Genetic diversity and demographic history of the leopard seal: A Southern Ocean top predator

PLOS ONE RESEARCH ARTICLE Genetic diversity and demographic history of the leopard seal: A Southern Ocean top predator Arona N. Bender ID1, Douglas J. Krause2, Michael E. Goebel3, Joseph I. Hoffman4,5, Eric A. Lewallen6, Carolina A. Bonin ID1,6* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Marine and Environmental Sciences Department, Hampton University, Hampton, VA, United States of America, 2 Antarctic Ecosystem Research Division, Southwest Fisheries Science Center, NOAA Fisheries, La Jolla, CA, United States of America, 3 Ecology and Evolutionary Biology Department, University of California, Santa Cruz, Santa Cruz, CA, United States of America, 4 Department of Animal Behaviour, University of Bielefeld, Bielefeld, Germany, 5 British Antarctic Survey, Cambridge, United Kingdom, 6 Department of Biological Sciences, Hampton University, Hampton, VA, United States of America * Abstract OPEN ACCESS Citation: Bender AN, Krause DJ, Goebel ME, Hoffman JI, Lewallen E., Bonin CA (2023) Genetic diversity and demographic history of the leopard seal: A Southern Ocean top predator. PLoS ONE 18(8): e0284640. https://doi.org/10.1371/journal. pone.0284640 Editor: Axel Janke, Senckenberg am Meer Deutsches Zentrum fur Marine Biodiversitatsforschung, GERMANY Received: April 3, 2023 Accepted: June 14, 2023 Published: August 11, 2023 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Leopard seals (Hydrurga leptonyx) are top predators that can exert substantial top-down control of their Antarctic prey species. However, population trends and genetic diversity of leopard seals remain understudied, limiting our understanding of their ecological role. We investigated the genetic diversity, effective population size and demographic history of leopard seals to provide fundamental data that contextualizes their predatory influence on Antarctic ecosystems. Ninety leopard seals were sampled from the northern Antarctic Peninsula during the austral summers of 2008–2019 and a 405bp segment of the mitochondrial control region was sequenced for each individual. We uncovered moderate levels of nucleotide (π = 0.013) and haplotype (Hd = 0.96) diversity, and the effective population size was estimated at around 24,000 individuals (NE = 24,376; 95% CI: 16,876–33,126). Consistent with findings from other ice-breeding pinnipeds, Bayesian skyline analysis also revealed evidence for population expansion during the last glacial maximum, suggesting that historical population growth may have been boosted by an increase in the abundance of sea ice. Although leopard seals can be found in warmer, sub-Antarctic locations, the species’ core habitat is centered on the Antarctic, making it inherently vulnerable to the loss of sea ice habitat due to climate change. Therefore, detailed assessments of past and present leopard seal population trends are needed to inform policies for Antarctic ecosystems. Data Availability Statement: Genetic sequences have been deposited in GenBank (accession numbers OQ451774-OQ451802 correspond to new haplotypes detected in this study). Funding: ANB: NA16SEC4810007 and NA11SEC4810002 (National Oceanic and Atmospheric Administration Living Marine Resources Cooperative Science Center, https:// www.noaa.gov/office-education/epp-msi/csc/noaaliving-marine-resources-cooperative-science- Introduction Marine mammals are increasingly being impacted by human-induced climate change and many polar species may not be able to respond at the rate required for their long-term survival [1, 2]. However, species-specific responses to changing environments are far from uniform, even within the same ecosystem (e.g., Arctic [3]). Surprisingly, population trends remain PLOS ONE | https://doi.org/10.1371/journal.pone.0284640 August 11, 2023 1 / 16 PLOS ONE center) CAB: NSF HRD # 2000211 and NSF OPP # 2146068 (National Science Foundation, https:// www.nsf.gov/awardsearch/showAward?AWD_ID= 2000211&HistoricalAwards=false; https://www.nsf. gov/awardsearch/showAward?AWD_ID= 2146068&HistoricalAwards=false) The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Leopard seal historical demography unknown for several conspicuous polar species, including top predators such as leopard seals, Hydrurga leptonyx [4]. Direct observations of this species in traditional surveys across the Antarctic are hindered by its broad and remote geographical distribution, low population density, and the adverse weather conditions that are commonly encountered in their main breeding habitats [5, 6].Therefore, indirect assessments, such as population genetic analyses, are invaluable for providing fundamental insights into the population dynamics and natural history of such species [7]. Contemporary neutral genetic variation retains valuable information that allows the inference of population sizes of past generations [8]. Specifically, the effective population size (NE) scales with the magnitude of genetic drift in an ideal population at equilibrium [9]. Most importantly, fluctuations in this parameter can be used to detect changes in species abundance over time, which can reveal past responses to environmentally and anthropogenically induced changes in habitat availability. For several species of pinnipeds, population genetic studies have uncovered past demographic impacts of large-scale climate change events driven by the El Niño Southern Oscillation [10] and the potential effects of post-glacial ice retreat on population expansion, recolonization and population structure [11–13]. These studies are fundamental for predicting how species will respond to future climate perturbations and for identifying taxonomic units that deserve prioritized conservation status. Explorations of large genetic datasets across pinniped lineages also highlight biological traits that influence genetic variation over time. For example, breeding habitat preference (land versus ice) is an important determinant of genetic variation in pinnipeds [14, 15], as substantial losses of genetic variation due to commercial sealing have been detected in gregarious pinniped species that breed on land [14]. Although this cumulative work represents a notable effort in terms of gathering samples and data for multiple pinniped species, some species have not yet been investigated. This reflects the difficulty of gathering samples from species breeding in remote, fluid and vast habitats such as the Antarctic pack ice. The Lobodontini tribe (Antarctic ice seals) includes four species: the Ross seal (Ommatophoca rossii), the crabeater seal (Lobodon carcinophagus), the Weddell seal (...truncated)