The genomic and ecological context of hybridization affects the probability that symmetrical incompatibilities drive hybrid speciation.

Aaron A Comeault

doi:10.1002/ece3.3872

Abstract

Despite examples of homoploid hybrid species, theoretical work describing when, where, and how we expect homoploid hybrid speciation to occur remains relatively rare. Here, I explore the probability of homoploid hybrid speciation due to “symmetrical incompatibilities” under different selective and genetic scenarios. Through simulation, I test how genetic architecture and selection acting on traits that do not themselves generate incompatibilities interact to affect the probability that hybrids evolve symmetrical incompatibilities with their parent species. Unsurprisingly, selection against admixture at “adaptive” loci that are linked to loci that generate incompatibilities tends to reduce the probability of evolving symmetrical incompatibilities. By contrast, selection that favors admixed genotypes at adaptive loci can promote the evolution of symmetrical incompatibilities. The magnitude of these outcomes is affected by the strength of selection, aspects of genetic architecture such as linkage relationships and the linear arrangement of loci along a chromosome, and the amount of hybridization following the formation of a hybrid zone. These results highlight how understanding the nature of selection, aspects of the genetics of traits affecting fitness, and the strength of reproductive isolation between hybridizing taxa can all be used to inform when we expect to observe homoploid hybrid speciation due to symmetrical incompatibilities.

Highlights

Modern genomic data and analyses are revealing that naturally occurring hybridization and admixture between divergent lineages is not rare (Maqbool et al 2015; Racimo et al 2015; Pease et al 2016; Wallbank et al 2016)
Genome-wide sequence data has led to an increased appreciation of the prevalence of admixture and introgression between species (Payseur & Rieseberg 2016; Pease et al 2016; Wallbank et al 2016)
While the consequences of hybridization have historically been viewed as maladaptive (Fisher 1930), others have proposed that hybridization can be a generative force that facilitates adaptive evolution and speciation (Seehausen 2004; Mallet 2007; Hedrick 2013; Nieto Feliner et al 2017)

Summary

Introduction

Modern genomic data and analyses are revealing that naturally occurring hybridization and admixture between divergent lineages is not rare (Maqbool et al 2015; Racimo et al 2015; Pease et al 2016; Wallbank et al 2016). The evolutionary consequences of hybridization are diverse. Hybridization has been described as “the grossest blunder in sexual preference which we can conceive of an animal making” (Fisher 1930). Hybridization can be a generative force, facilitating. Dasmahapatra et al 2012) or promoting diversification through hybrid speciation (Anderson & Stebbins 1954; Buerkle et al 2000; Gross & Rieseberg 2005; Mallet 2007). Guzman et al 2009; Salazar et al 2010; Nice et al 2013; Hermansen et al 2014; Lamichhaney et al 2017), and some have suggested that hybridization may be responsible for a larger fraction of species diversity than previously appreciated Linking the specific mechanism(s) through which hybridization causally leads to the evolution of reproductive isolation (RI) between hybrids and their parents, in many putative cases, remains a major challenge (Schumer et al 2014)

Methods

Results

Conclusion