variation in interactions with pollinators may result in differences in directional and correlational selection on floral traits in a plant with a semi-generalized pollination system, and suggest that differences in the relative importance of diurnal and nocturnal pollinators can cause variation in selection.
© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.
Identifying the molecular genetic basis of traits contributing to speciation is of crucial importance for understanding the ecological and evolutionary mechanisms that generate biodiversity. Despite several examples describing putative "speciation genes," it is often uncertain to what extent these genetic changes have contributed to gene flow reductions in nature. Therefore, considerable interest lies in characterizing the molecular basis of traits that actively confer reproductive isolation during the early stages of speciation, as these loci can be attributed directly to the process of divergence. In Southern California, two ecotypes of Mimulus aurantiacus are parapatric and differ primarily in flower color, with an anthocyanic, red-flowered morph in the west and an anthocyanin-lacking, yellow-flowered morph in the east. Evidence suggests that the genetic changes responsible for this shift in flower color have been essential for divergence and have become fixed in natural populations of each ecotype due to almost complete differences in pollinator preference. In this study, we demonstrate that a cis-regulatory mutation in an R2R3-MYB transcription factor results in differential regulation of enzymes in the anthocyanin biosynthetic pathway and is the major contributor to differences in floral pigmentation. In addition, molecular population genetic data show that, despite gene flow at neutral loci, divergent selection has driven the fixation of alternate alleles at this gene between ecotypes. Therefore, by identifying the genetic basis underlying ecologically based divergent selection in flower color between these ecotypes, we have revealed the ecological and functional mechanisms involved in the evolution of pre-mating isolation at the early stages of incipient speciation.
Patterns of morphological variation within the Tolumnia variegata complex of Puerto Rico, Hispaniola, and Cuba are described. Univariate and multivariate analyses of population data obtained from fresh material collected in Puerto Rico and the Dominican Republic indicated that three a priori groups (Puerto Rican spring- and fall-flowering populations, and Hispaniolan spring-flowering) are slightly different but considerable univariate overlap occurs in all characteristics measured, especially between the two phenological types in Puerto Rico. Among the flowering types, sympatric populations are either not different or are similar morphologically than pairs of allopatric populations. Similar analyses of herbaruim specimens, including type material, revealed that T. leiboldii, a species often confused with T. variegata, is restricted to Cuba, and is distinguished by having obovate instead of pandurate petals. Furthermore, spring- and fall-flowering T. variegata are more similar to each other within islands than among islands. Phenological and geographical groups are slightly different but the similarities among them are outstanding. Thus the Cuban, Hispaniolan, Puerto Rican, and Virgin Island populations of both phenological types represent a single species, T. variegata. Although some characteristics are plastic, especially vegetative features, the origin and maintenance of extraordinary levels of variation in T. variegata may involve hybridization, founder effects, and frequency dependent selection.
In most pollination systems, animals transfer pollen among plants of a given species. Pollinator visita-tions do not come without cost, so plants usually offer a reward. However, the flowers of some plant species, mostly orchids, lack rewards and deceive animals into visiting their flowers. Deceptive species are thought to have high levels of variation in traits associated with advertisement and pollinator attraction, which have been attributed to genetic drift, or disruptive selection due to pollinator behavior. Rewarding species are assumed to have less variation due to stabilizing selection. We compared vari-ability in floral morphology and fragrance composition between deceptive and rewarding species. Because both suites of traits are often linked with floral advertisement and pollinator attraction, we expected variation to be greater in species with deceptive pollination systems than in those offering rewards. We obtained floral morphology metrics for 20 deceptive species and 41 rewarding species native or naturalized in Puerto Rico, Venezuela, and Ecuador. Floral fragrances were sampled from eight deceptive species and four rewarding species. We found that the amplitude of variation in floral morphology and fragrance composition covaries significantly. Comparison of coefficients of variation for morphology indicated that, overall, deceptive species show significantly higher varia-tion than rewarding species, and this pattern was also found among just orchids or just nonorchids. There were no statistical differences in morphological variation between orchids and nonorchids within a functional pollination group. Fragrance variation, measured by Jaccard distance, tended to be greater for deceptive species than for rewarding species. Although overlap in measures of vari-ation occurs between the two groups, the data support the hypothesis that populations of deception-pollinated species are more variable than rewarding species in traits associ-ated with pollinator attraction.
Floral evolution has often been associated with differences in pollina-tion syndromes. Recently, this conceptual structure has been criticized on the grounds that flowers attract a broader spectrum of visitors than one might expect based on their syndromes and that flowers often diverge without excluding one type of pollinator in favor of another. Despite these criticisms, we show that pollination syndromes provide great utility in understanding the mechanisms of floral diversification. Our conclusions are based on the importance of organizing pollinators into functional groups according to presumed similarities in the selection pressures they exert. Furthermore, functional groups vary widely in their effectiveness as pollinators for particular plant species. Thus, although a plant may be visited by several functional groups, the relative se-lective pressures they exert will likely be very different. We discuss various methods of documenting selection on floral traits. Our review of the literature indicates over-whelming evidence that functional groups exert different selection pressures on floral traits. We also discuss the gaps in our knowledge of the mechanisms that underlie the evolution of pollination syndromes. In particular, we need more information about the relative importance of specific traits in pollination shifts, about what selective factors favor shifts between functional groups, about whether selection acts on traits inde-pendently or in combination, and about the role of history in pollination-syndrome evolution.
Sympatric plant species with similar flowering phenologies and floral mor-phologies may compete for pollination, and as a consequence potentially influence each other's reproductive success and mating system. Two likely competitors are Mimulus ringens and Lobelia siphilitica, which co-occur in wet meadows of central and eastern North Amer-ica, produce blue zygomorphic flowers, and share several species of bumble bee pollinators. To test for effects of competition for pollination, we planted experimental arrays of Mimulus ringens, each consisting of genets with unique combinations of homozygous marker ge-notypes. In two arrays we planted mixtures of Mimulus and Lobelia, and in two additional arrays we planted Mimulus without a competitor for pollination. Bumble bee pollinators frequently moved between Mimulus and Lobelia flowers in the mixed-species arrays, with 42% of plant-to-plant movements being interspecific transitions. Pollinator movements between species were associated with a reduction in the amount of conspecific pollen arriving on Mimulus stigmas. The presence of Lobelia led to a significant 37% reduction in the mean number of Mimulus seeds per fruit. In addition, Mimulus had a significantly lower rate of outcrossing in the mixed-species arrays (0.43) than in the ''pure'' arrays (0.63). This is the first study to demonstrate that competition for pollination directly in-fluences outcrossing rates. Our work suggests that in self-compatible populations with genetic load, competition for pollination may not only reduce seed quantity, but may also lower seed quality.
— Motivated by data demonstrating fluctuating relative and absolute fitnesses for white- versus blue-flowered morphs of the desert annual Linanthus parryae, we present conditions under which temporally fluctuating selection and fluctuating contributions to a persistent seed bank will maintain a stable single-locus polymorphism. In L. parryae, blue flower color is determined by a single dominant allele. To disentangle the underlying diversity-maintaining mechanism from the mathematical complications associated with departures from Hardy-Weinberg genotype frequencies and dominance, we successively analyze a haploid model, a diploid model with three distinguishable genotypes, and a diploid model with complete dominance. For each model, we present conditions for the maintenance of a stable polymorphism, then use a diffusion approximation to describe the long-term fluctuations associated with these polymorphisms. Our protected polymorphism analyses show that a genotype whose arithmetic and geometric mean relative fitnesses are both less than one can persist if its relative fitness exceeds one in years that produce the most offspring. This condition is met by data from a population of L. parryae whose white morph has higher fitness (seed set) only in years of relatively heavy rain fall. The data suggest that the observed polymorphism may be explained by fluctuating selection. However, the yearly variation in flower color frequencies cannot be fully explained by our simple models, which ignore age structure and possible selection in the seed bank. We address two additional questions–one mathematical, the other biological–concerning the applicability of diffusion approximations to intense selection and the applicability of long-term predictions to datasets spanning decades for populations with long-lived seed banks.
The innate preferences of inexperienced bumble bees, Bombus terrestris, for floral colour stimuli were studied using artificial flowers. The artificial flowers provided a colour pattern and consisted of a star-shaped corolla and of central colour patches similar to the nectar guide of natural flowers. The innate choice behaviour was assessed in terms of the number of approach flights from some distance towards the artificial flowers and the percentage of approach flights terminating in antennal contact with the floral guide. The colours of the floral guide, the corolla and the background were varied. It was shown that the innate flower colour preference in bumble bees has two components. 1. The frequency of approaches from a distance is correlated with the colour difference between the corolla and the background against which it is presented. If the corolla colour was constant but its background colour varied, the relative attractiveness of the corolla increased with its colour difference to the background. The colour difference assessment underlying this behaviour on a perceptual basis can be attained by means of colour opponent coding, a system well-established in Hymenoptera. 2. The frequency of antennal contacts with the floral guides relative to that of approach flights cannot be accounted for by colour opponent coding alone. Whether the approach flights are interrupted, or whether they end in an antennal contact with the nectar guide is strongly dependent on the direction (sign) of the colour difference, not only its magnitude. The choice behaviour requires a unique perceptual dimension, possibly that of colour saturation or that of hue perception comparable to components of colour perception in humans.
Rare albino morphs of the montane larkspur Delphinium nelsonii differ from common blue-flowered morphs in overall flower color, and in the strength of a contrasting color pattern at the center of the flower that presumably guides pollinators to concealed nectar. Previous studies showed that bumblebees and hummingbirds discriminate against albinos when presented with mixtures of the 2 morphs, and that it takes these pollinators longer to fly between successive flowers on albino than on blue-flowered inflorescences. To explore the link between these observations, we measured pollinator preferences and flower-to-flower flight times (handling times) before and after painting flowers in 2 alternative ways that enhanced albino nectar guides. In all of 16 experimental replicates discrimination against albinos was reduced or eliminated after painting, and albino handling times declined toward values for blue-flowered inflorescences. This consistent result indicates that an inferior nectar guide increases the energetic cost of foraging at albinos. Increased cost in turn explains discrimination, under the reasonable assumption that hummingbirds and bumblebees are sensitive to foraging economics.
The evolutionary tuning between floral colouration and the colour vision of flower-visiting Hymenoptera is quantified by evaluating the informational transfer from the signalling flower to the perceiving pollinator. The analysis of 180 spectral reflection spectra of angiosperm blossoms reveals that sharp steps occur precisely at those wavelengths where the pollinators are most sensitive to spectral differences. Straight-forward model calculations determine the optimal set of 3 spectral photoreceptor types for discrimination of floral colour signals on the basis of perceptual difference values. The results show good agreement with the sets of photoreceptors characterized electrophysiologically in 40 species of Hymenoptera.
Multivariate statistical methods are derived for measuring selection solely from observed changes in the distribution of phenotypic characters in a population within a generation. Selective effects are readily detectable in characters that do not change with age, such as meristic traits or adult characters in species with determinate growth. Ontogenetic characters, including allometric growth rates, can be analyzed in longitudinal studies where individuals are followed through time. Following an approach pioneered by Pearson (1903), this analysis helps to reveal the target(s) of selection, and to quantify its intensity, without identifying the selective agent(s). By accounting for indirect selection through correlated characters, separate forces of directional and stabilizing (or disruptive) selection acting directly on each character can be measured. These directional and stabilizing selection coefficients are respectively the parameters that describe the best linear and quadratic approximations to the selective surface of individual fitness as a function of the phenotypic characters. The theory is illustrated by estimating selective forces on morphological characters influencing survival in pentatomid bugs and in house sparrows during severe weather conditions.
Nectar guides, contrasting patterns on flowers that supposedly direct pollinators towards a concealed nectar reward, are taxonomically widespread. However, there have been few studies of their functional significance and effects on plant fitness. Most previous studies focused on pollinator behaviour and used artificial flowers in laboratory settings. We experimentally investigated the role of putative nectar guides in a natural system: the South African iris Lapeirousia oreogena, whose flowers have a clearly visible pattern of six white arrow-markings pointing towards the narrow entrance of the long corolla tube, and its sole pollinator, a long-proboscid nemestrinid fly. We painted over none, some or all of the white arrow-markings with ink that matched the colour of the corolla background. Although arrow-marking removal had little effect on the approaches by flies to flowers from a distance, it dramatically reduced the likelihood of proboscis insertion. Export of pollen dye analogue (an estimate of male fitness) was reduced to almost zero in flowers from which all nectar guides had been removed, and fruit set (a measure of female fitness) was also significantly reduced. Our results confirm that the markings on L. oreogena flowers serve as nectar guides and suggest that they are under strong selective maintenance through both male and female fitness components in this pollination system.
The reproductive organs and mating biology of angiosperms exhibit greater variety than those of any other group of organisms. Flowers and inflorescences are also the most diverse structures produced by angiosperms, and floral traits provide some of the most compelling examples of evolution by natural selection. Given that flowering plants include roughly 250,000 species, their reproductive diversity will not be explained easily by continued accumulation of case studies of individual species. ınstead a more strategic approach is now required, which seeks to identify general principles concerning the role of ecological function in the evolution of reproductive diversity. The Ecology and Evolution of Flowers uses this approach to expose new insights into the functional basis of floral diversity, and presents the very latest theoretical and empirical research on floral evolution. Floral biology is a dynamic and growing area and this book, written by the leading internationally recognized researchers in this field, reviews current progress in understanding the evolution and function of flowers. Chapters contain both new research findings and synthesis. Major sections in turn examine functional aspects of floral traits and sexual systems, the ecological influences on reproductive adaptation, and the role of floral biology in angiosperm diversification. Overall, this integrated treatment illustrates the role of floral function and evolution in the generation of angiosperm biodiversity. This advanced textbook is suitable for graduate level students taking courses in plant ecology, evolution, systematics, biodiversity and conservation. ıt will also be of interest and use to a broader audience of plant scientists seeking an authoritative overview of recent advances in floral biology.
Gene exchange between locally adapted plant populations can have significant evolutionary consequences, including changes in genetic diversity, introduction of adaptive or maladaptive traits, disruptive of coadaptive gene complexes, and the creation of new ecotypes or even species. The potential for introgression between divergent populations will depend on the strength of selection against nonnative characters. Morphologically variable F2 hybrids of two Gilia capitata subspecies were used to evaluate the strength of phenotypic selection and the response to selection in the home habitats of each subspecies. At both sites, traits diagnostic of the subspecies were subject to significant phenotypic selection, probably mediated by direct selection on unmeasured correlated characters. Phenotypic selection favored native morphologies in all but a single case; leaf shape of one subspecies was favored in both habitats. The strength of selection varied between sites, with one site selecting more strongly against nonnative characters. Offspring of the F2 hybrids showed a significant evolutionary response to selection when grown in a common environment. Evolution was in the direction of similarity with the subspecies native to the site where selection was imposed. This result reveals that native character states are adaptive and suggests that selection will maintain native morphologies even after a substantial influx of genes from an ecologically and morphologically distinct, and locally adapted subspecies.
The maintenance of floral-color variation within natural populations is enigmatic because directional selection through pollinator preferences combined with random genetic drift should lead to the rapid loss of such variation. Fluctuating, balancing, and negative frequency - dependent selection mediated through pollinators have been identified as factors that may contribute to the maintenance of floral-color variation, and recently it has been suggested that indirect responses to selection on correlated characters through agents of selection other than pollinators may substantially shape the evolution of floral traits. Here, I provide empirical support for this latter view in Claytonia virginica (Portulacaceae) through a multiseason field study, a pollen supplementation study, and an artificial herbivory experiment. These studies show that most individuals fall into one of four discrete color classes, and suggest pollinator-mediated selection for increased floral redness in concurrent years. Floral color is also an indirect target of opposing directional selection via herbivores and pathogens that fluctuates through time. Taken together, these data suggest a novel mechanism by which floral-color variation may be maintained, and illustrate the importance of an inclusive, pluralistic view of selection when investigating the evolution of complex phenotypes.
Geitonogamy (transfer of pollen among flowers on the same plant) may lead to reduced outcrossing and interfere with sex function. Orchids with pollen packaged into pollinaria would be expected to be particularly vulnerable to the loss of cross-mating opportunities imposed by geitonogamy. We tested the hypothesis that the absence of floral rewards in many orchid species is a means of reducing geitonogamy. Experiments with the deceptive species Orchis mascula and Orchis morio showed that queen bumble bees probe more flowers and stay longer on plants when artificial nectar is added to the flowers. Overall, the data indicated that the evolution of nectar production in deceptive Orchis species would result in moderate to high levels of geitonogamy, as a consequence of the greater number of flowers probed and longer visit duration (∼ 60 s) by pollinators. However, the estimated levels of geitonogamy were less than expected, due both to a time delay before freshly withdrawn pollinaria bend into the correct position to strike a stigma and to extensive carryover of pollen. The time elapsed before a freshly withdrawn pollinarium is in the correct position to strike the stigma was found to vary 30-80 s, depending on the orchid species. Since pollinators usually spend
Competition for pollination has been hypothesized to select for the divergence of floral traits between species and populations. A primary prediction of this hypothesis is that the strength of competition for pollination, mediated by variation in plant abundance, should directly influence the strength of selection on floral traits. To test this prediction, I examined the relationships between multiple components of plant abundance and pollination, reproductive success, and phenotypic selection via female fitness on four floral traits in artificial and natural populations of the hummingbird-pollinated Ipomopsis aggregata. In the artificial arrays, I manipulated the absolute density and interspersion of neighboring I. aggregata and a competitor for pollination (Castilleja linariaefolia). I also measured natural variation in the absolute and relative density of these two species within a 2.5-m radius of focal I. aggregata plants in three natural populations. The strength of competition for pollination in the I. aggregata-C, linariaefolia system was only weakly influenced by local plant abundance. Both the absolute density and interspersion of plants in the arrays significantly influenced at least one component of I. aggregata's pollination and reproductive success, but the effects were not consistent across these components. For example, the treatment groups that received more conspecific pollen were not the same ones that set more seeds/fruit. Within the natural populations, variation in relative and absolute plant density influenced two components of I. aggregata's pollination and reproductive success, but only in one to two populations per component. As would be expected from these inconsistent effects of plant abundance on pollination and reproduction, the strength of selection on floral traits of I. aggregata in both the arrays and natural populations was also only weakly dependent on abundance. Previous studies have indicated (1) that self-incompatible species such as I. aggregata should experience strong, abundance-dependent effects on pollination, and (2) that variation in plant abundance at a local scale should have a stronger effect on pollination than variation at a larger spatial scale. In contrast, my results suggest that the effect of plant abundance on pollination cannot be easily predicted from simple diagnostic traits such as breeding system or spatial scale.
Mutualists and antagonists are known to respond to similar floral cues, and may thus cause opposing selection on floral traits. However, we lack a quantitative understanding of their independent and interactive effects. In a population of the orchid Gymnadenia conopsea, we manipulated the intensity of pollination and herbivory in a factorial design to examine whether both interactions influence selection on flowering phenology, floral display, and morphology. Supplemental hand-pollination increased female fitness by 31% and one-quarter of all plants were damaged by herbivores. Both interactions contributed to selection. Pollinators mediated selection for later flowering and herbivores for earlier flowering, while both selected for longer spurs. The strength of selection was similar for both agents, and their effects were additive. As a consequence, there was no. net selection on phenology, whereas selection on spur length was strong. The experimental results demonstrate that both pollinators and herbivores can markedly influence the strength of selection on flowering phenology and floral morphology, and cause both conflicting and reinforcing selection. They also indicate that the direction of selection on phenology will vary with the relative intensity of the mutualistic and antagonistic interaction, potentially resulting in both temporal and among-population variation in optimal flowering time.
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Pollinator‐mediated selection is a major evolutionary driver of floral traits; yet, such selection has rarely been tested for floral extreme traits. The O ncocyclus irises have exceptionally large, dark‐colored flowers, associated with night‐sheltering pollination and heat reward by the dark flowers.
We quantified phenotypic selection on stem length, floral size and color in two species of iris ( I ris atropurpurea and I . haynei ), using an experimental approach. We estimated selection gradients for both flowers open to natural pollination and for flowers receiving supplementary hand pollination, assuming that open‐pollinated flowers are affected by all factors that could influence fitness, whereas supplementary pollination removes the possible influence of pollinators.
We found evidence for pollinator‐mediated selection to increase floral size and stem length in I . atropurpurea , but floral color in this species was not under pollinator‐mediated selection. In I . haynei , no pollinator‐mediated selection on any of the traits was detected.
We conclude that the extreme floral size of I . atropurpurea has probably evolved as a result of pollinator behavior. Lack of such evidence for I . haynei and for the dark floral color in both species suggests that other non‐pollinator agents are selecting for these prominent traits, or that phenotypic color variation in these irises is neutral.
Abstract Reinforcement is the process by which increased reproductive isolation between incipient species evolves due to selection against maladaptive hybrids or costly hybrid mating. Reinforcement is predicted to create a pattern of greater prezygotic reproductive isolation in regions where the two species co-occur, sympatry, than in allopatry. Although most research on reinforcement focuses on understanding the evolutionary forces acting in sympatry, here we consider what prevents the alleles conferring greater reproductive isolation from spreading into allopatry. We investigate flower color divergence in the wildflower Phlox drummondii, which is caused by reinforcement in the regions sympatric with its congener Phlox cuspidata. Specifically, we performed common garden field experiments and pollinator observations to estimate selection acting on flower color variation in allopatry. We combine our estimates of maternal and paternal fitness using simulations and predict how flower color alleles migrating from sympatry will evolve in allopatry. Our results suggest that strong pollinator preference for the ancestral flower color in allopatry can maintain divergence between allopatric and sympatric populations.
Spatial variation in pollinator-mediated selection (Δβpoll ) is a major driver of floral diversification, but we lack a quantitative understanding of its link to pollen limitation and net selection on floral traits. For 2-5 years, we quantified Δβpoll on floral traits in two populations each of two orchid species differing in pollen limitation. In both species, spatio-temporal variation in Δβpoll explained much of the variation in net selection. Selection was consistently stronger and the proportion that was pollinator-mediated was higher in the severely pollen-limited deceptive species than in the rewarding species. Within species, variation in pollen limitation could not explain variation in Δβpoll for any trait, indicating that factors influencing the functional relationship between trait variation and pollination success govern a major part of the observed variation in Δβpoll . Separating the effects of variation in mean interaction intensity and in the functional significance of traits will be necessary to understand spatio-temporal variation in selection exerted by the biotic environment. This article is protected by copyright. All rights reserved.
Seed production in natural populations is often limited by quantity of pollen received. This pollen limitation has the potential to generate natural selection through female function favouring certain floral traits (hereafter ‘pollen‐mediated’ selection). Floral traits can, however, also be under selection via other mechanisms, and the influence of a particular trait on pollen limitation of individuals is rarely quantified.
We took a trait‐based approach to pollen limitation by adding a quantitative trait to a previously published model. The modified model predicted impacts of both pollen supplementation and pollen reduction in seed production when the trait influences pollen receipt, and when the trait influences other model parameters. We then manipulated pollen availability in a population of the alpine New Zealand herb Wahlenbergia albomarginata varying in petal colour to test a long‐standing hypothesis that pale flower colour in that habitat is selected for via pollinators.
Under pollen‐mediated selection, supplementing pollination should eliminate fitness dependence on a trait, while reducing pollination could exacerbate it. In contrast, if selection through female function on a floral trait is not solely pollen‐mediated, seed production should change with the trait value even when excess pollen is added. Furthermore, if the effect is on maximum seed production, the trait effect should increase with higher pollen availability as greater resources can be used for filling seeds from more fertilised ovules.
In Wahlenbergia albomarginata , average seed production was strongly pollen‐limited, with supplemental pollen increasing seeds by 43%. Selection through female function also favoured whiter flowers as quantified with reflectance spectrometry. This selection on flower colour was stronger when supplemental pollen was added, consistent with an effect of the trait on asymptotic seed production rather than an effect on pollen receipt.
These results, along with previous behavioural studies of pollinators, show that pale flower colour, common in the habitat and often attributed to pollinator behaviour, is not maintained by pollen‐mediated selection but instead through another mechanism. This study illustrates the value of combining experimental pollen supplements and reductions with trait variation to study selection of floral traits, especially in species where compatible pollen receipt is difficult to measure.
Colour patterns on flowers can increase pollinator visitation and enhance foraging behaviour. Flowers uniform in colour to humans, however, can appear patterned to insects due to spatial variation in UV reflectance on petals. A UV ‘bullseye’ pattern that is common among angiosperms – UV ‐absorbing petal bases and UV‐reflective apices – purportedly functions as a nectar guide, enhancing pollinator orientation and experimental evidence suggests that UV reflectance increases floral apparency to pollinators.
We test the pollinator‐attracting and pollinator‐orienting functions of floral UV pattern and UV reflectance under natural conditions. Specifically, we address whether UV reflection alone, or UV pattern influences small bee and syrphid fly attraction rates (approaching, landing and foraging visits), foraging rates, and likelihood of foraging and orienting to the centre of flowers, using A rgentina anserina , a species whose flowers exhibit variability in the size of the UV bullseye. We manipulated UV properties while maintaining uniformly yellow petals to create three phenotypes – uniformly UV ‐absorptive, uniformly UV ‐reflective, and inversed bullseye (reflective bases and absorptive apices) and compared insect visitation and behaviour to control flowers with the common UV bullseye phenotype.
The presence of UV pattern increased attraction rates by both bees and syrphid flies relative to either fully UV reflective or absorptive flowers. However, only in the inverse array did the bullseye phenotype elicit higher foraging rates than the test flower. Neither the presence of pattern, nor the reversal of the common pattern influenced the likelihood of pollinator foraging or orientating to the flowers' centre during a visit.
We provide some of the first evidence to suggest that flowers with spatial variation in UV reflectance may be more conspicuous to insects than those with petals that uniformly absorb or reflect UV , all of which are naturally occurring phenotypes. Further, we verify that the most common UV pattern in nature increases insect attraction and foraging rate relative to the inverse pattern. Results confirm a distance apparency function of the UV bullseye, but we argue for reconsideration of the notion that pollinators benefit from this ubiquitous floral motif through enhanced foraging efficiency.
Even though the importance of selection for trait evolution is well established, we still lack a functional understanding of the mechanisms underlying phenotypic selection. Because animals necessarily use their sensory system to perceive phenotypic traits, the model of sensory bias assumes that sensory systems are the main determinant of signal evolution. Yet, it has remained poorly known how sensory systems contribute to shaping the fitness surface of selected individuals. In a greenhouse experiment, we quantified the strength and direction of selection on floral coloration in a population of cornflowers exposed to bumblebees as unique pollinators during 4 days. We detected significant selection on the chromatic and achromatic (brightness) components of floral coloration. We then studied whether these patterns of selection are explicable by accounting for the visual system of the pollinators. Using data on bumblebee colour vision, we first showed that bumblebees should discriminate among quantitative colour variants. The observed selection was then compared to the selection predicted by psychophysical models of bumblebee colour vision. The achromatic but not the chromatic channel of the bumblebee's visual system could explain the observed pattern of selection. These results highlight that (i) pollinators can select quantitative variation in floral coloration and could thus account for a gradual evolution of flower coloration, and (ii) stimulation of the visual system represents, at least partly, a functional mechanism potentially explaining pollinators' selection on floral colour variants.
1) The effect which the honey-guides of flowers have upon visiting bees is investigated with the use of large model flowers. 2) It is found that bumble-bees have a strong tendency to react to the edge of plain shapes, where there is a line of colour contrast with the background. If a contrasting honey-guide pattern is added, the bees still fly initially to the edge, but subsequently react often to the contrast margins formed by the pattern. On real flowers the honey-guide is arranged around the entrance to the nectaries and thus could direct the bees' reactions there. 3) The total patterns formed by honey-guides have no significance for bumble-bees. They follow converging lines to the flower's centre only because they always arrive first at the outer edge. 4) Bumble-bees do not distinguish between plain and honey-guided models when choosing from a distance, but having flown to a model, they hover longer over the latter. 5) Various observations on bees visiting real flowers are described and the validity of arguing from models to real flowers is discussed. It is believed that honey-guides will have qualitatively the same effect on both. 6) Some aspects of the effects of the honey-guides and the scent of flowers are discussed.
Flowers of the herbaceous perennial wildflower Delphinium nelsonii are normally deep blue. In Colorado populations we have studied, however, about 0.1% of all plants are "albinos" with pale or white flowers. This low frequency suggests an equilibrium between production of albinos through spontaneous mutation and selection against them. Indeed, selection against albinos in nature occurs in the form of consistent reductions in seed set relative to blue-flowered controls. Using field experiments with natural populations and artificial populations of potted plants, we have determined that seed set reductions correspond not to low intrinsic fecundity of albinos but rather to fixed discrimination against them by hummingbird and bumblebee pollinators. We discuss several possible reasons for discrimination, and conclude that pollinators may undervisit albino flowers because their nectar rewards are more time-consuming to extract than those of blue flowers.
Geitonogamy (transfer of pollen among flowers on the same plant) may lead to reduced outcrossing and interfere with sex function. Orchids with pollen packaged into pollinaria would be expected to be particularly vulnerable to the loss of cross-mating opportunities imposed by geitonogamy. We tested the hypothesis that the absence of floral rewards in many orchid species is a means of reducing geitonogamy. Experiments with the deceptive species Orchis mascula and Orchis morio showed that queen bumble bees probe more flowers and stay longer on plants when artificial nectar is added to the hewers. Overall, the data indicated that the evolution of nectar production in deceptive Orchis species would result in moderate to high levels of geitonogamy, as a consequence of the greater number of flowers probed and longer visit duration (similar to 60 s) by pollinators. However, the estimated levels of geitonogamy were less than expected, due both to a time delay before freshly withdrawn pollinaria bend into the correct position to strike a stigma and to extensive carryover of pollen. The time elapsed before a freshly withdrawn pollinarium is in the correct position to strike the stigma was found to vary 30-80 a, depending on the orchid species. Since pollinators usually spend <30 s on an inflorescence, we estimate that natural populations of the study species are highly outcrossed. The fraction of the pollen load carried over from flower to flower was found to be 0.67 in O. mascula. Selection should favor longer delays in pollinaria bending and extensive pollen carryover in nectar-producing orchids. This is corroborated by the nectariferous orchid Platanthera chlorantha, which we found to have a pollinaria bending delay of 80 s and a high pollen carryover fraction (0.87). In general, selection for traits that prevent geitonogamy should occur only when pollinators are abundant. Since fruit set of orchids is usually pollinator limited, additional explanations may have to be sought to explain deception. The most plausible complementary hypothesis is that resources in pollinator-limited orchids are invested in advertising display, rather than nectar production.
1. The functional significance of floral traits in Linum pubescens (Linaceae), a Mediterranean annual that is pollinated almost exclusively by the bee‐fly Usia bicolor (Bombyliidae), was investigated. The flies feed on both pollen and nectar, and use the flowers as mating rendezvous sites in the afternoon.
2. Choice experiments with model flowers were used to determine the response of U. bicolor to visual cues, such as shape, size, colour and pattern.
3. Bee‐flies strongly preferred models with a dissected outline over models with a simple outline. They also preferred pink models over other colours, and larger models over smaller models.
5. Flies landing on models with converging lines (‘nectar guides’) tended to follow the lines to the point where they meet in the centre of the model, while flies landing on plain models showed undirected behaviour, often moving to the edge of the model.
6. Flies were strongly attracted to flowers of L. pubescens which had a fly glued on to one of the petals, as well as flowers with a dark spot painted onto one of the petals. In addition, models with a dark spot were strongly preferred over plain models during the afternoon when flies exhibit mating behaviour. This evidence suggests that the dark centre of the L. pubescens flower may function as an attractant to mate‐seeking bee‐flies.
It has been debated whether pollination success in nonrewarding plants that flower in association with nectar-producing plants will be diminished by competition for pollinator visits or, alternatively, enhanced through increased local abundance of pollinators (the magnet species effect). We experimentally evaluated these effects using the nonre-warding bumblebee-pollinated orchid Anacamptis morio and associated nectar-producing plants at a site in Sweden. Pollination success (estimated as pollen receipt and pollen removal) in A. morio was significantly greater for individuals translocated to patches of nectar-producing plants (Geum rivale and Allium schoenoprasum) than for individuals placed outside (20 m away) such patches. These results provide support for the existence of a facilitative magnet species effect in the interaction between certain nectar plants and A. morio. To determine the spatial scale of these interactions, we correlated the visitation rate to flowers of A. morio with the density of sympatric nectar plants in 1-m 2 and 100-m 2 plots centered around groups of translocated plants, and at the level of whole meadows (0.5–2 ha). Visitation rate to flowers of A. morio was not correlated with the 1-m 2 patch density of G. rivale and A. schoenoprasum, but showed a significant positive relationship with density of these nectar plants in 100-m 2 plots. In addition, visitation to flowers of A. morio was strongly and positively related to the density of A. schoenoprasum at the level of the meadow. Choice experiments showed that bees foraging on the purple flowers of A. schoenoprasum (a particularly effective magnet species) visit the purple flowers of A. morio more readily (47.6% of choices) than bees foraging on the yellow flowers of Lotus cor-niculatus (17% of choices). Overall similarity in flower color and shape may increase the probability that a pollinator will temporarily shift from a nectar-producing ''magnet'' plant to a nonrewarding plant. We discuss the possibility of a mimicry continuum between those orchids that exploit instinctive food-seeking behavior of pollinators and those that show an adaptive resemblance to nectar-producing plants.
The tremendous diversity in flower color among angiosperms implies that there have been numerous evo-lutionary transitions in this character. The conventional wisdom is that a large proportion of these transitions reflect adaptation to novel pollinator regimes. By contrast, recent research suggests that many of these tran-sitions may instead have been driven by selection imposed by nonpollinator agents of selection acting on pleio-tropic effects of flower color genes. I evaluate the evidence for these alternative hypotheses and find that while there is circumstantial evidence consistent with each hypothesis, there are no definitive examples of flower color evolution conforming to either hypothesis. I also document four macroevolutionary trends in flower color evolution: color transitions rates are often asymmetrical; biases favoring loss of pigmentation or favoring gain of pigmentation are both observed, but bias favoring transition from blue to red flowers seems more common than the reverse bias; transitions from blue to red often involve inactivation of branches of the anthocyanin pathway; and color transitions often involve loss-of-function mutations. Finally, I discuss how these trends may be related to one another.
Outcrossing in plants is influenced by the availability of pollinators and compatible mates, both of which may be modified by the population and community context in which plant–pollinator interactions occur. Although indirect interactions among plants through shared pollinators are often expected to be competitive, pollinator sharing may be beneficial when plant species jointly attract or maintain populations of pollinators. In this study, I tested the hypothesis that pollinator-sharing congeners facilitate reproduction in a focal taxon, Clarkia xantiana ssp. xantiana, and that positive interactions are most pro-nounced in small and sparse populations. Population surveys revealed that C. x. xantiana frequently coexists with pollinator-sharing congeners except at the periphery of its range. Populations varied extensively in size and density, with small populations more likely associated with pollinator-sharing congeners; conversely, populations occurring alone were more likely large. Flowering schedules in Clarkia communities ranged from segregated to aggregated. Although there was not strong evidence of character displacement, modes in flowering time were often staggered among Clarkia species resulting in a protracted flow-ering season within plant communities. Studies of bee pollinator availability in 17 popu-lations and pollen limitation to reproduction in 39 replicate populations revealed that pop-ulations occurring with multiple congeners had high pollinator availability and low pollen limitation of reproduction compared to populations occurring alone. Population size was inversely related to pollen limitation but did not affect pollinator availability, suggesting that Allee effects were caused by mate limitation. Intraspecific interactions were also pos-itive at a fine spatial scale where pollen deposition increased with the density of closely neighboring conspecifics across 11 populations. Overall, inter-and intraspecific interactions through shared pollinators were generally facilitative, suggesting that population viability and the coexistence of ecologically similar Clarkia species may be promoted by positive reproductive interactions.
of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. Conflicting selection by pollinators and herbivores is thought to be an important mechanism maintaining variation in flower color within plant populations. However, evidence for this mechanism is lacking because selection and the agents of selection on flower color have rarely been estimated. We estimated selection by pollinators and a predispersal seed predator on the three fundamental components of color (brightness, chroma, and hue) of Lobelia siphilitica flowers. We compared phenotypic selection on flowers of supplemental hand-versus open-pollinated plants to infer whether pollinators were an agent of selection on color. We compared attacked and unattacked plants to infer whether the seed predator was an agent of selection on color. Selection on brightness, but not chroma or hue, differed significantly between both pollination treatments and predation categories. Both pollinators and the seed predator exerted selection for less bright flowers, suggesting that they do not cause conflicting selection on flower color. However, we also detected phenotypic selection for brighter flowers that was not caused by pollinators or by the seed predator. Consequently, pollinators and herbivores are not sufficient to generate conflicting selection that could contribute to the maintenance of flower color variation in L. siphilitica.
—Linanthus parryae, a diminutive desert annual with white or blue flowers, has been the focus of a longstanding debate among evolutionary biologists. At issue is whether the flower color polymorphism in this species is the product of random genetic drift, as Sewall Wright argued, or of natural selection, as proposed by Carl Epling and his colleagues. Our long-term studies of three polymorphic populations in the Mojave Desert demonstrate that flower color is subject to selection that varies in both time and space in its direction and magnitude. For all sites taken together, blue-flowered plants produced more seeds than white-flowered plants in years of relatively low seed production, whereas white-flowered plants had higher fitness in years of high seed production. Evidence of selection on flower color was found in two of the three study sites. Differences in fitness between the color morphs were sometimes large, with selection coefficients as high as 0.60 in some years. Our longest period of observations was at Pearblossom site 1, where plants reached appreciable densities in seven of the 11 years of study. Here we found significant differences in the seed production of the color morphs in six years, with three years of blue advantage and three years of white advantage. For all sites taken together, total spring precipitation (March and April) was positively correlated with both absolute and relative seed production of the color morphs. At Pearblossom site 1, blue-flowered plants typically had a fitness advantage in years of low spring precipitation, whereas white-flowered plants had a fitness advantage in years of high spring precipitation. This temporal variation in selection may contribute to the maintenance of the flower-color polymorphism at Pearblossom site 1, whereas gene flow from neighboring populations is proposed as the principal factor maintaining the polymorphism at the other study sites. We found no significant differences between the color morphs in pollinator visitation rate or in their carbon isotope ratio, a measure of water-use efficiency. Although the mechanism of selection remains elusive, our results refute Wright's conclusion that the flower color polymorphism in L. parryae is an example of isolation by distance, a key component of his shifting balance theory of evolution.
The flowers of European orchids contain cyanidin 3-monoglucoside, cyanidin 3-diglucoside and cyanidin 3,5-diglucoside. 2 complex anthocyanins, composed of cyanin and a 2nd organic compound were isolated from the flowers ofOrchis, Dactylorhiza andGymnadenia.
Reinforcement is the process by which reduced hybrid fitness generates selection favoring the evolution of stronger prezygotic
reproductive barriers between emerging species. Using common-garden field experiments, we quantified the strength of reinforcing
selection in nature by demonstrating strong selection favoring an allele conferring increased pigment intensity in the plant
Phlox drummondii in areas of sympatry with the closely related species Phlox cuspidata. Incomplete hybrid sterility between the two species generates selection for traits that decrease interspecies hybridization.
In contrast, selection on this locus is undetectable in the absence of P. cuspidata. We demonstrate that reinforcing selection is generated by nonrandom pollinator movement, in which pollinators move less
frequently between intensely pigmented P. drummondii and P. cuspidata than between lightly pigmented P. drummondii and P. cuspidata.
Segmentation is a very important pre-processing step towards image analysis or image compression. In this paper, we propose an original region segmentation method applied to color images. The two key elements of this method are:1. the use of a color space where hue is explicitly defined and processed according to its relevance which can be linked to chroma,2. the use of symbolic representations and rule-base systems combining color and luminance features in order to define homogeneity between pixels.As an illustration, this approach is applied to an iterative region growing method classically used in grey level image processing. Experimental results on real images are given.
Pollinators are expected to respond to low reward availability in an inflorescence by visiting fewer flowers before departure, thus potentially causing reduced visitation, but also reduced geitonogamous selfing. I tested this hypothesis using Anacamptis morio, an orchid that does not reward its pollinators. Supplementation of inflorescences with artificial nectar did not result in an increase in fruit set on supplemented inflorescences compared to control inflorescences and tended to reduce pollinia removal. Supplementation resulted in reduced fruit quality, but there was no evidence that this was as a result of inbreeding depression. Behavioral experiments showed that pollinating bumble bees, as predicted, visited more flowers on supplemented inflorescences. Bumble bees also deposited more self-pollen on supplemented inflorescences, but this was marginally significant. Bumble bee queens removed significantly more pollinia from control inflorescences, while Bombus terrestris and B. lucorum workers did not. I conclude that while pollinators behaved as predicted, there was weak evidence that pollinia removal, pollen deposition, and fruit set followed the predictions of the hypothesis. I argue that this was probably because some pollinators were more efficient at removing and depositing pollen on control inflorescences, while others were not.
Species formation generates biological diversity and occurs when traits evolve that prevent gene flow between populations. Discerning the number and distribution of genes underlying these traits and, in a few cases, identifying the genes involved, has greatly enhanced our understanding over the past 15 years of species formation (reviewed by Noor and Feder and Wolf et al.). However, this work has almost exclusively focused on traits that restrict gene flow between populations that have evolved as a by-product of genetic divergence between geographically isolated populations. By contrast, little is known about the characteristics of genes associated with reinforcement, the process by which natural selection directly favours restricted gene flow during the formation of species. Here we identify changes in two genes that appear to cause a flower colour change in Phlox drummondii, which previous work has shown contributes to reinforcement. Both changes involve cis-regulatory mutations to genes in the anthocyanin biosynthetic pathway (ABP). Because one change is recessive whereas the other is dominant, hybrid offspring produce an intermediate flower colour that is visited less by pollinators, and is presumably maladaptive. Thus genetic change selected to increase prezygotic isolation also appears to result in increased postzygotic isolation.
• A major gap in our understanding of floral evolution, especially micro-evolutionary processes, is the role of pollinators in generating patterns of natural selection on floral traits. Here we explicitly tested the role of pollinators in selecting floral traits in a herbaceous perennial, Penstemon digitalis. • We manipulated the effect of pollinators on fitness through hand pollinations and compared phenotypic selection in open- and hand-pollinated plants. • Despite the lack of pollen limitation in our population, pollinators mediated selection on floral size and floral display. Hand pollinations removed directional selection for larger flowers and stabilizing selection on flower number, suggesting that pollinators were the agents of selection on both of these traits. • We reviewed studies that measured natural selection on floral traits by biotic agents and generally found stronger signatures of selection imposed by pollinators than by herbivores and co-flowering plant species.
Flower-colour polymorphism within the British flora appears more common in species whose flowers typically contain pink, purple or blue anthocyanin pigments rather than other coloured pigments. In this study we test the hypothesis that this variation in anthocyanin pigmentation may be maintained by selection related to environmental heterogeneity and stress tolerance. Observations were made of stem pigmentation, shoot dry mass and seed production in five polymorphic species under different droughted and well watered conditions. The results show that over both treatments the morphs did not differ in their fitness. However, a significant morph times treatment interaction revealed that the pigmented plants performed relatively better in the droughted conditions, while the unpigmented plants performed relatively better in the well watered treatment. The results support the idea that anthocyanin based flower-colour polymorphisms may be better considered as polymorphism for the presence or absence of anthocyanin pigmentation throughout the entire plant. This variation may be maintained by selection related to environmental heterogeneity and stress tolerance. EU