Genetic architecture influences when and how hybridization contributes to colonization.

Bryan Reatini,Todd J Vision

doi:10.1111/evo.13972

Abstract

The role of genetic architecture in adaptation to novel environments has received considerable attention when the source of adaptive variation is de novo mutation. Relatively less is known when the source of adaptive variation is inter- or intraspecific hybridization. We model hybridization between divergent source populations and subsequent colonization of an unoccupied novel environment using individual-based simulations to understand the influence of genetic architecture on the timing of colonization and the mode of adaptation. We find that two distinct categories of genetic architecture facilitate rapid colonization but that they do so in qualitatively different ways. For few and/or tightly linked loci, the mode of adaptation is via the recovery of adaptive parental genotypes. With many unlinked loci, the mode of adaptation is via the generation of novel hybrid genotypes. The first category results in the shortest colonization lag phases across the widest range of parameter space, but further adaptation is mutation limited. The second category takes longer and is more sensitive to genetic variance and dispersal rate, but can facilitate adaptation to environmental conditions that exceed the tolerance of parental populations. These findings have implications for understanding the origins of biological invasions and the success of hybrid populations.

Highlights

A persistent question regarding the source of adaptive variation leading to colonization is why intra and interspecific admixture – hereafter collectively referred to as hybridization – sometimes leads to increased colonization success and sometimes does not (Bock et al, 2015; Dlugosch et al, 2015)
Range expansion may commonly be facilitated by gene flow rather than de novo mutation, and studies on the genetic architecture of colonization and range expansion stemming from hybridization are currently lacking
We test two underlying predictions: (1) that colonization lag phase duration is sensitive to the genetic architecture of invasiveness traits, (2) that architectures resistant to genetic swamping will produce relatively short lag phases

Summary

Introduction

A persistent question regarding the source of adaptive variation leading to colonization is why intra and interspecific admixture – hereafter collectively referred to as hybridization – sometimes leads to increased colonization success and sometimes does not (Bock et al, 2015; Dlugosch et al, 2015). Architectures dominated by alleles with large selection coefficients and/or tightly linked loci are more resistant to swamping than those dominated by alleles with small selection coefficients and/or unlinked loci (Tigano and Friesen, 2016; Yeaman and Whitlock, 2011), architectures characterized by many alleles of small effect may be robust to genetic swamping when genetic variance is sufficiently high (Yeaman, 2015) The implication of this is that, when looking retrospectively at adaptations in systems where there has been persistent gene flow, swampingresistant genetic architectures may be more likely to be observed. Using a source-sink model incorporating adaptation from mutation, Holt et al (2003) demonstrated that transient occupancy of a sink can persist for a long time before punctuated growth following adaptation Given these findings, we hypothesize that genetic architecture, which will influence the recovery of adaptive variation in newly formed hybrid populations, will influence the duration of the lag phase. We test an additional prediction: the filtering effect of colonization on genetic architecture will influence the ability of resulting colonist populations to occupy and adapt to more extreme environments – an important characteristic for hybrid speciation and adaptive radiation

Methods

Results

Literature Cited