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The role of lateral and vertical herkogamy in the divergence of the blue- and red-flowered lineages of Lysimachia arvensis
Abstract
Background and aims
Herkogamy, or anther-stigma separation, is known to reduce self-pollen deposition, but little is known about the relative efficacy of different modes or conformations of herkogamy. We assessed the effectiveness of vertical versus lateral herkogamy in preventing or promoting self-pollen deposition in the annual herb Lysimachia arvensis, a plant with lineages that differ in flower colour, and in which flowers first display lateral and then vertical herkogamy. Because mating between the two lineages compromises fitness through the production of low-quality hybrid offspring, we tested the prediction that individuals sampled from sites occupied by both lineages should have flowers that promote autonomous self-pollen deposition and self-fertilization as a result of selection to reduce deleterious reproductive interference.
Methods
We characterised variation in herkogamy within and among 25 pure and mixed populations of L. arvensis in its European range and assessed the effectiveness of lateral versus vertical herkogamy in avoiding self-pollen deposition.
Results
Lateral herkogamy was more effective than vertical herkogamy in limiting self-pollen deposition. In the case of vertical herkogamy, only approach herkogamy was effective. Lineages showed consistent differences in herkogamy traits. In general, angles were smaller for blue than red flowers in most populations, and blue flowers showed approach herkogamy, while red flowers showed predominantly reverse herkogamy. In sympatry, the red lineage showed a reduction of both herkogamy traits while for the blue lineage only lateral herkogamy was reduced.
Conclusions
Our results demonstrate that pollen deposition is affected not only by the degree but also the spatial conformation of herkogamy. They also highlight reduced herkogamy as a potential mechanism for promoting reproductive assurance under pollen limitation, as well as for avoiding reproductive interference between genetically divergent lineages.
... demonstrate that the conflict between accuracy in pollen transfer and avoidance of self-pollination (the "herkogamy dilemma" sensu Armbruster et al., 2009a) may be resolved, often through complete dichogamy (temporal separation of sexual functions; Lloyd and Webb, 1986) or other mechanisms such as movement herkogamy, as seen in Parnassia (Celastraceae; Armbruster et al., 2014), Ajuga (Lamiaceae; Ye et al., 2019), Prepusa (Gentianaceae; Lemos et al., 2020), and Lysimachia (Primulaceae;Jiménez-López et al., 2020). ...
Premise:
Flower phenotypes evolve to attract pollinators and to ensure efficient pollen transfer to and from the bodies of pollinators or, in self-compatible bisexual flowers, between anthers and stigmas. If functionally interacting traits are genetically correlated, response to selection may be subject to genetic constraints. Genetic constraints can be assessed by quantifying standing genetic variation in (multivariate) phenotypic traits and by asking how much the available variation is reduced under specific assumptions about phenotypic selection on functionally interacting and genetically correlated traits.
Methods:
We evaluated multivariate evolvability and potential genetic constraints underlying the evolution of the three-dimensional structure of Dalechampia blossoms. First, we used data from a greenhouse crossing design to estimate the G matrix for traits representing the relative positions of male and female sexual organs (anthers and stigmas) and used the G matrix to ask how genetic variation is distributed in multivariate space. To assess the evolutionary importance of genetic constraints, we related standing genetic variation across phenotypic space to evolutionary divergence of population and species in the same phenotypic directions.
Results:
Evolvabilities varied substantially across phenotype space, suggesting that certain traits or trait combinations may be subject to strong genetic constraint. Traits involved functionally in flower-pollinator fit and autonomous selfing exhibited considerable independent evolutionary potential, but population and species divergence tended to occur in phenotypic directions associated with greater-than-average evolvability.
Conclusions:
These results are consistent with the hypothesis that genetic constraints can hamper joint trait evolution towards optimum flower-pollinator fit and optimum self-pollination rates.
... Given that flowers with a high degree of herkogamy can receive large amounts of outcross pollen (Campbell, 1989), they may also readily receive heterospecific pollen, and as a consequence, suffer from reproductive interference associated with the reception of conspecific pollen and subsequent production of maladaptive hybrids. Thus, under conditions of reproductive interference, flowers with a low degree of herkogamy would have an advantage, in that they have the capacity to minimize reproductive interference by promoting self-pollination (Jiménez-L opez et al., 2020). In this regard, a previous study has reported that in urban environments O. corniculata can coexist with the alien congener Oxalis dillenii and that crosses between these two species often give rise to infertile hybrids (Fukatsu et al., 2019). ...
The evolutionary transition from outcrossing in heterostylous morphs to selfing in homostylous morphs has occurred in many plant lineages. Homostylous variants with a low degree of herkogamy may increase the reproductive advantage of autonomous self‐pollination when there is little inbreeding depression and/or low pollinator visitation. Oxalis corniculata , a self‐compatible perennial herb derived from a tristylous ancestor, is reported to have two floral morphs. Homostyled plants are broadly distributed in Japan, whereas long‐styled plants are reported to occur only in coastal areas. We examined the hypothesis that a reproductive advantage in avoiding inbreeding depression and/or frequent pollinator visits enables long‐styled plants to live in some areas. Studies on floral variation revealed that the degree of herkogamy varied widely and continuously within and among populations. Homostyled and long‐styled morphs were functionally defined based on the ability of autonomous self‐pollination. Homostyled plants were widely distributed, whereas long‐styled plants were found in and around the two coastal populations and relatively inland populations. Pollination experiments provided no evidence of inbreeding depression in either homostyled or long‐styled plants. Pollinator visitation frequency was higher in the two coastal populations than in the other populations. Thus, reproductive disadvantage in long‐styled plants lacking autonomous self‐pollination has reduced in the two coastal populations, and long‐styled plants may be maintained due to a competitive advantage of large seed size. In contrast, we recorded no comparable frequencies of pollinator visitation in other populations containing long‐styled plants, indicating that there are other factors contributing to the maintenance of long‐styled plants in these areas.
... The blue petals of L. arvensis contain malvidin derivatives, whereas orange petals contain pelargonidin derivatives (Lawrence et al., 1939;Harborne, 1968;Ishikura, 1981). Although both L. arvensis flower colors have long been described as different morphs, recent molecular phylogenetic studies indicate that these flower color phenotypes reflect very closely related, yet distinct, evolutionary lineages (Jiménez-López, 2019; Jiménez-López et al., in review) with some degree of reproductive isolation (Jiménez-López et al., 2020). Pollinators (mainly Halictus spp. ...
Anthocyanins are the primary pigments contributing to the variety of flower colors among angiosperms and are considered essential for survival and reproduction. Anthocyanins are members of the flavonoids, a broader class of secondary metabolites, of which there are numerous structural genes and regulators thereof. In western European populations of Lysimachia arvensis , there are blue- and orange-petaled individuals. The proportion of blue-flowered plants increases with temperature and daylength yet decreases with precipitation. Here, we performed a transcriptome analysis to characterize the coding sequences of a large group of flavonoid biosynthetic genes, examine their expression and compare our results to flavonoid biochemical analysis for blue and orange petals. Among a set of 140 structural and regulatory genes broadly representing the flavonoid biosynthetic pathway, we found 39 genes with significant differential expression including some that have previously been reported to be involved in similar flower color transitions. In particular, F3′5′H and DFR , two genes at a critical branchpoint in the ABP for determining flower color, showed differential expression. The expression results were complemented by careful examination of the SNPs that differentiate the two color types for these two critical genes. The decreased expression of F3′5′H in orange petals and differential expression of two distinct copies of DFR , which also exhibit amino acid changes in the color-determining substrate specificity region, strongly correlate with the blue to orange transition. Our biochemical analysis was consistent with the transcriptome data indicating that the shift from blue to orange petals is caused by a change from primarily malvidin to largely pelargonidin forms of anthocyanins. Overall, we have identified several flavonoid biosynthetic pathway loci likely involved in the shift in flower color in L. arvensis and even more loci that may represent the complex network of genetic and physiological consequences of this flower color polymorphism.
... Flower traits are frequently correlated (Mazer and Hultgård, 1993;Ishii and Morinaga, 2005). Diverse floral traits, such as floral display in Lobularia (Gómez, 2000), inflorescence production in Hydrophyllum (Wolfe, 1993), stigma-anther separation in Ipomoea (Sobrevila et al., 1989) and Lysimachia (Jiménez-López et al., 2020), nectar production in Ipomopsis (Meléndez-Ackerman and Campbell, 1998), or flower size in diverse crucifer species (Dukas and Shmida, 1989), have shown to be correlated to flower color. Given that biotic selective agents, such as pollinators and herbivores, also respond to other features apart from flower color, it is necessary to consider those correlations when studying selection on flower color (Kingsolver and Diamond, 2011). ...
Flower color, as other floral traits, may suffer conflicting selective pressures mediated by both mutualists and antagonists. The maintenance of intraspecific flower color variability has been usually explained as a result of direct selection by biotic agents. However, flower color might also be under indirect selection through correlated traits, since correlations among flower traits are frequent. In this study, we aimed to find out how flower color variability is maintained in two nearby populations of Silene littorea that consistently differ in the proportions of white-flowered plants. To do that, we assessed natural selection on floral color and correlated traits by means of phenotypic selection analysis and path analysis. Strong directional selection on floral display and flower production was found in both populations through either male or female fitness. Flower color had a negative indirect effect on the total male and female fitness in Melide population, as plants with lighter corollas produced more flowers. In contrast, in Barra population, plants with darker corollas produced more flowers and have darker calices, which in turn were selected. Our results suggest that the prevalence of white-flowered plants in Melide and pink-flowered plants in Barra is a result of indirect selection through correlated flower traits and not a result of direct selection of either pollinators or herbivores on color.
... Genetic differentiation between color morphs strongly suggests that gene flow between them is restricted, being to some extent reproductively isolated. This is also supported by other results found in previous studies and in other previous papers: niche differentiation with the blue-flowered plants more adapted to dry habitats (Arista et al., 2013), differences in flowering phenology found here and in a previous study (Arista et al., 2013) that hinder pollen flow between morphs at least partially, pollinator visitation in polymorphic populations where bees show floral constancy and prefer blue-flowered plants Jiménez-López et al., 2020a), differences in inbreeding depression and mating system (in this study), and the low frequency of intermediate phenotypes in polymorphic populations (Jiménez-López et al., 2019a;2020b). These facts clearly indicate a history of gene flow limitation between morphs, suggesting they are different lineages. ...
Flower color polymorphism, an infrequent but phylogenetically widespread condition in plants, is captivating because it can only be maintained under a few selective regimes but also because it can drive intra-morph assortative mating and promote speciation. Lysimachia arvensis is a polymorphic species with red or blue flowered morphs. In polymorphic populations, which are mostly Mediterranean, pollinators prefer blue-flowered plants to the red ones, and abiotic factors also favors blue-flowered plants. We hypothesize that the red morph is maintained in Mediterranean areas due to its selfing capacity. We assessed inbreeding depression in both color morphs in two Mediterranean populations and genetic diversity was studied via SSR microsatellites in 20 natural populations. Results showed that only 44-47% of selfed progeny of the red plants reached reproduction while about 72-91% of blue morph progeny did it. Between-morph genetic differentiation was high and the red morph had a lower genetic diversity and a higher inbreeding coefficient, mainly in the Mediterranean. Results suggest that selfing maintaining the red morph in Mediterranean areas despite its inbreeding depression. In addition, genetic differentiation between morphs suggests a low gene flow between them, suggesting reproductive isolation.
... (Figure 4(a,b)), the blue-flowered form is better adapted to xeric conditions than the red-flowered form, which accounts for its high frequency in the Mediterranean region compared to the red form (Ortiz et al. 2015). A difference in herkogamy between these morphs was recently described, blue flowers showing approach herkogamy while red flowers showed reverse herkogamy, with an effect on pollen deposition (Jiménez-López et al. 2020). Colour polymorphism is frequent in species with deceptive pollination, and this may be due to disruptive selection caused by inaccurate discrimination by pollinators (Kagawa and Takimoto 2016). ...
Flowers are the flagship structure of angiosperms (flowering plants). This spectacular innovation has probably contributed in a significant way to the extraordinary success of angiosperms, which today make up 90% of land plant species. Flowering plants display a beautiful and spectacular diversity of floral forms that results largely from the diversification of reproductive strategies, including co-adaptation with pollinators. One of the most spectacular variations concerns flower colour, with an almost endless range of shades varying from pure white to near black. In many plants, floral colours contrast with the rest of the plant, and are generally produced by the presence of pigments other than chlorophyll, although in some cases colour is created by light-reflecting structures. The biosynthetic pathways of carotenoids, anthocyanins and betalains, the three main classes pigment, have been deciphered. In many species, flower colour plays a key role in pollination as a visual cue to attract biotic pollinators. Although petals are often the most colourful and showy part of the flower, there are many exceptions, including examples where bracts are showier than the flowers themselves. Colour is usually stable within a species, resulting from adaptive processes linked to plant-pollinator relationships. The evolutionary and genetic mechanisms involved in flower colour shifts have been described in several taxa, providing insights into some of the processes that have shaped the diversity of flowering plants.
Genetic divergence between species depends on reproductive isolation (RI) due to traits that reduce interspecific mating (prezygotic isolation) or are due to reduced hybrid fitness (postzygotic isolation). Previous research found that prezygotic barriers tend to be stronger than postzygotic barriers, but most studies are based on the evaluation of F 1 hybrid fitness in early life cycle stages.
We combined field and experimental data to determine the strength of 17 prezygotic and postzygotic reproductive barriers between two Lysimachia species that often co‐occur and share pollinators. We assessed postzygotic barriers up to F 2 hybrids and backcrosses.
The two species showed near complete RI due to the cumulative effect of multiple barriers, with an uneven and asymmetric contribution to isolation. In allopatry, prezygotic barriers contributed more to reduce gene flow than postzygotic barriers, but their contributions were more similar in sympatry.
The strength of postzygotic RI was up to three times lower for F 1 progeny than for F 2 or backcrossed progenies, and RI was only complete when late F 1 stages and either F 2 or backcrosses were accounted for. Our results thus suggest that the relative strength of postzygotic RI may be underestimated when its effects on late stages of the life cycle are disregarded.
RESUMEN: Se analiza la información bibliográfica y los pliegos de herbario en los que se apoya la
presencia de Anagallis monelli en la Comunidad Valenciana (España). Se aporta un apartado relativo a la
nomenclatura de algunas de las especies implicadas y se tipifican algunos de los nombres mencionados
en este trabajo. Palabras clave: Anagallis; Comunidad Valenciana; España; corología; Myrsinaceae;
nomenclatura; Primulaceae; taxonomía; tipificación.
ABSTRACT: On the presence of Anagallis monelli L. (Primulaceae) in the Valencian Community
(Spain). The bibliographic information and herbarium sheets on the presence of Anagallis monelli in the
Valencian Community (Spain) are analyzed. A section related to the nomenclature of some of the species
involved in this work is provided, and some of the names cited in this paper are typified. Keywords:
Anagallis; Valencian Community; Spain; chorology; Myrsinaceae; nomenclature; Primulaceae;
taxonomy; typification.
Flower colour has played a decisive role as an evolutionary force in many groups of plants by driving speciation. A well-known example of colour polymorphism is found across the Mediterranean populations of Lysimachia arvensis and L. monelli, in which blue- and red-flowered plants can be found. Previous studies recognized two lineages within L. arvensis differing in flower colour, but this variation has not yet been considered in a phylogenetic context. We have reconstructed the ancestral states of flower colour across Mediterranean Lysimachia spp. aiming at understanding its phylogenetic signal using the nuclear internal transcribed spacer (ITS) sequences and three plastid markers. All blue- and red-flowered specimens were nested in different clades in the ITS tree, thus supporting that L. arvensis and L. monelli are polyphyletic, whereas low phylogenetic resolution was found in plastid markers. Monophyly was reconstructed for blue-flowered L. arvensis and L. monelli samples, and similarly for red-flowered individuals of each species: (1) blue-flowered L. arvensis was reconstructed as sister to the strictly blue-flowered L. talaverae in a monophyletic clade sister to remaining Lysimachia; (2) red-flowered L. arvensis was resolved as sister to red-flowered L. monelli in a monophyletic clade; and (3) clade 2 was sister to blue-flowered L. monelli and the strictly blue-flowered L. foemina. Our results suggest that colour lineages in L. arvensis and L. monelli constitute different species, but flower colour did not promote the separation of these lineages. We propose a new name for blue-flowered L. arvensis (L. loeflingii) and a new combination for red-flowered L. monelli (L. collina), maintaining L. arvensis for red-flowered plants and L. monelli for blue-flowered plants.
The success of species depends on their ability to exploit ecological resources in order to optimize their reproduction. However, species are not usually found within single-species ecosystems but in complex communities. Because of their genetic relatedness, closely related lineages tend to cluster within the same ecosystem, rely on the same resources and be phenotypically similar. In sympatry, they will, therefore, compete for the same resources and in the case of flowering plants, exchange their genes through heterospecific pollen transfer. These interactions, nevertheless, pose significant challenges to species coexistence because they can lead to resource limitation and reproductive interference. In such cases, divergent selective pressures on floral traits will favour genotypes that isolate or desynchronise the reproduction of sympatric lineages. The resulting displacement of reproductive characters will, in turn, lead to premating isolation and promote intraspecific divergence, thus initiating or reinforcing the speciation process. In this review, we discuss the current theoretical and empirical knowledge on the influence of heterospecific pollen transfer on flower evolution, highlighting its potential to uncover the ecological and genomic constraints shaping the speciation process.
Premise of Study
In a seminal body of theory, Lloyd showed that the fitness consequences of selfing will depend on its timing in anthesis. Selfing that occurs after opportunities for outcrossing or pollen dispersal can provide reproductive assurance when pollinators are limited and is expected to incur little cost, even when inbreeding depression is high. As a result, delayed selfing is often interpreted as a “best‐of‐both‐worlds” mating system that combines the advantages of selfing and outcrossing.
Methods
We surveyed 65 empirical studies of delayed selfing, recording floral mechanisms and examining information on inbreeding depression, autofertility, and other parameters to test the support for delayed selfing as a best‐of‐both‐worlds strategy.
Key Results
Phylogenetic distribution of the diverse floral mechanisms suggests that some basic floral structures may predispose plant taxa to evolve delayed selfing. Delayed selfing appears to serve as a best‐of‐both‐worlds strategy in some but not all species. While the capacity for autonomous selfing is often high, it is lower, in some cases, than in related species with earlier modes of selfing. In other delayed‐selfers, low inbreeding depression and reduced investment in corollas and pollen suggest limited benefits from outcrossing.
Conclusions
Despite a growing literature on the subject, experimental evidence for delayed selfing is limited and major gaps in knowledge remain, particularly with respect to the stability of delayed selfing and the conditions that may favor transitions between delayed and earlier selfing. Finally, we suggest a potential role of delayed selfing in facilitating transitions from self‐incompatibility to selfing.
Ecological factors that reduce the effectiveness of cross-pollination are likely to play a role in the frequent evolution of routine self-fertilization in flowering plants. However, we lack empirical evidence linking the reproductive assurance value of selfing in poor pollination environments to evolutionary shifts in mating system. Here, we investigated the adaptive significance of prior selfing in the polymorphic annual plant Arenaria uniflora (Caryophyllaceae), in which selfer populations occur only in areas of range overlap with congener A. glabra. To examine the hypothesis that secondary contact between the two species contributed to the evolution and maintenance of selfing, we used field competition experiments and controlled hand-pollinations to measure the female fitness consequences of pollinator-mediated interspecific interactions. Uniformly high fruit set by selfers in the naturally pollinated field arrays confirmed the reproductive assurance value of selfing, whereas substantial reductions in outcrosser fruit set (15%) and total seed production (20-35%) in the presence of A. glabra demonstrated that pollinator-mediated interactions can provide strong selection for self-pollination. Heterospecific pollen transfer, rather than competition for pollinator service, appears to be the primary mechanism of pollinator-mediated competition in Arenaria. Premating barriers to hybridization between outcrossers and A. glabra are extremely weak. The production of a few inviable hybrid seeds after heterospecific pollination and intermediate seed set after mixed pollinations indicates that A. glabra pollen can usurp A. uniflora ovules. Thus, any visit to A. uniflora by shared pollinators carries a potential female fitness cost. Moreover, patterns of fruit set and seed set in the competition arrays relative to controls were consistent with the receipt of mixed pollen loads, rather than a lack of pollinator visits. Competition through pollen transfer favors preemptive self-pollination and may be responsible for the evolution of a highly reduced floral morphology in A. uniflora selfers as well as their current geographical distribution.
In plants that are able to self‐fertilize, autonomous selfing has been hypothesized to function as an effective mechanism that prevents heterospecific mating. However, there have only been few studies that have assessed the relative and absolute contribution of different modes of selfing to total reproductive isolation acting between species. Because selfing can be expected to increase fitness costs when offspring are sired from more outcrossing sister taxa, it can be hypothesized that the contribution of post‐zygotic barriers to total reproductive isolation becomes stronger in selfing than in more outcrossing relatives.
To assess the efficiency of different modes of selfing against heterospecific mating, we conducted mixed‐pollination experiments in three C entaurium species showing strong differences in mating system (i.e. delayed selfing in C entaurium erythraea , competing selfing in C . littorale and prior selfing in C . pulchellum ). The contribution of selfing to total reproductive isolation was further examined by quantifying the strength of three pre‐zygotic (flowering phenology, pollinator fidelity and pollen production) and four intrinsic post‐zygotic (seed set and germination, survival and flowering capacity) barriers for each of the six species pair combinations.
Although autonomous selfing as a reproductive barrier was unable to completely impede gene flow, its efficiency as a mechanism to prevents heterospecific pollination strongly depended on the mode of selfing, with prior selfing being by far the most efficient mechanism and delayed selfing only offering a limited protection against hybrid fertilization at the end of a flower's lifetime. Apart from the prevention effect of selfing, differences in pollinator fidelity and pollen production also contributed substantially to total reproductive isolation.
Post‐zygotic hybrid costs were high and most prevalent for seed production and germination success. Reductions in hybrid vigour were significantly associated with the mating system of the maternal species, with the highest reductions in the most selfing C . pulchellum and the lowest reductions in predominant outcrossing C . erythraea .
Synthesis . Our findings indicate that selfing may prevent species from interspecific gene flow and hybridization. The association between the capacity to self‐autonomously and hybrid vigour further suggests that selfing may foster post‐zygotic costs following hybridization.
Background
Decreases in mate and/or pollinator availability would be expected to affect the selective pressure on plant mating systems. An increase in self-fertilization may evolve to compensate for the negative effects of pollination failure. However, the benefit of selfing in variable pollination environments depends on the relative fitnesses of selfed and outcrossed progeny. We investigated the potential for selfing to provide reproductive assurance over the lifetime of a long-lived perennial species and its variation between plant patches of various sizes. Patch size is likely to affect mate and pollinator availabilities, thereby affecting pollination success and the rate of selfing. We estimated fruit and seed set, reproductive assurance, self-compatibility, the multilocus patch selfing rate and lifetime inbreeding depression in natural patches of Rhododendron ferrugineum (Ericaceae), a mass-flowering species characterized by considerable patch size variation (as estimated by the total number of inflorescences).ResultsOpen seed set declined linearly with increasing patch size, whereas pollinator-mediated seed set (emasculated flowers) was not significantly affected. Progeny array analysis indicated that the selfing rate declined with increasing patch size, consistent with greater reproductive assurance in small sparse patches than in large, dense patches. However, fruit set and adult fitness decreased with decreasing patch size, with an estimated mean lifetime inbreeding depression of 0.9 (obtained by comparing F values in adults and progenies).Conclusions
Lifetime inbreeding depression strongly counteracts the advantage of reproductive assurance due to selfing in this long-lived species. The poor fitness of selfed offspring should counteract any evolution towards selfing, despite its potential to alleviate the negative consequences of pollen limitation. This study highlights the need to estimate lifetime inbreeding depression, together with mating system and pollination parameters, if we are to understand the actual benefit of selfing and avoid the overestimation of reproductive assurance.
Many flowering plants reduce sexual interference between male and female functions through herkogamy, the spatial separation of anthers and stigmas. Many species are monomorphic and present stigmas either above or below the anthers, "approach" or "reverse" herkogamy, respectively. Although numerous studies have examined species that are polymorphic for approach and reverse herkogamy, species with continuous variation in sex organ position have received little attention. We examined continuous variation in anther position, style length, herkogamy, and flower shape in the self-sterile perennial herb Polemonium brandegei. We observed pollinators, measured flower shape and sex organ position in the field, and estimated heritabilities and genetic correlations among floral traits in the greenhouse. The two major pollinators were hummingbirds Selasphorus platycercus and hawkmoths Hyles lineata and Hyles gallii, which are believed to select for exserted and recessed sex organs, respectively. Herkogamy was not polymorphic but rather ranged continuously from reverse to approach, independent of corolla shape, size, and age. Corolla tube length and width, sex organ heights, and herkogamy were all heritable. Genetic variation for the spatial separation of stigmas and anthers was particularly high (h2 = 0:851; CVa = 36:88; CVa is the coefficient of additive genetic variation). Temporal fluctuations in pollinator frequency likely maintain the variation in herkogamy by imposing heterogeneous selection on floral traits.
Develops a model which incorporates both a general form of pollen discounting and the possibility of fitness loss to selfed progeny. It provides greater insight than hitherto into the forces controlling the evolution of the selfing rate within a single population. -P.J.JarvisDept. of Botany, Univ. of Californa, Berkeley, CA 94720, USA.
1. The effect of variation in floral morphology and display on the level of outcrossing was investigated in a Rocky Mountain population of the self-compatible, protandrous, perennial herb, Aquilegia caerulea. ANOVA revealed substantial variation among 36 plants in floral traits including herkogamy (CV = 35%), protandry (23%), pollen production (12%), flower size (8%), the daily number of flowers in male phase (58%) and autofertility, seed production in the absence of pollinators (192%).
2. Whether this floral variation affected the outcrossing rates of individual plants was assessed using both a categorical analysis, in which outcrossing rates were estimated separately for groups of plants that differed with respect to floral features, and a correlation analysis involving outcrossing rates estimated for individual plants from large progeny arrays (n≥ 40). Both analyses indicated significant positive correlations between the outcrossing rate and herkogamy (r = + 0·71) and protandry (+ 0·54), negative correlations with the number of flowers in male phase during each day of female phase (– 0·42) and autofertility (– 0·36), but no correlation with flower size or pollen production.
3. Partial correlation indicated that both herkogamy and dichogamy, although weakly intercorrelated, were positively correlated with the outcrossing rate and that these effects were only partly mediated by their negative correlation with autofertility.
4. The extent to which floral features and the outcrossing rate covaried across the flowering sequence within plants was also examined in this study. As expected for a plant with strong protandry and sequential blooming, the number of flowers in male phase decreased strongly with flowering sequence position. However, categorical analysis did not support the prediction that the first flowers to open on an inflorescence outcrossed at a lower rate than later-opening flowers.
5. These results suggest that self-fertilization in A. caerulea is the result of all three major modes: autonomous and facilitated autogamy as well as geitonogamy. Although the geitonogamous component of selfing cannot be selected for directly, autogamy may be selected if it provides reproductive assurance.
Anthropogenic perturbations including habitat loss and emerging disease are changing pollinator communities and generating novel selection pressures on plant populations. Disruption of plant-pollinator relationships is predicted to cause plant mating system evolution, although this process has not been directly observed. This study demonstrates the immediate evolutionary effects of pollinator loss within experimental populations of a predominately outcrossing wildflower. Initially equivalent populations evolved for five generations within two pollination treatments: abundant bumblebee pollinators versus no pollinators. The populations without pollinators suffered greatly reduced fitness in early generations but rebounded as they evolved an improved ability to self-fertilize. All populations diverged in floral, developmental, and life-history traits, but only a subset of characters showed clear association with pollination treatment. Pronounced treatment effects were noted for anther-stigma separation and autogamous seed set. Dramatic allele frequency changes at two chromosomal polymorphisms occurred in the no pollinator populations, explaining a large fraction of divergence in pollen viability. The pattern of phenotypic and genetic changes in this experiment favors a sequential model for the evolution of the multitrait "selfing syndrome" observed throughout angiosperms.
Reproductive assurance through autonomous selfing is thought to be one of the main advantages of self-fertilization in plants. Floral mechanisms that ensure autonomous seed set are therefore more likely to occur in species that grow in habitats where pollination is scarce and/or unpredictable.
Emasculation and pollen supplementation experiments were conducted under laboratory conditions to investigate the capacity for, and timing of autonomous selfing in three closely related Centaurium species (Centaurium erythraea, C. littorale and C. pulchellum). In addition, observations of flower visitors were combined with emasculation and pollen addition experiments in natural populations to investigate the degree of pollinator limitation and pollination failure and to assess the extent to which autonomous selfing conferred reproductive assurance.
All three species were capable of autonomous selfing, although this capacity differed significantly between species (index of autonomous selfing 0·55 ± 0·06, 0·68 ± 0·09 and 0·92 ± 0·03 for C. erythraea, C. littorale and C. pulchellum, respectively). The efficiency and timing of autogamous selfing was primarily associated with differences in the degree of herkogamy and dichogamy. The number of floral visitors showed significant interspecific differences, with 1·6 ± 0·6, 5·4 ± 0·6 and 14·5 ± 2·1 floral visitors within a 2 × 2 m(2) plot per 20-min observation period, for C. pulchellum, C. littorale and C. erythraea, respectively. Concomitantly, pollinator failure was highest in C. pulchellum and lowest in C. erythraea. Nonetheless, all three study species showed very low levels of pollen limitation (index of pollen limitation 0·14 ± 0·03, 0·11 ± 0·03 and 0·09 ± 0·02 for C. erythraea, C. littorale and C. pulchellum, respectively), indicating that autonomous selfing may guarantee reproductive assurance.
These findings show that limited availability of pollinators may select for floral traits and plant mating strategies that lead to a system of reproductive assurance via autonomous selfing.
We recognize four major classes of stylar polymorphisms in flowering plants: the heterostylous conditions distyly and tristyly, stigma-height dimorphism, and enantiostyly. These polymorphisms differ in the relative positions of sexual organs and in the number of floral morphs that occur within populations. In heterostyly, stigma and anther heights are reciprocally positioned in the two or three floral morphs; in stigma-height dimorphism the two morphs vary in style length but not anther height; whereas in enantiostyly, flowers differ in whether the style is deflected to the left- or right-side of the flower. We distinguish two forms of enantiostyly depending on whether both style orientations occur on the same plant (monomorphic enantiostyly) or on different plants (dimorphic enantiostyly). Stylar polymorphisms have originated independently in numerous animal-pollinated flowering plant families. Both heterostyly and enantiostyly involve distinct floral syndromes suggesting functional convergence in which the position of the pollinator is important for pollen dispersal and male reproductive success. The function of stigma-height dimorphism remains enigmatic although the occurrence of populations with 1:1 style-morph ratios suggest that, like heterostyly and dimorphic enantiostyly, they are maintained by disassortative mating. We interpret these sexual polymorphisms as floral designs that increase the precision of cross-pollination and reduce lost mating opportunities associated with self-interference, especially geitonogamy. A single adaptive explanation based on frequency-dependent male mating proficiency can explain the evolution and maintenance of the four stylar polymorphisms in plants.
Many species expanded their geographic ranges from core "refugium" populations when the global climate warmed after the Pleistocene. The bottlenecks that occur during such range expansions diminish genetic variation in marginal populations, rendering them less responsive to selection. Here, we show that range expansion also strongly depletes inbreeding depression. We compared inbreeding depression among 20 populations across the expanded range of a common European plant, and found that marginal populations had greatly reduced inbreeding depression. Similar patterns were also revealed by multilocus computer simulations. Low inbreeding depression is predicted to ease conditions for the evolution of self-fertilization, and selfing is known to be particularly frequent in marginal populations. Therefore, our findings expose a remarkable aspect of evolution at range margins, where a history of expansion can reverse the direction of selection on the mating system, providing a parsimonious explanation for the high incidence of selfing in marginal populations.
Classical models studying the evolution of self-fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed-plant species are reported to have rates of self-fertilization between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self-fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self-fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing-rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution.
The transition from outcrossing to self-fertilization is one of the most common evolutionary trends in plants. Reproductive assurance, where self-fertilization ensures seed production when pollinators and/or potential mates are scarce, is the most long-standing and most widely accepted explanation for the evolution of selfing, but there have been few experimental tests of this hypothesis. Moreover, many apparently adaptive floral mechanisms that ensure the autonomous production of selfed seed might use ovules that would have otherwise been outcrossed. This seed discounting is costly if selfed offspring are less viable than their outcrossed counterparts, as often happens. The fertility benefit of reproductive assurance has never been examined in the light of seed discounting. Here we combine experimental measures of reproductive assurance with marker-gene estimates of self-fertilization, seed discounting and inbreeding depression to show that, during 2 years in 10 Ontario populations of Aquilegia canadensis (Ranunculaceae), reproductive assurance through self-fertilization increases seed production, but this benefit is greatly outweighed by severe seed discounting and inbreeding depression.
Flower colour polymorphism (FCP) is frequently associated with differences in pollinator attraction. FCP maintenance is intriguing, as positive directional selection by pollinators should result in the loss of polymorphism. Autonomous selfing could confer reproductive assurance when pollen is limited, and could be a mechanism for maintaining polymorphism unless inbreeding depression is high. We study the role of selfing in maintaining FCP in Lysimachia arvensis, a species with blue and red morphs co-occurring in Mediterranean populations, where pollinators negatively select for the red morph. We experimentally assessed inbreeding depression in both morphs in two Mediterranean populations and genetic diversity was studied via AFLP and SSR microsatellites in 20 populations. Between-morph genetic differentiation was high and the red morph had a lower genetic diversity, mainly in the Mediterranean. Results also show strong phenological differences between selfed and outcrossed progeny, and a high ID of the red morph. The low genetic diversity of the red morph is in concordance with a reproductive system based predominantly on selfing. However, ID suggests a limited capacity for red morph recruitment, according to its low frequency in polymorphic populations. Genetic differentiation between morphs indicates a low gene flow between them, opening the possibility of reproductive isolation and speciation in Lysimachia arvensis.
Floral colour determines pollinator behaviour, strongly affecting plant-mating systems. Lysimachia arvensis has blue- and red-flowered plants and colour inheritance remains largely unknown. A control of floral colour based on one locus, with the red allele as dominant, has been proposed. This proposal cannot explain the sporadic appearance of other floral colours in wild populations. We studied floral colour segregation in L. arvensis and assessed the possibility that pollinators can visually distinguish colour morphs by using Chittka’s hexagon model, sigmoidal model of bee discrimination and experimental studies on pollinator attendance for two years. Hand crossing between morphs originated a homogeneous F1 with salmon-coloured flowers. In the F2, blue, red, salmon morphs and other plants with intermediate colours appeared, suggesting that more than one single locus are involved in colour segregation. Results from the sigmoidal discrimination model suggest that blue, red and salmon flowers can be discriminated by pollinators. In fact, pollinators showed strong colour constancy and discriminated against the salmon morph. Our study shows that "Flower colour" is a natural marker to assess the rate of crossing between morphs. The extreme rarity of salmon flowers in wild populations and flower constancy of L. arvensis pollinators indicates assortative mating.
Herkogamy, spatial separation between stigma and anthers within a flower, is important in regulating plant‐mating systems. We studied phenotypic variation and heritability of herkogamy traits in Lysimachia arvensis (=Anagallis arvensis) that show both lateral and vertical herkogamy in the same flower, a rare strategy in flowering plants. Both lateral and vertical herkogamy showed continuous variation in 15 natural populations. Lateral herkogamy, measured as the angle between style and stamens, ranged from 5.6 to 66.5°; vertical herkogamy ranged from reverse to approach herkogamy. Herkogamy traits were constant within plants but variable among plants and populations. Flowers with marked lateral herkogamy showed mainly reverse herkogamy, whereas flowers with low lateral herkogamy showed mainly approach herkogamy. Both herkogamy traits showed a high degree of narrow sense heritability (h2 = 0.843 for lateral and h2 = 0.635 for vertical herkogamy). We discuss the possibility that variation in both herkogamy traits among populations of L. arvensis is a consequence of differential selective pressures under different pollination environments. Lysimachia arvensis shows two consecutive types of herkogamy in the same flower, a very rare fact in flowering plants. Both herkogamy types showed a continuous variation, were very variable among plants and populations and showed a high degree of narrow sense heritability. Variation in both herkogamy traits among populations could be a consequence of differential selective pressures under different pollination environments.
Premise of research. Phenotypic traits that consistently mediate species’ responses to environmental variation (functional traits) provide a promising approach toward generalizing ecological and evolutionary patterns and thereby gaining insights into the processes generating them. In the plant functional ecology literature, most trait-based studies have focused on traits mediating either resource competition or responses to variation in the abiotic environment, while traits mediating reproductive interactions have often been neglected. Methodology. Here, I discuss the value of herkogamy, the spatial separation of male and female functions in flowers, as a functional trait in plant reproductive biology and review the evidence relevant to the hypothesis that taxa exhibiting greater herkogamy have historically experienced more reliable pollination and more outcrossed mating systems. Pivotal results. A large body of work in the field of plant reproductive biology has identified a set of nearly ubiquitous correlations between average herkogamy and features of plant mating systems, notably, autofertility (seed set in the absence of pollinators) and outcrossing rate. Herkogamy often varies extensively among populations and species, and the adaptive interpretation is that herkogamy exhibits local adaptation to the reliability of the pollination environment. Conclusions. These results underline the value of herkogamy as a functional trait representing variation in mating histories. Many important insights are likely to emerge from studies leveraging herkogamy as an easily measured proxy of plant mating systems, as already demonstrated in comparative studies and studies of reproductive interactions. Greater consideration of herkogamy and other reproductive-function traits in studies of species coexistence may provide a more complete understanding of community assembly processes.
We inferred Lloyd's modes of selfing in a natural population of the common monkeyflower, Mimulus guttatus. Estimates were obtained using floral manipulations combined with seed counts and isozyme analyses of selfing rates. Of the 25% selfing estimated from isozyme markers, about one-half was competing, about one-third was geitonogamous, and at least one-fifth (perhaps twice this) was due to biparental inbreeding. Estimates of prior and delayed selfing were small and did not significantly differ from zero. These results were obtained using plants with the characteristic pair of open flowers at an inflorescence node. The second-opening flower showed twice the rate of selfing, presumably because of protogynous-based geitonogamy differences. Solitary-flowered plants, which have smaller flowers but no geitonogamy, showed about 50% selfing, consisting of about equal components of competing selfing and biparental inbreeding. While geitonogamy and biparental inbreeding might be unavoidable by-products of adaptations for outcrossing, competing selfing is subject to more direct natural selection and warrants adaptive explanations.
A century of research on heterostylous plants has passed since the publication of Charles Darwin's book "The Different Forms of Flowers on Plants of the Same Species" in 1877 summarizing his extensive observations and experiments on these complex breeding systems involving genetic polymorphisms of floral sex organs. Since then heterostylous plants have provided a rich source of material for evolutionary biologists and today they represent one of the classic research paradigms for approaches to the study of evolution and adaptation. The present book is the first modern and comprehensive accont of the subject. In 10 chapters it is concerned with the evolution, genetics, development, morphology, and adaptive significance of heterostyly. Broad syntheses of research on heterostyly as well as new theoretical ideas and experimental data are included.
Capacity for autonomous self-fertilization provides reproductive assurance, has evolved repeatedly in the plant kingdom, and typically involves several changes in flower morphology and development (the selfing syndrome). Yet, the relative importance of different traits and trait combinations for efficient selfing and reproductive success in pollinator-poor environments is poorly known. In a series of experiments, we tested the importance of anther-stigma distance and the less studied trait anther orientation for efficiency of selfing in the perennial herb Arabis alpina. Variation in flower morphology among eight self-compatible European populations was correlated with efficiency of self-pollination and with pollen limitation in a common-garden experiment. To examine whether anther-stigma distance and anther orientation are subject to directional and/or correlational selection, and whether this is because these traits affect pollination success, we planted a segregating F2 population at two native field sites. Selection strongly favored a combination of introrse anthers and reduced anther-stigma distance at a site where pollinator activity was low, and supplemental hand-pollination demonstrated that this was largely because of their effect on securing self-pollination. The results suggest that concurrent shifts in more than one trait can be crucial for the evolution of efficient self-pollination and reproductive assurance in pollinator-poor habitats. This article is protected by copyright. All rights reserved.
The evolutionary and functional relationships among breeding systems and floral morphology were investigated in the Turnera ulmifolia complex. Predictions of a model of breeding system evolution among distylous and homostylous varieties were tested. Chromosome counts of 73 accessions revealed an association between breeding system and chromosome number. Diploid and tetraploid populations of five taxonomic varieties are distylous and self-incompatible, whereas hexaploid populations of three varieties are homostylous and self-compatible. The latter occur at different margins of the geographical range of the complex. Crossing studies and analyses of pollen and ovule fertility in F1 's revealed that the three homostylous varieties are intersterile. To test the prediction that, homostylous varieties are long homostyles that have originated by crossing over within the distyly supergene, a crossing program was undertaken among distylous and homostylous plants. Residual incompatibility was observed in styles and pollen of each homostylous variety with patterns consistent with predictions of the cross-over model. The intersterility of hexaploid varieties suggests that long homostyly has arisen on at least three occasions in the complex by recombination within the supergene controlling distyly. Deviation from expected compatibility behavior occurs in populations of var. angustifolia that have the longest styles. These phenotypes displayed the greatest separation between anthers and stigmas (herkogamy) and set little seed in crosses with long- or short-styled plants. This suggests that they are derived from long homostyles with shorter length styles. It is proposed that selection for increased outcrossing has favored the evolution of herkogamy in long homostyles. Estimates of outcrossing rate in a distylous population using allozyme markers confirmed that dimorphic incompatibility enforces complete outcrossing. Significant genetic variation for floral traits likely to influence the mating system, such as stigma-anther separation, occurs within and among homostylous populations of var. angustifolia on Jamaica. Estimates of the mating system of families from a population with varying degrees of stigma-anther separation, using five isozyme loci, were heterogeneous and ranged from t = 0.04-0.79. Families exhibiting the largest mean stigma-anther separation have higher outcrossing rates than those with little separation.
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.
The amounts of inbreeding depression upon selfing and of heterosis upon outcrossing determine the strength of selection on the selfing rate in a population when this evolves polygenically by small steps. Genetic models are constructed which allow inbreeding depression to change with the mean selfing rate in a population by incorporating both mutation to recessive and partially dominant lethal and sublethal alleles at many loci and mutation in quantitative characters under stabilizing selection. The models help to explain observations of high inbreeding depression (> 50%) upon selfing in primarily outcrossing populations, as well as considerable heterosis upon outcrossing in primarily selfing populations. Predominant selfing and predominant outcrossing are found to be alternative stable states of the mating system in most plant populations. Which of these stable states a species approaches depends on the history of its population structure and the magnitude of effect of genes influencing the selfing rate.
Charles Darwin was fascinated by the phenomenon of heterostyly. He described (1862, 1877) how he first thought that pin and thrum plants of Primula species represented female and male sexes respectively, but found that they were both functionally hermaphroditic. He demonstrated the infertility of self-pollinations and crosses between plants of the same form, and concluded that the two forms, although hermaphrodites, are “related to each other like males and females… [because plants of each form]… must unite with one of the other form” (Darwin 1862)3.
In outcrossing hermaphrodite plants, the separate functions of pollen dispersal and pollen receipt may interfere with one another so that fitness as a paternal or maternal parent is compromised (van der Pijl, 1978; Bawa and Opler, 1975; Lloyd and Yates, 1982; Lloyd and Webb, 1986; Webb and Lloyd, 1986; Bertin and Newman, 1993; Harder and Barrett, 1995). This is particularly likely in flowers in which the sex organs are close together and mature at the same time. Interference can potentially take several forms, including the obstruction by pistils of efficient pollen dispatch by pollinators, stamens restricting access by pollinators to stigmas, thus reducing pollen deposition, and the deleterious effects of self-pollination on maternal function due to stigmatic, stylar, or ovular clogging. Although there is some experimental evidence for self-pollen interference (Shore and Barrett, 1984; Barrett and Glover, 1985; Bertin and Sullivan, 1988; Palmer et al., 1989; Waser and Price, 1991; Scribailo and Barrett, 1994), the other two forms of pollen-pistil interference have seldom been investigated (see, however, Barrett and Glover, 1985; Kohn and Barrett, 1992a).
Pollination becomes a constraint when conspecific plants and/or their pollinators become scarce. Many plant species have evolved autogamous self-pollination as a means of reproductive assurance (RA) under pollination-uncertain environments. So far RA has been studied and discussed largely with reference to self-compatible species producing bisexual flowers. RA seems to have evolved across all other sexual and breeding systems - monoecy, dioecy and self-incompatibility (SI). Both monoecy and dioecy produce bisexual flowers (andro/gyno-monoecy, andro/gynodioecy and polygamous conditions) which may provide RA. Similarly, most of the SI species are leaky and do set some seeds upon self-pollination. This phenomenon termed 'partial self-compatibility' is quite common and does provide RA in SI species. Although dioecy and SI have evolved as obligate outbreeding systems, they seem to have reached an evolutionary dead end because of the constraints for outcross pollination. In the light of habitat destruction leading to a reduction in the diversity and density of native pollinators, it is likely that many of the obligate outbreeders tend to shift to mixed mating system in the coming decades. Similarly, obligate mutualism in which each plant species is dependent on one animal species for pollination also seems to have reached a dead end and the trend is to abandon such obligate mutualism as a survival strategy. In the absence of such a change, obligate outbreeders and those with highly specialized pollination system are likely to become endangered or even extinct.
We recognize four major classes of stylar polymorphisms in flowering plants: the heterostylous conditions distyly and tristyly,
stigma-height dimorphism, and enantiostyly. These polymorphisms differ in the relative positions of sexual organs and in the
number of floral morphs that occur within populations. In heterostyly, stigma and anther heights are reciprocally positioned
in the two or three floral morphs; in stigma-height dimorphism the two morphs vary in style length but not anther height;
whereas in enantiostyly, flowers differ in whether the style is deflected to the left- or right-side of the flower. We distinguish
two forms of enantiostyly depending on whether both style orientations occur on the same plant (monomorphic enantiostyly)
or on different plants (dimorphic enantiostyly). Stylar polymorphisms have originated independently in numerous animal-pollinated
flowering plant families. Both heterostyly and enantiostyly involve distinct floral syndromes suggesting functional convergence
in which the position of the pollinator is important for pollen dispersal and male reproductive success. The function of stigma-height
dimorphism remains enigmatic although the occurrence of populations with 1:1 style-morph ratios suggest that, like heterostyly
and dimorphic enantiostyly, they are maintained by disassortative mating. We interpret these sexual polymorphisms as floral
designs that increase the precision of cross-pollination and reduce lost mating opportunities associated with self-interference,
especially geitonogamy. A single adaptive explanation based on frequency-dependent male mating proficiency can explain the
evolution and maintenance of the four stylar polymorphisms in plants.
Sympatric congeneric species of flowering plants are precluded from freely exchanging genes by reproductive barriers which are operative prior to pollination, between pollination and fertilization and after fertilization. The barriers may be the by-products of divergent evolution, or may have been selected for their ability to reduce hybridization and disruptive gene flow, or competition for similar elements of the pollinator fauna. Autogamy and hybrid floral isolation are included in a classification of reproductive isolating barriers. The origin of reproductive barriers is discussed in light of new information and insight on pollinator behavior and perception, the S-gene complex, pollen-tube competition, and population level selection. It is suggested that reproductive barriers are not inherent properties of species, but reside in the interface between species, and arise from the incongruities in the reproductive formats of species paired in nature or by the systematist.
The amounts of inbreeding depression upon selfing and of heterosis upon outcrossing determine the strength of selection on the selfing rate in a population when this evolves polygenically by small steps. Genetic models are constructed which allow inbreeding depression to change with the mean selfing rate in a population by incorporating both mutation to recessive and partially dominant lethal and sublethal alleles at many loci and mutation in quantitative characters under stabilizing selection. The models help to explain observations of high inbreeding depression (>50%) upon selfing in primarily outcrossing populations, as well as considerable heterosis upon outcrossing in primarily selfing populations. Predominant selfing and predominant outcrossing are found to be alternative stable states of the mating system in most plant populations. Which of these stable states a species approaches depends on the history of its population structure and the magnitude of effect of genes influencing the selfing rate.
1. Flower colour polymorphism is traditionally attributed to pollinator selection although other factors, such as indirect selection on correlated traits, can play an important role.
2. Lysimachia arvensis is a widespread annual species with two colour morphs differing in anthocyanin composition. We explored the hypothesis that colour polymorphism is maintained by selection related to environmental heterogeneity. Morph frequencies and environmental traits were recorded in 51 populations along a wide geographical range. To explore the existence of morph-by-environment interactions, we conducted an experimental study comparing the two morphs under treatments differing in water and light availability.
3. A geographical pattern was found with a negative association between blue frequencies and latitude. The proportion of the blue morph increased with temperature and sunshine hours, but decreased with precipitation. Flowering onset and flower size differed between morphs and scarcely varied across treatments. In contrast, several fitness components such as germination, seedling survival, seedling mass and flower production showed important morph-by-environment interactions. The blue morph showed higher overall male and female fitness in all the treatment combinations excepting in sun-wet conditions where the red morph had higher fitness.
4. Synthesis. Our results indicate that the mechanism of selection on flower colour seems to be related to differences in fitness of both morphs due to abiotic factors. These differences could explain the geographical distribution of flower colour morphs and the maintenance of the colour polymorphism. The marked difference in flowering time between morphs leaves open the potential for assortative mating and speciation in Lysimachia arvensis.
In closely related plant species that display strong similarities in phenology and pollinator communities, differences in breeding system and associated shifts in floral traits may have important effects on the magnitude and direction of heterospecific pollen flow and hybridization. Here, we quantified the strength of several pre- and postzygotic barriers acting between the facultatively outcrossing Centaurium erythraea and the predominantly selfing C. littorale via a suite of experiments, and estimated the frequency of hybridization in the field using molecular markers. The reproductive barriers primarily responsible for preventing hybridization were essentially prezygotic and these acted asymmetrically. Due to differences in floral display, pollen production and pollen transfer rates, heterospecific pollen flow occurred predominantly from C. erythraea to C. littorale. In C. littorale, on the other hand, close anther-stigma positioning and resulting higher capacity for autonomous selfing functioned as an efficient barrier to counterbalance the higher risk for hybrid mating. In both species the action of all reproductive barriers resulted in a small opportunity for hybrid establishment, which was confirmed by the occurrence of only ∼1% putative hybrids in the field. Our findings confirm that differences in breeding system affect heterospecific pollen transfer patterns and that autonomous selfing may efficiently prevent hybridization. This article is protected by copyright. All rights reserved.
Outline The assurance of reproduction when outcrossing is unpredictable is a venerable and widely invoked explanation for uniparental reproduction via self-fertilization or asexuality. This hypothesis is supported by evidence that seed production by outcrossing plants is frequently pollen limited. How- ever, its intuitive simplicity belies its considerable complexity. Theory cautions that selfing may increase geometric mean fitness in unpredictable pollination environments, but may also compromise current and future outcrossing through physiological and demographic trade-offs. Moreover, reproductive assurance (RA) may affect population and metapopulation dynamics, introducing complex feedbacks plus alternative equilibria and multiple levels of selection. Experimental manipulations of pollination and mating have tested whether RA explains widespread mixed-mating systems, although definitive evidence of this is still lacking. Species exhibiting geographic variation in floral traits have been exploited to determine the role of RA in transitions between outcrossing and selfing, a very common evolutionary trend in plants. Transplant experiments are particularly useful for detecting divergent selection on floral traits underlying mating-system variation. Recent work by our research group suggests that small, selfing flowers benefit from RA by avoiding parasitism rather than pollen limitation, empha- sizing that self-pollination and associated floral traits can ameliorate an array of ecological pressures faced by outcrossing plants. Although evolution of asexuality and selfing can be studied using a common theoretical framework, whether asexuality evolves because it provides RA remains virtually unstudied. Wide variation in sexuality within diverse species provides underexploited opportunities for experi- mentation, which could ultimately provide a better understanding of the general role of RA in plant reproductive evolution.
Dichogamy is the separation of the presentation of pollen and stigmas in time within a plant. It is a common but neglected feature of outcrossing angiosperms. Dichogamy has been almost universally interpreted as an outcrossing mechanism, but many dichogamous species are also self-incompatible (and sometimes also herkogamous and/or with unisexual flowers). In outcrossing species, there is almost invariably a clash between selection to place pollen and stigmas in similar positions for effective pollination and selection to keep the androecia and gynoecia apart to avoid interference between them. We suggest that the separation of pollen and stigmas acts in general to reduce this self-interference and it often also reduces self-fertilisation. Mechanisms preventing self-fertilisation primarily increase maternal fitness, whereas mechanisms avoiding self-interference primarily promote paternal fitness.Five independent ways of subdividing dichogamy are recognised: protandry or protogyny; intrafloral or interfloral dichogamy; complete or incomplete dichogamy; various intervals between the successive presentations of pollen and stigmas; asynchronous, hemisynchronous, or synchronous dichogamy (the latter of several subtypes). In a sample of British species, protandry is almost twice as common as protogyny in biotically pollinated species but protogyny is six times as common as protandry in abiotically pollinated species.To obtain testable hypotheses of the selective forces responsible for dichogamy, four selective forces that influence whether pollen or stigmas are presented first are examined. (1) Effectiveness in avoiding self-fertilisation; (2) Selection for prolonged pollen presentation; (3) Optimal positions for dispatching and receiving pollen; (4) Interference between stamens and carpels, involved in seven different contexts: (a) The relative ease of moving androecia and gynoecia; (b) Vertical wind-pollinated inflorescences; (c) Vertical animal-pollinated inflorescences; (d) Refuge, trap, and brood blossoms; (e) One type of sporophyll facilitates the presentation of the other; (f) Stamen signals or rewards; (g) Post-presentation changes in flowers. The most important factor overall may be the relative ease of moving stamens and carpels after they have functioned. For many species there may be a combination of selective causes of the direction of dichogamy.Besides pollen-stigma interference, other types of interference (in which two activities obstruct each other because they have the same optima) and conflicts (in which two activities have divergent optima) occur in plants.
Procedures are described for partitioning the selfing rate into contributions resulting from the different modes of chasmogamous selfing (geitonogamous, facilitated, prior, competing, and delayed) and for examining several functional aspects of self-fertilization associated with the different modes (reproductive assurance, degree of seed and pollen discounting, and relative abilities of cross- and self-pollen to fertilize ovules). The procedures involve floral manipulations, eg exclusion of pollinators, emasculation, and covering of stigmas. The method of partitioning selfing into modes is illustrated using data from a natural population of the annual plant Impatiens pallida. Selfing in the chasmogamous flowers of this species results primarily from geitonogamy. -from Authors
Presents a phenotypic model of the selection of self-fertilization that applies to any mode of self-pollination. A novel factor, seed discounting (loss of outcrossing maternal fitness accompanying an increase in self-fertilization) is introduced, and pollen discounting is reformulated. The model incorporates the effects of five principal factors - the cost of meiosis, inbreeding depression, reproductive assurance, and seed and pollen discounting. Either complete cross- or self-fertilization is selected, depending on the values of the parameters, but a number of additional factors can lead to intermediate frequencies of self-fertilization. Specific conditions for the selection of each mode of chasmogamous self-pollination and the effects of some special circumstances are derived by substituting the appropriate values of seed and pollen discounting in the general model. Geitonogamy and facilitated selfing are primarily nonadaptive by-products of mechanisms for outcrossing. Delayed selfing is most advantageous, but competing and prior selfing may be selected when structural constraints prevent delayed selfing or the prepotency of outcrossed pollen reduces seed discounting. The model predicts environmental modification of the frequency of self-fertilization and can explain the observed associations between frequent self-fertilization and both the annual habitat and poor conditions for cross-pollination. -Author
The fitnesses of two phenotypes which differ in their frequency of self-fertilization are expressed exactly in terms of various parameters, including the relative fitness of progeny from selfing, i, and the proportion of available ovules fertilized with the aid of an external agent, e. Strategic models of natural selection find stationary conditions where the two phenotypes have the same fitness. Conditions when selfing is advantageous to populations and to individuals are not usually identical. Conditions favoring self-fertilization are more stringent when selfing competes with crossing (for individual selection, i > 1/2) and less stringent when selfing occurs prior to crossing (i > e/2). When selfing is delayed until after all opportunities for crossing, it is always advantageous if the parameters vary independently. Some functional interactions between parameters, as when an increase in selfing simultaneously reduces the efficiency of external pollinating agents, result in stationary conditions with mixed self- and cross-fertilization under certain conditions. Following a change in the level of self-fertilization, certain evolutionary adjustments increase the advantage of the acquired mode of fertilization. The models demonstrate that the evolution of various levels of self-fertilization in plants can be explained by individual selection without recourse to postulates of long-term advantages to populations.
Herkogamy is the spatial separation of pollen presentation and pollen receipt within or between blossoms of an individual plant. Several classes of herkogamy are recognised; these are defined by whether all blossoms are identical (homomorphic herkogamy), all blossoms dispatch and receive pollen but reciprocal forms occur (reciprocal herkogamy), or some or all blossoms perform only one function (interfloral herkogamy). Within homomorphic herkogamy, unordered herkogamy, in which pollinator contacts with stigmas and pollen within a blossom are many and occur in no particular sequence, is distinguished from ordered herkogamy in which contacts are few and ordered. For ordered herkogamy further divisions are based on the operation of the pollination mechanism.Herkogamy is usually interpreted as a mechanism which reduces self-fertilisation and promotes outcrossing. However, as many herkogamous plants are also self-incompatible, it is suggested that the various classes of herkogamy also function in part or solely as mechanisms which avoid interference between pollen receipt by stigmas and pollen dispatch from anthers. Although for herkogamous blossoms these two functions are separated in space, many such flowers control pollinator behaviour so that both pollination surfaces are contacted during a single visit. In dichogamous blossoms separation of pollen dispatch and receipt is temporal rather than spatial and this difference has several important consequences for the pollination biology of dichogamous and herkogamous blossoms.
Controlled pollination experiments were performed on the self-incompatible distylous herb Turnera ulmifolia L. to investigate the effects of pollination intensity and large amounts of incompatible pollen on seed set. In the first experiment, known numbers of compatible pollen grains ranging from 1 to 100 were applied to stigmas of the floral morphs. In both morphs, increasing amounts of pollen generally resulted in increased levels of seed set, although considerable variance was observed at all pollination intensities. Approximately two to seven pollen grains are required to produce a single seed and more than 95 grains are required to achieve maximum seed set in T. ulmifolia. Regression analysis of the seed set data failed to detect a difference in the response of the floral morphs to pollination intensity. In the second experiment, known proportions of compatible and incompatible pollen were applied to stigmas at various time intervals. Most treatments involving mixtures of compatible and incompatible pollen had no significant effect on seed set when compared with the controls. Clogging was only observed in the long-styled morph when one anther of compatible pollen was applied to stigmas 1.5 and 3.0 h after pollination with five anthers of incompatible pollen. The clogging of stigmas by incompatible pollen seems unlikely to have played a major role in the evolution and maintenance of distyly in Turnera ulmifolia.
Selfing, the fusion of male and female gametes from a single genetic individual or colony, is possible in many plants and also in hermaphrodite animals. We review the occurrence of selfing and mechanisms for its avoidance, in functionally hermaphrodite animal and plants. We discuss means by which selfing can be detected and briefly review techniques for estimation of selfing frequencies in natural populations. Although many functionally hemaphrodite species are probably almost complete outcrossers or inbreeders, mixed mating systems are also found in both plant and animal populations. We review theories for the advantages and disadvantages of selfing, and for the maintenance of mixed mating systems, together with empirical data showing that at least some of the factors involved in the theories (for instance, reproductive assurance, cost of mating, and inbreeding depression) are detectable in actually or potentially selfing organisms. More work is still needed on animal selfing and selfing avoidance and, for both animals and plants, on the evolutionary origins of selfing and on the effects of selfing on genetic diversity.
New combinations are proposed for species of Anagallis, Pelletiera and Trientalis in accordance with the results of phylogenetic analyses of the Lysimachia complex, based on molecular and morphological data. These three genera as well as Glaux and Asterolinon, for the species of which names in Lysimachia are already available, have been found to be derived, specialized groups that have evolved within Lysimachia. The present classification therefore does not reflect our current understanding of evolutionary relationships within the Lysimachia complex. Merging all the genera in Lysimachia is here considered better than splitting the latter into several smaller genera. For Anagallis crassifolia and A. filifolia new names are validated and for A. alternifolia and A. pumila the names change since their epithets have already been used in Lysimachia. Lectotypes are selected for A. filifolia, A. filiformis, A. kingaënsis, A. monelli, A. schliebenii, A. serpens and Pelletiera verna, and a neotype is designated for A. foemina.
1. Human-induced impoverishment of pollinator faunas may affect plant–pollinator interactions and limit pollen availability. Under these conditions, chronic outcross pollen limitation is expected to select for floral characters that maintain seed production, including autonomous selfing.
2. In this study, the impact of anthropogenic disturbances of the pollinator environment of the short-lived Centaurium erythraea on mating patterns was investigated. First floral traits and the capacity for autonomous selfing were compared between two contrasting pollinator environments. In addition, transplantation experiments were combined with hand-pollination and emasculation treatments to assess the extent of pollen limitation and the contribution of autonomous selfing to total seed production in these pollinator environments.
3. Under severe pollinator impoverishment, C. erythraea produced fewer and smaller flowers that showed no herkogamy and strongly reduced P/O ratios. The capacity for autonomous selfing was 36·1% higher in these pollinator-limited environments than in more natural, pollinator-rich environments, where plants developed more, larger and markedly herkogamous flowers.
4. When assigned to the pollinator-rich environments, plants from pollinator-limited populations showed significantly higher outcross pollen limitation compared with the original plants. In contrast, plants from pollinator-rich environments assigned to pollinator-poor populations did not experience higher pollinator-mediated seed production and showed lower total seed production than plants originally occurring in these pollinator-limited environments.
5. These results demonstrate that human-induced pollen limitation selects for selfing as a means of reproductive assurance, whereas in the pollinator-rich environments, traits that support outcrossing are favoured.
Competition for pollination may occur between pollinator-sharing sympatric plants and this may cause character displacement of their floral traits. We examined this possibility by comparing flower morphology of the sympatric population of Clerodendrum trichotomum and its co-flowering congener, C. izuinsulare, with that of the allopatric populations. The two species were visited in common by such insects as diurnal hawkmoths, bees, swallowtails and nocturnal hawkmoths, and were pollinated nocturnally as well as diurnally. Interspecific pollen transfer can occur by sharing pollinators; however, they did not hybridize when artificially pollinated. Flower size, including stamen and style lengths, is larger in C. trichotomum with an overlap in range. The style of C. izuinsulare in the sympatric population was significantly shorter than that in the allopatric population, while there was no significant difference in style length between the allopatric and the sympatric C. trichotomum. This seems to facilitate avoidance of interspecific pollen transfer in the sympatric population.
Many functional (ecological, morphological, and physiological) factors affect the occurrence of self-fertilization. Six modes of self-pollination are distinguished. These differ in whether they utilize specialized flowers, whether they involve the transfer of pollen within or between flowers, whether they are autonomous or mediated by vectors, and their timing relative to opportunities for outcrossing. Various modes of selfing are subject to different structural constraints. Prepotency, the preferential success of cross-pollen in achieving fertilizations when it competes with self-pollen, influences the frequency of self-fertilization in some species. The amount of self-fertilization may depend on environmental conditions and the vector species visiting each flower and may vary among the flowers of one plant. To gain information on the prevalence of autonomous self-pollination, 66 species for which the degrees of self-compatibility and autofertility (seed set in isolation) have been published were surveyed. Partially self-incompatible species(in which the seed set is lower after self-pollination than after separate outcrosses) have on average lower autofertility than self-compatible species (in which self- and cross-pollinations succeed equally well), but some partially self-incompatible species have considerable autofertility and some self-compatible species have none. A number of features of floral morphology and phenology are associated with high autofertility indices. -Authors
Sympatric sister species are predicted to have greater divergence in reproductive traits than allopatric sister species, especially if mating system shifts, such as the evolution of self-fertilization, are more likely to originate within the geographic range of the outcrossing ancestor. We present evidence that supports this expectation-sympatric sister species in the monkeyflower genus, Mimulus, exhibit greater divergence in flower size than allopatric sister species. Additionally, we find that sympatric sister species are more likely to have one species with anthers that overtop their stigmas than allopatric sister species, suggesting that the evolution of automatic self-pollination may contribute to this pattern. Potential mechanisms underlying this pattern include reinforcement and a stepping stone model of parapatric speciation.
Evolutionary theory predicts that interactions between species such as resource competition or reproductive interference will generate selection for character displacement where similar species co-occur. However, the rate and direction of character displacement will depend not only on the strength of selection for trait divergence, but also on the amount of genetic variation for selected traits and the nature of genetic correlations between them. To assess the importance of genetic constraints for the evolution of character displacement, we examined the genetic architecture of a suite of floral traits previously shown to be under selection in the annual plant Ipomoea hederacea when this species co-occurs with Ipomoea purpurea. We found that the six floral traits we measured are all positively genetically correlated. We also demonstrate, using new statistical approaches, that the predicted response to selection for four of these six traits is substantially constrained by their genetic correlation structure. Most notably, the response to selection for reduced separation of the tallest and shortest anthers, which reduces the degree of detrimental heterospecific pollen flow, is substantially constrained. Our results suggest that the rate of evolution of reproductive character displacement in I. hederacea is limited by the genetic architecture of floral traits.
A polymorphism for anthocyanin production was used as a genetic marker to document the relationship between anther-stigma separation and outcrossing rate in the predominantly self-fertilizing weed Datura stramonium. White-flowered plants that differed in anther-stigma separation were placed into populations consisting exclusively of purple-flowered plants. Self vs. outcross origin of progeny was evident in the hypocotyl color of the seedlings. Outcrossing rates measured for single flowers were significantly positively correlated with anther-stigma separation, albeit with some scatter around the regression line, especially for flowers with exserted stigmas. We also performed an 8 × 8 diallel cross to determine whether anther-stigma separation is genetically determined. Heritability in two field plots was ∼0.3 and in the greenhouse was ∼0.2. Maternal effects, epistasis, and dominance appeared to be relatively unimportant. Genotypes performed consistently across the three environments, although total plant size varied more than fivefold. It appears that the mixed-mating system of D. stramonium has a heritable basis and would be capable of responding to selection.