Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene.

About 15,000 angiosperm species (∼6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy.

Overestimation of the adaptive substitution rate in fluctuating populations.

Estimating the proportion of adaptive substitutions (α) is of primary importance to uncover the determinants of adaptation in comparative genomic studies. Several methods have been proposed to estimate α from patterns polymorphism and divergence in coding sequences. However, estimators of α can be biased when the underlying assumptions are not met. Here we focus on a potential source of bias, i.e. variation through time in the long-term population size (N) of the considered species. We show via simulations that ancient demographic fluctuations can generate severe overestimations of α, and this is irrespective of the recent population history.

Patterns of Genome-Wide Nucleotide Diversity in the Gynodioecious Plant Thymus vulgaris Are Compatible with Recent Sweeps of Cytoplasmic Genes.

Gynodioecy is a sexual dimorphism where females coexist with hermaphrodite individuals. In most cases, this dimorphism involves the interaction of cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Two scenarios can account for how these interactions maintain gynodioecy. Either CMS genes recurrently enter populations at low frequency via mutation or migration and go to fixation unimpeded (successive sweeps), or CMS genes maintain polymorphism over evolutionary time through interactions with a nuclear restorer allele (balanced polymorphism). To distinguish between these scenarios, we used transcriptome sequencing in gynodioecious Thymus vulgaris and surveyed genome-wide diversity in 18 naturally occurring individuals sampled from populations at a local geographic scale. We contrast the amount and patterns of nucleotide diversity in the nuclear and cytoplasmic genome, and find ample diversity at the nuclear level (π = 0.019 at synonymous sites) but reduced genetic diversity and an excess of rare polymorphisms in the cytoplasmic genome relative to the nuclear genome. Our finding is incompatible with the maintenance of gynodioecy via scenarios invoking long-term balancing selection, and instead suggests the recent fixation of CMS lineages in the populations studied.

Inference of Distribution of Fitness Effects and Proportion of Adaptive Substitutions from Polymorphism Data.

The distribution of fitness effects (DFE) encompasses the fraction of deleterious, neutral, and beneficial mutations. It conditions the evolutionary trajectory of populations, as well as the rate of adaptive molecular evolution (α). Inferring DFE and α from patterns of polymorphism, as given through the site frequency spectrum (SFS) and divergence data, has been a longstanding goal of evolutionary genetics. A widespread assumption shared by previous inference methods is that beneficial mutations only contribute negligibly to the polymorphism data. Hence, a DFE comprising only deleterious mutations tends to be estimated from SFS data, and α is then predicted by contrasting the SFS with divergence data from an outgroup. We develop a hierarchical probabilistic framework that extends previous methods to infer DFE and α from polymorphism data alone. We use extensive simulations to examine the performance of our method. While an outgroup is still needed to obtain an unfolded SFS, we show that both a DFE, comprising both deleterious and beneficial mutations, and α can be inferred without using divergence data. We also show that not accounting for the contribution of beneficial mutations to polymorphism data leads to substantially biased estimates of the DFE and α We compare our framework with one of the most widely used inference methods available and apply it on a recently published chimpanzee exome data set.