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

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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. In order to understand how biodiversity is generated and maintained over time, we need to understand the process by which populations form and diverge. Natural variation within species is typically partitioned among populations, which sometimes forms the basis for speciation events. One mechanism for the establishment of novel variation at the population level is through a response to emerging habitat. Here we use data from ancient DNA to show how elephant seal populations responded when new breeding habitat was gained and then lost over the course of approximately 7,000 years. We show that the seals quickly took advantage of newly available breeding habitat, far from the nearest extant breeding site, and that a highly diverse and genetically differentiated population was established over a matter of generations. The key factors were likely the abundant local food resource and extensive physical habitat that allowed rapid expansion after the initial founder event and a tendency for females to return to annual breeding sites in this species. Tracking the founder-extinction dynamics of historical populations provides insight into the likely implications of future environmental change. This is an important tool in our efforts to mitigate the impact of human-induced change.

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