Mating system and speciation I: Accumulation of genetic incompatibilities in allopatry

Abstract

Self-fertilisation is widespread among hermaphroditic species across the tree of life. Selfing has many consequences on the genetic diversity and the evolutionary dynamics of populations, which may in turn affect macroevolutionary processes such as speciation. On the one hand, because selfing increases genetic drift and reduces migration rate among populations, it may be expected to promote speciation. On the other hand, because selfing reduces the efficacy of selection, it may be expected to hamper ecological speciation. To better understand under which conditions and in which direction selfing affects the build-up of reproductive isolation, an explicit population genetics model is required. Here, we focus on the interplay between genetic drift, selection and genetic linkage by studying speciation without gene flow. We test how fast populations with different rates of selfing accumulate mutations leading to genetic incompatibilities. When speciation requires populations to pass through a fitness valley caused by underdominant and compensatory mutations, selfing reduces the depth and/or breadth of the valley, and thus overall facilitates the fixation of incompatibilities. When speciation does not require populations to pass through a fitness valley, as for Bateson-Dobzhanzky-Muller incompatibilities (BDMi), the lower effective population size and higher genetic linkage in selfing populations both facilitate the fixation of incompatibilities. Interestingly, and contrary to intuitive expectations, local adaptation does not always accelerate the fixation of incompatibilities in outcrossing relative to selfing populations. Our work helps to clarify how incompatibilities accumulate in selfing vs. outcrossing lineages, and has repercussions on the pace of speciation as well as on the genetic architecture of reproductive isolation.