Hostname: page-component-745bb68f8f-hvd4g Total loading time: 0 Render date: 2025-01-10T21:31:50.967Z Has data issue: false hasContentIssue false
  • English
  • Français

Population genetic structure and gene flow of Adélie penguins (Pygoscelis adeliae) breeding throughout the western Antarctic Peninsula

Part of: Antarctic Science International Bursary collection: Biosciences

Published online by Cambridge University Press:  28 July 2017

Kristen B. Gorman ,
Sandra L. Talbot ,
Sarah A. Sonsthagen ,
George K. Sage ,
Meg C. Gravely ,
William R. Fraser  and
Tony D. Williams
Kristen B. Gorman*
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada Polar Oceans Research Group, Sheridan, MT 59749, USA Prince William Sound Science Center, Cordova, AK 99574, USA
Sandra L. Talbot
Affiliation:
US Geological Survey, Alaska Science Center, Anchorage, AK 99508, USA
Sarah A. Sonsthagen
Affiliation:
US Geological Survey, Alaska Science Center, Anchorage, AK 99508, USA
George K. Sage
Affiliation:
US Geological Survey, Alaska Science Center, Anchorage, AK 99508, USA
Meg C. Gravely
Affiliation:
US Geological Survey, Alaska Science Center, Anchorage, AK 99508, USA
William R. Fraser
Affiliation:
Polar Oceans Research Group, Sheridan, MT 59749, USA
Tony D. Williams
Affiliation:
Department of Biological Sciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada
*
[email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Adélie penguins (Pygoscelis adeliae) are responding to ocean–climate variability throughout the marine ecosystem of the western Antarctic Peninsula (WAP) where some breeding colonies have declined by 80%. Nuclear and mitochondrial DNA (mtDNA) markers were used to understand historical population genetic structure and gene flow given relatively recent and continuing reductions in sea ice habitats and changes in numbers of breeding adults at colonies throughout the WAP. Genetic diversity, spatial genetic structure, genetic signatures of fluctuations in population demography and gene flow were assessed in four regional Adélie penguin colonies. The analyses indicated little genetic structure overall based on bi-parentally inherited microsatellite markers (FST =-0.006–0.004). No significant variance was observed in overall haplotype frequency (mtDNA ΦST =0.017; P=0.112). Some comparisons with Charcot Island were significant, suggestive of female-biased philopatry. Estimates of gene flow based on a two-population coalescent model were asymmetrical from the species’ regional core to its northern range. Breeding Adélie penguins of the WAP are a panmictic population and hold adequate genetic diversity and dispersal capacity to be resilient to environmental change.

Keywords

climate warmingmicrosatellitemitochondrial DNApopulation delineationsea ice
Type
Biological Sciences
Information
Antarctic Science , Volume 29 , Issue 6 , December 2017 , pp. 499 - 510
Check for updates
Copyright
© Antarctic Science Ltd 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmed, S., Hart, T., Dawson, D.A., Horsburgh, G.J., Trathan, P.N. & Rogers, A.D. 2009. Isolation and characterization of macaroni penguin (Eudyptes chrysolophus) microsatellite loci and their utility in other penguin species (Spheniscidae, AVES). Molecular Ecology Resources, 9, 1530–1535.CrossRefGoogle ScholarPubMed
Ainley, D., Russell, J., Jenouvrier, S., Woehler, E., Lyver, P.O., Fraser, W.R. & Kooyman, G.L. 2010. Antarctic penguin response to habitat change as Earth’s troposphere reaches 2 degrees C above preindustrial levels. Ecological Monographs, 80, 49–66.CrossRefGoogle Scholar
Ainley, D.G. 2002. The Adélie penguin: bellwether of climate change. New York, NY: Columbia University Press, 310 pp.Google Scholar
Ainley, D.G., LeReseche, R.E. & Sladen, W.J. 1983. Breeding biology of the Adélie penguin. Berkeley, CA: University of California Press, 198 pp.Google Scholar
Avise, J.C. 2000. Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press, 464 pp.Google Scholar
Baker, A.J., Pereira, S.L., Haddrath, O.P. & Edge, K.A. 2006. Multiple gene evidence for expansion of extant penguins out of Antarctica due to global cooling. Proceedings of the Royal Society - Biological Sciences, B273, 11–17.Google Scholar
Bandelt, H.J., Forster, P. & Rohl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.Google Scholar
Beerli, P. & Felsenstein, J. 2001. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences of the United States of America, 98, 4563–4568.CrossRefGoogle Scholar
Belkhir, K., Castric, V. & Bonhomme, F. 2002. IDENTIX, a software to test for relatedness in a population using permutation methods. Molecular Ecology Notes, 2, 611–614.Google Scholar
Billing, T.M., Guay, P.J., Peucker, A.J. & Mulder, R.A. 2007. Isolation and characterization of polymorphic microsatellite loci for the study of paternity and population structure in the little penguin Eudyptula minor . Molecular Ecology Notes, 7, 425–427.CrossRefGoogle Scholar
Chapman, E.W., Hofmann, E.E., Patterson, D.L., Ribic, C.A. & Fraser, W.R. 2011. Marine and terrestrial factors affecting Adelie penguin Pygoscelis adeliae chick growth and recruitment off the western Antarctic Peninsula. Marine Ecology Progress Series, 436, 273–289.Google Scholar
Clarke, A.L., Saether, B.E. & Roskaft, E. 1997. Sex biases in avian dispersal: a reappraisal. Oikos, 79, 429–438.CrossRefGoogle Scholar
Clucas, G.V., Dunn, M.J., Dyke, G., Emslie, S.D, Levy, H., Naveen, R., Polito, M.J., Pybus, O.G., Rogers, A.D. & Hart, T. 2014. A reversal of fortunes: climate change ‘winners’ and ‘losers’ in Antarctic Peninsula penguins. Scientific Reports, 10.1038/srep05024.Google Scholar
Cornuet, J.M. & Luikart, G. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001–2014.Google Scholar
Cronin, M.A., Amstrup, S.C., Talbot, S.L., Sage, G.K. & Amstrup, K.S. 2009. Genetic variation, relatedness, and effective population size of polar bears (Ursus maritimus) in the southern Beaufort Sea, Alaska. Journal of Heredity, 100, 681–690.Google Scholar
DiRienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. & Freimer, N.B. 1994. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America, 91, 3166–3170.CrossRefGoogle Scholar
Ducklow, H.W., Fraser, W.R., Meredith, M.P., Stammerjohn, S.E., Doney, S.C., Martinson, D.G., Sailley, S.F., Schofield, O.M., Steinberg, D.K., Venables, H.J. & Amsler, C.D. 2013. West Antarctic Peninsula: an ice-dependent coastal marine ecosystem in transition. Oceanography, 26, 190–203.Google Scholar
Dugger, K.M., Ballard, G., Ainley, D.G. & Barton, K.J. 2006. Effects of flipper bands on foraging behavior and survival of Adélie penguins (Pygoscelis adeliae). Auk, 123, 858–869.Google Scholar
Dugger, K.M., Ainley, D.G., Lyver, P.O., Barton, K. & Ballard, G. 2010. Survival differences and the effect of environmental instability on breeding dispersal in an Adélie penguin meta-population. Proceedings of the National Academy of Sciences of the United States of America, 107, 12 375–12 380.Google Scholar
Dugger, K.M., Ballard, G., Ainley, D.G., Lyver, P.O.B. & Schine, C. 2014. Adélie penguins coping with environmental change: results from a natural experiment at the edge of their breeding range. Frontiers in Ecology and Evolution, 10.3389/fevo.2014.00068.Google Scholar
Emslie, S.D. & McDaniel, J.D. 2002. Adelie penguin diet and climate change during the middle to late Holocene in northern Marguerite Bay, Antarctic Peninsula. Polar Biology, 25, 222–229.Google Scholar
Emslie, S.D., Ritchie, P. & Lambert, D. 2003. Late Holocene penguin occupation and diet at King George Island, Antarctic Peninsula. Antarctic Research Series, 79, 171–180.Google Scholar
Emslie, S.D., Fraser, W., Smith, R.C. & Walker, W. 1998. Abandoned penguin colonies and environmental change in the Palmer Station area, Anvers Island, Antarctic Peninsula. Antarctic Science, 10, 257–268.CrossRefGoogle Scholar
Esler, D., Iverson, S.A. & Rizzolo, D.J. 2006. Genetic and demographic criteria for defining population units for conservation: the value of clear messages. Condor, 108, 480–483.Google Scholar
Evans, S.R. & Sheldon, B.C. 2008. Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conservation Biology, 22, 1016–1025.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. 2005. ARLEQUIN (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–50.Google Scholar
Foden, W.B., Butchart, S.H., Stuart, S.N., Vié, J.-C., Akçakaya, H.R., Angulo, A., DeVantier, L.M., Gutsche, A., Turak, E., Cao, L., Donner, S.D., Katariya, V., Bernard, R., Holland, R.A., Hughes, A.F., O’Hanlon, S.E., Garnett, S.T., Şekercioğlu, Ç.H. & Mace, G.M. 2013. Identifying the world’s most climate change vulnerable species: a systematic trait-based assessment of all birds, amphibians and corals. PLoS ONE, 8, 10.1371/journal.pone.0065427.Google Scholar
Forcada, J. & Trathan, P.N. 2009. Penguin responses to climate change in the Southern Ocean. Global Change Biology, 15, 1618–1630.Google Scholar
Fraser, W.R., Patterson-Fraser, D.L., Ribic, C.A., Schofield, O. & Ducklow, H. 2013. A nonmarine source of variability in Adélie penguin demography. Oceanography, 26, 207–209.Google Scholar
Fraser, W.R., Trivelpiece, W.Z., Ainley, D.G. & Trivelpiece, S.G. 1992. Increases in Antarctic penguin populations: reduced competition with whales or a loss of sea ice due to environmental warming. Polar Biology, 11, 525–531.Google Scholar
Friesen, V.L., Burg, T.M. & McCoy, K.D. 2007. Mechanisms of population differentiation in seabirds. Molecular Ecology, 16, 1765–1785.Google Scholar
Fu, Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915–925.Google Scholar
Gauthier-Clerc, M., Gendner, J.P., Ribic, C.A., Fraser, W.R., Woehler, E.J., Descamps, S., Gilly, C., Le Bohec, C. & Le Maho, Y. 2004. Long-term effects of flipper bands on penguins. Proceedings of the Royal Society - Biological Sciences, B271, S423–S426.Google Scholar
Gorman, K.B., Williams, T.D. & Fraser, W.R. 2014. Ecological sexual dimorphism and environmental variability within a community of Antarctic penguins (genus Pygoscelis). PLoS ONE, 9, 10.1371/journal.pone.0090081.CrossRefGoogle ScholarPubMed
Goudet, J. 1995. FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86, 485–486.CrossRefGoogle Scholar
Goudet, J., Raymond, M., de Meeus, T. & Rousset, F. 1996. Testing differentiation in diploid populations. Genetics, 144, 1933–1940.Google Scholar
Greenwood, P.J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour, 28, 1140–1162.Google Scholar
Henderson, I. 1976. Summer log of travel and work of sledge kilo in northern Alexander Island and Charcot Island, 1975/1976. British Antarctic Survey internal report: Ref: T/1975/K11. Cambridge: British Antarctic Survey.Google Scholar
Hinke, J.T., Salwicka, K., Trivelpiece, S.G., Watters, G.M. & Trivelpiece, W.Z. 2007. Divergent responses of Pygoscelis penguins reveal a common environmental driver. Oecologia, 153, 845–855.Google Scholar
Hubisz, M.J., Falush, D., Stephens, M. & Pritchard, J.K. 2009. Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources, 9, 1322–1332.Google Scholar
Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120.Google Scholar
Kuhner, M.K., Yamato, J. & Felsenstein, J. 1998. Maximum likelihood estimation of population growth rates based on the coalescent. Genetics, 149, 429–434.Google Scholar
Longmire, J.L., Lewis, A.K., Brown, N.C., Buckingham, J.M., Clark, L.M., Jones, M.D., Meincke, L.J., Meyne, J., Ratliff, R.L., Ray, F.A., Wagner, R.P. & Moyzis, R.K. 1988. Isolation and molecular characterization of a highly polymorphic centromeric tandem repeat in the family Falconidae. Genomics, 2, 14–24.Google Scholar
Lynch, H.J. & LaRue, M.A. 2014. First global census of the Adélie penguin. Auk, 131, 457–466.Google Scholar
Lynch, H.J., Naveen, R., Trathan, P.N. & Fagan, W.F. 2012. Spatially integrated assessment reveals widespread changes in penguin populations on the Antarctic Peninsula. Ecology, 93, 1367–1377.Google Scholar
Maruyama, T. & Fuerst, P.A. 1985. Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics, 111, 675–689.Google Scholar
Medrano, J.F, Aasen, E. & Sharrow, L. 1990. DNA extraction from nucleated red blood cells. Biotechniques, 8, 43.Google Scholar
Millar, C.D., Subramanian, S., Heupink, T.H., Swaminathan, S., Baroni, C. & Lambert, D.M. 2012. Adelie penguins and temperature changes in Antarctica: a long-term view. Integrative Zoology, 7, 113–120.CrossRefGoogle ScholarPubMed
Moritz, C. 1994. Defining ‘evolutionarily significant unit’ for conservation. Trends in Ecology & Evolution, 9, 373–375.Google Scholar
Ohta, T. & Kimura, M. 1973. A model of mutation appropriate to estimate number of electrophoretically detectable alleles in a finite population. Genetical Research, 22, 201–204.Google Scholar
Park, S.D.E. 2001. The Excel microsatellite toolkit. Dublin: Animal Genomics Laboratory.Google Scholar
Piry, S., Luikart, G. & Cornuet, J.M. 1999. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity, 90, 502–503.CrossRefGoogle Scholar
Poncet, S. & Poncet, J. 1987. Censuses of penguin populations of the Antarctic Peninsula, 1983–87. British Antarctic Survey Bulletin, No. 77, 109–129.Google Scholar
Raymond, M. & Rousset, F. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248–249.CrossRefGoogle Scholar
Ritchie, P.A., Millar, C.D., Gibb, G.C., Baroni, C. & Lambert, D.M. 2004. Ancient DNA enables timing of the Pleistocene origin and Holocene expansion of two Adélie penguin lineages in Antarctica. Molecular Biology and Evolution, 21, 240–248.Google Scholar
Roeder, A.D., Marshall, R.K., Mitchelson, A.J., Visagathilagar, T., Ritchie, P.A., Love, D.R., Pakai, T.J., McPartlan, H.C., Murray, N.D., Robinson, N.A., Kerry, K.R. & Lambert, D.M. 2001. Gene flow on the ice: genetic differentiation among Adélie penguin colonies around Antarctica. Molecular Ecology, 10, 1645–1656.Google Scholar
Rogers, A.R. & Harpending, H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569.Google Scholar
Sailley, S.F., Ducklow, H.W., Moeller, H.V., Fraser, W.R., Schofield, O.M., Steinberg, D.K., Garzio, L.M. & Doney, S.C. 2013. Carbon fluxes and pelagic ecosystem dynamics near two western Antarctic Peninsula Adélie penguin colonies: an inverse model approach. Marine Ecology Progress Series, 492, 253–272.Google Scholar
Shepherd, L.D., Millar, C.D., Ballard, G., Ainley, D.G., Wilson, P.R., Haynes, G.D., Baroni, C. & Lambert, D.M. 2005. Microevolution and mega-icebergs in the Antarctic. Proceedings of the National Academy of Sciences of the United States of America, 102, 16 717–16 722.Google Scholar
Sonsthagen, S.A., Talbot, S.L. & White, C.M. 2004. Gene flow and genetic characterization of northern goshawks breeding in Utah. Condor, 106, 826–836.Google Scholar
Sorenson, M.D. & Fleischer, R.C. 1996. Multiple independent transpositions of mitochondrial DNA control region sequences to the nucleus. Proceedings of the National Academy of Sciences of the United States of America, 93, 15 239–15 243.Google Scholar
Stammerjohn, S., Massom, R., Rind, D. & Martinson, D. 2012. Regions of rapid sea ice change: an inter-hemispheric seasonal comparison. Geophysical Research Letters, 39, 10.1029/2012GL050874.Google Scholar
Stammerjohn, S.E., Martinson, D.G., Smith, R.C. & Iannuzzi, R.A. 2008. Sea ice in the western Antarctic Peninsula region: spatio-temporal variability from ecological and climate change perspectives. Deep-Sea Research II - Topical Studies in Oceanography, 55, 2041–2058.Google Scholar
Tajima, F. 1989. The effect of change in population size on DNA polymorphism. Genetics, 123, 597–601.CrossRefGoogle ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.Google Scholar
Trivelpiece, W.Z., Hinke, J.T., Miller, A.K., Reiss, C.S., Trivelpiece, S.G. & Watters, G.M. 2011. Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proceedings of the National Academy of Sciences of the United States of America, 108, 7625–7628.Google Scholar
van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538.Google Scholar
Williams, T.D. 1995. The penguins: Spheniscidae. New York, NY: Oxford University Press, 309 pp.Google Scholar
Younger, J., Emmerson, L., Southwell, C., Lelliott, P. & Miller, K. 2015. Proliferation of East Antarctic Adelie penguins in response to historical deglaciation. BMC Evolutionary Biology, 10.1186/s12862-015-0502-2.Google Scholar
Zink, R.M. & Barrowclough, G.F. 2008. Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17, 2107–2121.Google Scholar
Supplementary material: PDF

Gorman supplementary material

Table S1

Download Gorman supplementary material(PDF)
PDF 47.8 KB