Divergent selection and drift shape the genomes of two avian sister species spanning a saline-freshwater ecotone.

Jennifer Walsh,Gemma V Clucas,Adrienne I Kovach,W Kelley Thomas,Matthew D Macmanes

doi:10.1002/ece3.5804

Abstract

The role of species divergence due to ecologically based divergent selection—or ecological speciation—in generating and maintaining biodiversity is a central question in evolutionary biology. Comparison of the genomes of phylogenetically related taxa spanning a selective habitat gradient enables discovery of divergent signatures of selection and thereby provides valuable insight into the role of divergent ecological selection in speciation. Tidal marsh ecosystems provide tractable opportunities for studying organisms' adaptations to selective pressures that underlie ecological divergence. Sharp environmental gradients across the saline–freshwater ecotone within tidal marshes present extreme adaptive challenges to terrestrial vertebrates. Here, we sequence 20 whole genomes of two avian sister species endemic to tidal marshes—the saltmarsh sparrow (Ammospiza caudacutus) and Nelson's sparrow (A. nelsoni)—to evaluate the influence of selective and demographic processes in shaping genome‐wide patterns of divergence. Genome‐wide divergence between these two recently diverged sister species was notably high (genome‐wide F ST = 0.32). Against a background of high genome‐wide divergence, regions of elevated divergence were widespread throughout the genome, as opposed to focused within islands of differentiation. These patterns may be the result of genetic drift resulting from past tidal march colonization events in conjunction with divergent selection to different environments. We identified several candidate genes that exhibited elevated divergence between saltmarsh and Nelson's sparrows, including genes linked to osmotic regulation, circadian rhythm, and plumage melanism—all putative candidates linked to adaptation to tidal marsh environments. These findings provide new insights into the roles of divergent selection and genetic drift in generating and maintaining biodiversity.

Highlights

The role of differential adaptation to divergent selective environments in generating and maintaining biodiversity has become an increasing focus for evolutionary biologists over the past decade and has been termed ecological speciation (Schluter 2001; Rundle and Nosil, 2005; Funk et al 2006)
The genomics era holds promise for ecological speciation research, as it has allowed for the detection of divergent signatures of selection on a genome-wide scale
Our findings differ from genomic comparisons between other shallowly diverged, hybridizing taxa

Summary

Introduction

The role of differential adaptation to divergent selective environments in generating and maintaining biodiversity has become an increasing focus for evolutionary biologists over the past decade and has been termed ecological speciation (Schluter 2001; Rundle and Nosil, 2005; Funk et al 2006). While the concept of ecologically-based divergent selection is not new (Mayr 1942; Rundle and Nosil 2005), disentangling the contribution of ecological forces from nonecologically based evolutionary forces (i.e., reductions in population size, genetic drift) remains a challenge. Despite these challenges, increasing accessibility and improvement of current sequencing technologies have allowed for application of whole-genome sequencing to questions in natural populations (Ellegren 2014; Toews et al 2016; Campagna et al 2017). It has provided insight into the genomic architecture of adaptation and speciation (Strasburg et al 2011, Cruickshank and Hahn, 2014, Larson et al 2017)

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