Genomics of rapid ecological divergence and parallel adaptation in four tidal marsh sparrows.

Jennifer Walsh,Chris S Elphick,Bronwyn G Butcher,Virginia L Winder,Petra E Deane-Coe,Brian J Olsen,Phred M Benham,W Gregory Shriver,Peter Arcese,Yvonne L Chan,Zachary A Cheviron,Adrienne I Kovach,Irby J Lovette

doi:10.1002/evl3.126

Abstract

Theory suggests that different taxa having colonized a similar, challenging environment will show parallel or lineage‐specific adaptations to shared selection pressures, but empirical examples of parallel evolution in independent taxa are exceedingly rare. We employed comparative genomics to identify parallel and lineage‐specific responses to selection within and among four species of North American sparrows that represent four independent, post‐Pleistocene colonization events by an ancestral, upland subspecies and a derived salt marsh specialist. We identified multiple cases of parallel adaptation in these independent comparisons following salt marsh colonization, including selection of 12 candidate genes linked to osmoregulation. In addition to detecting shared genetic targets of selection across multiple comparisons, we found many novel, species‐specific signatures of selection, including evidence of selection of loci associated with both physiological and behavioral mechanisms of osmoregulation. Demographic reconstructions of all four species highlighted their recent divergence and small effective population sizes, as expected given their rapid radiation into saline environments. Our results highlight the interplay of both shared and lineage‐specific selection pressures in the colonization of a biotically and abiotically challenging habitat and confirm theoretical expectations that steep environmental clines can drive repeated and rapid evolutionary diversification in birds.

Highlights

IntroductionAdaptive variation in avian taxa that span such salinity gradients is well documented for both physiological and morphological traits (Grinnell 1913; Luttrell et al 2015), including convergence in (1) bill size, as salt marsh birds have larger bills to facilitate greater heat exchange in harsh, open environments such as salt marshes (Grenier and Greenberg 2006; Greenberg and Olsen 2010; Tattersall et al 2017); (2) modified kidney structure, as well as modified drinking behaviors in response to salt water, as salt marsh birds curb the volume of their drinking at saline concentrations below their osmotic tolerance, whereas their upland relatives do not (Poulson 1969; Goldstein 2006); and (3) coloration, as salt marsh birds are typically more melanic than their upland relatives, an adaptation potentially linked to UV protection and resistance to bacterial degradation (Greenberg and Droege 1990; Luttrell et al 2015)
GENOME-WIDE PATTERNS OF DIVERGENCE BETWEEN UPLAND AND SALT MARSH ENVIRONMENTS For each of the four species pairs, we documented a clear division between salt marsh and upland populations based on 2.3–13 million single-nucleotide polymorphisms (SNPs; Fig. 2 and Fig. S2)
The magnitude of differentiation between upland and salt marsh populations varied, we found a strong delineation between all pairs of salt marsh and upland populations, highlighting the clear potential for similar processes of ecological divergence across the freshwater-saline habitat barrier

Summary

Introduction

Adaptive variation in avian taxa that span such salinity gradients is well documented for both physiological and morphological traits (Grinnell 1913; Luttrell et al 2015), including convergence in (1) bill size, as salt marsh birds have larger bills to facilitate greater heat exchange in harsh, open environments such as salt marshes (Grenier and Greenberg 2006; Greenberg and Olsen 2010; Tattersall et al 2017); (2) modified kidney structure, as well as modified drinking behaviors in response to salt water, as salt marsh birds curb the volume of their drinking at saline concentrations below their osmotic tolerance, whereas their upland relatives do not (Poulson 1969; Goldstein 2006); and (3) coloration, as salt marsh birds are typically more melanic than their upland relatives, an adaptation potentially linked to UV protection and resistance to bacterial degradation (Greenberg and Droege 1990; Luttrell et al 2015) Despite these known parallels in heritable phenotypic traits, neutral genetic differentiation between upland and salt marsh populations is notably low in many species, suggesting a strong role for ecological selection in salt marsh populations (Chan and Arcese 2002; Greenberg et al 2016). By studying divergence across these steep ecological gradients across multiple lineages, we can explore the genetic architecture of convergent evolution and begin to answer the question: do taxa experiencing shared selective pressures adapt via parallel selection on the same genes and pathways or via lineagespecific selection on different genes and pathways that lead to a similar functional endpoint?

Methods

Results

Discussion

Conclusion