The subspecies of Antarctic Terns (Sterna vittata) wintering on the South African coast: evidence from morphology, genetics and stable isotopes
Maëlle Connan A G H , Peter R. Teske A B C , Anthony J. Tree D , Philip A. Whittington E F and Christopher D. McQuaid A
+ Author Affiliations
- Author Affiliations
A Department of Zoology and Entomology, Rhodes University, PO Box 77000, Port Elizabeth 6031, South Africa.
B School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia.
C Department of Zoology, University of Johannesburg, PO Box 524, Auckland Park 2006, Johannesburg, South Africa.
D Box 2793, Port Alfred 6170, South Africa.
E Department of Zoology, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa.
F East London Museum, PO Box 11021, Southernwood 5213, South Africa.
G Present address: Department of Zoology, Nelson Mandela Metropolitan University, PO Box 77000, Port Elizabeth 6031, South Africa.
H Corresponding author. Email: maelle.connan@gmail.com
Emu 115(3) 223-236 https://doi.org/10.1071/MU14089
Submitted: 9 May 2014 Accepted: 24 January 2015 Published: 28 April 2015
Abstract
Five to seven subspecies of Antarctic Tern (Sterna vittata) are recognised, with at least three (S. v. vittata, S. v. tristanensis and S. v. sanctipauli) wintering in South Africa. Morphological characters used to define these subspecies are not perfectly reliable, but fidelity to nesting site suggests they could be genetically distinct. We used morphological data and DNA to investigate the validity of subspecies. We further used stable isotope analysis of feather samples collected from the non-breeding grounds in South Africa to attempt to ascertain the population of origin. Nuclear and mitochondrial DNA sequence data identified two major genetic clades: one mostly comprised individuals partially or completely matching the morphological description of S. v. tristanensis, the other included individuals from S. v. vittata and S. v. sanctipauli. Stable isotope values indicated that juveniles originated from at least three populations. Irrespective of their morphological and genetic characteristics, most immatures moulted in Antarctic waters, and adults moulted in various habitats. Their colony of origin could not therefore be inferred from stable isotope values from feathers. Results indicate that morphological groupings may reflect a north–south cline across the Indian Ocean. Adequate conservation strategies require rigorous reassessment of the currently accepted subspecies, including DNA analyses of samples from the breeding grounds, particularly on Amsterdam and St Paul Islands.
Additional keywords: carbon and nitrogen stable isotopes, feathers, intron sequences, microsatellites, mtDNA, population structure, Southern Ocean.
References
Ainley, D. G., Ribic, C. A., and Fraser, W. R. (1992). Does prey preference affect habitat choice in Antarctic seabirds? Marine Ecology Progress Series 90, 207–221.| Does prey preference affect habitat choice in Antarctic seabirds?Crossref | GoogleScholarGoogle Scholar |
Avise, J. C. (2000). ‘Phylogeography.’ (Harvard University Press: Boston, MA.)
BirdLife International (2013). Species factsheet: Sterna vittata. (BirdLife International: Cambridge, UK.) Available from http://www.birdlife.org [accessed 6 November 2013].
Blévin, P., Carravieri, A., Jaeger, A., Chastel, O., Bustamante, P., and Cherel, Y. (2013). Wide range of mercury contamination in chicks of Southern Ocean seabirds. PLoS ONE 8, e54508.
| Wide range of mercury contamination in chicks of Southern Ocean seabirds.Crossref | GoogleScholarGoogle Scholar | 23349912PubMed |
Bridge, E. S., Jones, A. W., and Baker, A. J. (2005). A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: implications for taxonomy and plumage evolution. Molecular Phylogenetics and Evolution 35, 459–469.
| A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: implications for taxonomy and plumage evolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1ajurg%3D&md5=23d21c1e94ae1589bfa4c84084f6da0aCAS | 15804415PubMed |
Brooke, R. K., Cooper, J., Hockey, P. A. R., Ryan, P. G., Sinclair, J. C., Suter, W., and Tree, A. J. (1988). Distribution, population size and conservation of the Antarctic Tern Sterna vittata in southern Africa. Cormorant 16, 107–113.
Brownstein, M. J., Carpten, J. D., and Smith, J. R. (1996). Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. BioTechniques 20, 1004–1010.
| 1:CAS:528:DyaK28XjtlGmtr8%3D&md5=f0f9d31cd1efcd517f3e297a88349c95CAS | 8780871PubMed |
Burg, T. M., and Croxall, J. P. (2004). Global population structure and taxonomy of the Wandering Albatross species complex. Molecular Ecology 13, 2345–2355.
| Global population structure and taxonomy of the Wandering Albatross species complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsl2rurc%3D&md5=f52fca3e14145b8fca1982fbb88e923cCAS | 15245406PubMed |
Casaux, R., Baroni, A., Ramón, A., Favero, M., and Silva, P. (2008). Aspects of the foraging behaviour of the Antarctic Tern Sterna vittata gaini at Harmony Point, South Shetland Islands. Polar Biology 31, 327–331.
| Aspects of the foraging behaviour of the Antarctic Tern Sterna vittata gaini at Harmony Point, South Shetland Islands.Crossref | GoogleScholarGoogle Scholar |
Cherel, Y., and Hobson, K. A. (2007). Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology Progress Series 329, 281–287.
| Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXislChtLc%3D&md5=04b6a18eaa72efdef4ae658b41119346CAS |
Croxall, J. P., Butchart, S. H. M., Lascelles, B., Stattersfield, A. J., Sullivan, B., Symes, A., and Taylor, P. (2012). Seabird conservation status, threats and priority actions: a global assessment. Bird Conservation International 22, 1–34.
| Seabird conservation status, threats and priority actions: a global assessment.Crossref | GoogleScholarGoogle Scholar |
de Beer, S. J., Lockwood, G. M., Raijmakers, J. H. F. A., Raijmakers, J. M. H., Scott, W. A., Oschadleus, H. D., and Underhill, L. G. (2001). ‘SAFRING Bird Ringing Manual.’ ADU Guide 5. (Avian Demography Unit, University of Cape Town: Cape Town.)
Earl, D. A., and von Holdt, B. M. (2012). STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
| STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |
Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=f7fa449787db685923e407b00a24cb4cCAS | 15969739PubMed |
Excoffier, L., and Lischer, H. E. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.
| Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows.Crossref | GoogleScholarGoogle Scholar | 21565059PubMed |
Excoffier, L., Laval, G., and Schneider, S. (2005). Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 47–50.
| 1:CAS:528:DC%2BD28XjsFSltg%3D%3D&md5=ed142530bee91deedcae18152d11d961CAS |
Falla, R. A. (1937). ‘B.A.N.Z. Antarctic Research Expedition 1929–1931, under the Command of Sir Douglas Mawson. Reports—Series B, Volume II. Birds.’ (B.A.N.Z.A.R. Expedition Committee: Adelaide, SA.)
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.
| Confidence limits on phylogenies: an approach using the bootstrap.Crossref | GoogleScholarGoogle Scholar |
Friesen, V. L., Burg, T. M., and McCoy, K. D. (2007). Mechanisms of population differentiation in seabirds. Molecular Ecology 16, 1765–1785.
| Mechanisms of population differentiation in seabirds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2szgtlGqtw%3D%3D&md5=173ab80a343d42e7d3d71ba51642d6e4CAS | 17444891PubMed |
Gay, L., Neubauer, G., Zagalska-Neubauer, M., Debain, C., Pons, J.-M., David, P., and Crochet, P.-A. (2007). Molecular and morphological patterns of introgression between two large white-headed gull species in a zone of recent secondary contact. Molecular Ecology 16, 3215–3227.
| Molecular and morphological patterns of introgression between two large white-headed gull species in a zone of recent secondary contact.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVert77K&md5=49924fcfc67adf4ab35a3413aac7ffd6CAS | 17651198PubMed |
Gill, F., and Donsker, D. (2013). ‘IOC World Bird List (v 3.4).’ Available at http://www.worldbirdnames.org [accessed 28 November 2013].
Given, A. D., Mills, J. A., and Baker, A. J. (2002). Isolation of polymorphic microsatellite loci from the Red-billed Gull (Larus novaehollandiae scopulinus) and amplification in related species. Molecular Ecology Notes 2, 416–418.
| Isolation of polymorphic microsatellite loci from the Red-billed Gull (Larus novaehollandiae scopulinus) and amplification in related species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVSjtrk%3D&md5=be83157434dd6e84d8306d44717bcac7CAS |
Gochfeld, M., and Burger, J. (1996) Family Sternidae (Terns). In ‘Handbook of the Birds of the World. Vol. 3: Hoatzin to Auks.’ (Eds J. del Hoyo, A. Elliott and J. Sargatal.) pp. 624–667 (Lynx Edicions: Barcelona, Spain.)
Gosler, A. (2004) Birds in the hand. In ‘Bird Ecology and Conservation: A Handbook of Techniques’. (Eds W. J. Sutherland, I. Newton and R. E. Green), pp. 85–118. (Oxford University Press Inc.: New York, NY.)
Guo, S., and Thompson, E. (1992). Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48, 361–372.
| Performing the exact test of Hardy–Weinberg proportion for multiple alleles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zksFGgsA%3D%3D&md5=e11ffd856423a46d5d12656a0980dc15CAS | 1637966PubMed |
Haig, S. M., Beever, E. A., Chambers, S. M., Draheim, H. M., Dugger, B. D., Dunham, S., Elliott-Smith, E., Fontaine, J. B., Kesler, D. C., Knaus, B. J., Lopes, I. F., Loschl, P., Mullins, T. D., and Sheffield, L. M. (2006). Taxonomic considerations in listing subspecies under the US Endangered Species Act. Conservation Biology 20, 1584–1594.
| Taxonomic considerations in listing subspecies under the US Endangered Species Act.Crossref | GoogleScholarGoogle Scholar | 17181793PubMed |
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: palaeontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.
Hasegawa, M., Kishino, H., and Yano, T. (1985). Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
| Dating of the human–ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=8ff6060dadb14c34995d9a0140376a23CAS | 3934395PubMed |
Hatch, J. J. (2002). Arctic Tern (Sterna paradisaea). In ‘The Birds of North America’. (Eds A. Poole and F. Gill.) No. 707, pp. 1–39. (The Birds of North America Inc.: Philadelphia, PA.)
Higgins, P. J., and Davies, S. J. J. F. (Eds) (1996). ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 3: Snipe to Pigeons.’ (Oxford University Press: Melbourne.)
Hobson, K. A., and Clark, R. G. (1992). Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94, 189–197.
| Assessing avian diets using stable isotopes II: factors influencing diet-tissue fractionation.Crossref | GoogleScholarGoogle Scholar |
Hockey, P. A. R., Dean, W. R. J., and Ryan, P. G. (Eds) (2005). ‘Roberts Birds of Southern Africa.’ 7th edn. (The Trustees of the John Voelcker Bird Book Fund: Cape Town.)
Hodum, P. J., and Hobson, K. A. (2000). Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable-isotope (δ15N and δ13C) analyses. Marine Ecology Progress Series 198, 273–281.
| Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable-isotope (δ15N and δ13C) analyses.Crossref | GoogleScholarGoogle Scholar |
Jaeger, A. (2009). Etude isotopique des variations saisonnières et à long terme de l’écologie alimentaire des oiseaux marins de l’Océan Austral. Ph.D. Thesis, Université Pierre et Marie Curie, Paris.
Jaeger, A., Lecomte, V. J., Weimerskirch, H., Richard, P., and Cherel, Y. (2010). Seabird satellite tracking validates the use of latitudinal isoscapes to depict predators’ foraging areas in the Southern Ocean. Rapid Communications in Mass Spectrometry 24, 3456–3460.
| Seabird satellite tracking validates the use of latitudinal isoscapes to depict predators’ foraging areas in the Southern Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2nu7vN&md5=f400f6b6088ecb981e04b07ffa546289CAS | 21072802PubMed |
Jakobsson, M., and Rosenberg, N. A. (2007). CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
| CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1ahtbs%3D&md5=d998d780ed255f295c32d5a197314521CAS | 17485429PubMed |
Jarman, S. N., Ward, R. D., and Elliott, N. G. (2002). Oligonucleotide primers for PCR amplification of coelomate introns. Marine Biotechnology 4, 347–355.
| Oligonucleotide primers for PCR amplification of coelomate introns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosVGrur0%3D&md5=e38b8ceee63a6069748d49bc578e64cdCAS | 14961246PubMed |
Jukes, T. H., and Cantor, C. R. (1969). Evolution of protein molecules. In ‘Mammalian Protein Metabolism’. (Ed. H. N. Munro.) pp. 21–132. (Academic Press: New York.)
Küpper, C., Horsburgh, G. J., Dawson, D. A., French-Constant, R., Székely, T., and Burke, T. (2007). Characterization of 36 polymorphic microsatellite loci in the Kentish Plover (Charadrius alexandrinus) including two sex-linked loci and their amplification in four other Charadrius species. Molecular Ecology Notes 7, 35–39.
| Characterization of 36 polymorphic microsatellite loci in the Kentish Plover (Charadrius alexandrinus) including two sex-linked loci and their amplification in four other Charadrius species.Crossref | GoogleScholarGoogle Scholar |
Küpper, C., Burke, T., Székely, T., and Dawson, D. A. (2008). Enhanced cross-species utility of conserved microsatellite markers in shorebirds. BMC Genomics 9, 502.
| Enhanced cross-species utility of conserved microsatellite markers in shorebirds.Crossref | GoogleScholarGoogle Scholar | 18950482PubMed |
Meirmans, P. G., and Hedrick, P. W. (2011). Assessing population structure: F ST and related measures. Molecular Ecology Resources 11, 5–18.
| Assessing population structure: F ST and related measures.Crossref | GoogleScholarGoogle Scholar | 21429096PubMed |
Mizutani, H., Fukuda, M., Kabaya, Y., and Wada, E. (1990). Carbon isotope ratio of feathers reveals feeding behavior of cormorants. Auk 107, 400–403.
| Carbon isotope ratio of feathers reveals feeding behavior of cormorants.Crossref | GoogleScholarGoogle Scholar |
Moore, J. K., Abbott, M. R., and Richman, J. G. (1999). Location and dynamics of the Antarctic Polar Front from satellite sea surface temperature data. Journal of Geophysical Research 104, 3059–3073.
| Location and dynamics of the Antarctic Polar Front from satellite sea surface temperature data.Crossref | GoogleScholarGoogle Scholar |
Murphy, R. C. (1938). Birds collected during the Whitney South Sea expedition. XXXVII. On Pan-Antarctic terns. American Museum Novitates 977, 1–17.
Orsi, A. H., Whitworth, T., and Nowlin, W. D. (1995). On the meridional extent and fronts of the Antarctic Circumpolar Current. Deep-sea Research. Part I, Oceanographic Research Papers 42, 641–673.
| On the meridional extent and fronts of the Antarctic Circumpolar Current.Crossref | GoogleScholarGoogle Scholar |
Palmer, J. (2006). Lack of mitochondrial DNA differentiation in four subspecies of Antarctic Tern, Sterna vittata. B. Sc. Hons Thesis, Rhodes University, Grahamstown, South Africa.
Patten, M. A., and Unitt, P. (2002). Diagnosability versus mean differences of Sage Sparrow subspecies. Auk 119, 26–35.
| Diagnosability versus mean differences of Sage Sparrow subspecies.Crossref | GoogleScholarGoogle Scholar |
Peakall, R., and Smouse, P. E. (2012). GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28, 2537–2539.
| GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVehtbjI&md5=72f4e09250930a7f5efe1dfa3b2f62eaCAS | 22820204PubMed |
Prevost, Y. (1983). The moult of the Osprey Pandion haliaetus. Ardea 71, 199–209.
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=6884cd003ac4e3e93a1a262ad70fc53dCAS | 10835412PubMed |
Quillfeldt, P., McGill, R. A. R., and Furness, R. W. (2005). Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson’s Storm-Petrel. Marine Ecology Progress Series 295, 295–304.
| Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson’s Storm-Petrel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVClu7vF&md5=fc87722a5d95923f1a1bd3b681fcab09CAS |
Quillfeldt, P., Masello, J. F., McGill, R. A. R., Adams, M., and Furness, R. W. (2010). Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird? Frontiers in Zoology 7, 15–26.
| Moving polewards in winter: a recent change in the migratory strategy of a pelagic seabird?Crossref | GoogleScholarGoogle Scholar | 20482826PubMed |
Rosenberg, N. A. (2004). Distruct: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
| Distruct: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |
Rubenstein, D. R., and Hobson, K. A. (2004). From birds to butterflies: animal movement patterns and stable isotopes. Trends in Ecology & Evolution 19, 256–263.
| From birds to butterflies: animal movement patterns and stable isotopes.Crossref | GoogleScholarGoogle Scholar |
Sadleir, R. M. F. S., Taylor, R. H., and Taylor, G. A. (1986). Breeding of Antarctic Terns. Notornis 33, 264–265.
Sagar, P. M. (1991). Aspects of the breeding and feeding of Kerguelen and Antarctic Terns at the Kerguelen Islands. Notornis 38, 191–198.
Schuelke, M. (2000). An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18, 233–234.
| An economic method for the fluorescent labeling of PCR fragments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtVOksbk%3D&md5=e9570243b5e2c90c0c14163a29c8e552CAS | 10657137PubMed |
Sears, J., Hatch, S. A., and O’Brien, D. M. (2009). Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159, 41–48.
| Disentangling effects of growth and nutritional status on seabird stable isotope ratios.Crossref | GoogleScholarGoogle Scholar | 18975007PubMed |
Slatkin, M., and Excoffier, L. (1996). Testing for linkage disequilibrium in genotypic data using the EM algorithm. Heredity 76, 377–383.
| Testing for linkage disequilibrium in genotypic data using the EM algorithm.Crossref | GoogleScholarGoogle Scholar | 8626222PubMed |
Techow, N. M. S. M., Ryan, P. G., and O’Ryan, C. (2009). Phylogeography and taxonomy of White-chinned and Spectacled Petrels. Molecular Phylogenetics and Evolution 52, 25–33.
| Phylogeography and taxonomy of White-chinned and Spectacled Petrels.Crossref | GoogleScholarGoogle Scholar |
Tirard, C., Helfenstein, F., and Danchin, E. (2002). Polymorphic microsatellites in the Black-legged Kittiwake Rissa tridactyla. Molecular Ecology Notes 2, 431–433.
| Polymorphic microsatellites in the Black-legged Kittiwake Rissa tridactyla.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVSjt7g%3D&md5=204ab6de8bc8718b451e3eaefa55f7acCAS |
Tree, A. J., and Klages, N. T. W. (1998). Ageing techniques and age structure of a mid-winter roost of Antarctic Tern. Safring News 27, 15–17.
Tree, A. J., and Klages, N. T. W. (2001). A reassessment of plumage characters in ageing Antarctic Terns. Afring News 30, 28–29.
Tree, A. J., and Klages, N. T. W. (2004). Population size, distribution and origins of Antarctic Terns Sterna vittata wintering in South Africa. Marine Ornithology 32, 55–61.
Weimerskirch, H., Jouventin, P., Mougin, J. L., Stahl, J. C., and van Beveren, M. (1985). Banding recoveries and the dispersal of seabirds breeding in French Austral and Antarctic territories. Emu 85, 22–33.
| Banding recoveries and the dispersal of seabirds breeding in French Austral and Antarctic territories.Crossref | GoogleScholarGoogle Scholar |
Winker, K. (2010). Subspecies represent geographically partitioned variation, a gold mine of evolutionary biology, and a challenge for conservation. Ornithological Monographs 67, 6–23.
| Subspecies represent geographically partitioned variation, a gold mine of evolutionary biology, and a challenge for conservation.Crossref | GoogleScholarGoogle Scholar |
Wright, S. (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19, 395–420.
| The interpretation of population structure by F-statistics with special regard to systems of mating.Crossref | GoogleScholarGoogle Scholar |