Sexual selection is a cornerstone of evolutionary biology in animals but remains underexplored in plants, where empirical work is often disconnected from sexual selection theory. A major barrier to crosstaxonomic synthesis is the inconsistent definition of core concepts, especially mating success. We advocate for a unified, taxon-neutral three-phase framework of sexual selection (premating, postmating, and postfertilization), grounded in traditional practice and applicable to both animals and plants. Parallels and differences across taxa are highlighted, capturing universal processes alongside biological diversity. Traits common in plants and historically seen as incompatible with sexual selection—such as modularity, pollen dispersal by third-party vectors, and lack of physical contact between mates—do not preclude its action and instead offer new biological processes to study.

Abstract Female choice is a central process of sexual selection that has shaped numerous phenotypes in animals. It may operate broadly across sexually reproducing organisms, including plants, not only because sex differences in sexual selection arise from anisogamy, wich refers to the unequal investment in gametes between sexes, but also because it can emerge from simple variation in female reproductive morphology. Here, we provide the first empirical test of cryptic female choice in an angiosperm by examining whether pollen and pistil traits jointly influence paternal fertilization success. Using experimental pollen competition, paternity analyses, and trait measurements, we show that pistil traits can bias paternity toward pollen donors with specific pollen traits. These results demonstrate that cryptic female choice operates in plants, paralleling mechanisms described in animals.

Cryptic female choice - female-mediated bias in fertilization after mating - is well established in animals and can also occur in plants when multiple pollens compete on the same pistil. However, whether interactions between pollen and pistil tissues after pollen deposition contribute to this process remains unknown. Here, we experimentally test whether such interactions mediate cryptic female choice in the angiosperm Brassica rapa. We quantified fertilization success of pollen donors competing on the same pistil using paternity analyses, and in parallel, made semi-in vivo assays to measure pollen tubes trajectories emerging from the excised styles and growing toward unfertilized ovules for each donor-recipient pair. We show that pollen tube growth towards ovules predicts higher fertilization success under pollen competition. Thus, we document a previously unobserved mechanism of cryptic female choice based on physical interactions between male and female components of reproduction. In addition, different recipient plants favour different pollen donors, consistent with non-directional female choice. Plants with longer styles bias paternities more strongly towards the most successful pollen donor. Overall, our study demonstrates that interactions between pollen tubes and pistil tissues after pollen germination enable plants to bias paternity toward particular donors.

Thanks to significant advances in genomics and bioinformatics, research on plant sex-determining genes has made remarkable progress over the past decade. Since the discovery of the OGI-MeGI sex-determination system in persimmons in 2014, candidate sex-determining genes have been identified in a dozen flowering plant species. In this review, we examine these newly discovered genes and explore what they reveal about the genetic basis of the evolution of dioecy. While these genes are diverse, many belong to key developmental pathways previously described in other species. Two primary evolutionary routes from hermaphroditism to dioecy have been proposed: gynodioecy and monoecy. The gynodioecy pathway has been modeled with two genes and two sterility mutations, whereas recent theoretical work on the monoecy route suggests a gradual differentiation of sexual morphs involving multiple genes. Current data align with these models, particularly in the expected number of sex-determining genes. The gynodioecy pathway is typically associated with two or more genes, while the monoecy route varies, involving either one or two genes. From a molecular evolution perspective, loss-of-function mutations are frequent, but gene duplication appears to be the most common mechanism driving the emergence of new sex-determining genes. Future research should aim to characterize additional systems to gain a comprehensive view of plant sex determination and employ functional approaches to validate proposed candidate genes.

Understanding the drivers of biodiversity is a central goal in evolutionary biology. In particular, sexual selection has long been proposed as a potential catalyst of speciation, but empirical evidence remains inconclusive. Here, we present a comprehensive meta-analysis synthesizing 145 effect sizes from 50 comparative studies testing the relationship between proxies of sexual selection and species diversity across the animal kingdom. Our results reveal a modest but consistent positive association (global effect size: r = 0.201; 95% confidence interval: 0.035-0.366), supporting the hypothesis that sexual selection contributes to speciation. However, the global effect size corresponds to an R 2 of only 0.04, suggesting that sexual selection is not a dominant driver of speciation. We also uncover substantial heterogeneity among effect sizes, largely attributable to between-study variation and taxonomic affinities of effect sizes. Studies that fail to account for phylogenetic non-independence tend to report stronger effects. In contrast, other tested methodological and biological moderators, such as the proxies used to estimate the strength of sexual selection or proxies of speciation, do not explain the observed heterogeneity in effect sizes. Sensitivity analyses confirm the robustness of our results, and we find no signatures of publication bias. We highlight the need for broader taxonomic coverage and a greater focus on understudied mechanisms, such as post-copulatory sexual selection, to refine our understanding of the role of sexual selection in shaping species diversity.

Sexual selection is a cornerstone of evolutionary biology potentially operating in all sexually-reproducing organisms. Modern developments in the field revealed that this selective force extends beyond Darwin’s initial focus on access to mates in terms of competition for access to gametes of the other sex. Despite its presumed universality, sexual selection theory remains largely untested in plants compared to animals. This gap may partly stem from challenges in quantifying sexual selection using approaches that account for a critical plant-specific factor: the reliance on pollinators as third-party agents for accessing mates. Here, we quantified sexual selection along consecutive episodes of selection in the hermaphroditic plant Brassica rapa by integrating the monitoring of pollinator movements with genetic paternity analyses in experimental populations. Our approach identifies pollen competition for ovules as the primary arena for sexual selection in B. rapa. Darwinian competition for access to mates constitutes a secondary force, and was stronger in the male compared to the female sex function, as predicted by classic theory. Importantly, experimentally induced variation in pollinator abundance modulated the balance between pre- and post-pollination sexual selection. Under reduced pollinator abundance, the opportunity for selection on mate acquisition increased. Crucially, we demonstrate that ignoring pollinator movements among plants leads to erroneous quantification of pre-pollination sexual selection. We argue that a unifying theory of sexual selection requires a more comprehensive quantification of pre- and post-pollination episodes of selection, taking into account the specificities of gamete transfer in plants. ### Competing Interest Statement The authors have declared no competing interest.

Natural populations are constantly exposed to complex environments, characterized by the simultaneous variation of multiple stressors, such as osmotic and thermal stress, and diverse pollutants. As a consequence, population persistence often depends on the potential to rapidly evolve in the face of these challenges. However, while evolution in response to single stressors has been widely studied, experimental evidence for adaptation to multiple stressors is sparse and remains inconclusive, due to a lack of consistent experimental designs and metrics across systems. To overcome this limitation, we here used a meta-experimental evolution approach to test how environmental complexity shapes adaptive evolution across a diversity of taxa. We exposed 14 species of bacteria, unicellular eukaryotes, and plants, to single versus multiple stressors for multiple generations, and measured their fitness in the presence or absence of stressors. We show that across taxa, populations evolving under multiple stressors adapted more slowly, and exhibited fitness costs when exposed back to control environments. The magnitude of these effects varied with the identity of the stressors (e.g., temperature, salinity, copper). Further, all species followed a consistent pattern of greater fitness gains with greater initial fitness reduction at the start of the experiment. Our results are consistent with the predicted cost of complexity when selection acts on pleiotropic genes. Accounting for the complexity of environmental stress should thus prove crucial to prevent biodiversity loss and its cascading effects on ecosystem functioning. ### Competing Interest Statement The authors have declared no competing interest. Occitanie Regional Council’s program “Key challenge BiodivOc”, ComplexAdapt Agence Nationale de la Recherche, ANR-21-CE02-0026 Agence Nationale de la Recherche, https://ror.org/00rbzpz17, ANR-19-CE02-0021-01 Agence Nationale de la Recherche, ANR-17-CE02-0018-01 Agence Nationale de la Recherche, ANR-10-LABX-41

Variation in plant sex ratios is often attributable to sex-specific mortality in heterogeneous environments that differentially limit male and female plant reproduction. Yet sexual dimorphism and plastic responses to environmental heterogeneity are common and may co-vary with variation in sex ratios. Here, we show that the sex ratio and the degree of sexual dimorphism for a number of plant traits varied along climatic and elevation gradients in three wind-pollinated dioecious species, Rumex lunaria, Urtica dioica and Salix helvetica. Some of the observed sex-specific responses to climatic variation are consistent with greater sensitivity of females to water scarcity, but most responses rather point to the greater sensitivity of males to ecological stress, consistent with larger male reproductive effort, as has been commonly reported for wind-pollinated plants. In contrast, we found no evidence for variation in either sex ratios or sexual dimorphism expected under sexual selection. Interestingly, sex ratios and sexual dimorphism varied both along distinct and the same ecological axes of variation, suggesting that the evolution of sexual dimorphism in the measured traits was not sufficient to prevent sex-specific mortality.

Sexual selection is the basis of some of the most striking phenotypic variation in nature.1,2 In animals, sexual selection in males can act on traits that improve access to mates prior to copulation,3-8 but also on sperm traits filtered by sperm competition,9-14 or female choice expressed simply by the morphology and physiology of genital tracts.14-16 Although long overlooked as a mode of selection on plant traits, sexual selection should act on land plants too because they are anisogamous: males produce more, and smaller, gametes than females.17-19 Numerical asymmetry in gamete production is thought to play a central role in selection on traits that affect pollen transfer to mates,20,21 but very little is known about how pollen competition or cryptic female choice might affect the evolution of traits expressed after pollination.22,23 Here, we report the divergence of pollen and pistil traits of the dioecious wind-pollinated annual herb Mercurialis annua during evolution over three generations between populations at low versus high plant density, corresponding to low versus higher levels of polyandry;24 we expected selection under higher polyandry to strengthen competition among pollen donors for fertilizing ovules. We found that populations at high density evolved faster-growing pollen tubes (an equivalent of greater sperm velocity), greater expression of pollen proteins involved in pollen growth, and larger stigmas (a trait likely enhancing the number of pollen donors and thus competition for ovules). Our results identify the post-pollination phase of plant mating as an important arena for the action of sexual 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.

Plant sexual dimorphism is thought to evolve in response to sex-specific selection associated with competition for access to mates or resources, both of which may be density dependent. In wind-pollinated plants in particular, vegetative traits such as plant size and architecture may influence resource acquisition and both pollen dispersal and receipt, with potential conflict between these two components of fitness. We evaluated the role of plant density in shaping plant traits by measuring evolutionary responses in experimental populations of the sexually dimorphic wind-pollinated plant Mercurialis annua. After three generations of evolution, we observed divergence between high- and low-density populations in several vegetative traits, whereas there was no divergence for reproductive traits. A reversal in the direction of sexually dimorphic traits expressed in young plants evolved in both low- and high-density populations compared to the original population (stored as seeds). Compared to the source population, males at high density evolved to be taller when young, whereas at low density young females tended to become smaller. These results demonstrate that a simple change in plant density can induce age-dependent and sex-specific evolution in the ontogeny of vegetative organs, and illustrates the power of experimental evolution for investigating plant trait evolution.

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.

Sexual dimorphism in plants may emerge as a result of sex-specific selection on traits enhancing access to nutritive resources and/or to sexual partners. Here we investigated sex-specific differences in selection of sexually dimorphic traits and in the spatial distribution of effective fecundity (our fitness proxy) in a highly dimorphic dioecious wind-pollinated shrub, Leucadendron rubrum. In particular, we tested for the effect of density on male and female effective fecundity. We used spatial and genotypic data of parent and offspring cohorts to jointly estimate individual male and female effective fecundity on the one hand and pollen and seed dispersal kernels on the other hand. This methodology was adapted to the case of dioecious species. Explicitly modelling dispersal avoids the confounding effects of heterogeneous spatial distribution of mates and sampled seedlings on the estimation of effective fecundity. We also estimated selection gradients on plant traits while modelling sex-specific spatial autocorrelation in fecundity. Males exhibited spatial autocorrelation in effective fecundity at a smaller scale than females. A higher local density of plants was associated with lower effective fecundity in males but was not related to female effective fecundity. These results suggest sex-specific sensitivities to environmental heterogeneity in L. rubrum. Despite these sexual differences, we found directional selection for wider canopies and smaller leaves in both sexes, and no sexually antagonistic selection on strongly dimorphic traits in L. rubrum. Many empirical studies in animals similarly failed to detect sexually antagonistic selection in species expressing strong sexual dimorphism, and we discuss reasons explaining this common pattern.

The ecological niche of a species describes the variation in population growth rates along environmental gradients that drives geographic range dynamics. Niches are thus central for understanding and forecasting species' geographic distributions. However, theory predicts that migration limitation, source-sink dynamics, and time-lagged local extinction can cause mismatches between niches and geographic distributions. It is still unclear how relevant these niche-distribution mismatches are for biodiversity dynamics and how they depend on species life-history traits. This is mainly due to a lack of the comprehensive, range-wide demographic data needed to directly infer ecological niches for multiple species. Here we quantify niches from extensive demographic measurements along environmental gradients across the geographic ranges of 26 plant species (Proteaceae; South Africa). We then test whether life history explains variation in species' niches and niche-distribution mismatches. Niches are generally wider for species with high seed dispersal or persistence abilities. Life-history traits also explain the considerable interspecific variation in niche-distribution mismatches: poorer dispersers are absent from larger parts of their potential geographic ranges, whereas species with higher persistence ability more frequently occupy environments outside their ecological niche. Our study thus identifies major demographic and functional determinants of species' niches and geographic distributions. It highlights that the inference of ecological niches from geographical distributions is most problematic for poorly dispersed and highly persistent species. We conclude that the direct quantification of ecological niches from demographic responses to environmental variation is a crucial step toward a better predictive understanding of biodiversity dynamics under environmental change.

Aim: The Hutchinsonian niche is a foundational concept in ecology and evolutionary biology that describes fundamental characteristics of any species: the global maximum population growth rate (rmax); the niche optimum (the environment for which rmax is reached); and the niche width (the environmental range for which intrinsic population growth rates are positive). We examine whether these characteristics are related to inter- and intraspecific variation in functional traits. Location: Cape Floristic Region, South Africa. Time period: Present day. Major taxa studied: Twenty-six plant species (Proteaceae). Methods: We measured leaf, plant-architectural and seed traits across species geographical ranges. We then examined how species-mean traits are related to demographically derived niche characteristics of rmax, in addition to niche optima and widths in five environmental dimensions, and how intraspecific trait variation is related to niche widths. Results: Interspecific trait variation generally exceeded range-wide intraspecific trait variation. Species-mean trait values were associated with variation in rmax (R-2 = 0.27) but were more strongly related to niche optima (mean R-2 = 0.56). These relationships generally matched trait-environment associations described in the literature. Both species-mean traits and intraspecific trait variability were strongly related to niche widths (R-2 = 0.66 and 0.59, respectively). Moreover, niche widths increased with intraspecific trait variability. Overall, the different niche characteristics were associated with few, largely non-overlapping sets of traits. Main conclusions: Our study relating functional traits to Hutchinsonian niches demonstrates that key demographic properties of species relate to few traits with relatively strong effects. Our results further support the hypothesis that intraspecific trait variation increases species niche widths. Given that niche characteristics were related to distinct sets of traits, different aspects of environmental change might affect axes of trait variation independently. Trait-based studies of Hutchinsonian niches thus yield important insights into the mechanisms shaping functional biodiversity, which should reinforce the role of traits in functional biogeography.

Sexual selection may contribute to the evolution of plant sexual dimorphism by favoring architectural traits in males that improve pollen dispersal to mates. In both sexes, larger individuals may be favored by allowing the allocation of more resources to gamete production (a "budget" effect of size). In wind-pollinated plants, large size may also benefit males by allowing the liberation of pollen from a greater height, fostering its dispersal (a "direct" effect of size). To assess these effects and their implications for trait selection, we measured selection on plant morphology in both males and females of the wind-pollinated dioecious herb Mercurialis annua in two separate experimental common gardens at contrasting density. In both gardens, selection strongly favored males that disperse their pollen further. Selection for pollen production was observed in the high-density garden only, and was weak. In addition, male morphologies associated with increased mean pollen dispersal differed between the two gardens, as elongated branches were favored in the high-density garden, whereas shorter plants with longer inflorescence stalks were favored in the low-density garden. Larger females were selected in both gardens. Our results point to the importance of both a direct effect of selection on male traits that affect pollen dispersal, and, to a lesser extent, a budget effect of selection on pollen production.

The ecological niche of a species describes the variation in population growth rates along environmental gradients that drives geographic range dynamics. Niches are thus central for understanding species geographic distributions and forecasting biodiversity responses to environmental change. However, theory predicts that migration limitation, source-sink dynamics and time-lagged local extinction can cause mismatches between niches and geographic distributions. It is still unclear how relevant these niche-distribution mismatches are for biodiversity dynamics and how they depend on species life history traits. This is mainly due to a lack of the comprehensive, range-wide demographic data needed to directly infer ecological niches for multiple species. Here we quantify niches from extensive demographic measurements along environmental gradients across the geographic ranges of 26 plant species (Proteaceae; Cape Floristic Region, South Africa). We then test whether life history explains variation in species niches and niche-distribution mismatches. Niches are generally wider for species with high seed dispersal and/or persistence abilities. Life history traits also explain the considerable interspecific variation in niche-distribution mismatches: poorer dispersers are absent from larger parts of their potential geographic ranges, whereas species with higher persistence ability more frequently occupy environments outside their ecological niche. Our study thus identifies major demographic and functional determinants of species niches and geographic distributions. It highlights that the inference of ecological niches from geographical distributions is most problematic for poorly dispersed and highly persistent species. We conclude that the direct quantification of ecological niches from demographic responses to environmental variation is a crucial step towards a better predictive understanding of biodiversity dynamics under environmental change.

The ecological niche of a species describes the variation in population growth rates along environmental gradients that drives geographic range dynamics. Niches are thus central for understanding and forecasting species’ geographic distributions. However, theory predicts that migration limitation, source-sink dynamics and time-lagged local extinction can cause mismatches between niches and geographic distributions. It is still unclear how relevant these niche-distribution mismatches are for biodiversity dynamics and how they depend on species life history traits. This is mainly due to a lack of the comprehensive, range-wide demographic data needed to directly infer ecological niches for multiple species. Here we quantify niches from extensive demographic measurements along environmental gradients across the geographic ranges of 26 plant species (Proteaceae; South Africa). We then test whether life history explains variation in species’ niches and niche-distribution mismatches. Niches are generally wider for species with high seed dispersal or persistence abilities. Life history traits also explain the considerable interspecific variation in niche-distribution mismatches: poorer dispersers are absent from larger parts of their potential geographic ranges, whereas species with higher persistence ability more frequently occupy environments outside their ecological niche. Our study thus identifies major demographic and functional determinants of species’ niches and geographic distributions. It highlights that the inference of ecological niches from geographical distributions is most problematic for poorly dispersed and highly persistent species. We conclude that the direct quantification of ecological niches from demographic responses to environmental variation is a crucial step towards a better predictive understanding of biodiversity dynamics under environmental change.

Bateman's principles posit that male fitness varies more, and relies more on mate acquisition, than female fitness. While Bateman's principles should apply to any organism producing gametes of variable sizes, their application to plants is potentially complicated by the high levels of polyandry suspected for plants, and by variation in the spatial distribution of prospective mates. Here we quantify the intensity of sexual selection by classical Bateman metrics using two common gardens of the wind-pollinated dioecious plant Mercurialis annua . Consistent with Bateman's principles, males displayed significantly positive Bateman gradients (a regression of fitness on mate number), whereas the reproductive success of females was independent of their ability to access mates. A large part of male fitness was explained by their mate number, which in turn was associated with males' abilities to disperse pollen. Our results suggest that sexual selection can act in plant species in much the same way as in many animals, increasing the number of mates through traits that promote pollen dispersal.

Objective Mercurialis annua is a wind-pollinated annual plant that has long been used as a model for the study of ploidy and sexual-systems evolution. However, no molecular markers are yet available for genetic studies of its diploid populations. Here, we develop and characterize a set of eight polymorphic microsatellite markers for diploid dioecious M. annua . Results Following an SSR-enrichment protocol, 13 microsatellite markers were proposed, eight of which yielded successful amplification and polymorphism. We screened the eight microsatellite loci in 100 individuals. The number of alleles per marker ranged from 6 to 12, and observed heterozygosity ranged from 0.57 to 0.76. To estimate potential allele scoring errors, these individuals’ offspring were genotyped for the same loci, and error rates were estimated from parentage analyses. Error rates ranged from 0 to 6.8%. Cross-amplification tests were performed for congeneric M. huetti and M. canariensis , with successful amplification for seven and six of the eight loci, respectively. The novel microsatellite markers proposed here will be crucial for a multitude of genetic studies of M. annua and further establish its importance as a model species for addressing ecological and population genetic questions.