Jeanne Tonnabel

Sexual selection is a central force in evolutionary biology that has been shown to shape phenotypes and population dynamics in animals. While this selective force is increasingly recognized in flowering plants, theory predicts that anisogamy generates sex differences in the fitness benefits of acquiring additional mates—a pattern well supported in animals but with limited tests in plants. Plant studies rely solely on genetic parentage analyses to estimate mate numbers, thereby conflating performance in accessing mates with success in gamete fertilization. Pollinators add an ecological layer, as their behavior and abundance can influence competition for access to mates and their gametes. Here, we disentangle consecutive episodes of sexual selection in the hermaphroditic plant Brassica rapa by combining direct observations of Bombus terrestris movements with genetic paternity analyses in experimental populations, thus providing independent estimates of the observational number of mates acquired and realized fertilization success. Our approach identifies pollen competition for ovules as the primary arena for sexual selection in B. rapa . Competition for access to mates constitutes a secondary force and was found to be stronger in the male compared to the female sex function, as predicted by classic theory. Experimentally reduced pollinator abundance modulated the balance between pre- and post-pollination sexual selection, increasing the opportunity for selection on mate acquisition. Ignoring pollinator movements led to biased estimates of pre-pollination sexual selection. Our findings demonstrate that sexual selection in plants unfolds across multiple, sequential episodes shaped by ecological context.

1. Quantitatively assessing wildlife damage to food crops in tropical agroforestry systems is notoriously problematic. At the same time, the animal species likely to destroy these crops, such as primates, are often endangered and a source of conflict. Resolving these conflicts may require the implementation of financial compensation where non-monetary solutions are unavailable. Currently, however, there is no suitable method for assessing fruit losses due to the complexities of agroforestry plots used by most small households practising polyculture-based agriculture. 2. We constructed an energy balance model to predict the quantity of cultivated fruit and other locally sourced food required by crop-dependent primates to meet their metabolic needs. The proposed method is based on the principle that, under conditions of energy balance, an animal’s daily energy intake corresponds to its total energy expenditure. The ecophysiological model incorporated the daily food and energy intake of wild primates, measured using the bite-size method and the nutritional composition of food, as well as their total energy expenditure and body composition, measured using doubly labelled water. We tested the model’s predictions on lemurs foraging in several agroforests in Mayotte, and on two frugivorous primate species in Madagascar during different seasons. Additionally, we evaluated whether more conventional dietary analysis methods (feeding-time sampling), or published energetics data could reliably inform the model, and reduce the costs and constraints of field observations. 3. The predictions were generally consistent with direct estimates of food intake (91% ± 25%, n = 14 across different seasons), though this was influenced by the lemurs’ evolutionary-driven seasonal fattening strategy. Time-derived estimates using correction factors or published measurements of total energy expenditure were also consistent, but further studies are required to confirm these findings. 4. Policy implications . The study provides proof of concept for a promising approach to quantifying wildlife-related agricultural losses in small-scale agroforestry. This innovative method provides policymakers, farmers’ associations, and non-governmental organisations with sufficiently accurate quantitative estimates to support the development of evidence-based financial compensation schemes.

Summary: 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.

The definition of biological sex has become a renewed focus of societal debate, fuelled by the conflation of biological principles with discussions of human gender diversity. Here, we argue that conceptual clarity critically depends on separating these domains. Drawing on evolutionary theory and empirical evidence, we maintain that biological sex is best defined as a binary classification of male and female reproductive strategies rooted in anisogamy, characterised by the production of two discrete gamete types of different sizes. We stress that gamete size constitutes the ultimate criterion for biological sex and that this definition applies consistently across sexual systems, from separate‐sexed species to hermaphrodites, irrespective of variation in karyotype, hormonal profile, somatic phenotype, or behaviour. Further, we emphasise that evolutionary insights offer a coherent explanation for recurring, though not universal, associations between biological sex and patterns of sex‐specific selection, sexual dimorphism and parental care. We conclude that the definition of biological sex as a binary classification based on gamete size is a powerful scientific framework compatible with the diversity of sexual phenotypes found in anisogamous organisms and distinct from the concept of human gender.

Évolution des traits d'histoire de vie dans les milieux soumis au feu : approches théoriques et empiriques, le cas des Leucadendron dans le Fynbos sud-africain: Dans les milieux soumis au feu, les plantes ont développé une diversité de stratégies d'histoire de vie qui sont supposément adaptées à différentes conditions environnementales, comme différents régimes de feu. Au cours de ma thèse, j'ai cherché à expliquer la diversité de stratégies adoptées par les plantes pérennes en cherchant à déterminer comment des facteurs intrinsèques et extrinsèques ont influencé l'évolution de ces traits d'histoire de vie. Mais également si cette connaissance peut nous permettre d'améliorer notre compréhension de l'impact à venir de changements environnementaux ou renseigner des politiques de conservation. Les régimes de feux ont été proposés comme étant une force sélective majeure influençant les traits d'histoire de vie dans les milieux soumis au feu. J'ai donc particulièrement étudié l'impact de la distribution des intervalles de feux. Un modèle d'optimisation d'allocation des ressources a été construit afin d'étudier les stratégies d'histoire de vie optimales sous différents régimes de feu. Ce modèle prédit qu'il est optimal de diminuer l'allocation des ressources au maintien des cônes lorsque la variance des intervalles de feu augmente et lorsque la disponibilité en ressources diminue. De même, les prédictions montrent que l'allocation des ressources à la sérotinie diminue lorsque la disponibilité des ressources diminue au profit de l'allocation à la croissance et à la production de graines. De façon, à tester ces prédictions, nous utilisons des analyses comparatives appliquées le long d'une nouvelle phylogénie du genre Leucadendron. Un protocole de recherche de marqueurs permettant de maximiser le polymorphisme et la probabilité d'orthologie de ceux-ci a été construit de façon à définir de nouveaux marqueurs spécifiques du genre Leucadendron. L'estimation des valeurs de traits d'histoire de vie le long de cette nouvelle phylogénie montre une évolution complexe de tous les traits d'histoire de vie considérés ainsi qu'une évolution conjointe entre certains traits d'histoire de vie. Des analyses comparatives prenant en compte l'incertitude phylogénétique et la variabilité environnementale intra-spécifique, montrent notamment que les espèces sérotineuses ont évolué des niches environnementales impliquant des événements climatiques extrêmes (i.e. sécheresse et gel) moins importants que les espèces avec banques de graines dans le sol. De même, les espèces non-réitératives semblent avoir été moins tolérantes que les espèces réitératives à des événements climatiques extrêmes.

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 R2 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.

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.

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 will often be density-dependent. In wind-pollinated plants in particular, vegetative traits can have an important influence on both resource acquisition and the 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 rapid, age-dependent and sex-specific evolution in the ontogeny of vegetative organs, and illustrates the power of experimental evolution for investigating plant trait evolution.