The challenges of detecting subtle population structure and its importance for the conservation of emperor penguins

Jane L. Younger, Gemma V. Clucas, Damian Kao, Alex D. Rogers, Karim Gharbi, Tom Hart, Karen J. Miller

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Abstract

Understanding the boundaries of breeding populations is of great importance for conservation efforts and estimates of extinction risk for threatened species. However, determining these boundaries can be difficult when population structure is subtle. Emperor penguins are highly reliant on sea ice, and some populations may be in jeopardy as climate change alters sea-ice extent and quality. An understanding of emperor penguin population structure is therefore urgently needed. Two previous studies have differed in their conclusions, particularly whether the Ross Sea, a major stronghold for the species, is isolated or not. We assessed emperor penguin population structure using 4,596 genome-wide single nucleotide polymorphisms (SNPs), characterized in 110 individuals (10–16 per colony) from eight colonies around Antarctica. In contrast to a previous conclusion that emperor penguins are panmictic around the entire continent, we find that emperor penguins comprise at least four metapopulations, and that the Ross Sea is clearly a distinct metapopulation. Using larger sample sizes and a thorough assessment of the limitations of different analytical methods, we have shown that population structure within emperor penguins does exist and argue that its recognition is vital for the effective conservation of the species. We discuss the many difficulties that molecular ecologists and managers face in the detection and interpretation of subtle population structure using large SNP data sets, and argue that subtle structure should be taken into account when determining management strategies for threatened species, until accurate estimates of demographic connectivity among populations can be made.

Original languageEnglish
Pages (from-to)3883-3897
Number of pages15
JournalMolecular Ecology
Volume26
Issue number15
Early online date10 May 2017
DOIs
Publication statusPublished - 27 Jul 2017

Funding

This research was funded by the Australian Antarctic Science Program (Project 4184 ? KM & JY), a Holsworth Wildlife Research Endowment (JY), the Sea World Research and Rescue Foundation (JY & KM), the Natural Environment Research Council (Award 1272500 - GC), an Endeavour Research Fellowship (JY), The Darwin Initiative (DPLUS 002 - TH), an NSF Creative Science Award (DPP-87-15864), the Charities Advisory Trust (TH) and by public donations, in particular through Quark Expeditions Ltd (TH). We gratefully acknowledge the following people and organizations for their kind donations of emperor penguin samples: the Kooyman team at the Ross Sea; Barbara Wienecke and the Australian Antarctic Division at Fold Island, Amanda Bay and Auster; Francoise Amelineau at Pointe G?ologie; Phil Trathan and assistants from the British Antarctic Survey at Halley Bay; and Dick Filby and Hannah McKeand from Adventure Network International at Gould Bay. We would like to thank the Edinburgh Genomics staff for library preparation and sequencing. Edinburgh Genomics is partly supported through core grants from NERC (R8/H10/56), MRC (MR/K001744/1) and BBSRC (BB/J004243/1). We acknowledge the use of the University of Oxford Advanced Research Computing (ARC) facility in carrying out this work (https://doi.org/10.5281/zenodo.22558). We would like to thank Barbara Wienecke and Jerry Kooyman for helpful discussions about emperor penguin population dynamics. Finally, we are very grateful to Michelle LaRue, Laura Benestan, Bruce Deagle and two anonymous reviewers, all of whom gave considered, insightful feedback on both our analytical methods and interpretation of the ecological patterns.

Keywords

  • Antarctica
  • dispersal
  • population genomics
  • RAD-seq
  • Ross Sea
  • Southern Ocean

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

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