Abstract

Evidence is rapidly accumulating that hybridization generates adaptive variation. Transgressive segregation in hybrids could promote the colonization of new environments. Here, we use an assay to select hybrid genotypes that can proliferate in environmental conditions beyond the conditions tolerated by their parents, and we directly compete them against parental genotypes in habitats across environmental clines. We made 45 different hybrid swarms by crossing yeast strains (both Saccharomyces cerevisiae and S.paradoxus) with different genetic and phenotypic divergence. We compared the ability of hybrids and parents to colonize seven types of increasingly extreme environmental clines, representing both natural and novel challenges (mimicking pollution events). We found that a significant majority of hybrids had greater environmental ranges compared to the average of both their parents' ranges (mid-parent transgression), but only a minority of hybrids had ranges exceeding their best parent (best-parent transgression). Transgression was affected by the specific strains involved in the cross and by the test environment. Genetic and phenotypic crossing distance predicted the extent of transgression in only two of the seven environments. We isolated a set of potentially transgressive hybrids selected at the extreme ends of the clines and found that many could directly outcompete their parents across whole clines and were between 1.5- and 3-fold fitter on average. Saccharomyces yeast is a good model for quantitative and replicable experimental speciation studies, which may be useful in a world where hybridization is becoming increasingly common due to the relocation of plants and animals by humans.

Highlights

  • Evidence is accumulating rapidly from all parts of the tree of life that hybridization between species or highly diverged populations can generate adaptive variation

  • We looked at the differences between the environmental ranges of each hybrid and its parent with the largest range, rather than the mean range of both parents

  • Our transgression assay was designed to select hybrid genotypes from swarms that could grow beyond the environmental range of their clonal parents

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Summary

Introduction

Evidence is accumulating rapidly from all parts of the tree of life that hybridization between species or highly diverged populations can generate adaptive variation. Hybrids often have trait values that lie between those of their parents. They usually become outcompeted by the parent species because their phenotypic intermediacy leaves them poorly adapted to both ancestral habitats (Vamosi et al, 2000; Gow et al, 2007; Svedin et al, 2008). Hybrids can express trait values that fall outside the range of both parent species, which is known as transgression (Slatkin & Lande, 1994; Rieseberg et al, 1999). Transgression has been a 2014 THE AUTHORS.

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