Opposing effects of plant traits on diversification.

Species diversity can vary dramatically across lineages due to differences in speciation and extinction rates. Here, we explore the effects of several plant traits on diversification, finding that most traits have opposing effects on diversification. For example, outcrossing may increase the efficacy of selection and adaptation but also decrease mate availability, two processes with contrasting effects on lineage persistence. Such opposing trait effects can manifest as differences in diversification rates that depend on ecological context, spatiotemporal scale, and associations with other traits. The complexity of pathways linking traits to diversification suggests that the mechanistic underpinnings behind their correlations may be difficult to interpret with any certainty, and context dependence means that the effects of specific traits on diversification are likely to differ across multiple lineages and timescales. This calls for taxonomically and context-controlled approaches to studies that correlate traits and diversification.

Sex-specific selection patterns in a dioecious insect-pollinated plant.

Competition for mate acquisition is the hallmark of any sexual organism. In insect-pollinated plants, competition to attract pollinators is expected to result in pollinator-mediated selection on attractive floral traits. This could overlap with sexual selection if the number of mating partners increases with pollinator attraction, resulting in an improved reproductive success. In this study, we measured a set of floral traits and estimated individual fitness in male and female Silene dioica in an experimental population. Results align with the predictions of Bateman's principles, in the absence of pollen limitation. In females, natural selection acted on traits that are typically linked with fertility (number of flowers and number of gametes), and selection strength was similar in open- and hand-pollinated females, suggesting a limited role of pollinator-mediated selection. In males, flowering duration and corolla width were positively associated with both reproductive success and number of mates, suggesting that sexual selection has played a role in the evolution of these traits. The use of Bateman's metrics further confirmed stronger sexual selection in males than in females. Taken together, our results shed light on the occurrence of sex-specific patterns of selection in an insect-pollinated plant population.

On the function of flower number: disentangling fertility from pollinator-mediated selection.

In animal-pollinated angiosperms, the 'male-function' hypothesis claims that male reproductive success (RS) should benefit from large floral displays, through pollinator attraction, while female RS is expected to be mainly limited by resource availability. As appealing as this theory might be, studies comparing selection strength on flower number in both sexes rarely document the expected asymmetry. This discrepancy could arise because flower number impacts both pollinator attraction and overall gamete number. In this study, we artificially manipulate floral displays to disentangle the fertility versus pollinator attraction components of selection, both in terms of mating and RS. In females, flower number was under strong fertility selection, as predicted in the absence of pollen limitation. By contrast, in males, flower number was mainly under sexual selection, which in turn increased male RS. However, these selection patterns were not different in males with artificially increased floral displays. This suggests that sexual selection acting on flower number in males does not occur because flower number increases pollinator attraction, but rather because more pollen is available to disperse on more mates. Our study illustrates the power of disentangling various components of selection with potentially sex-specific effects for understanding the evolution of sexual dimorphism.

Ozone Pollution Alters Olfaction and Behavior of Pollinators.

Concentration of air pollutants, particularly ozone (O3), has dramatically increased since pre-industrial times in the troposphere. Due to the strong oxidative potential of O3, negative effects on both emission and lifetime in the atmosphere of plant volatile organic compounds (VOCs) have already been highlighted. VOCs alteration by O3 may potentially affect the attraction of pollinators that rely on these chemical signals. Surprisingly, direct effects of O3 on the olfaction and the behavioral response of pollinators have not been investigated so far. We developed a comprehensive experiment under controlled conditions to assess O3 physiological and behavioral effects on two pollinator species, differing in their ecological traits. Using several realistic concentrations of O3 and various exposure times, we investigated the odor antennal detection and the attraction to VOCs present in the floral scents of their associated plants. Our results showed, in both species, a clear effect of exposure to high O3 concentrations on the ability to detect and react to the floral VOCs. These effects depend on the VOC tested and its concentration, and the O3 exposure (concentration and duration) on the pollinator species. Pollination systems may, therefore, be impaired in different ways by increased levels of O3, the effects of which will likely depend on whether the exposure is chronic or, as in this study, punctual, likely causing some pollination systems to be more vulnerable than others. While several studies have already shown the negative impact of O3 on VOCs emission and lifetime in the atmosphere, this study reveals, for the first time, that this impact alters the pollinator detection and behavior. These findings highlight the urgent need to consider air pollution when evaluating threats to pollinators.

The Scope for Postmating Sexual Selection in Plants.

Sexual selection is known to shape plant traits that affect access to mates during the pollination phase, but it is less well understood to what extent it affects traits relevant to interactions between pollen and pistils after pollination. This is surprising, because both of the two key modes of sexual selection, male-male competition and female choice, could plausibly operate during pollen-pistil interactions where physical male-female contact occurs. Here, we consider how the key processes of sexual selection might affect traits involved in pollen-pistil interactions, including 'Fisherian runaway' and 'good-genes' models. We review aspects of the molecular and cellular biology of pollen-pistil interactions on which sexual selection could act and point to research that is needed to investigate them.

Polygamy or subdioecy? The impact of diallelic self-incompatibility on the sexual system in Fraxinus excelsior (Oleaceae).

How flowering plants have recurrently evolved from hermaphroditism to separate sexes (dioecy) is a central question in evolutionary biology. Here, we investigate whether diallelic self-incompatibility (DSI) is associated with sexual specialization in the polygamous common ash (Fraxinus excelsior), which would ultimately facilitate the evolution towards dioecy. Using interspecific crosses, we provide evidence of strong relationships between the DSI system and sexual phenotype. The reproductive system in F. excelsior that was previously viewed as polygamy (co-occurrence of unisexuals and hermaphrodites with varying degrees of allocation to the male and female functions) and thus appears to actually behave as a subdioecious system. Hermaphrodites and females belong to one SI group and functionally reproduce as females, whereas males and male-biased hermaphrodites belong to the other SI group and are functionally males. Our results offer an alternative mechanism for the evolution of sexual specialization in flowering plants.

Understanding intraspecific variation of floral scent in light of evolutionary ecology.

Background and Aims: Among the various floral traits involved in pollinator attraction and potentially under selection mediated by pollinators, floral scent/fragrance has been less investigated than other components of floral phenotype. Whether or not pollinator-mediated selection impacts floral scents depends on the heritability of scent/fragrance and the occurrence of some variation within species. Although most studies have investigated how scent varies among species, growing amounts of data are available on variation at the intraspecific level. Methods: The results of 81 studies investigating intraspecific variation of floral scents in 132 taxa were reviewed. For each study, whether variation was found in either identity, proportion or absolute quantities of volatile organic compounds (VOCs) was recorded, as well as information with the potential to explain variation, such as methodology, plant origin or pollination biology. Key Results: Variation was found for almost all investigated species, both among individuals (among and sometimes within populations) and within individuals across different temporal scales. Cases in which such variation is a possible result of pollinator-mediated selection were analysed, by discussing separately selection related to variation in pollinator identity/behaviour among populations or across time, deceit pollination and sex-specific selection. Not surprisingly, in many cases, pollinator-mediated selection alone does not explain the observed variation in floral scent. This led us to review current knowledge on less investigated factors, such as selection mediated by natural enemies, genetic drift and gene flow, environmental constraints, phylogenetic inertia, or biochemical constraints that could be invoked to explain scent variation. Conclusions: This review highlights the great potential of analysing floral scent variation and including it in integrated studies of floral phenotypes. We also have identified the current gaps in our understanding of this complex signal and we propose several methodological and conceptual future directions in this research area.

Lineages of Silene nutans developed rapid, strong, asymmetric postzygotic reproductive isolation in allopatry.

Reproductive isolation can rise either as a consequence of genomic divergence in allopatry or as a byproduct of divergent selection in parapatry. To determine whether reproductive isolation in gynodioecious Silene nutans results from allopatric divergence or from ecological adaptation following secondary contact, we investigated the pattern of postzygotic reproductive isolation and hybridization in natural populations using two phylogeographic lineages, western (W1) and eastern (E1). Experimental crosses between the lineages identified strong, asymmetric postzygotic isolation between the W1 and the E1 lineages, independent of geographic overlap. The proportion of ovules fertilized, seeds aborted, and seeds germinated revealed relatively little effect on the fitness of hybrids. In contrast, hybrid mortality was high and asymmetric: while half of the hybrid seedlings with western lineage mothers died, nearly all hybrid seedlings with E1 mothers died. This asymmetric mortality mirrored the proportion of chlorotic seedlings, and is congruent with cytonuclear incompatibility. We found no evidence of hybridization between the lineages in regions of co-occurrence using nuclear and plastid markers. Together, our results are consistent with the hypothesis that strong postzygotic reproductive isolation involving cytonuclear incompatibilities arose in allopatry. We argue that the dynamics of cytonuclear gynodioecy could facilitate the evolution of reproductive isolation.

When is it worth being a self-compatible hermaphrodite? Context-dependent effects of self-pollination on female advantage in gynodioecious Silene nutans.

In gynodioecious plant species with nuclear-cytoplasmic sex determination, females and hermaphrodites plants can coexist whenever female have higher seed fitness than hermaphrodites. Although the effect of self fertilization on seed fitness in hermaphrodites has been considered theoretically, this effect is far from intuitive, because it can either increase the relative seed fitness of the females (if it leads hermaphrodites to produce inbred, low quality offspring) or decrease it (if it provides reproductive assurance to hermaphrodites). Hence, empirical investigation is needed to document whether relative seed fitness varies with whether pollen is or is not limiting to seed production. In the current study, we measured fruit set and seed production in both females and hermaphrodites and the selfing rate in hermaphrodites in two experimental patches that differed in sex ratios in the gynodioecious plant Silene nutans. We found an impact of plant gender, patch, and their interaction, with females suffering from stronger pollen limitation when locally frequent. In the most pollen-limited situation, the selfing rate of hermaphrodites increased and provided hermaphrodites with a type of reproductive assurance that is not available to females. By integrating both the beneficial (reproductive assurance) and costly effects (through inbreeding depression) of self-pollination, we showed that whether females did or did not exhibit higher seed fitness depended on the degree of pollen limitation on seed production.

How does pollination mutualism affect the evolution of prior self-fertilization? A model.

The mode of pollination is often neglected regarding the evolution of selfing. Yet the distribution of mating systems seems to depend on the mode of pollination, and pollinators are likely to interfere with selfing evolution, since they can cause strong selective pressures on floral traits. Most selfing species reduce their investment in reproduction, and display smaller flowers, with less nectar and scents (referred to as selfing syndrome). We model the evolution of prior selfing when it affects both the demography of plants and pollinators and the investment of plants in pollination. Including the selfing syndrome in the model allows to predict several outcomes: plants can evolve either toward complete outcrossing, complete selfing, or to a stable mixed-mating system, even when inbreeding depression is high. We predict that the evolution to high prior selfing could lead to evolutionary suicides, highlighting the importance of merging demography and evolution in models. The consequence of the selfing syndrome on plant-pollinator interactions could be a widespread mechanism driving the evolution of selfing in animal-pollinated taxa.

How selfing, inbreeding depression, and pollen limitation impact nuclear-cytoplasmic gynodioecy: a model.

Gynodioecy, the co-occurrence of females and hermaphrodites, is often due to conflicting interactions between cytoplasmic male sterility genes and nuclear restorers. Although gynodioecy often occurs in self-compatible species, the effect of self-pollination, inbreeding depression, and pollen limitation acting differently on females and hermaphrodites remains poorly known in the case of nuclear-cytoplasmic gynodioecy (NCG). In this study, we model NCG in an infinite population and we study the effect of selfing rate, inbreeding depression, and pollen limitation on the maintenance of gynodioecy and on sex ratios at equilibrium. We found that selfing and inbreeding depression have a strong impact, which depends on whether restorer cost acts on male or female fitness. When cost affects male fitness, the strength of cost has no effect, whereas selfing and inbreeding depression only impact gynodioecy by modifying the value of the female advantage. When cost affects female fitness, selfing facilitates NCG and reduces the role of strength of the cost, even when no inbreeding depression occurs, whereas inbreeding depression globally restricts the maintenance of the polymorphism. Finally, we found that pollen limitation could additionally strongly modify the dynamic of gynodioecy. We discuss our findings in the light of empirical data available in gynodioecious species.

How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species.

BACKGROUND: Gynodioecy is a reproductive system of interest for evolutionary biologists, as it poses the question of how females can be maintained while competing with hermaphrodites that possess both male and female functions. One necessary condition for the maintenance of this polymorphism is the occurrence of a female advantage, i.e. a better seed production or quality by females compared with hermaphrodites. Theoretically, its magnitude can be low when sterility mutations are cytoplasmic, while a 2-fold advantage is needed in the case of nuclear sterility. Such a difference is often thought to be due to reduced inbreeding depression in obligatory outcrossed females. Finally, variation in sex ratio and female advantage occur among populations of some gynodioecious species, though the prevalence of such variation is unknown. SCOPE: By reviewing and analysing the data published on 48 gynodioecious species, we examined three important issues about female advantage. (1) Are reduced selfing and inbreeding depression likely to be the major cause of female advantage? (2) What is the magnitude of female advantage and does it fit theoretical predictions? (3) Does the occurrence or the magnitude of female advantage vary among populations within species and why? CONCLUSIONS: It was found that a female advantage occurred in 40 species, with a magnitude comprised between 1 and 2 in the majority of cases. In many species, reduced selfing may not be a necessary cause of this advantage. Finally, female advantage varied among populations in some species, but both positive and negative correlations were found with female frequency. The role of reduced selfing in females for the evolution of gynodioecy, as well as the various processes that affect sex ratios and female advantage in populations are discussed.

Effects of fine-scale genetic structure on male mating success in gynodioecious Beta vulgaris ssp. maritima.

Plant mating systems are known to influence population genetic structure because pollen and seed dispersal are often spatially restricted. However, the reciprocal outcomes of population structure on the dynamics of polymorphic mating systems have received little attention. In gynodioecious sea beet (Beta vulgaris ssp. maritima), three sexual types co-occur: females carrying a cytoplasmic male sterility (CMS) gene, hermaphrodites carrying a non-CMS cytoplasm and restored hermaphrodites that carry CMS genes and nuclear restorer alleles. This study investigated the effects of fine-scale genetic structure on male reproductive success of the two hermaphroditic forms. Our study population was strongly structured and characterized by contrasting local sex-ratios. Pollen flow was constrained over short distances and depended on local plant density. Interestingly, restored hermaphrodites sired significantly more seedlings than non-CMS hermaphrodites, despite the previous observation that the former produce pollen of lower quality than the latter. This result was explained by the higher frequency of females in the local vicinity of restored (CMS) hermaphrodites as compared to non-CMS hermaphrodites. Population structure thus strongly influences individual fitness and may locally counteract the expected effects of selection, suggesting that understanding fine scale population processes is central to predicting the evolution of gender polymorphism in angiosperms.

The effect of pollen versus seed flow on the maintenance of nuclear-cytoplasmic gynodioecy.

Gynodioecy, where females co-occur with hermaphrodites, is a relatively common sexual system in plants that is often the result of a genetic conflict between maternally inherited male sterility genes in the mitochondrial genome and the biparentally inherited male fertility restorer genes in the nucleus. Previous models have shown that nuclear-cytoplasmic gynodioecy can be maintained under certain conditions by negative frequency-dependent selection, but the effect of other evolutionary processes such as genetic drift and population subdivision is only partially understood. Here, we investigate the joint effects of frequency-dependent selection, drift, and migration through either pollen or seeds on the maintenance of nuclear-cytoplasmic gynodioecy in a subdivided population. We find that the combination of drift and selection causes the loss of gynodioecy under scenarios that would maintain it under the influence of selection alone, and that both seed and, more surprisingly, pollen flow can maintain the polymorphism. In particular, although pollen flow could not avoid the loss of cytoplasmic polymorphism within demes, it allowed the maintenance of nuclear-cytoplasmic polymorphism at the metapopulation level.

Sex ratio variation among gynodioecious populations of sea beet: can it be explained by negative frequency-dependent selection?

This study is devoted to assess sex ratio variation among 33 populations of the gynodioecious Beta vulgaris ssp. maritima in Brittany (France) and to explore the causes of this variation. We showed that three different CMS (cytoplasmic male sterility) cytotypes occurred in populations, but strongly differed for their frequencies and the frequency of their associated nuclear restorer alleles (which counteract the effect of CMS and restore male fertility). No correlation was found between CMS and restorer frequencies within populations, which has been previously interpreted as a result of stochasticity. However, neutral genetic variation did not indicate recent population bottlenecks in studied populations. Moreover, no significant correlation was found between female frequency or variance and current population size. Consequently, stochastic processes could not be the major cause of sex ratio variation. Alternatively, empirical estimations of the variation of females, CMS genes and nuclear restorer allele's frequencies were compared to theoretical predictions based on a frequency-dependent selection model of gynodioecy. In particular, we showed that an absence of correlation between CMS and restorer frequencies could also occur without stochasticity. The large variation of sex ratio in Beta vulgaris could thus be explained by frequency-dependent selection acting on CMS genes and restorer alleles.

Temporal and sexual variation of leaf-produced pollinator-attracting odours in the dwarf palm.

Information on intra-specific variation in pollinator-attracting floral traits provides clues to selective pressures imposed by pollinators. However, these traits also reflect constraints related to floral phenology or morphology. The specific weevil pollinator Derelomus chamaeropsis of the dioecious Mediterranean dwarf palm Chamaerops humilis is attracted by volatile compounds that leaves, and not flowers, release during anthesis. Production of these olfactory cues is thus probably not constrained by any other floral function. This provides the opportunity to study variation of a "floral" trait that is not produced by a floral organ. We studied volatile compounds emitted by leaves of 12 individual C. humilis over the whole flowering season. The quantity of volatile compounds emitted by leaves reached a maximum when plants required pollinator visits. The relationship between odour emission and floral phenology was slightly different between male and female plants, probably reflecting differences in the exact time at which females and males benefit from pollinator visitation. Male plants produced higher quantities of volatile compounds than females. Odour composition was highly variable among individuals but did not differ between male and female plants. In this system, female C. humilis are pollinated by deceit and pollinators should be selected to avoid visiting them. The absence of sexual difference in blend composition may thus prevent pollinators from discriminating between male and female plants.