On the impermanence of species: The collapse of genetic incompatibilities in hybridizing populations

Abstract

Species pairs often become genetically incompatible during divergence, which is an important source of reproductive isolation. An idealized picture is often painted where incompatibility alleles accumulate and fix between diverging species. However, recent studies have shown both that incompatibilities can collapse with ongoing hybridization, and that incompatibility loci can be polymorphic within species. This paper suggests some general rules for the behavior of incompatibilities under hybridization. In particular, we argue that redundancy of genetic pathways can strongly affect the dynamics of intrinsic incompatibilities. Since fitness in genetically redundant systems is unaffected by introducing a few foreign alleles, higher redundancy decreases the stability of incompatibilities during hybridization, but also increases tolerance of incompatibility polymorphism within species. We use simulations and theories to show that this principle leads to two types of collapse: in redundant systems, exemplified by classical Dobzhansky–Muller incompatibilities, collapse is continuous and approaches a quasi‐neutral polymorphism between broadly sympatric species, often as a result of isolation‐by‐distance. In nonredundant systems, exemplified by co‐evolution among genetic elements, incompatibilities are often stable, but can collapse abruptly with spatial traveling waves. As both types are common, the proposed principle may be useful in understanding the abundance of genetic incompatibilities in natural populations.

The role of conflict in shaping plant biodiversity

“…Coughlan, 2023b), are much less understood. Both the genetic architecture and the generation in which incompatibility manifests can influence patterns of introgression, with incompatibilities that are more genetically complex and redundant, and/or those that manifest earlier, playing a potentially stronger role in diminishing introgression (Lindtke & Buerkle, 2015;Xiong & Mallet, 2022). Although the genetic architecture of most incompatibilities is unknown, and empirical tests of their role in preventing introgression are scarce, we might expect some incompatibilities to attenuate introgression more than others.…”

Strong postmating reproductive isolation in Mimulus section Eunanus

“…These signals are likely ancient, and may have predated the postmating barriers we see today. Without postmating reproductive barriers, even small amounts of introgression can lead to species collapse in sympatry, especially if premating barriers are weak or are disrupted by environmental change (Behm et al, 2010; Kleindorfer et al, 2014; Xiong & Mallet, 2022). Alternatively, species can persist despite ongoing introgression, depending on the circumstances (Kay et al, 2018; Kenney & Sweigart, 2016; Servedio & Hermisson, 2020).…”

Strong postmating reproductive isolation inMimulussectionEunanus

“…Taken as a whole, however, they demonstrate a high degree of complexity in the divergence process, consistent with reticulate evolutionary histories of other groups within Mimulus (e.g., Brandvain et al, 2014; Nelson et al, 2021; Stankowski et al, 2019), in plants more broadly (e.g., Curtu et al, 2009; Goulet et al, 2017; Hamlin et al, 2020; Kay et al, 2018; Scascitelli et al, 2010), and across the tree of life (e.g., D’Angiolo et al, 2020; Green et al, 2010; Kleindorfer et al, 2014; Mallet et al, 2007; Schumer et al, 2018). Without postmating reproductive barriers, even small amounts of introgression can lead to species collapse in sympatry, especially if premating barriers are disrupted by environmental change (Behm et al, 2010; Kleindorfer et al, 2014; Xiong & Mallet, 2022). Alternatively, species can persist despite ongoing introgression, depending on the circumstances (Kay et al, 2018; Kenney & Sweigart, 2016; Servedio & Hermisson, 2020).…”