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Emission Rates of Species-Specific Volatiles Vary across Communities of Clarkia Species: Evidence for Multimodal Character Displacement
Abstract
AbstractA current frontier of character displacement research is to determine whether displacement occurs via multiple phenotypic pathways and varies across communities with different species compositions. Here, we conducted the first test for context-dependent character displacement in multimodal floral signals by analyzing variation in floral scent in a system that exhibits character displacement in flower size and that has multiple types of sympatric communities. In a greenhouse common garden experiment, we measured quantitative variation in volatile emission rates of the progeny of two species of Clarkia from replicated parental communities that contain one, two, or four Clarkia species. The first two axes of a constrained correspondence analysis, which explained 24% of the total variation in floral scent, separated the species and community types. Of the 23 compounds that were significantly correlated with these axes, nine showed patterns consistent with character displacement. Two compounds produced primarily by C. unguiculata and two compounds produced primarily by C. cylindrica were emitted in higher amounts in sympatry. Character displacement in some volatiles varied across sympatric parental communities and occurred in parallel with displacement in flower size, demonstrating that this evolutionary process can be context dependent and may occur through multiple pathways.
... To address whether scent composition varied among the different taxa and across elevation, we used canonical analysis of principal coordinates (CAP, Anderson and Willis 2003;Powers et al. 2020;Eisen et al. 2022) with the R package "vegan" (Oksanen et al. 2013). CAP is a constrained ordination that is suitable to examine multivariate patterns among predefined categorical (plant taxa) and continuous variables (elevation). ...
... Following CAP, we used a permutation method to test each model term (plant taxa, elevation and their interaction) sequentially with "vegan" (Oksanen et al. 2013). To determine differences of particular compounds among taxa and elevation, we performed univariate tests on the compounds that showed a strong significant correlation, |r|≥ 0.50, with the first, second or both first CAP axes after applying a false discovery rate correction for conducting 32 tests (see Eisen et al. 2022 for similar approach). ...
Divergence in floral traits attractive to different pollinators can promote reproductive isolation in related species. When isolation is incomplete, hybridization may occur, which offers the opportunity to explore mechanisms underlying reproductive isolation. Recent work suggests that divergence in floral scent may frequently contribute to reproductive barriers, although such divergence has seldom been examined in species with generalized pollination. Here, we used two closely related Penstemon species, P. newberryi and P. davidsonii, and their natural hybrids from an elevational gradient with pollinator communities that are predicted to vary in their reliance on floral scent (i.e., primarily hummingbirds at low elevation vs. bees at high elevation). The species vary in a suite of floral traits, but scent is uncharacterized. To address whether scent varies along elevation and potentially contributes to reproductive isolation, we genetically characterized individuals collected at field and identified whether they were parental species or hybrids. We then characterized scent amount and composition. Although the parental species had similar total emissions, some scent characteristics (i.e., scent composition, aromatic emission) diverged between them and may contribute to their isolation. However, the species emitted similar compound sets which could explain hybridization in the contact area. Hybrids were similar to the parents for most scent traits, suggesting that their floral scent would not provide a strong barrier to backcrossing. Our study suggests floral scent may be a trait contributing to species boundaries even in plants with generalized pollination, and reinforces the idea that evolutionary pollinator transitions may involve changes in multiple floral traits.
... Despite their wellestablished role in attracting pollinating insects, olfactory signals remain less well-studied than visual signals (Raguso, 2008), presumably owing to their typically more complex nature. However, recent literature presents a growing number of studies that documented patterns of within and between population variation in floral scents (e.g. de Manincor et al., 2022;Eisen, Geber, et al., 2022;Friberg et al., 2019;Gfrerer et al., 2021, also reviewed in Delle-Vedove et al., 2017, as well as some studies that investigated phenotypic selection on olfactory signals (e.g. Chapurlat et al., 2019;Gfrerer et al., 2021;Gross et al., 2016;Majetic et al., 2009a;Parachnowitsch et al., 2012) and experimental evolution studies exploring the adaptative dynamics of these particular traits (Gervasi & Schiestl, 2017;Ramos & Schiestl, 2020). ...
Although attractive scents play a crucial role in reproduction in insect‐pollinated plants, the degree of variation of this signal within and among populations remains understudied. Depending on the specifics of the reproductive system of the plant under scrutiny, it is possible to formulate predictions regarding this variation. In plants with separate sexes (dioecious species) and with highly specific pollination, one would predict (i) males to emit more scent than females, owing to sexual selection, (ii) scent bouquets to have a strictly similar composition between sexes, to guarantee efficient pollen transfer and (iii) variation of scent bouquet among populations that should mirror neutral genetic divergence.
These hypotheses were tested in the European fan palm, Chamaerops humilis, by collecting scent in eight populations from three regions, Spain, Sardinia and Sicily, quantifying densities of pollinators—Derelomus sp. and Meligethinus pallidulus—and genotyping the plants on a set of neutral markers.
Males emitted more scent than females. We detected some differences in bouquet composition between sexes, showing an imperfect inter‐sex mimicry in some populations. We also found a strong geographical effect, with individuals sampled in Sicily emitting a strikingly different scent bouquet, which contained high proportions of a volatile compound that was never detected in the other two regions.
Geographical variation of scent composition did not mirror neutral genetic structure: Sardinian and Spanish populations emitted similar scent bouquets but displayed very high levels of genetic differentiation. On the reverse, Sicilian populations showed both strong scent differences and appeared clearly genetically differentiated from populations found elsewhere, without any depletion in neutral genetic diversity.
Synthesis: Our study confirmed higher scent emission rates in males compared to females, consistent with expectations of sexual selection. However, we also discovered significant variation in the composition of the floral bouquet, which was unexpected given the highly specific pollination context. Together with observations of spatial genetic structure, these findings suggest a shift in plant‐pollinator interactions within the species across different regions.
... Floral volatiles are heritable and have the capacity to evolve rapidly in response to pollinators at the intraspecific level, with both selection experiments detecting substantial changes within just a few generations (Gervasi & Schiestl, 2017;Opedal et al., 2022;Ramos & Schiestl, 2020;Zu et al., 2016) and the observation of strong contemporary selection relative to other floral traits (Parachnowitsch et al., 2012). At broader scales, the observations of high olfactory signal disparity among sympatric species, both at macroevolutionary and community levels, further demonstrate the capacity of natural selection to act upon these traits to maintain species boundaries (Eisen et al., 2022;Friberg et al., 2019;Weber et al., 2018). ...
Floral volatiles play key roles as signaling agents that mediate interactions between plants and animals. Despite their importance, few studies have investigated broad patterns of volatile variation across groups of plants that share pollinators, particularly in a phylogenetic context. The “perfume flowers”, Neotropical plant species exhibiting exclusive pollination by male euglossine bees in search of chemical rewards, present an intriguing system to investigate these patterns due to the unique function of their chemical phenotypes as both signaling agents and rewards. We leverage recently-developed phylogenies and knowledge of biosynthesis along with decades of chemical ecology research to characterize axes of variation in the chemistry of perfume flowers, as well as understand their evolution at finer taxonomic scales. We detect pervasive chemical convergence, with many species across families exhibiting similar volatile phenotypes. Scent profiles of most species are dominated by compounds of either the phenylpropanoid or terpenoid biosynthesis pathways, while terpenoid compounds drive more subtle axes of variation. We find recapitulation of these patterns within two independent radiations of perfume flower orchids, in which we further detect evidence for rapid evolution of divergent floral chemistries, consistent with the putative importance of scent in the process of adaptation and speciation.
... VOCs have been found to not be particularly plastic in some systems (Friberg et al., 2017;Luizzi et al., 2021), phenotypic plasticity appears to play a major role in others (de Manincor et al., 2022). However, be- (Bakhtiari et al., 2021;Defossez et al., 2021;Eisen et al., 2022;Pearse & Hipp, 2012), while instead we mostly observe patterns of chemical divergence among sites (Becerra et al., 2009;Kursar et al., 2009;Salazar et al., 2018). ...
The diversity of specialized molecules produced by plants radiating along ecological gradients is thought to arise from plants' adaptations to local conditions. Therefore, closely related species growing in similar habitats should phylogenetically converge, or diverge, in response to similar climates, or similar interacting animal communities. We here asked whether closely related species in the genus Haplopappus (Asteraceae) growing within the same elevation bands in the Andes, converged to produce similar floral odors. To do so, we combine untargeted analysis of floral volatile organic compounds with insect olfactory bioassay in congeneric Haplopappus (Asteraceae) species growing within the same elevation bands along the Andean elevational gradient. We then asked whether the outcome of biotic interactions (i.e., pollination vs. seed predation) would also converge across species within the same elevation. We found that flower odors grouped according to their elevational band and that the main floral visitor preferred floral heads from low-elevation band species. Furthermore, the cost-benefit ratio of predated versus fertilized seeds was consistent within elevation bands, but increased with elevation, from 6:1 at low to 8:1 at high elevations. In the light of our findings, we propose that climate and insect community changes along elevation molded a common floral odor blend, best adapted for the local conditions. Moreover, we suggest that at low elevation where floral resources are abundant, the per capita cost of attracting seed predators is diluted, while at high elevation, sparse plants incur a higher herbivory cost per capita. Together, our results suggest that phytochemical convergence may be an important factor driving plant-insect interactions and their ecological outcomes along ecological gradients.
... Second, we measured scent at the level of the inflorescence, which meant that we were not able to relate variation in scent to variation in nectar at the flower level. Quantitative variation in scent (compound emission rates) is commonly measured at the inflorescence level, as sampling from multiple open flowers may be either essential to detecting signal in weakly scented species Eisen et al., 2021) or it may be unavoidable if flowers are tightly clustered on inflorescences (Becklin et al., 2011;Gross et al., 2016). For both reasons, single flower dynamic headspace sampling is not feasible for A. alpina, but static headspace sampling of single cut flowers could be informative. ...
In flowering plants that produce concealed rewards, pollinator foraging preferences may select for floral advertisement traits that are correlated with rewards. To date, studies have not focused on the potential for honest signals to vary across populations, which could occur due to differences in pollinator communities or plant mating system.
We tested for variation in honest signals across and within populations and mating systems in Arabis alpina, a broadly distributed arctic‐alpine perennial herb that is visited by a variable community of insects. In a greenhouse common garden, we tested for correlations between corolla area, floral scent and nectar volume in 29 populations. In 12 field populations, we examined variation in pollen limitation and corolla area.
Across and within populations and mating systems, larger flowers generally produced more nectar. Total scent emission was not correlated with nectar production, but two compounds—phenylacetaldehyde and benzyl alcohol—may be honest signals in some populations. Corolla area was correlated with pollen limitation only across populations.
Our results suggest that honest signals may be similar across populations but may not result from contemporary direct selection on floral advertisements.
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... The researcher should optimize methods for their system and question, both to enhance the sensitivity and consistency of data analysis and to minimize costs, especially when high replication is needed. Method optimization may involve tradeoffs between slower GC runs needed to resolve all peaks to baseline (Adams, 2001) and faster runs promoting more data replication per unit of analytical time (Eisen et al., 2022). Truncated GC programs that accelerate oven temperature ramps during intervals when few peaks are eluting can shave run times and costs (Doubleday et al., 2013). ...
Research on floral volatiles has grown substantially in the last 20 years, which has generated insights into their diversity and prevalence. These studies have paved the way for new research that explores the evolutionary origins and ecological consequences of different types of variation in floral scent, including community-level, functional, and environmentally induced variation. However, to address these types of questions, novel approaches are needed that can handle large sample sizes, provide quality control measures, and make volatile research more transparent and accessible, particularly for scientists without prior experience in this field. Drawing upon a literature review and our own experiences, we present a set of best practices for next-generation research in floral scent. We outline methods for data collection (experimental designs, methods for conducting field collections, analytical chemistry, compound identification) and data analysis (statistical analysis, database integration) that will facilitate the generation and interpretation of quality data. For the intermediate step of data processing, we created the R package bouquet, which provides a data analysis pipeline. The package contains functions that enable users to convert chromatographic peak integrations to a filtered data table that can be used in subsequent statistical analyses. This package includes default settings for filtering out non-floral compounds, including background contamination, based on our best-practice guidelines, but functions and workflows can be easily customized as necessary. Next-generation research into the ecology and evolution of floral scent has the potential to generate broadly relevant insights into how complex traits evolve, their genomic architecture, and their consequences for ecological interactions. In order to fulfill this potential, the methodology of floral scent studies needs to become more transparent and reproducible. By outlining best practices throughout the lifecycle of a project, from experimental design to statistical analysis, and providing an R package that standardizes the data processing pipeline, we provide a resource for new and seasoned researchers in this field and in adjacent fields, where high-throughput and multi-dimensional datasets are common.
... Second, because different pollinators may detect and prefer distinct floral compounds (Friberg et al. 2014;Gervasi and Schiestl 2017), floral scent differentiation can contribute to pollination niche partitioning within plant communities and ensure reproductive isolation between close relatives (Peakall and Whitehead 2014;Hetherington-Rauth and Ramírez 2016;Kantsa et al. 2019). To our knowledge, only two studies have explored the potential for character displacement in floral scent and have shown that (i) in a clade of California Jewelflowers, sympatric species pairs exhibit more divergent scents than allopatric ones (Weber et al. 2018), and (ii) in Clarkia cylindrica and C. unguiculata, volatiles produced by either one of these two species are emitted in higher amounts in sympatry than in allopatry (Eisen et al. 2021). ...
Pollinator sharing between close relatives can be costly, which can promote pollination niche partitioning and floral divergence. This should be reflected by a higher species divergence in sympatry than in allopatry. We tested this hypothesis in two orchid congeners with overlapping distributions and flowering times. We characterized floral traits and pollination niches and quantified pollen limitation in 15 pure and mixed populations, and we measured phenotypic selection on floral traits and performed controlled crosses in one mixed site. Most floral traits differed between species, yet pollinator sharing was extensive. Only the timing of scent emission diverged more in mixed than in pure sites, and this was not mirrored by the timing of pollinator visitation. We did not detect divergent selection on floral traits. Seed production was pollen limited in most populations, but not more severely in mixed than in pure sites. Interspecific crosses produced the same or a higher proportion of viable seeds than intraspecific ones. The two orchid species attract the same pollinator species despite showing divergent floral traits. Yet, this does not promote character displacement, implying a low cost of pollinator sharing. Our results highlight the importance of characterizing both traits and ecological niches in character displacement studies. This article is protected by copyright. All rights reserved
... In this study, we use observations of plant-pollinator contact in the field and two different molecular and limited number of species make this particular Clarkia system ideal as a case study for testing the use of multiple approaches to understand its pollination ecology (see Section 2.1). In particular, studies of the four Clarkia in their range of sympatry have alternately found signatures of Clarkia reproductive interference (Arceo-Gómez et al., 2016), facilitation of pollination success (Moeller, 2004) and character displacement of floral traits (Eisen & Geber, 2018;Eisen et al., 2021) in response to pollinator sharing, thereby implicating pollen transfer as an important ecological force in the system. However, though observations of the pollinators in this system suggest that bee visitation behaviours can affect such outcomes (Singh, 2014), no study has demonstrated how pollinators actually carry Clarkia pollens. ...
Determining how pollinators visit plants vs. how they carry and transfer pollen is an ongoing project in pollination ecology. The current tools for identifying the pollens that bees carry have different strengths and weaknesses when used for ecological inference. In this study we use three methods to better understand a system of congeneric, coflowering plants in the genus Clarkia and their bee pollinators: observations of plant–pollinator contact in the field, and two different molecular methods to estimate the relative abundance of each Clarkia pollen in samples collected from pollinators. We use these methods to investigate if observations of plant–pollinator contact in the field correspond to the pollen bees carry; if individual bees carry Clarkia pollens in predictable ways, based on previous knowledge of their foraging behaviors; and how the three approaches differ for understanding plant–pollinator interactions. We find that observations of plant–pollinator contact are generally predictive of the pollens that bees carry while foraging, and network topologies using the three different methods are statistically indistinguishable from each other. Results from molecular pollen analysis also show that while bees can carry multiple species of Clarkia at the same time, they often carry one species of pollen. Our work contributes to the growing body of literature aimed at resolving how pollinators use floral resources. We suggest our novel relative amplicon quantification method as another tool in the developing molecular ecology and pollination biology toolbox.
Premise of the study:
Floral scent is a complex trait that mediates many plant-insect interactions, but our understanding of how floral scent variation evolves, either independently or in concert with other traits, remains limited. Assessing variation in floral scent at multiple levels of biological organization and comparing patterns of variation in scent to variation in other floral traits can contribute to our understanding of how scent variation evolves in nature.
Methods:
We used a greenhouse common garden experiment to investigate variation in floral scent at three scales-within plants, among plants, and among populations-and to determine whether scent alone or in combination with morphology and rewards contribute to population differentiation in Oenothera cespitosa subsp. marginata. The range of O. c. marginata spans most of the biomes in the western US, such that variation in both the abiotic and biotic environment could contribute to trait variation.
Key results:
Multiple analytical approaches demonstrated substantial variation both among and within populations in compound-specific and total floral scent measures. Overall, populations were differentiated in morphology and reward traits and in scent. Across populations, coupled patterns of variation in linalool, leucine-derived compounds, and hypanthium length are consistent with a long-tongued moth pollination syndrome.
Conclusions:
The considerable variation in floral scent detected within populations suggests that, similar to other floral traits, variation in floral scent may have a heritable genetic component. Differences in patterns of population differentiation in floral scent and in morphology and rewards indicate that these traits may be shaped by different selective pressures. This article is protected by copyright. All rights reserved.
AbstractA pressing issue is to understand how biological complexity impacts the persistence and adaptation of populations. Natural environments are under unprecedented pressure as a result of climate change and land use change, which makes biological populations and ecological communities vulnerable. Evolution by natural selection-that is, genetic change in response to selection-is one important way species can cope with such changes. Selection often operates on complex traits, and much of selection is due to ecological interactions that, in turn, often form complex networks of species. In this sense, ecological interactions play a dual role: ecological interactions are essential to guarantee the resilience of communities and the functioning of ecosystem services, and they are a source of selection that shapes complex traits. The development of a new integrative framework combining the complexity of selected traits with the complexity of interaction patterns is essential to address potential cascading effects and extinctions. Unfortunately, studies that focus on these two levels of complexity, whether using theoretical or empirical approaches, are still scarce. In this special feature, we bring together articles that contribute to bridging this gap in the study of species coevolution and the evolution of complex traits.
Competition has long been recognized as a central force in shaping evolution, particularly through character displacement. Yet research on character displacement is biased, as it has focused almost exclusively on pairs of interacting species while ignoring multispecies interactions. Communities are seldom so simple that only pairs of species interact, and it is not clear whether inferences from pairwise interactions are sufficient to explain patterns of phenotypes in nature. Here, we test for character displacement in a natural system of freshwater fishes in western Mexico that contains up to four congeneric species of the genus Poeciliopsis. We analyzed body shape differences between populations with different numbers of competitors while accounting for confounding environmental variables. Surprisingly, we found evidence for convergent character displacement in populations of P. prolifica, P. viriosa, and P. latidens. We also found that the convergence in body shape was not consistently in the same direction, meaning that when three or more competitors co-occurred, we did not find more extreme body shapes compared with when there were only two competitors. Instead, when three or more competitors co-occurred, body shape was intermediate between the shape found with a pair of species and the shape found with no competitor present. This intermediate shape suggests that evolution in multispecies communities likely occurs in response to several competitors rather than to simple pairwise interactions. Overall, our results suggest that competition among multiple species is more complex than simple pairwise competitive interactions.
While the importance of floral odours for pollinator attraction relative to visual cues is increasingly appreciated, how they structure community‐level plant–pollinator interactions is poorly understood. Elucidating the functional roles of flowering plant species with respect to their floral volatile organic compounds (VOCs) and how those roles vary over the growing season is an initial step towards understanding the contribution of floral VOCs to plant–pollinator interaction structure.
We sampled the floral VOCs, phenologies and bee visitors of naturally growing plants in a montane meadow in the Northern Rocky Mountains of USA in order to acquire a base understanding of how floral VOCs and other plant traits may structure plant–pollinator interactions across the growing season. We expected forb species with floral VOCs that were original (far from the community mean) and unique (far from the nearest neighbour) would have few pollinating partners (i.e. specialists), while forbs with non‐original or highly variable floral VOCs would form the generalist core of interactors, thereby contributing to network nestedness (specialists interacting with nested subsets of generalists). Network modularity (patterns of distinct, highly connected subnetworks) could be influenced by groups of pollinators that are attracted to or repelled by certain floral bouquets.
Species blooming in early spring emitted similar floral VOC blends containing generalist attractants, whereas floral VOC complexity was highest in mid to late summer. Forb species varied in the originality, uniqueness, and intraspecific variation (i.e. dispersion) of their floral VOCs, indicating the potential for different functional roles in plant–pollinator networks. Specifically, the originality, uniqueness and dispersion of forb species’ floral VOCs increased across the growing season.
Floral VOCs influenced forb interactions with pollinators. Floral VOCs contributed to the nested structure, but not modular structure, of community‐level plant–pollinator network structure. Forb species with more original floral VOCs were less connected, while forb species emitting more compounds and with higher intraspecific variation in floral VOCs were more connected to pollinators.
These findings show that floral scent plays important roles in structuring bee–forb interactions and guiding seasonal patterns in complex communities. Understanding seasonal patterns in floral VOCs may have important implications for plant–pollinator interactions among communities differing in species composition, or as shifts occur in suites of co‐flowering species due to climate change.
A free Plain Language Summary can be found within the Supporting Information of this article.
Chemosensory communication between flowers and pollinators is a fundamental component of terrestrial biodiversity, given the importance of olfaction to foraging animals. In this respect, exploring chemically mediated interspecific interactions in natural assemblies may provide novel insights into the ecofunctional significance of volatile organic compounds (VOCs) for plant–insect co‐evolution. However, multispecies datasets of associations between plant semiochemicals and arthropods are still very rare and tend to lack community context. Here, we present the first insect–floral VOC meta‐network using plant–pollinator visitation data and the plants’ floral scent blends, collected in a Mediterranean scrubland.
We assembled the insect–VOC meta‐network by substituting each plant species in the plant–pollinator network with the blend of VOCs it emits. Furthermore, we identified the modules of the network that is the most densely connected insect–VOC groups. After describing the role of the species in the network, we focused on the bees of the community, and by building phylogenetically informed GLS models, we found the species traits predicting the degree of chemical specialization.
Modularity analysis of the meta‐network revealed tight associations between several classes of VOCs and pollinator groups. Linkage patterns suggest positive associations between (a) Megachilidae bees and sesquiterpenes, (b) Apidae and Andrenidae bees and benzenoids/phenylpropanoids, and (c) wasps, C6 green‐leaf volatiles and specific terpenoids. Benzenoids were found to be the least influential and most specialized chemical class in the community, whereas sesquiterpenes represented the most influential one. Furthermore, the degree of chemical generalization of the bees in the meta‐network was significantly associated with their ecological generalization, body mass and phenology, whereas their contribution to the network's structure was related to their level of sociality.
Synthesis. Our findings help to disclose the ecofunctional significance of the floral volatile landscape and contribute novel testable hypotheses on the behavioural trends and chemical niches of pollinators in a natural community. The insect–volatilome meta‐network is thus shown to be advantageous for detecting and visualizing patterns of chemically mediated interspecific interactions. Given the ubiquity of chemosensory biocommunication, our approach can be applied for investigating various types of ecological interactions in community contexts.
Floral scent is a crucial trait for pollinator attraction. Yet only a handful of studies have estimated selection on scent in natural populations and no study has quantified the relative importance of pollinators and other agents of selection.
In the fragrant orchid Gymnadenia conopsea, we used electroantennographic data to identify floral scent compounds detected by local pollinators and quantified pollinator‐mediated selection on emission rates of 10 target compounds as well as on flowering start, visual display and spur length.
Nocturnal pollinators contributed more to reproductive success than diurnal pollinators, but there was significant pollinator‐mediated selection on both diurnal and nocturnal scent emission. Pollinators selected for increased emission of two compounds and reduced emission of two other compounds, none of which were major constituents of the total bouquet. In three cases, pollinator‐mediated selection was opposed by nonpollinator‐mediated selection, leading to weaker or no detectable net selection.
Our study demonstrates that minor scent compounds can be targets of selection, that pollinators do not necessarily favour stronger scent signalling, and that some scent compounds are subject to conflicting selection from pollinators and other agents of selection. Hence, including floral scent traits into selection analysis is important for understanding the mechanisms behind floral evolution.
Despite long‐standing interest in the evolutionary ecology of plants that share pollinators, few studies have explored how these interactions may affect communities during both community assembly (ecological sorting) and through ongoing, in situ evolution (character displacement), and how the effects of these interactions may change with community context. To determine if communities display patterns consistent with ecological sorting, we assessed the frequency of co‐occurrence of four species of Clarkia in the southern Sierra foothills (Kern County, CA, USA). To investigate potential character displacement, we measured pollination‐related traits on plants grown in a greenhouse common garden from seed collected in communities with one, two, or four Clarkia species. Among the four species of Clarkia in this region, the two species that are often found in multi‐species communities also co‐occur with one another more frequently than expected under a null model. This pattern is consistent with ecological sorting, although further investigation is needed to determine the role of pollinators in shaping community assembly. Patterns of trait variation in a common garden suggest that these two species have diverged in floral traits and converged in flowering time where they co‐occur, which is consistent with character displacement. Trait variation across community types also suggests that the process and outcome of character displacement may vary with community context. Because community context appears to affect both the direction and magnitude of character displacement, change in more species‐rich communities may not be predictable from patterns of change in simpler communities.
This article is protected by copyright. All rights reserved.
Despite progress in understanding pollination network structure, the functional roles of floral sensory stimuli (visual, olfactory) have never been addressed comprehensively in a community context, even though such traits are known to mediate plant-pollinator interactions. Here, we use a comprehensive dataset of floral traits and a novel dynamic data-pooling methodology to explore the impacts of floral sensory diversity on the structure of a pollination network in a Mediterranean scrubland. Our approach tracks transitions in the network behaviour of each plant species throughout its flowering period and, despite dynamism in visitor composition, reveals significant links to floral scent, and/or colour as perceived by pollinators. Having accounted for floral phenology, abundance and phylogeny, the persistent association between floral sensory traits and visitor guilds supports a deeper role for sensory bias and diffuse coevolution in structuring plant-pollinator networks. This knowledge of floral sensory diversity, by identifying the most influential phenotypes, could help prioritize efforts for plant-pollinator community restoration.
Species that coexist in diverse natural communities interact in complex ways that alter each other’s abundances and affect selection on each other’s traits. Consequently, predicting trait evolution in natural communities may require understanding ecological and evolutionary dynamics involving a number of species. In August 2016, the American Society of Naturalists sponsored a symposium to explore evolution in a community context, focusing on microevolutionary processes. Here we provide an introduction to our perspectives on this topic by defining the context and describing some examples of when and how microevolutionary responses to multiple species may differ from evolution in isolation or in two-species communities. We find that indirect ecological and evolutionary effects can result in nonadditive selection and evolution that cannot be predicted from pairwise interactions. Genetic correlations of ecological traits in one species can alter trait evolution and adaptation as well as the abundances of other species. In general, evolution in multispecies communities can change ecological interactions, which then feed back to future evolutionary changes in ways that depend on these indirect effects. We suggest avenues for future research in this field, including determining the circumstances under which pairwise evolution does not adequately describe evolutionary trajectories.
One of the frequent questions by users of the mixed model function lmer of the lme4 package has been: How can I get p values for the F and t tests for objects returned by lmer? The lmerTest package extends the 'lmerMod' class of the lme4 package, by overloading the anova and summary functions by providing p values for tests for fixed effects. We have implemented the Satterthwaite's method for approximating degrees of freedom for the t and F tests. We have also implemented the construction of Type I - III ANOVA tables. Furthermore, one may also obtain the summary as well as the anova table using the Kenward-Roger approximation for denominator degrees of freedom (based on the KRmodcomp function from the pbkrtest package). Some other convenient mixed model analysis tools such as a step method, that performs backward elimination of nonsignificant effects - both random and fixed, calculation of population means and multiple comparison tests together with plot facilities are provided by the package as well.
Geographically structured phenotypic selection can lead to adaptive divergence. However, in flowering plants, such divergent selection has rarely been shown, and selection on floral signals is generally little understood. In this study, we measured phenotypic selection on display size, floral color, and floral scent in four lowland and four mountain populations of the nectar-rewarding terrestrial orchid Gymnadenia odoratissima in two years. We also quantified population differences in these traits and pollinator community composition. Our results show positive selection on display size and positive, negative, or absence of selection on different scent compounds and floral color. Selection on the main scent compounds was consistently stronger in the lowlands than in the mountains, and lowland plants emitted higher amounts of most of these compounds. Pollinator community composition also differed between regions, suggesting different pollinators select for differences in floral volatiles. Overall, our study is the first to document consistent regional differences in selection on floral scent, suggesting this pattern of selection is one of the evolutionary forces contributing to regional divergence in floral chemical signaling.
The evolution of the vast diversity of floral volatiles is little understood, although they serve fundamental functions, such as pollinator attraction and herbivore deterrence. Floral volatiles are often species specific, yet highly variable and sensitive to environmental factors. To date, nothing is known about the heritability of floral volatiles, and whether individual compounds can evolve independently or solely in concert with the whole volatile bouquet.
We conducted bi‐directional artificial selection on four target floral volatiles to estimate heritability and correlated pleiotropic responses in the wild turnip ( Brassica rapa ).
The realized heritability of the four target volatiles ranged from 20% to 45%. The average narrow‐sense heritability of all 13 analyzed floral volatiles was 18% based on parent–offspring regressions. There were pleiotropic effects of the selected floral volatile compounds on other constituents of the floral scent bouquet, on flowering time and on some morphological traits. We found that the whole floral scent bouquet changed, even when there was selection only on single compounds, with the overall phenotypic covariance being unaffected.
Our study demonstrates that floral scent can evolve rapidly under phenotypic selection, but with additional correlated responses in traits that are not direct targets of selection.
Variability in floral volatile emissions can occur temporally through floral development, during diel cycles, as well as spatially within a flower. These spatiotemporal patterns are hypothesized to provide additional information to floral visitors, but they are rarely measured, and their attendant hypotheses are even more rarely tested. In Penstemon digitalis, a plant whose floral scent has been shown to be under strong phenotypic selection for seed fitness, we investigated spatiotemporal variation in floral scent by using dynamic headspace collection, respectively solid-phase microextraction, and analyzed the volatile samples by combined gas chromatography-mass spectrometry. Total volatile emission was greatest during flowering and peak pollinator activity hours, suggesting its importance in mediating ecological interactions. We also detected tissue and reward-specific compounds, consistent with the hypothesis that complexity in floral scent composition reflects several ecological functions. In particular, we found tissue-specific scents for the stigma, stamens, and staminode (a modified sterile stamen common to all Penstemons). Our findings emphasize the dynamic nature of floral scents and highlight a need for greater understanding of ecological and physiological mechanisms driving spatiotemporal patterns in scent production.
Flowers are multisensory displays used by plants to influence the behavior of pollinators. Although we know a great deal about how individual signal components are produced by plants and detected or learned by pollinators, very few experiments directly address the function of floral signal complexity, i.e. how the multicomponent nature of these signals benefits plant or pollinator. Yet, experimental psychology suggests that increasing complexity can enhance subjects' ability to detect, learn and remember stimuli, and the plant's reproductive success depends upon ensuring that pollinators learn their signals and so transport pollen to other similar (conspecific) flowers. Here we explore functional hypotheses for why plants invest in complex floral displays, focusing on hypotheses in which floral signals interact to promote pollinator learning and memory. Specifically, we discuss how an attention-altering or context-providing function of one signal may promote acquisition or recall of a second signal. Although we focus on communication between plants and pollinators, these process-based hypotheses should apply to any situation where a sender benefits from enhancing a receiver's acquisition or recall of information.
The majority of flowering plants rely on animals as pollen vectors. Thus, plant mating systems and pollen dispersal are strongly influenced by pollinator behaviour. In Australian sexually deceptive orchids pollinated by male thynnine wasps, outcrossing and extensive pollen flow is predicted due to floral deception, which minimises multiple flower visitations within patches, and the movement of pollinators under mate search rather than foraging behaviours. This hypothesis was tested using microsatellite markers to reconstruct and infer paternity in two clonal, self-compatible orchids. Offspring from naturally pollinated Chiloglottis valida and C. aff. jeanesii were acquired through symbiotic culture of seeds collected over three seasons. In both species, outcrossing was extensive (tm = 0.924 - 1.00) despite clone sizes up to 11 m wide. The median pollen flow distance based on paternity for both taxa combined was 14.5 m (n=18, range 0 - 69 m), being larger than typically found by paternity analyses in other herbaceous plants. Unexpectedly for orchids, some capsules were sired by more than one father, with an average of 1.35 pollen donors per fruit. This is the first genetic confirmation of polyandry in orchid capsules. Further, we report a possible link between multiple paternity and increased seed fitness. Together, these results demonstrate that deceptive pollination by mate-searching wasps enhances offspring fitness by promoting both outcrossing and within-fruit paternal diversity. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Abstract Classic niche theory predicts that competing species will evolve to use different resources and interact less, whereas recent niche-converge ideas predict that species evolve to use similar resources and interact more. Most data supporting niche evolution are based on observations of contemporary niche use, whereas experimental support is quite sparse. We followed the evolution of four species of Protozoa during succession in the water-filled leaves of the pitcher plant, Sarracenia purpurea, and found that evolution in multispecies systems follows a surprising pattern. Over several hundred generations, weak competitors evolved to be stronger, while strong competitors evolved to become weaker, which does not conform to expectations of either niche divergence or convergence. Evolution in this system appears to occur in response to characteristics of a suite of several competitors in the community, rather than pairwise interactions. Ecologists may need to rethink the roles of competition and evolution in structuring communities.
Maximum likelihood or restricted maximum likelihood (REML) estimates of the
parameters in linear mixed-effects models can be determined using the lmer
function in the lme4 package for R. As for most model-fitting functions in R,
the model is described in an lmer call by a formula, in this case including
both fixed- and random-effects terms. The formula and data together determine a
numerical representation of the model from which the profiled deviance or the
profiled REML criterion can be evaluated as a function of some of the model
parameters. The appropriate criterion is optimized, using one of the
constrained optimization functions in R, to provide the parameter estimates. We
describe the structure of the model, the steps in evaluating the profiled
deviance or REML criterion, and the structure of classes or types that
represents such a model. Sufficient detail is included to allow specialization
of these structures by users who wish to write functions to fit specialized
linear mixed models, such as models incorporating pedigrees or smoothing
splines, that are not easily expressible in the formula language used by lmer.
Variation in traits across species distribution ranges is often indicative of diversifying evolution that can lead to speciation. Of particular interest is whether traits vary clinally or abruptly because the latter pattern can be indicative of incipient speciation. Understanding of intraspecific variation in chemical traits is still in its infancy because studies of population variation have tended to focus on morphology or neutral genetic markers. To address these issues, the composition of cone volatile odours was examined in ten populations of the South African cycad Encephalartos villosus across its range in the Eastern Cape and KwaZulu Natal using headspace sampling and analysis by gas chromatography‐mass spectrometry. Because volatiles play a key role in attracting pollinators to cones of Encephalartos cycads and may thus reflect local adaptation to pollinators, pollinator assemblages were also investigated in the ten populations of E. villosus. Volatile compounds from populations in the north of the distribution range were dominated by unsaturated hydrocarbons, whereas, in the southern populations, nitrogen‐containing compound and terpenoids were the major compounds. A shift between southern and northern populations appeared to occur at the Umtamvuna River, where populations had odour profiles with components of both the northern and southern populations. However, one population in the north (Vernon Crookes Nature Reserve) had a quantitatively similar odour profile to the populations in the extreme south of the range. These results reveal strong interpopulation variation in the cone scent of E. villosus, including variation in the relative emission of dominant compounds that may play key functional role in this pollination system. However, pollinator assemblages did not differ across the different populations, which suggest that these patterns were produced by co‐evolution or drift, rather than by pollinator shifts. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 514–527.
The evidence for character displacement as a widespread response to competition is now building. This progress is largely the result of the establishment of rigorous criteria for demonstrating character displacement in the animal literature. There are, however, relatively few well-supported examples of character displacement in plants. This review explores the potential for character displacement in plants by addressing the following questions: (1) Why aren't examples of character displacement in plants more common? (2) What are the requirements for character displacement to occur and how do plant populations meet those requirements? (3) What are the criteria for testing the pattern and process of character displacement and what methods can and have been used to address these criteria in the plant literature? (4) What are some additional approaches for studying character displacement in plants? While more research is needed, the few plant systems in which character displacement hypotheses have been rigorously tested suggest that character displacement may play a role in shaping plant communities. Plants are especially amenable to character displacement studies because of the experimental ease with which they can be used in common gardens, selection analyses, and breeding designs. A deeper investigation of character displacement in plants is critical for a more complete understanding of the ecological and evolutionary processes that permit the coexistence of plant species.
Background and AimsFloral traits, such as floral volatiles, can contribute to pre-zygotic reproductive isolation by promoting species-specific pollinator foraging. When hybrid zones form, floral traits could also influence post-zygotic isolation. This study examined floral volatiles in parental species and natural hybrids in order to explore potential scent mediation of pre-zygotic and post-zygotic isolation.Methods
Floral bouquets were analysed for the sister species Ipomopsis aggregata and I. tenuituba and their natural hybrids at two contact sites differing in both hybridization rate and temporal foraging pattern of hawkmoth pollinators. Floral volatiles were quantified in diurnal and nocturnal scent samples using gas chromatography-mass spectrometry.Key ResultsThe bouquets of parental species and hybrids showed qualitative overlap. All flowers emitted similar sets of monoterpenoid, sesquiterpenoid, aliphatic and benzenoid compounds, but separated into groups defined by multivariate analysis of quantitative emissions. The parental species differed most strikingly in the nitrogenous compound indole, which was found almost exclusively in nocturnal bouquets of I. tenuituba. Natural hybrid bouquets were highly variable, and showed emission rates of several compounds that appeared transgressive. However, indole emission rates were intermediate in the hybrids compared with rates in the parents. Volatile bouquets at the contact site with lower hybridization did not show greater species specificity in overall scent emission, but I. tenuituba presented a stronger indole signal during peak hawkmoth activity at that site.Conclusions
The two species of Ipomopsis differed in patterns of floral bouquets, with indole emitted in nocturnal I. tenuituba, but not in I. aggregata. Natural hybrid bouquets were not consistently intermediate between the parents, although hybrids were intermediate in indole emission. The indole signal could potentially serve as a hawkmoth attractant that mediates reproductive isolation both before and after hybrid formation.
Plant-pollinator systems may be considered as biological markets in which pollinators choose between different flowers that advertise their nectar/pollen rewards. Although expected to play a major role in structuring plant-pollinator interactions, community-wide patterns of flower scent signals remain largely unexplored. Here we show for the first time that scent advertisement is higher in plant species that bloom early in the flowering period when pollinators are scarce relative to flowers than in species blooming later in the season when there is a surplus of pollinators relative to flowers. We also show that less abundant flowering species that may compete with dominant species for pollinator visitation early in the flowering period emit much higher proportions of the generalist attractant β-ocimene. Overall, we provide a first community-wide description of the key role of seasonal dynamics of plant-specific flower scent emissions, and reveal the coexistence of contrasting plant signaling strategies in a plant-pollinator market.
Many pollinators specialize on a few plants as food sources and rely on flower scents to recognize their hosts. However, the specific compounds mediating this recognition are mostly unknown. We investigated the chemical basis of host location/recognition in the Campanula-specialist bee Chelostoma rapunculi using chemical, electrophysiological, and behavioral approaches. Our findings show that Ca. trachelium flowers emit a weak scent consisting of both widespread and rare (i.e., spiroacetals) volatiles. In electroantennographic analyses, the antennae of bees responded to aliphatics, terpenes, aromatics, and spiroacetals; however, the bioassays revealed a more complex response picture. Spiroacetals attracted host-naive bees, whereas spiroacetals together with aliphatics and terpenes were used for host finding by host-experienced bees. On the intrafloral level, different flower parts of Ca. trachelium showed differences in the absolute and relative amounts of scent, including spiroacetals. Scent from pollen-presenting flower parts elicited more feeding responses in host-naive bees as compared to a scentless control, whereas host-experienced bees responded more to the nectar-presenting parts. Our study demonstrates the occurrence of learning (i.e., change in the bee's innate chemical search-image) after bees gain foraging experience on host flowers. We conclude that highly specific floral volatiles play a key role in host-flower recognition by this pollen-specialist bee, and discuss our findings into the broader context of host-recognition in oligolectic bees.
Background and aims:
Floral diversification driven by shifts between pollinators has been one of the key explanations for the radiation of angiosperms. According to the Grant-Stebbins model of pollinator-driven speciation, these shifts result in morphologically distinct 'ecotypes' which may eventually become recognizable as species. The current circumscription of the food-deceptive southern African orchid Eulophia parviflora encompasses a highly variable monophyletic species complex. In this study, two forms were identified within this complex that differ in distribution, floral morphology, scent chemistry and phenology, and a test was made of whether these differences represent adaptations for different pollinators.
Methods and results:
Multivariate analysis of floral and vegetative traits revealed that there are at least two discrete morphological forms in the species complex. Field observations revealed that each form is pollinated by a different insect species, and thus represent distinct ecotypes. The early-flowering coastal form which has long spurs and floral scent dominated by sesquiterpene compounds is pollinated exclusively by the long-tongued bee Amegilla fallax (Apidae, Anthophorinae), while the late-flowering inland form with short spurs and floral scent dominated by benzenoid compounds is pollinated exclusively by the beetle Cyrtothyrea marginalis (Cetoniinae; Scarabaeidae). Choice experiments in a Y-maze olfactometer showed that beetles are preferentially attracted to the scent of the short-spurred form. A spur-shortening experiment showed that long spurs are required for effective pollination of the bee-pollinated form. Although it was initially thought likely that divergence occurred across a geographical pollinator gradient, plants of the long-spurred form were effectively pollinated when transplanted to an inland locality outside the natural coastal range of this form. Thus, the underlying geographical basis for the evolution of ecotypes in the E. parviflora complex remains uncertain, although early flowering in the long-spurred form to exploit the emergence of naïve bees may restrict this form to coastal areas where there is no frost that would damage flower buds. Later flowering of the short-spurred form coincides closely with the emergence of the pollinating beetles following winter frosts.
Conclusions:
This study identifies a shift between bee and beetle pollination as the main driver of floral divergence in an orchid species complex. Floral scent and spur length appear to be key traits in mediating this evolutionary transition.
Plants cannot avoid being attacked by an almost infinite number of microorganisms and insects. Consequently, they arm themselves with molecular weapons against their attackers. Plant defense responses are the result of a complex signaling network, in which the hormones jasmonic acid (JA), salicylic acid (SA) and ethylene (ET) are the usual suspects under the magnifying glass when researchers investigate host-pest interactions. However, Green Leaf Volatiles (GLVs), C6 molecules, which are very quickly produced and/or emitted upon herbivory or pathogen infection by almost every green plant, also play an important role in plant defenses. GLVs are semiochemicals used by insects to find their food or their conspecifics. They have also been reported to be fundamental in indirect defenses and to have a direct effect on pests, but these are not the only roles of GLVs. These volatiles, being probably one of the fastest weapons exploited, are also able to directly elicit or prime plant defense responses. Moreover, GLVs, via crosstalk with phytohormones, mostly JA, can influence the outcome of the plant’s defense response against pathogens. For all these reasons GLVs should be considered as co-protagonists in the play between plants and their attackers.
In natural biological communities, species interact with many other species. Multiple species interactions can lead to indirect ecological effects that have important fitness consequences and can cause nonadditive patterns of natural selection. Given that indirect ecological effects are common in nature, nonadditive selection may also be quite common. As a result, quantifying nonadditive selection resulting from indirect ecological effects may be critical for understanding adaptation in natural communities composed of many interacting species. We describe how to quantify the relative strength of nonadditive selection resulting from indirect ecological effects compared to the strength of pairwise selection. We develop a clear method for testing for nonadditive selection caused by indirect ecological effects and consider how it might affect adaptation in multispecies communities. We use two case studies to illustrate how our method can be applied to empirical data sets. Our results suggest that nonadditive selection caused by indirect ecological effects may be common in nature. Our hope is that trait-based approaches, combined with multifactorial experiments, will result in more estimates of nonadditive selection that reveal the relative importance of indirect ecological effects for evolution in a community context.
While the evolution and diversification of flowers is often attributed to pollinator‐mediated selection, interactions between co‐occurring plant species can alter patterns of selection mediated by pollinators and other agents. The extent to which both floral density and congeneric species richness affect patterns of net and pollinator‐mediated selection on multiple co‐occurring species in a community is unknown and is likely to depend on whether co‐occurring plants experience competition or facilitation for reproduction. We conducted an observational study of selection on four species of Clarkia (Onagraceae) and tested for pollinator‐mediated selection on two Clarkia species in communities differing in congeneric species richness and local floral density. When selection varied with community context, selection was generally stronger in communities with fewer species, where local conspecific floral density was higher, and where local heterospecific floral density was lower. These patterns suggest that intraspecific competition at high densities and interspecific competition at low densities may affect the evolution of floral traits. However, selection on floral traits was not pollinator‐mediated in C. cylindrica or C. xantiana, despite variation in pollinator visitation and the extent of pollen limitation across communities for C. cylindrica. As such, interactions between co‐occurring species may alter patterns of selection mediated by abiotic agents of selection.
This article is protected by copyright. All rights reserved
Significance
A major challenge in biology is to understand how complex traits important for ecological interactions between species coevolve and diversify across contrasting ecosystems. Floral scents are complex, and are often composed of a diverse array of chemicals important for interactions between plants and pollinators, herbivores, and microbial symbionts. We studied diversification of floral scents among populations of all woodland star species ( Lithophragma ) across far-western North America. Floral scent variation was structured not only phylogenetically among species and geographically among populations, but some of the divergence was driven by local differences in the presence of coevolved Greya moth pollinators. These results highlight the importance of conserving multiple populations of species if we are to maintain the evolutionary potential of coevolving interactions.
Odors of pollen and whole flowers were compared in taxonomically unrelated species that offer pollen as the only food reward to pollinators. Volatiles were collected using headspace adsorption and analyzed by gas chromatography and mass spectrometry. The odor of pollen was found to be chemically distinct from the total flower odor, and this pollen-odor distinctness varied among the three species. In Papaver rhoeas (Papaveraceae), the contrast between pollen and whole-flower odors was most subtle, with differences observed only in the proportions of individual volatiles (almost exclusively aliphatic hydrocarbons). In Filipendula vulgaris (Rosaceae), pollen volatiles were fewer than in the flowers (comprising mainly benzenoids and fatty-acid derivatives) and their relative proportions produced an odor dominated by 2-heptadecanone that contrasted strikingly with the flower odor dominated by 2-phenyl ethanol. In Lupinus polyphyllus (Fabaceae), the pollen odor contained fewer volatiles and in differing proportions than the flower fragrance (comprising almost exclusively isoprenoids). The findings add to earlier chemical evidence of odor contrasts between pollen and other flower parts in two other species. Drawing on information from pollination studies of these various species, it is suggested that pollen odor is used by pollen-foraging insects both to discriminate between plant species and to assess reward availability in individual flowers, and that it might in addition serve a protective function against destructive flower-feeding insects and pathogens.
Background and aims:
Floral scent is considered an integral component of pollination syndromes, and its composition and timing of emission are thus expected to match the main pollinator type and time of activity. While floral scent differences among plant species with different pollination systems can be striking, studies on intraspecific variation are sparse, which limits our understanding of the role of pollinators in driving scent divergence.
Methods:
Here, we used dynamic headspace sampling to quantify floral scent emission and composition during the day and at night in the natural habitat of six Scandinavian populations of the fragrant orchid Gymnadenia conopsea. We tested whether diel scent emission and composition match pollinator type by comparing four populations in southern Sweden, where nocturnal pollinators are more important for plant reproductive success than are diurnal pollinators, with two populations in central Norway, where the opposite is true. To determine to what extent scent patterns quantified in the field reflected plasticity, we also measured scent emission in a common growth chamber environment.
Key results:
Both scent composition and emission rates differed markedly between day and night, but only the latter varied significantly among populations. The increase in scent emission rate at night was considerably stronger in the Swedish populations compared with the Norwegian populations. These patterns persisted when plants were transferred to a common environment, suggesting a genetic underpinning of the scent variation.
Conclusions:
The results are consistent with a scenario where spatial variation in relative importance of nocturnal and diurnal pollinators has resulted in selection for different scent emission rhythms. Our study highlights the importance of adding a characterization of diel variation of scent emission rates to comparative studies of floral scent, which so far have often focused on scent composition only.
Character displacement is one of the most studied phenomena in evolutionary biology, yet research has narrowly focused on demonstrating whether or not displacement has occurred. We propose a new experimental approach, adopted from the coexistence literature, that directly measures interspecific competition among sympatric and allopatric populations of species. Doing so allows increased ability to (i) test predictions of character displacement without biases inherent to character-centric tests, (ii) quantify its effect on the stability of coexistence, (iii) resolve the phenotypic pathways through which competitive divergence is achieved, and (iv) perform comparative tests. Our approach extends research to forms of character displacement not readily identified by past methods and will lead to a broader understanding of its consequences for community structure.
Background and aims:
Many plant-pollinator interactions are mediated by floral scents that can vary among species, among populations within species and even among individuals within populations. This variation could be innate and unaffected by the environment, but, because many floral volatiles have amino-acid precursors, scent variation also could be affected by differences in nutrient availability among environments. In plants that have coevolved with specific pollinators, natural selection is likely to favour low phenotypic plasticity in floral scent even under different conditions of nutrient availability if particular scents or scent combinations are important for attracting local pollinators.
Methods:
Clonal pairs of multiple seed-families of two Lithophragma bolanderi (Saxifragaceae) populations were subjected to a high and a low nutrient treatment. These plants are pollinated primarily by host-specific Greya moths. It was evaluated how nutrient treatment affected variation in floral scent relative to other vegetative and reproductive traits.
Key results:
Floral scent strength (the per-flower emission rate) and composition were unaffected by nutrient treatment, but low-nutrient plants produced fewer and lighter leaves, fewer scapes and fewer flowers than high-nutrient plants. The results held in both populations, which differed greatly in the number and composition of floral scents produced.
Conclusions:
The results reveal a strong genetic component both to scent composition and emission level, and partly contrasts with the only previous study that has assessed the susceptibility of floral volatile signals to variation in the abundance of nutrients. These results, and the tight coevolutionary relationship between Lithophragma plants and their specialized Greya moth pollinators, indicate that reproductive traits important to coevolving interactions, such as the floral scent of L. bolanderi , may be locally specialized and more canalized than other traits important for plant fitness.
Plants of the red- and pink-flowered P. drummondii were introduced into a natural population of P. cuspidata. Their seeds were progeny-tested, and the percentage hybrid seed determined for each variant. Thirty-eight percent of the seed from the pink variant were hybrid compared to 13% of the red. The difference in hybrid production is best explained by corolla color. The self- and cross-compatibility of nine sympatric and nine allopatric populations were studied in the greenhouse. On the average, sympatric populations are more self-compatible than allopatric populations. Pollen germination is 13.7% vs. 7.3%, the difference being statistically significant. The self-compatibility differential was accompanied by a self seedset differential. On the average, sympatric populations are more cross-compatible with P. cuspidata than are allopatric populations. The germination of P. cuspidata pollen on sympatric P. drummondii stigmas was 13.3% vs. 9.8% on allopatric stigmas. However, the difference is not statistically significant. The presence of P. cuspidata has promoted reproductive character divergence in P. drummondii. The shift in corolla color and the increase in self-compatibility reduce the potential for gametic wastage and interspecific hybridization.
Natural communities are well known to be maintained by many complex processes. Despite this, the practical aspects of studying them often require some simplification, such as the widespread assumption that direct, additive competition captures the important details about how interactions between species impact community diversity. More complex non-additive ‘higher-order’ interactions are assumed to be negligible or absent. Notably, these assumptions are poorly supported and have major consequences for the accuracy with which patterns of natural diversity are modelled and explained. We present a mathematically simple framework for incorporating biologically meaningful complexity into models of diversity by including non-additive higher-order interactions. We further provide empirical evidence that such higher-order interactions strongly influence species’ performance in natural plant communities, with variation in seed production (as a proxy for per capita fitness) explained dramatically better when at least some higher-order interactions are considered. Our study lays the groundwork for a long overdue shift in how species interactions are used to study the diversity of natural communities.
Plant species can influence the pollination and reproductive success of coflowering neighbors that share pollinators. Because some individual pollinators habitually forage in particular areas, it is also possible that plant species could influence the pollination of neighbors that bloom later. When flowers of a preferred forage plant decline in an area, site-fidelity may cause individual flower feeders to stay in an area and switch plant species rather than search for preferred plants in a new location. A newly blooming plant species may quickly inherit a set of visitors from a prior plant species, and therefore experience higher pollination success than it would in an area where the first species never bloomed. To test this, we manipulated the placement and timing of two plant species, Delphinium barbeyi and later-blooming Gentiana parryi. We recorded the responses of individually marked bumble bee pollinators. About 63% of marked individuals returned repeatedly to the same areas to forage on Delphinium. When Delphinium was experimentally taken out of bloom, most of those site-faithful individuals (78%) stayed and switched to Gentiana. Consequently, Gentiana flowers received more visits in areas where Delphinium had previously flowered, compared to areas where Delphinium was still flowering or never occurred. Gentiana stigmas received more pollen in areas where Delphinium disappeared than where it never bloomed, indicating that Delphinium increases the pollination of Gentiana when they are separated in time. Overall, we show that individual bumble bees are often site-faithful, causing one plant species to increase the pollination of another even when separated in time, which is a novel mechanism of pollination facilitation.
A common structural feature of natural communities is the non‐random distribution of pairwise interactions between organisms of different trophic levels. For plant–animal interactions, it is predicted that both stochastic processes and functional plant traits that facilitate or prevent interactions are responsible for these patterns.
However, unbiased manipulative field experiments that rigorously test the effects of individual traits on community structure are lacking. We address this gap by manipulating floral scent bouquets in the field.
Manipulation of floral scent bouquets led to quantitative as well as qualitative restructuring of flower–visitor networks, making them more generalized. Olfactometer trials confirmed both positive and negative responses to scent bouquets.
Our results clearly show that the distribution of insect visitors to the two abundant study plant species reflects the insects' species‐specific preferences for floral scents, rather than for visual or morphological floral traits.
Thus, floral scents may be of major importance in partitioning flower–visitor interactions. Integrating experimental manipulations of plant traits with field observations of interaction patterns thus represents a promising approach for revealing the processes that structure species assemblages in natural communities.
Character displacement is a potentially important process driving trait evolution and species diversification. Floral traits may experience character displacement in response to pollinator-mediated competition (ecological character displacement) or the risk of forming hybrids with reduced fitness (reproductive character displacement). We test these and alternative hypotheses to explain a yellow-white petal color polymorphism in Leavenworthia stylosa, where yellow morphs are spatially associated with a white-petaled congener (L. exigua) that produces hybrids with complete pollen sterility. A reciprocal transplant experiment found limited evidence of local adaptation of yellow color morphs via increased survival and seed set. Pollinator observations revealed that Leavenworthia attract various pollinators that generally favor white petals and exhibit color constancy. Pollen limitation experiments showed that yellow petals do not alleviate competition for pollination. Interspecific pollinator movements were infrequent and low hybridization rates (∼0.40% - 0.85%) were found in each morph, with natural rates likely being lower. Regardless, hybridization rates were significantly higher in white morphs of L. stylosa, yielding a small selection coefficient of s = 0.0042 against this phenotype in sympatry with L. exigua. These results provide support for reproductive character displacement as a mechanism contributing to the pattern of petal color polymorphism in L. stylosa. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Lack of standardization of floral scent analysis using dynamic headspace collection and GC-MS has prevented meaningful biological comparisons of results from different studies. We explored technique-related sources of variation by comparing the relative performances of different trapping sorbents, elution solvents and vacuum pump flow rates in the collection of known volatiles from (a) synthetic blends on filter papers and (b) living flowers of Clarkia breweri (Onagraceae). The greatest amounts of volatiles were collected when Porapak Q sorbent and hexane solvent were used, but most analyses were qualitatively similar. Low and high pump flow rates yield a tradeoff, with higher rates trapping low volatility compounds but also raising ambient contamination levels. Significant variation was associated with the use of different sorbents and solvents, but detailed statistical comparisons were precluded by significant interaction effects involving other experimental variables. Given the tightly controlled experimental conditions and use of inbred plant lines, this unexpected result suggests that analyses of small samples carry a high risk of experimental artifact. We recommend that floral scent analyses incorporate experimental and statistical approaches that address as many method-related variables as possible, that samples of 10 or more individuals be used, and that GC-MS parameters be held constant for all comparative analyses.
The genus Clarkia is comprised of species of annuals that occur in disjunct colonies of various size. The flowers are characteristically insect pollinated and for the most part designed to promote outcrossing. However, all individuals are normally self-compatible and at least some degree of self-pollination is general. Different species as well as populations within a species are characterized by the same kind of traits that may distinguish individuals within a population. Morphological, physiological, and chromosomal differences, including differences in chromosome arrangement and number, as well as differences in potential fertility are found to vary between individuals within many populations. Furthermore, the differences which characterize species are reflected in the differences found between populations within a species. The latter may involve not only morphological, physiological, and chromosomal differences but also the capacity to exchange genes. A complete spectrum exists extending from those colonies that are highly interfertile to those in which the F2 is partly or largely degenerate, to those in which the hybrids are but partly fertile or even sterile and finally to those that are unable to cross. Morphological and perhaps chromosomal differentiation between populations may in many cases have resulted from chance loss and fixation of particular alleles or chromosome arrangements in small populations, particularly as a consequence of the meager beginning and subsequent inbreeding that of necessity occurs in establishing a new colony. However, adaptive changes have doubtlessly played a more fundamental role. Speciation has been a by-product of the production of barriers to gene exchange in the course of adaptive and chance differentiation. The factors contributing to the production of these barriers are several. However, the most important single factor contributing to speciation in this group has probably been the differential accumulation of chromosomal rearrangements. This accumulation, either by chance or more frequently as a result of association with adapted gene combinations, will immediately or eventually lead to a reduction in fertility between different populations. Furthermore, chromosomal rearrangements have been directly or indirectly involved in changes in chromosome number at the diploid level. At the same time, by reducing the structural homology between genomes, the accumulation of structural rearrangements has set the stage for successful alloploidy. The occurrence of populations which are intersterile but morphologically similar, as well as adjacent populations that are morphologically distinct but apparently interfertile, suggests that differentiation which may lead to speciation in this genus may frequently occur rapidly. Most of the genetically isolated populations thus formed are probably short lived, but a few may become successful species. Gradual segregation of geographic races also occurs but the success of the genus seems not to lie so much in the gradual segregation of adaptive races as in the production of a multiplicity of locally adapted, genetically isolated and often ephemeral segregates. It is suggested that patterns of evolution similar to that of Clarkia will be found in other comparable groups of annuals.
Background/Question/Methods
In natural biological communities, species interact with many other species. Multiple species interactions lead to indirect ecological effects that have important fitness consequences and can also result in non-additive patterns of natural selection. Given that ecological indirect effects are common in nature, non-additive selection may also be quite common, and thus may be critical for predicting evolution in natural communities composed of many interacting species. Here we develop a clear method for testing for non-additive selection and consider how it might affect adaptation in multispecies communities.
Results/Conclusions
We tested our null hypothesis for non-additive selection using a simulation model. The model validates our null hypothesis, but importantly, indicates that fitness must be standardized across, rather than within, experimental treatments. We used our approach to quantify the strength of non-additive selection relative to pairwise selection in two case studies. In one case, insect herbivores and an invasive plant species impose strong non-additive selection on herbivore resistance in a native plant species. In a second case, three pollinators impose strong non-additive selection on anther exsertion in wild radish. Our results suggest that non-additive selection may be common in nature, and may often be just as important as pairwise selection gradients in determining how traits will evolve in natural communities. We call for further studies using the methodology outlined here to determine how common non-additive selection is and under what conditions it is most likely to occur.
Theory predicts that lack of heritable trait variation and/or maladaptive gene flow can promote the formation of species geographical range boundaries even in the absence of barriers to dispersal. Little is known, however, about the patterns and drivers of differentiation across species' ranges and whether they influence boundary formation in the field.
Using field measurements, two common garden studies, and Q ST – F ST analyses, we examined environmental and genetic influences on plant phenotype across the geographical range of Clarkia xantiana ssp . xantiana . This annual plant endemic to California has an eastern range border that lacks obvious physical barriers to dispersal.
We find that across opposing environmental gradients that span the species core range, populations are likely to be locally adapted. Populations are phenotypically differentiated from each other in the field as well as common gardens. Traits are correlated with field environmental variables in both settings, and Q ST – F ST comparisons indicate variation in flowering time, degree of branching, and herkogamy may be adaptive. The strength and direction of environment‐trait correlations at the range edge are similar to the range centre, and quantitative genetic variation is not reduced. Genetic correlations between traits are generally weak, also suggesting little constraint on trait evolution at the range edge.
Synthesis . For traits measured here, it is unlikely that either low heritable variation at the range edge or maladaptive gene flow strongly inhibits eastward range expansion. Our results suggest that across environmentally complex landscapes, patterns of diversity generated by locally adaptive selection do not necessarily contribute broadly to the formation of range boundaries as predicted.
Background and AimsPlant populations experiencing divergent pollination environments may be under selection to modify floral traits in ways that increase both attractiveness to and efficiency of novel pollinators. These changes may come at the cost of reducing overall effectiveness of other pollinators. The goal of this study was to examine differences in attractiveness and efficiency between Clarkia concinna and C. breweri, sister species of annual plants with parapatric distributions.Methods
An assessment was made as to whether observed differences in visitors between natural populations are driven by differences in floral traits or differences in the local pollination environment. Differences in floral attractiveness were quantified by setting out arrays of both species in the geographical range of each species and exposing both species to nocturnal hawkmoths (Hyles lineata) in flight cages. Differences in visitor efficiency were estimated by measuring stigma-visitor contact frequency and pollen loads for diurnal visitors, and pollen deposition on stigmas for hawkmoths.Key ResultsThe composition of visitors to arrayed plants was similar between plant species at any particular site, but highly divergent among sites, and reflected differences in visitors to natural populations. Diurnal insects visited both species, but were more common at C. concinna populations. Hummingbirds and hawkmoths were only observed visiting within the range of C. breweri. Despite attracting similar species when artificially presented together, C. concinna and C. breweri showed large differences in pollinator efficiency. All visitors except hawkmoths pollinated C. concinna more efficiently.Conclusions
Differences in the available pollinator community may play a larger role than differences in floral traits in determining visitors to natural populations of C. concinna and C. breweri. However, floral traits mediate differences in pollinator efficiency. Increased effectiveness of the novel hawkmoth pollinator on C. breweri comes at relatively little cost in attractiveness to other visitors, but at large cost in their efficiency as pollinators.
Background and AimsThe events leading to speciation are best investigated in systems where speciation is ongoing or incomplete, such as incipient species. By examining reproductive barriers among incipient sister taxa and their congeners we can gain valuable insights into the relative timing and importance of the various barriers involved in the speciation process. The aim of this study was to identify the reproductive barriers among sexually deceptive orchid taxa in the genus Chiloglottis.Methods
The study targeted four closely related taxa with varying degrees of geographic overlap. Chemical, morphological and genetic evidence was combined to explore the basis of reproductive isolation. Of primary interest was the degree of genetic differentiation among taxa at both nuclear and chloroplast DNA markers. To objectively test whether or not species boundaries are defined by the chemistry that controls pollinator specificity, genetic analysis was restricted to samples of known odour chemistry.Key ResultsFloral odour chemical analysis was performed for 600+ flowers. The three sympatric taxa were defined by their specific chiloglottones, the semiochemicals responsible for pollinator attraction, and were found to be fully cross-compatible. Multivariate morphometric analysis could not reliably distinguish among the four taxa. Although varying from very low to moderate, significant levels of genetic differentiation were detected among all pairwise combinations of taxa at both nuclear and chloroplast loci. However, the levels of genetic differentiation were lower than expected for mature species. Critically, a lack of chloroplast DNA haplotype sharing among the morphologically indistinguishable and most closely related taxon pair confirmed that chemistry alone can define taxon boundaries.Conclusions
The results confirmed that pollinator isolation, mediated by specific pollinator attraction, underpins strong reproductive isolation in these taxa. A combination of large effective population sizes, initial neutral mutations in the genes controlling floral scent, and a pool of available pollinators likely drives diversity in this system.
Behavioral field studies were conducted to determine if bumble bees (Bombus terrestris L.) can use pollen odor to assess pollen availability in flowers of Rosa rugosa (Rosaceae), a nectarless species with a distinctive pollen odor. Pollen volatiles were added singly and in mixtures to newly opened flowers from which anthers were removed and were offered to free-flying bumble bees in an array that included intact flowers as controls. The addition of 2-tridecanone and geranyl acetate reduced landing responses, but the addition of tetradecyl acetate and especially eugenol significantly increased landing frequency as well as the display of vibratile pollen-collecting behavior, suggesting that they are key chemicals in a bee’s assessment of pollen availability in individual flowers. Bee responses to flowers in which androecia were exchanged between first-day flowers (with pollen reward) and second-day flowers (without pollen reward) provide evidence that bee discrimination between flowers is based mainly on stimuli from the anthers. Overall, the findings show that bumble bees foraging on R. rugosa use primarily pollen odor in concert with visual stimuli from the androecium and secondarily petals odors and colors in selecting rewarding flowers. Controlled pollination and bagging studies indicate that R. rugosa requires cross-pollination by insects, pointing to the selective advantage that pollen odor provides by increases plant fitness through the enhanced foraging efficiency of bumble bee pollinators.
Clarkia lingulata is a tetrasomic derivative of C. biloba. It occurs locally at the southern limit of distribution of the parental species. They cross readily but the hybrids are essentially sterile. When first studied, they were found to occur in adjacent but not in mixed colonies. Since then, C. lingulata has extended its range and has become established at the margin of an adjacent colony of C. biloba. Experimental sympatric populations were established by sowing a mixture of the two species in selected sites south of their natural area of distribution. Populations in the driest sites died out rapidly and showed little or no reproduction; in other sites reproduction has been evident and the populations still persist after five generations. In these artificial populations, C. lingulata has consistently matured about two weeks earlier than C. biloba. This suggests that C. lingulata is adapted to a shorter growing season than C. biloba, and may explain the occurrence of C. lingulata at the margin of distr...
Consideration of the possibilities and difficulties of detecting character displacement leads to a re-definition of the phenomenon; character displacement is the process by which a morphological character state of a species changes under Natural Selection arising from the presence, in the same environment, of one or more species similar to it ecologically and/or reproductively. This incorporates the principal ideas in the original definition given by Brown & Wilson (1956), but eliminates the restriction of making comparisons of the character states of a species in sympatry and allopatry.
The evidence for the ecological (competitive) aspect of character displacement is assessed by analyzing in detail the best documented and well publicized examples in the literature. Some of the examples either do not exhibit displaced characters or, if they do, the “displacement” can be interpreted in other and perhaps simpler ways; this applies to the so-called classical case of character displacement, Sitta tephronota and S. neumayer in Iran. Other examples, involving lizards and birds, constitute better evidence for character displacement, but in no single study is it entirely satisfactory. It is concluded that the evidence for the ecological aspect of character displacement is weak.
A pollinator that restricts its visits to one flower type, even when other rewarding types are accessible, can be said to exhibit flower constancy. This usage distinguishes constancy from fixed preference or labile preference for the most rewarding flower type; I discuss a quantitative constancy index that is insensitive to preference changes. Because a constant visitor avoids flowers with acceptable rewards, the behavior is inefficient unless there are constraints such as an inability to learn quickly or to remember simultaneously how to deal with many flower types. If such constraints are the basis for constancy, it should be most pronounced when flowers in a mixture differ strongly in morphology or color. I observed bees foraging in outdoor flower arrays and found that constancy always increased with increasing differences among flower types; similar results can be gleaned from one other study. The available experimental evidence thus suggests that constancy reflects behavioral constraints.