Comparative population genomics reveals key barriers to dispersal in Southern Ocean penguins.

Gemma V Clucas,Sarah Crofts,Louise Emmerson,Patrick Lelliott,Karen J Miller,Jane L Younger,Tom Hart,Damian Kao,Michael J Dunn,Michael J Polito,Alex D Rogers,Barbara Wienecke,Colin Southwell,Richard A Phillips,Charles‐André Bost,Jonathan Handley,Gary D Miller

doi:10.1111/mec.14896

Abstract

The mechanisms that determine patterns of species dispersal are important factors in the production and maintenance of biodiversity. Understanding these mechanisms helps to forecast the responses of species to environmental change. Here, we used a comparative framework and genomewide data obtained through RAD-Seq to compare the patterns of connectivity among breeding colonies for five penguin species with shared ancestry, overlapping distributions and differing ecological niches, allowing an examination of the intrinsic and extrinsic barriers governing dispersal patterns. Our findings show that at-sea range and oceanography underlie patterns of dispersal in these penguins. The pelagic niche of emperor (Aptenodytes forsteri), king (A. patagonicus), Adélie (Pygoscelis adeliae) and chinstrap (P. antarctica) penguins facilitates gene flow over thousands of kilometres. In contrast, the coastal niche of gentoo penguins (P. papua) limits dispersal, resulting in population divergences. Oceanographic fronts also act as dispersal barriers to some extent. We recommend that forecasts of extinction risk incorporate dispersal and that management units are defined by at-sea range and oceanography in species lacking genetic data.

Highlights

During the last 2.58 million years, periods of global warming and cooling have shaped the evolutionary trajectories of species around the globe (Hewitt, 2004), with those inhabiting the polar regions having been subject to the most extreme climatic shifts
There was no evidence for lane effects in our data: Sequencing depth did not vary significantly among lanes, the locations of single nucleotide polymorphism (SNP) called within reads were even and similar across lanes, and the patterns of population structure that we found showed no relationship to the lanes on which individuals were sequenced
Given the large number of outliers in the gentoo penguin data set, we investigated whether loci putatively under selection were influencing patterns of genetic differentiation by comparing pairwise FST values from both the neutral and total SNP data sets (Supporting information Tables S4, S5)

Summary

| INTRODUCTION

During the last 2.58 million years, periods of global warming and cooling have shaped the evolutionary trajectories of species around the globe (Hewitt, 2004), with those inhabiting the polar regions having been subject to the most extreme climatic shifts. Seabirds are highly threatened (Croxall et al, 2012), mobile and capable of dispersing large distances with few apparent abiotic barriers to movement, yet most are characterized by high levels of philopatry (Coulson, 2002). This appears to be the case for Antarctic and sub-Antarctic penguins, but they present a significant logistical challenge for studying dispersal (defined here as movement away from natal colonies to alternate breeding sites), as the vast majority of colonies are in remote locations. We generated robust single nucleotide polymorphism (SNP) data sets for five species of penguin, covering the majority of each species’ range (Figure 1), and compared the levels of dispersal within each species

| METHODS

| DISCUSSION

Findings

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