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Polar Biology

, Volume 38, Issue 9, pp 1493–1502 | Cite as

Limited genetic differentiation among chinstrap penguin (Pygoscelis antarctica) colonies in the Scotia Arc and Western Antarctic Peninsula

  • Jennifer J. Freer
  • Barbara K. Mable
  • Gemma Clucas
  • Alex D. Rogers
  • Michael J. Polito
  • Michael Dunn
  • Ron Naveen
  • Hila Levy
  • Tom HartEmail author
Original Paper

Abstract

Long-term monitoring of seabird numbers around Antarctica has revealed that the chinstrap penguin (Pygoscelis antarctica) is largely declining throughout its range in the Scotia Arc. Whether archipelagos across this large area remain connected via dispersal or represent genetically isolated groups has not yet been established. The purpose of this study was to assess the level of genetic differentiation between four breeding colonies on the Western Antarctic Peninsula (WAP), South Shetland, South Orkney, and South Sandwich Islands using microsatellite-based analysis of population structure. All colonies had similar levels of genetic diversity (mean heterozygosity, H O = 0.583) but colonies from the WAP and South Orkney Island had significant inbreeding coefficients. Hierarchical and pairwise F-statistics revealed very limited population structure in the Scotia Arc, with weak differentiation between colonies from the WAP, South Shetland and South Orkney Islands relative to the South Sandwich Islands, which are situated at least 1000 km apart from these other archipelagos. Bayesian model-based clustering methods found no evidence of significant population structuring, suggesting that whilst some isolation by distance may occur, there are no strong barriers to dispersal across this wide geographic range. No evidence of sex-biased dispersal was detected. We conclude that chinstrap penguin colonies across the Scotia Arc represent one interconnected breeding population. High levels of gene flow may be important in maintaining smaller, less stable colonies, and this status should be preserved by creating dispersal corridors throughout the Scotia Arc.

Keywords

Scotia Arc Population genetics Microsatellite Molecular sexing Pygoscelis antarctica 

Notes

Acknowledgments

The authors would like to thank Aileen Adam and Elizabeth Kilbride from the University of Glasgow for their help in the laboratory, especially during initial DNA screening and marker optimisation processes. Sampling was conducted under permits from the Government of South Georgia and the South Sandwich Islands, the UK Foreign and Commonwealth Office and the US National Science Foundation. Fieldwork on the South Sandwich Islands would not have been possible without the knowledge and assistance of Jérôme Poncet and the crew of the Golden Fleece. Fieldwork in the Antarctic Peninsula was carried out with the assistance of Quark Expeditions Ltd, and W. Trivelpiece and the US Antarctic Marine Living Resource Program provided logistical support for sampling at King George Island. This work was funded by the Charities Advisory Trust, the Holly Hill Charitable Trust, and the Zoological Society of London (TH).

Supplementary material

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Supplementary material 1 (DOCX 18 kb)
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Supplementary material 4 (DOCX 46 kb)

References

  1. Aguirre CA, Acero JM (1995) Distribution and abundance of birds in the Errera Channel, Antarctic Peninsula, during the 1992/93 breeding season. Mar Ornithol 23:129–134Google Scholar
  2. Ahmed S, Hart T, Dawson DA, Horsburgh GJ, Trathan PN, Rogers AD (2009) Isolation and characterization of macaroni penguin (Eudyptes chrysolophus) microsatellite loci and their utility in other penguin species (Spheniscidae, AVES). Mol Ecol Resour 9:1530–1535PubMedCrossRefGoogle Scholar
  3. Ainley D, Russell J, Jenouvrier S, Woehler E, Lyver PO, Fraser WR, Kooyman GL (2010) Antarctic penguin response to habitat change as Earth’s troposphere reaches 2 degrees C above preindustrial levels. Ecol Monogr 80:49–66CrossRefGoogle Scholar
  4. Ancel A, Beaulieu M, Gilbert C (2013) The different breeding strategies of penguins: a review. C R Biol 336:1–12PubMedCrossRefGoogle Scholar
  5. Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103PubMedCrossRefGoogle Scholar
  6. Barbosa A, Benzal J, De Leon A, Moreno J (2012) Population decline of chinstrap penguins (Pygoscelis antarctica) on Deception Island, South Shetlands, Antarctica. Polar Biol 35:1453–1457CrossRefGoogle Scholar
  7. Billing TM, Guay PJ, Peucker AJ, Mulder RA (2006) PRIMER NOTE: isolation and characterization of polymorphic microsatellite loci for the study of paternity and population structure in the little penguin Eudyptula minor. Mol Ecol Notes 7:425–427CrossRefGoogle Scholar
  8. Biuw M, Lydersen C, Nico De Bruyn PJ, Arriola A, Hofmeyr GGJ, Kritzinger P, Kovacs KM (2009) Long-range migration of a chinstrap penguin from Bouvetøya to Montagu Island, South Sandwich Islands. Antarct Sci 22:157–162CrossRefGoogle Scholar
  9. Boessenkool S, Star B, Waters JM, Seddon PJ (2009) Multilocus assignment analyses reveal multiple units and rare migration events in the recently expanded yellow-eyed penguin (Megadyptes antipodes). Mol Ecol 18:2390–2400PubMedCrossRefGoogle Scholar
  10. Bouzat JL, Walker BG, Boersma PD (2009) Regional genetic structure in the Magellanic penguin (Spheniscus magellanicus) suggests metapopulation dynamics. Auk 126:326–334CrossRefGoogle Scholar
  11. CCAMLR (2009) Protection of the South Orkney Islands southern shelf. Conservation measure 91-03. Commission reportGoogle Scholar
  12. Clarke AL, Saether BE, Roskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 79:429–438CrossRefGoogle Scholar
  13. Clucas GV, Dunn MJ, Dyke G, Emslie SD, Levy H, Naveen R, Polito MJ, Pybus OG, Rogers AD, Hart T (2014) A reversal of fortunes: climate change ‘winners’ and ‘losers’ in Antarctic Peninsula penguins. Sci Rep 4:5024PubMedCentralPubMedCrossRefGoogle Scholar
  14. Convey P, Morton A, Poncet J (1997) Survey of marine birds and mammals of the South Sandwich Islands. Pol Rec 35:107–124CrossRefGoogle Scholar
  15. Croxall JP (1987) The status and conservation of Antarctic seals and seabirds—a review. Environ Int 13:55–70CrossRefGoogle Scholar
  16. Croxall JP, Trathan PN, Murphy EJ (2002) Environmental change and Antarctic seabird populations. Science 297:1510–1514PubMedCrossRefGoogle Scholar
  17. Dieringer D, Schlotterer C (2003) MICROSATELLITE ANALYSER (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  18. Ducklow HW, Baker K, Martinson DG, Quetin LB, Ross RM, Smith RC, Stammerjohn SE, Vernet M, Fraser W (2007) Marine pelagic ecosystems: the West Antarctic Peninsula. Philos Trans R Soc B Biol Sci 362:67–94CrossRefGoogle Scholar
  19. Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  20. Emslie SD, Patterson WP (2007) Abrupt recent shift in delta C-13 and delta N-15 values in Adelie penguin eggshell in Antarctica. Proc Natl Acad Sci USA 104:11666–11669PubMedCentralPubMedCrossRefGoogle Scholar
  21. Emslie SD, Fraser W, Smith RC, Walker W (1998) Abandoned penguin colonies and environmental change in the Palmer Station area, Anvers Island, Antarctic Peninsula. Antarct Sci 10:257–268CrossRefGoogle Scholar
  22. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620Google Scholar
  23. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  24. Excoffier L, Slatkin M (1998) Incorporating genotypes of relatives into a test of linkage disequilibrium. Am J Hum Genet 62:171–180PubMedCentralPubMedCrossRefGoogle Scholar
  25. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491PubMedCentralPubMedGoogle Scholar
  26. Forcada J, Trathan PN (2009) Penguin responses to climate change in the Southern Ocean. Glob Change Biol 15:1618–1630CrossRefGoogle Scholar
  27. Forcada J, Trathan PN, Reid K, Murphy EJ, Croxall JP (2006) Contrasting population changes in sympatric penguin species in association with climate warming. Glob Change Biol 12:411–423CrossRefGoogle Scholar
  28. Fraser WR, Trivelpiece WZ, Ainley DG, Trivelpiece SG (1992) Increases in Antarctic penguin populations—reduced competition with whales or a loss of sea ice due to environmental warming. Polar Biol 11:525–531CrossRefGoogle Scholar
  29. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  30. Friesen VL, Burg TM, Mccoy KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785PubMedCrossRefGoogle Scholar
  31. Goudet J (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 21/01/15
  32. Goudet J, Perrin N, Waser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114PubMedCrossRefGoogle Scholar
  33. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  34. Hinke JT, Salwicka K, Trivelpiece SG, Watters GM, Trivelpiece WZ (2007) Divergent responses of Pygoscelis penguins reveal a common environmental driver. Oecologia 153:845–855PubMedCrossRefGoogle Scholar
  35. Hogan FE, Cooke R, Burridge CP, Normano JA (2008) Optimizing the use of shed feathers for genetic analysis. Mol Ecol Resour 8:561–567PubMedCrossRefGoogle Scholar
  36. Jenouvrier S, Caswell H, Barbraud C, Holland M, Str Ve J, Weimerskirch H (2009) From the cover: demographic models and IPCC climate projections predict the decline of an emperor penguin population. Proc Natl Acad Sci USA 106:1844–1847PubMedCentralPubMedCrossRefGoogle Scholar
  37. Johansson MP, Mcmahon BJ, Hoglund J, Segelbacher G (2012) Amplification success of multilocus genotypes from feathers found in the field compared with feathers obtained from shot birds. Ibis 154:15–20CrossRefGoogle Scholar
  38. Korczak-Abshire M, Chwedorzewska KJ, Wasowicz P, Bednarek PT (2012) Genetic structure of declining chinstrap penguin (Pygoscelis antarcticus) populations from South Shetland Islands (Antarctica). Polar Biol 35:1681–1689CrossRefGoogle Scholar
  39. Kramer AM, Dennis B, Liebhold AM, Drake JM (2009) The evidence for allee effects. Popul Ecol 51:341–354CrossRefGoogle Scholar
  40. Laws RM (1977) Seals and whales of the Southern Ocean. Philos Trans R Soc B Biol Sci 279:81–96CrossRefGoogle Scholar
  41. Lemaho Y, Karmann H, Briot D, Handrich Y, Robin JP, Mioskowski E, Cherel Y, Farni J (1992) Stress in birds due to routine handling and a technique to avoid it. Am J Physiol 263:R775–R781Google Scholar
  42. Lynch HJ, Naveen R, Trathan PN, Fagan WF (2012) Spatially integrated assessment reveals widespread changes in penguin populations on the Antarctic Peninsula. Ecology 93:1367–1377PubMedCrossRefGoogle Scholar
  43. Meredith MP, King JC (2005) Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys Res Lett 32:L19604CrossRefGoogle Scholar
  44. Naveen R, Lynch HJ, Forrest S, Mueller T, Polito M (2012) First direct, site-wide penguin survey at Deception Island, Antarctica, suggests significant declines in breeding chinstrap penguins. Polar Biol 35:1879–1888Google Scholar
  45. Overeem RL, Peucker AJ, Austin CM, Dann P, Burridge CP (2008) Contrasting genetic structuring between colonies of the World’s smallest penguin, Eudyptula minor (Aves: Spheniscidae). Conserv Genet 9:893–905CrossRefGoogle Scholar
  46. Poncet S, Poncet J (1987) Censuses of Penguin populations of the Antarctic Peninsula, 1983–87. Br Antarct Surv B 77:109–129Google Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  48. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  49. Roeder AD, Marshall RK, Mitchelson AJ, Visagathilagar T, Ritchie PA, Love DR, Pakai TJ, Mcpartlan HC, Murray ND, Robinson NA, Kerry KR, Lambert DM (2001) Gene flow on the ice: genetic differentiation among Adelie penguin colonies around Antarctica. Mol Ecol 10:1645–1656PubMedCrossRefGoogle Scholar
  50. Roeder AD, Ritchie PA, Lambert DM (2002) New DNA markers for penguins. Conserv Genet 3:341–344CrossRefGoogle Scholar
  51. Sander M, Balbao TC, Polito MJ, Costa ES, Carneiro APB (2007) Recent decrease in chinstrap penguin (Pygoscelis antarctica) populations at two of Admiralty Bay’s islets on King George Island, South Shetland Islands, Antarctica. Polar Biol 30:659–661CrossRefGoogle Scholar
  52. Schlosser JA, Dubach JM, Garner TWJ, Araya B, Bernal M, Simeone A, Smith KA, Wallace RS (2009) Evidence for gene flow differs from observed dispersal patterns in the Humboldt penguin, Spheniscus humboldti. Conserv Genet 10:839–849CrossRefGoogle Scholar
  53. Scribner KT, Petersen MR, Fields RL, Talbot SL, Pearce JM, Chesser RK (2001) Sex-biased gene flow in spectacled eiders (anatidae): inferences from molecular markers with contrasting modes of inheritance. Evolution 55:2105–2115PubMedCrossRefGoogle Scholar
  54. Shuford WD, Spear LB (1988) Surveys of breeding chinstrap penguins in the South Shetland Islands, Antarctica. Br Antarct Surv B 81:19–30Google Scholar
  55. Taberlet P, Luikart G (1999) Non-invasive genetic sampling and individual identification. Biol J Linn Soc 68:41–55CrossRefGoogle Scholar
  56. Trivelpiece W, Trivelpiece S (2013) Chinstrap Penguin (Pygoscelis antarctica). In: Borboroglu PG, Boersma PD (eds) Penguins: Natural history and conservation. University of Washington Press, Seattle, pp 59–72Google Scholar
  57. Trivelpiece WZ, Buckelew S, Reiss C, Trivelpiece SG (2007) The winter distribution of chinstrap penguins from two breeding sites in the South Shetland Islands of Antarctica. Polar Biol 30:1231–1237CrossRefGoogle Scholar
  58. Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci USA 108:7625–7628PubMedCentralPubMedCrossRefGoogle Scholar
  59. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  60. Vili N, Nemeshazi E, Kovacs S, Horvath M, Kalmar L, Szabo K (2013) Factors affecting DNA quality in feathers used for non-invasive sampling. J Ornithol 154:587–595CrossRefGoogle Scholar
  61. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  62. Williams TD (1995) The Penguins. Oxford University Press, OxfordGoogle Scholar
  63. Wilson RP (1997) A method for restraining penguins. Mar Ornithol 25:72–73Google Scholar
  64. Wilson RP, Culik BM, Kosiorek P, Adelung D (1998) The over-winter movements of a chinstrap penguin (Pygoscelis antarctica). Polar Rec 34:107–112CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary and Life SciencesUniversity of GlasgowGlasgowUK
  2. 2.Ocean and Earth SciencesUniversity of SouthamptonSouthamptonUK
  3. 3.Department of ZoologyUniversity of OxfordOxfordUK
  4. 4.Department of Oceanography and Coastal SciencesLouisiana State UniversityBaton RougeUSA
  5. 5.British Antarctic SurveyCambridgeUK
  6. 6.Oceanites IncChevy ChaseUSA

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