Rapid Response of a Marine Mammal Species to Holocene Climate and Habitat Change

Mark De Bruyn,A Rus Hoelzel,Carlo Baroni,Lucas F Chauke,Paul L Koch,Brenda L Hall,Molly Przeworski

doi:10.1371/journal.pgen.1000554

Abstract

Environmental change drives demographic and evolutionary processes that determine diversity within and among species. Tracking these processes during periods of change reveals mechanisms for the establishment of populations and provides predictive data on response to potential future impacts, including those caused by anthropogenic climate change. Here we show how a highly mobile marine species responded to the gain and loss of new breeding habitat. Southern elephant seal, Mirounga leonina, remains were found along the Victoria Land Coast (VLC) in the Ross Sea, Antarctica, 2,500 km from the nearest extant breeding site on Macquarie Island (MQ). This habitat was released after retreat of the grounded ice sheet in the Ross Sea Embayment 7,500–8,000 cal YBP, and is within the range of modern foraging excursions from the MQ colony. Using ancient mtDNA and coalescent models, we tracked the population dynamics of the now extinct VLC colony and the connectivity between this and extant breeding sites. We found a clear expansion signal in the VLC population ∼8,000 YBP, followed by directional migration away from VLC and the loss of diversity at ∼1,000 YBP, when sea ice is thought to have expanded. Our data suggest that VLC seals came initially from MQ and that some returned there once the VLC habitat was lost, ∼7,000 years later. We track the founder-extinction dynamics of a population from inception to extinction in the context of Holocene climate change and present evidence that an unexpectedly diverse, differentiated breeding population was founded from a distant source population soon after habitat became available.

Highlights

Populations can respond to changing habitats by adapting, moving, by adjusting population size, or some combination of the above
While a large degree of reticulation was evident for the Victoria Land Coast (VLC) samples (Figure 2), all methods unambiguously defined two major lineages; the ancient VLC samples together with extant samples from Macquarie Island (MQ), and a lineage including all other extant colonies (Figure 2; only median-joining network reconstructions are shown)
Bayesian analyses of the ancient VLC data, incorporating an explicit post-mortem damage model [15], calibrated against the estimated calendar age of the ancient samples (Table S1) produced a mitochondrial DNA (mtDNA) hypervariable region (HVR) rate estimate of 9.8061027 (Figure S1; 95% highest posterior density interval (HPDI) 1.6761029–2.0661026) substitutions per site per year (s.s.yr21). This rate is in agreement with estimates obtained from various other ancient DNA (aDNA) datasets [16] including a close match with an HVR rate of 9.661027 s.s.yr21 calculated over a similar timeframe (6,424 YBP) from Adelie penguin aDNA [17], and with the mean human HVR pedigree rate estimate derived from a meta-analysis (9.561027 s.s.yr21) [18]

Summary

Introduction

Populations can respond to changing habitats by adapting (through natural selection or phenotypic plasticity), moving (to avoid habitat of reduced suitability, or take advantage of emerging habitat), by adjusting population size, or some combination of the above. Both natural selection and genetic drift can shape populations as they evolve in this context. It is unusual for there to be an opportunity to track population dynamics and genetics during extended periods of environmental change, but a extinct population of elephant seals from the Victoria Land Coast (VLC) in the Ross Sea, Antarctica provides such an opportunity. Today the region is mostly enclosed by year round land-fast sea ice, and is unsuitable for southern elephant seal breeding.

Methods

Results

Conclusion