Mitogenomics data reveal effective population size, historical bottlenecks, and the effects of hunting on New Zealand fur seals (Arctocephalus forsteri)

Abstract The New Zealand fur seal (Arctocephalus forsteri) passed through a population bottleneck due to commercial sealing during the eighteenth to nineteenth centuries. To facilitate future management options, we reconstructed the demographic history of New Zealand fur seals in a Bayesian framework using maternally inherited, mitochondrial DNA sequences. Mitogenomic data suggested two separate clades (most recent common ancestor 5000 years ago) of New Zealand fur seals that survived large-scale human harvest. Mitochondrial haplotype diversity was high, with 45 singletons identified from 46 individuals although mean nucleotide diversity was low (0.012 ± 0.0061). Variation was not constrained geographically. Analyses of mitogenomes support the hypothesis for a population bottleneck approximately 35 generations ago, which coincides with the peak of commercial sealing. Mitogenomic data are consistent with a pre-human effective population size of approximately 30,000 that first declined to around 10,000 (due to the impact of Polynesian colonization, particularly in the first 100 years of their arrival into New Zealand), and then to 100–200 breeding individuals during peak of commercial sealing.

[1]  N. Gemmell,et al.  Myth or relict: Does ancient DNA detect the enigmatic Upland seal? , 2016, Molecular phylogenetics and evolution.

[2]  Jean-Marie Cornuet,et al.  DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data , 2014, Bioinform..

[3]  Rasmus Heller,et al.  The Confounding Effect of Population Structure on Bayesian Skyline Plot Inferences of Demographic History , 2013, PloS one.

[4]  F. W. Hutton,et al.  The animals of New Zealand , 2013 .

[5]  E. Cook,et al.  Rapid landscape transformation in South Island, New Zealand, following initial Polynesian settlement , 2010, Proceedings of the National Academy of Sciences.

[6]  B. Goossens,et al.  The Confounding Effects of Population Structure, Genetic Diversity and the Sampling Scheme on the Detection and Quantification of Population Size Changes , 2010, Genetics.

[7]  J. Mann,et al.  Inbreeding tolerance and fitness costs in wild bottlenose dolphins , 2010, Proceedings of the Royal Society B: Biological Sciences.

[8]  F. Zachos,et al.  Non-invasive genetic analysis reveals high levels of mtDNA variability in the endangered South-American marine otter (Lontra felina) , 2010, Conservation Genetics.

[9]  C. Baroni,et al.  Rapid Response of a Marine Mammal Species to Holocene Climate and Habitat Change , 2009, PLoS genetics.

[10]  W. Stephan,et al.  The Impact of Sampling Schemes on the Site Frequency Spectrum in Nonequilibrium Subdivided Populations , 2009, Genetics.

[11]  Dirk Husmeier,et al.  TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops , 2008, Bioinform..

[12]  R. Toonen,et al.  Extremely low genetic diversity in the endangered Hawaiian monk seal (Monachus schauinslandi). , 2008, The Journal of heredity.

[13]  Janet M. Wilmshurst,et al.  Dating the late prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat , 2008, Proceedings of the National Academy of Sciences.

[14]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[15]  L. Excoffier,et al.  Statistical evaluation of alternative models of human evolution , 2007, Proceedings of the National Academy of Sciences.

[16]  G. Stenson,et al.  Panmictic population structure in the hooded seal (Cystophora cristata) , 2007, Molecular ecology.

[17]  J. Kingston,et al.  Hybridization between two sympatrically breeding species of fur seal at Iles Crozet revealed by genetic analysis , 2007, Conservation Genetics.

[18]  G. Amato,et al.  Microsatellite diversity and fitness in stranded juvenile harp seals (Phoca groenlandica). , 2006, The Journal of heredity.

[19]  N. Gemmell,et al.  Colony growth and pup condition of the New Zealand fur seal (Arctocephalus forsteri) on the Kaikoura coastline compared with other east coast colonies , 2006 .

[20]  N. Gemmell,et al.  Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction , 2006, Molecular ecology.

[21]  Mary K. Kuhner,et al.  LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters , 2006, Bioinform..

[22]  K. Tolley,et al.  Mitochondrial DNA sequence data of the Cape fur seal (Arctocephalus pusillus pusillus) suggest that population numbers may be affected by climatic shifts , 2006 .

[23]  T. Loughlin,et al.  VARIATION OF MITOCHONDRIAL CONTROL REGION SEQUENCES OF STELLER SEA LIONS: THE THREE-STOCK HYPOTHESIS , 2005 .

[24]  O. Pybus,et al.  Bayesian coalescent inference of past population dynamics from molecular sequences. , 2005, Molecular biology and evolution.

[25]  Jean-Marie Cornuet,et al.  Bayesian Analysis of an Admixture Model With Mutations and Arbitrarily Linked Markers , 2005, Genetics.

[26]  S. Schneider,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[27]  R. Frankham,et al.  Most species are not driven to extinction before genetic factors impact them. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Garza,et al.  Low genetic variability in the highly endangered mediterranean monk seal. , 2004, The Journal of heredity.

[29]  I. Boyd,et al.  Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus) , 2004, Molecular ecology.

[30]  N. Lehman,et al.  Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). , 2004, The Journal of heredity.

[31]  R. Nowak,et al.  Walker's Marine Mammals of the World , 2003 .

[32]  W. Amos,et al.  Inbreeding: Disease susceptibility in California sea lions , 2003, Nature.

[33]  David Penny,et al.  Four new mitochondrial genomes and the increased stability of evolutionary trees of mammals from improved taxon sampling. , 2002, Molecular biology and evolution.

[34]  B. L. Boeuf,et al.  Impact of a population bottleneck on symmetry and genetic diversity in the northern elephant seal , 2002 .

[35]  E. Korpimäki,et al.  Changes in population structure and reproduction during a 3‐yr population cycle of voles , 2002 .

[36]  J. Bickham,et al.  Phylogenetic relationships within the eared seals (Otariidae: Carnivora): implications for the historical biogeography of the family. , 2001, Molecular phylogenetics and evolution.

[37]  J. Croxall,et al.  The influence of parental relatedness on reproductive success , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  C. Bradshaw,et al.  Folklore and chimerical numbers: Review of a millennium of interaction between fur seals and humans in the New Zealand region , 2001 .

[39]  R. Harcourt.  Advances in New Zealand mammalogy 1990–2000: Pinnipeds , 2001 .

[40]  N. Lehman,et al.  An empirical genetic assessment of the severity of the northern elephant seal population bottleneck , 2000, Current Biology.

[41]  R. Fleischer,et al.  Variation in the mitochondrial control region in the Juan Fernández fur seal (Arctocephalus philippii). , 2000, The Journal of heredity.

[42]  R. Holdaway,et al.  Rapid extinction of the moas (Aves: Dinornithiformes): model, test, and implications. , 2000, Science.

[43]  I. Boyd,et al.  Postsealing genetic variation and population structure of two species of fur seal (Arctocephalus gazella and A. tropicalis) , 2000, Molecular ecology.

[44]  L. Excoffier,et al.  Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. , 1999, Genetics.

[45]  N. Lehman.  Conservation biology: Genes are not enough , 1998, Current Biology.

[46]  D. Coltman,et al.  Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[47]  Robert C. Lacy,et al.  Importance of Genetic Variation to the Viability of Mammalian Populations , 1997 .

[48]  G. Lento,et al.  Genetic variation of southern hemisphere fur seals (Arctocephalus spp.): investigation of population structure and species identity. , 1997, The Journal of heredity.

[49]  R. Lande,et al.  THE ROLE OF GENETIC VARIATION IN ADAPTATION AND POPULATION PERSISTENCE IN A CHANGING ENVIRONMENT , 1996, Evolution; international journal of organic evolution.

[50]  J. Baker,et al.  Natal site fidelity in northern fur seals, Callorhinus ursinus , 1995, Animal Behaviour.

[51]  P. Wilson,et al.  Population status and breeding of New Zealand fur seals (Arctocephalus forsteri) in the Nelson‐northern Marlborough region, 1991–94 , 1995 .

[52]  R. Harcourt,et al.  Pup production of the New Zealand fur seal on Otago Peninsula, New Zealand , 1995 .

[53]  M. Lynch,et al.  EVOLUTION AND EXTINCTION IN A CHANGING ENVIRONMENT: A QUANTITATIVE‐GENETIC ANALYSIS , 1995, Evolution; international journal of organic evolution.

[54]  Peter Arcese,et al.  Selection against inbred song sparrows during a natural population bottleneck , 1994, Nature.

[55]  G. Lento,et al.  Geographic distribution of mitochondrial cytochrome b DNA haplotypes in New Zealand fur seals (Arctocephalus forsteri) , 1994 .

[56]  T. Caro,et al.  Ecological and genetic factors in conservation: a cautionary tale. , 1994, Science.

[57]  S. O’Brien,et al.  Elephant seal genetic variation and the use of simulation models to investigate historical population bottlenecks. , 1993, The Journal of heredity.

[58]  M. Goebel,et al.  THE CAPTURE AND HANDLING OF FEMALE SOUTH AMERICAN FUR SEALS AND THEIR PUPS , 1992 .

[59]  M. Soulé,et al.  Conservation Biology: The Science of Scarcity and Diversity , 1986 .

[60]  P. Fuerst,et al.  Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. , 1985, Genetics.

[61]  F. Tajima.  Evolutionary relationship of DNA sequences in finite populations. , 1983, Genetics.

[62]  R. H. Taylor.  New Zealand fur seals at the Bounty Islands , 1982 .

[63]  D. Hartl,et al.  Principles of population genetics , 1981 .

[64]  G. A. Watterson.  On the number of segregating sites in genetical models without recombination. , 1975, Theoretical population biology.

[65]  M. Nei,et al.  THE BOTTLENECK EFFECT AND GENETIC VARIABILITY IN POPULATIONS , 1975, Evolution; international journal of organic evolution.

[66]  M. Kuefer.  The Encyclopedia Of Mammals , 2016 .

[67]  Mark A. Beaumont,et al.  Joint determination of topology, divergence time, and immigration in population trees , 2008 .

[68]  H. Kishino,et al.  Dating of the human-ape splitting by a molecular clock of mitochondrial DNA , 2005, Journal of Molecular Evolution.

[69]  T. Beebee,et al.  An introduction to molecular ecology , 2004 .

[70]  S. Goldsworthy,et al.  Trophic interactions between marine mammals and Australian fisheries: An ecosystem approach , 2003 .

[71]  A. Paul.  POPULATION BOTTLENECKS AND NONEQUILIBRIUM MODELS IN POPULATION GENETICS. 111. GENIC HOMOZYGOSITY IN POPULATIONS WHICH EXPERIENCE PERIODIC BOTTLENECKS , 2003 .

[72]  C. Bradshaw,et al.  Clustering of colonies in an expanding population of New Zealand fur seals (Arctocephalus forsteri) , 2000 .

[73]  J. Avise.  Speciation and Hybridization , 1994 .

[74]  C. King,et al.  The handbook of New Zealand mammals , 1990 .

[75]  M. McGlone.  The Polynesian settlement of New Zealand in relation to environmental and biotic changes , 1989 .

[76]  Daniel Simberloff,et al.  The Contribution of Population and Community Biology to Conservation Science , 1988 .

[77]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.