Balancing selection and the crossing of fitness valleys in structured populations: diversification in the gametophytic self-incompatibility system.

The self-incompatibility locus (S-locus) of flowering plants displays a striking allelic diversity. How such a diversity has emerged remains unclear. In this article, we performed numerical simulations in a finite island population genetics model to investigate how population subdivision affects the diversification process at a S-locus, given that the two-gene architecture typical of S-loci involves the crossing of a fitness valley. We show that population structure slightly reduces the parameter range allowing for the diversification of self-incompatibility haplotypes (S-haplotypes), but at the same time also increases the number of these haplotypes maintained in the whole metapopulation. This increase is partly due to a higher rate of diversification and replacement of S-haplotypes within and among demes. We also show that the two-gene architecture leads to a higher diversity in structured populations compared with a simpler genetic architecture, where new S-haplotypes appear in a single mutation step. Overall, our results suggest that population subdivision can act in two opposite directions: it renders S-haplotypes diversification easier, although it also increases the risk that the self-incompatibility system is lost.

The evolution of recombination in self-fertilizing organisms.

Cytological data from flowering plants suggest that the evolution of recombination rates is affected by the mating system of organisms, as higher chiasma frequencies are often observed in self-fertilizing species compared with their outcrossing relatives. Understanding the evolutionary cause of this effect is of particular interest, as it may shed light on the selective forces favoring recombination in natural populations. While previous models showed that inbreeding may have important effects on selection for recombination, existing analytical treatments are restricted to the case of loosely linked loci and weak selfing rates, and ignore the stochastic effect of genetic interference (Hill-Robertson effect), known to be an important component of selection for recombination in randomly mating populations. In this article, we derive general expressions quantifying the stochastic and deterministic components of selection acting on a mutation affecting the genetic map length of a whole chromosome along which deleterious mutations occur, valid for arbitrary selfing rates. The results show that selfing generally increases selection for recombination caused by interference among mutations as long as selection against deleterious alleles is sufficiently weak. While interference is often the main driver of selection for recombination under tight linkage or high selfing rates, deterministic effects can play a stronger role under intermediate selfing rates and high recombination, selecting against recombination in the absence of epistasis, but favoring recombination when epistasis is negative. Individual-based simulation results indicate that our analytical model often provides accurate predictions for the strength of selection on recombination under partial selfing.

Evolution of self-incompatibility in the Brassicaceae: Lessons from a textbook example of natural selection.

Self-incompatibility (SI) is a self-recognition genetic system enforcing outcrossing in hermaphroditic flowering plants and results in one of the arguably best understood forms of natural (balancing) selection maintaining genetic variation over long evolutionary times. A rich theoretical and empirical population genetics literature has considerably clarified how the distribution of SI phenotypes translates into fitness differences among individuals by a combination of inbreeding avoidance and rare-allele advantage. At the same time, the molecular mechanisms by which self-pollen is specifically recognized and rejected have been described in exquisite details in several model organisms, such that the genotype-to-phenotype map is also pretty well understood, notably in the Brassicaceae. Here, we review recent advances in these two fronts and illustrate how the joint availability of detailed characterization of genotype-to-phenotype and phenotype-to-fitness maps on a single genetic system (plant self-incompatibility) provides the opportunity to understand the evolutionary process in a unique perspective, bringing novel insight on general questions about the emergence, maintenance, and diversification of a complex genetic system.