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, selfing may be expected to promote speciation. On the other hand, because selfing reduces the efficacy of selection, selfing 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 the population 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 the population 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 facilitates the fixation of incompatibilities. Interestingly, and contrary to intuitive expectations, local selection does not always accelerate the build-up of reproductive isolation in outcrossing relative to selfing populations. Our work helps to clarify how selfing lineages may speciate and diversify over time, and emphasizes the need to account for interactions among segregating mutations within populations to better understand macroevolutionary dynamics. Author summaryHermaphroditic organisms may use their male gametes to fertilise their own female gametes, and species vary greatly in how much they self-fertilise. Self-fertilisation induces many genetic modifications in the population, which may ultimately affect the rates at which lineages diversify. Here we aim to build predictions on how self-fertilisation affects the rate at which reproductive isolation arises between geographically isolated populations. Specifically, we develop theoretical models in which populations varying in their rates of self-fertilisation may fixate mutations leading to reproductive isolation. We first explored scenarios in which reproductive isolation is made by mutations whose fixations necessitate the population to experience temporally deleterious effects (i.e., a fitness valley), and found that self-fertilisation reduces the breadth and depth of the fitness valley and thereby overall facilitates the accumulation of such mutations. Second, we explored scenarios in which genetic incompatibilities are caused by interactions between derived alleles of different genes (i.e., BDMi). By allowing the BDMi to occur within populations, we found that self-fertilisation reduces the manifestation of BDMi within population, and thereby facilitates their fixation. This effect prevails even in the face of local adaptation. Thus, our study clarifies how fast species are expected to arise in self-fertilisation lineages.