Relative importance of gene flow and individual reproductive fitness in sex ratio variation in a gynodioecious species, Beta vulgaris ssp. maritima

Chez les plantes à fleurs, où une immense variété de stratégies de reproduction est rencontrée, la dispersion des gènes s’opère classiquement via des flux de pollen pour la voie mâle, et via des flux de graines pour la voie femelle. La gynodioécie correspond à un système de reproduction original, caractérisé par la coexistence de plantes femelles et de plantes hermaphrodites au sein de populations naturelles. Ce système de reproduction suscite depuis longtemps un intérêt particulier, du fait d’un paradoxe évolutif apparent : les individus femelles, ayant perdu une voie de transmission de leur information génétique, devraient être désavantagés par rapport aux hermaphrodites, dotés des deux voies de transmission des gènes. L’objet de ce travail thèse était d’expliquer le maintien des femelles et les importantes variations spatiales de sex ratio fréquemment observées dans les populations naturelles de betterave maritime (Beta vulgaris ssp. maritima), chez laquelle le déterminisme du sexe implique des interactions entre des gènes cytoplasmiques induisant la stérilité mâle (CMS) et des allèles nucléaires de restauration de la fonction mâle. En mêlant des approches de biologie et de génétique des populations, trois thématiques ont ainsi été abordées. (i) La valeur sélective des différents types sexuels a été mesurée, en faisant appel à des mesures phénotypiques en conditions contrôlées et à des analyses de paternité en populations naturelles. Ceci a permis de révéler un avantage femelle extrêmement restreint ainsi que des variations importantes du succès reproducteur mâle chez les hermaphrodites, liées notamment au génotype des individus et à l’existence d’un coût de la restauration. (ii) La caractérisation moléculaire de la diversité génétique au sein de plusieurs populations naturelles et entre plusieurs cohortes successives nous a permis de mettre en lumière l’importance relative des effets de la migration, des évènements de fondation et de la dérive génétique sur la structure spatiale des phénotypes sexuels. Les variations observées de sex ratio à très fine échelle semblent ainsi expliquées par des effets de fondation multiples couplés à des flux de pollen et de graines restreints dans l’espace. (iii) Finalement, nous mettons en évidence l’effet important que cette forte structure spatiale des sexes peut avoir, à la fois sur les individus hermaphrodites et sur les individus femelles. L’ensemble de nos résultats montre qu’une structure spatiale à fine échelle, générée par des évènements de fondation et des flux de gènes limités, peut affecter de façon importante la dynamique de la gynodioécie dans la nature.In flowering plants, which exhibit a spectacular diversity of reproductive strategies, gene dispersal generally occurs through two distinct pathways: pollen for the male function, and seed for the female function. Among sexually polymorphic flowering plants, gynodioecy refers to a particular breeding system in which females and hermaphrodites co-occur in natural populations. Since females reproduce only through seeds, they apparently transmit their genes only half as frequently as hermaphrodites, which gain fitness through both seed and pollen production. This apparent evolutionary paradox has attracted the attention of evolutionary biologists as far as the mid-nineteenth century. The aim of this PhD thesis was to understand the successful maintenance of female individuals and the important spatial variations in sex ratio that are often observed in natural populations of gynodioecious Beta vulgaris ssp. maritima, in which sex is determined by interactions between cytoplasmic male sterility (CMS) genes and nuclear restorers of male fertility. Using population biology and population genetics approaches, three distinct themes were considered. (i) First, male and female fitness of the different sexual types were compared, using both measures in controlled conditions and paternity analyses in the wild. While our results only suggest a very restricted female advantage, we detected strong male fitness differences among hermaphrodites that were partially explained by the genotype of individuals and by the occurrence of a cost of restoration. (ii) The study of the distribution of genetic diversity in several natural populations and in several consecutive cohorts allowed us to quantify the relative impact of migration, founder events and genetic drift on the spatial distribution of sexes. Overall, random founder effects with spatially restricted pollen and seed flow appeared to be the primary determinants of sex ratio variations. (iii) Finally, we explore how such sex ratio variation can affect the reproductive output of hermaphrodites and females. Altogether, we show that fine-scale spatial structure, resulting from the joint action of founder events and limited gene flow, can notably modify the dynamics of gynodioecy in natural populations

Effects of sexual dimorphism on pollinator behaviour in a dioecious species

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On the function of flower number: disentangling fertility from pollinatormediated selection

In animal-pollinated angiosperms, the "male-function" hypothesis claims that male reproductive success should benefit from large floral displays, through pollinator attraction, while female reproductive success 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 reproductive success. In females, flower number was under strong fertility selection, as predicted in the absence of pollen limitation. In contrast, in males, flower number was mainly under sexual selection, which in turn increased male reproductive success. 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 do 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

Data from: Gynodioecy in structured populations: understanding fine-scale sex ratio variation in Beta vulgaris ssp. maritima

Natural selection, random processes, and gene flow are known to generate sex ratio variations among sexually polymorphic plant populations. In gynodioecious species, in which hermaphrodites and females coexist, the relative effect of these processes on the maintenance of sex polymorphism is still up for debate. The aim of this study was to document sex ratio and cytonuclear genetic variation at a very local scale in wind-pollinated gynodioecious Beta vulgaris ssp. maritima, and attempt to elucidate which processes explained the observed variation. The study sites were characterized by geographically distinct patches of individuals and appeared to be dynamic entities, with recurrent establishment of distinct haplotypes through independent founder events. Along with substantial variation in sex ratio and unexpectedly low gene flow within study sites, our results showed a high genetic differentiation among a mosaic of genetically distinct demes, with isolation by distance or abrupt genetic discontinuities taking place within a few tens of meters. Overall, random founder events with restricted gene flow could be primary determinants of sex structure, by promoting the clumping of sex-determining genes. Such high levels of sex structure provide a landscape for differential selection acting on sex-determining genes, which could modify the conditions of maintenance of gynodioecy in structured populations

Does pollination syndrome reflect pollinator efficiency in Silene nutans?

International audienc

Data from: Fine-scale genetic structure in a wild bird population: the role of limited dispersal and environmentally-based selection as causal factors

Individuals are typically not randomly distributed in space; consequently ecological and evolutionary theory depends heavily on understanding the spatial structure of populations. The central challenge of landscape genetics is therefore to link spatial heterogeneity of environments to population genetic structure. Here, we employ multivariate spatial analyses to identify environmentally induced genetic structures in a single breeding population of 1174 great tits Parus major genotyped at 4701 single-nucleotide polymorphism (SNP) loci. Despite the small spatial scale of the study relative to natal dispersal we found multiple axes of genetic structure. We built distance-based Moran's eigenvector maps to identify axes of pure spatial variation, which we used for spatial correction of regressions between SNPs and various external traits known to be related to fitness components (avian malaria infection risk, local density of conspecifics, oak tree density and altitude). We found clear evidence of fine-scale genetic structure, with 21, 7 and 9 significant SNPs respectively associated with infection risk by two species of avian malaria (Plasmodium circumflexum and P. relictum) and local conspecific density. Such fine-scale genetic structure relative to dispersal capabilities suggests ecological and evolutionary mechanisms maintain within-population genetic diversity in this population with the potential to drive micro-evolutionary change

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Individual great tits with associated SNP