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Range-wide patterns of population differentiation of Eurasian Black Terns (Chlidonias niger niger) related to use of discrete post-nuptial staging sites

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Abstract

The Eurasian Black Tern, Chlidonias niger niger, nests in marshes continuously distributed across Eurasia, but migration routes, staging sites, and non-breeding distributions are not well understood. In western Europe some populations have declined substantially over several decades (>90%), thus a more complete understanding of breeding site connectivity and migratory routes is needed. We collected tissue samples of terns in breeding colonies in the Netherlands, Latvia, southern Ukraine, eastern Siberian Russia, and from individuals at one important post-nuptial staging site in The Netherlands. Microsatellite data suggest significant differentiation among all breeding sites and the pattern is supported by differences among sites in most morphological measures. Conversely, mitochondrial DNA suggests similarity and population expansion especially from the region around Ukraine. We assigned 70% of the birds sampled on the staging site to the Netherlands/Latvia breeding population, but none to the southern Ukrainian or eastern Russian population. Our data indicated limited contact at post-nuptial staging sites contribute to genetic structure among breeding sites for this species. Our study demonstrates the utility of genetic data in migration studies to delineate migratory flyways and highlight the importance of specific staging sites to specific breeding subpopulations.

Zusammenfassung

Verbreitungsgebietweite Muster der Populationsdifferenzierung bei der Trauerseeschwalbe Chlidonias niger niger im Zusammenhang mit der Nutzung definierter nachbrutzeitlicher Sammelplätze

Die Trauerseeschwalbe brütet in Sumpfgebieten und ist über ganz Eurasien verbreitet; über ihre Zugwege, Sammelplätze und über ihre Verbreitung außerhalb der Brutzeit ist dagegen wenig bekannt. In Westeuropa haben manche Populationen über mehrere Jahrzehnte hinweg merklich (>90%) abgenommen, daher besteht Bedarf an umfassenderen Kenntnissen über Brutplatzkonnektivität und Zugstrecken. Wir sammelten Gewebeproben von Seeschwalben aus Brutkolonien in den Niederlanden, Lettland, der Südukraine, aus dem ostsibirischen Russland und von Individuen an einem bedeutenden nachbrutzeitlichen Sammelplatz in den Niederlanden. Daten auf der Basis von Mikrosatelliten-DNA weisen auf eine signifikante Differenzierung zwischen allen Brutgebieten hin, und dieses Muster wird von morphometrischen Unterschieden bestätigt. Umgekehrt spricht die mitochondriale DNA für Ähnlichkeit und eine Populationsexpansion speziell aus der Region um die Ukraine. Wir konnten 70% der am Sammelplatz beprobten Vögel der niederländischen/lettischen Brutpopulation zuordnen, dagegen keine den Populationen der Südukraine oder Ostrusslands. Unsere Daten deuten darauf hin, dass eingeschränkter Kontakt an den nachbrutzeitlichen Sammelplätzen bei dieser Art zur genetischen Struktur zwischen den Brutgebieten beiträgt. Unsere Studie verdeutlicht die Nützlichkeit genetischer Daten für Zuguntersuchungen, um Zugwege aufzuzeigen und die Bedeutung spezifischer Sammelplätze für spezifische Sub-Brutpopulationen zu unterstreichen.

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References

  • Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48

    Article  CAS  PubMed  Google Scholar 

  • Becker P, Ezard HG, Ludwigs T, Sauer-Gürth JD, Wink M (2008) Population sex ratio shift from fledging to recruitment: consequences for demography in a philopatric seabird. Oikos 117:60–68

    Article  Google Scholar 

  • Beerli P (2006) Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics 22:341–345

    Article  CAS  PubMed  Google Scholar 

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Birdlife International (2015) European Red List of Birds. Office for Official Publications of the European Communities, Luxembourg

    Google Scholar 

  • Boutilier ST, Taylor SA, Morris-Pocock JA, Lavoie RA, Friesen VL (2014) Evidence for genetic differentiation among Caspian Tern (Hydroprogne caspia) populations in North America. Conserv Genet 15:275–281

    Article  Google Scholar 

  • Bridge ES, Jones AW, Baker AJ (2005) A phylogenetic framework for the terns (Sternini) inferred from mtDNA sequences: implications for taxonomy and plumage evolution. Mol Phyl Evol 32:459–469

    Article  Google Scholar 

  • Buehler DM, Baker AJ (2005) Population divergence times and historical demography in Red Knots and Dunlins. Condor 107:497–513

    Article  Google Scholar 

  • Buehler DM, Baker AJ, Piersma T (2006) Reconstructing palaeoflyways of the late Pleistocene and early Holocene Red Knot Calidris canutus. Ardea 93:485–498

    Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  • Clarke AL, Sæther BE, Røskaft E (1997) Sex biases in avian dispersal: a reappraisal. Oikos 97:429–38

    Article  Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The last glacial maximum. Science 325:710–714

    Article  CAS  PubMed  Google Scholar 

  • Conklin JR, Reneerkens J, Verkuil YI, Tomkovich PR, Palsboll PJ, Piersmam T (2016) Low genetic differentiation between Greenlandic and Siberian Sanderling populations implies a different phylogenetic history than found in Red Knots. J Ornithol 157:325–332

    Article  Google Scholar 

  • Connan M, Teske PR, Tree AJ, Whittington PA, McQuaid CD (2015) The subspecies of Antarctic Terns (Sterna vittata) wintering on the South African coast: evidence from morphology, genetics and stable isotopes. Emu 115:223–236

    Article  Google Scholar 

  • Cramp S (1985) The birds of the Western Palearctic, vol 4. Oxford University Press, Oxford

    Google Scholar 

  • Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resour 10:556–557

    Article  PubMed  Google Scholar 

  • Draheim HM, Miller MP, Baird P, Haig SM (2010) Subspecific status and population genetic structure of Least Terns (Sternula antillarum) inferred by mitochondrial DNA control-region sequences and microsatellite DNA. Auk 127:807–819

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • 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 10:564–567

    Article  PubMed  Google Scholar 

  • Faria PJ, Campos FP, Branco JO, Musso CM, Morgante JS, Bruford MW (2010) Population structure in the South American Tern Sterna hirundinacea in the South Atlantic: two populations with distinct breeding phenologies. J Avian Biol 41:378–387

    Article  Google Scholar 

  • Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 1:116–121

    Article  Google Scholar 

  • Friesen VL, Burg TM, McCoy KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785

    Article  CAS  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Given AD, Mills A, Baker AJ (2002) Isolation of polymorphic microsatellite loci from the red-billed gull (Larus novaehollandiae scopulinus) and amplification in related species. Mol Ecol Notes 2:416–418

    Article  CAS  Google Scholar 

  • Glutz von Blotzheim UN, Bauer KM (1982) Handbuch der Vögel Mitteleuropas, vol 8. Akademische Verlaggesellschaft, Wiesbaden

    Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Haverschmidt F (1978) Die Trauerseeschwalbe Chlidonias niger. Die Neue Brehm-Bücherei, A. Ziemsen Verlag, Wittenberg Lutherstadt

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evol 53:1898–1914

    Article  Google Scholar 

  • Jones KL, Krapu GL, Brandt DA, Ashley MV (2005) Population genetic structure in migratory sandhill cranes and the role of Pleistocene glaciations. Mol Ecol 14:2645–2657

    Article  CAS  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg N, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraaijeveld K (2008) Non-breeding habitat preference affects ecological speciation in migratory waders. Naturwissenschaften 95:347–354

    Article  CAS  PubMed  Google Scholar 

  • Maudet C, Miller C, Bassano B, Breitenmoser-Wursten C, Gauthier D, Obexer-Ruff G, Michallet J, Taberlet P, Luikart G (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Mol Ecol 11:421–436

    Article  CAS  Google Scholar 

  • Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Resour 14:726–733

    Article  PubMed  Google Scholar 

  • Miller MP, Mullins TD, Haig SM (2013) Genetic structure, diversity and subspecies status of Gull-billed Terns (Gelochelidon nilotica) from the United States. Waterbirds 36:310–318

    Article  Google Scholar 

  • Mossman CA, Waser PM (1999) Genetic detection of sex-biased dispersal. Mol Ecol 8:1063–1067

    Article  CAS  PubMed  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Olsen KM, Larsson H (1995) Terns of Europe and North America. A&C Black, London

    Google Scholar 

  • Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall ROD, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peck DR, Congdon BC (2004) Reconciling historical processes and population structure in the sooty tern Sterna fuscata. J Avian Biol 35:327–335

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • PopArt version 1.7. http://popart.otago.ac.nz

  • Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol Ecol Resour 16:608–627

    Article  PubMed  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing, version 3.3.1. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Szczys P, Hughes CR, Kesseli RV (2005) Novel microsatellite markers used to determine the population genetic structure of the endangered Roseate Tern, Sterna dougallii, in Northwest Atlantic and Western Australia. Conserv Genet 6:461–466

    Article  CAS  Google Scholar 

  • Szczys P, Nisbet IC, Wingate DB (2012) Conservation genetics of the Common Tern (Sterna hirundo) in the North Atlantic region; implications for the critically endangered population at Bermuda. Conserv Genet 13:1039–1043

    Article  Google Scholar 

  • Szostek KL, Schaub M, Becker PH (2014) Immigrants are attracted by local pre-breeders and recruits in a seabird colony. J Anim Ecol 83:1015–1024

    Article  PubMed  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tirard C, Helfenstein F, Danchin E (2002) Polymorphic microsatellites in the black-legged kittiwake Rissa tridactyla. Mol Ecol Notes 2:431–433

    Article  CAS  Google Scholar 

  • Trimbos KB, Musters CJM, Verkuil YI, Kentie R, Piersma T, de Snoo GR (2011) No evident spatial genetic structuring in the rapidly declining Black-tailed Godwit Limosa limosa limosa in The Netherlands. Conserv Genet 12:629–636

    Article  Google Scholar 

  • Van der Winden J (2002) The odyssey of the Black Tern Chlidonias niger: migration ecology in Europe and Africa. Ardea 90:421–435

    Google Scholar 

  • Van der Winden J (2004) Ringonderzoek aan de Zwarte Stern Chlidonias niger in het Groene Hart. Het Vogeljaar 52:155–161

    Google Scholar 

  • Van der Winden J (2008) A review of population estimates of the Eurasian Black Tern Chlidonias niger niger. Vogelwelt 129:47–50

    Google Scholar 

  • Van der Winden J, Fijn RC, van Horssen PW, Gerritsen-Davidse D, Piersma T (2014) Idiosyncratic migrations of Black Terns (Chlidonias niger): diversity in routes and stopovers. Waterbirds 37:162–174

    Article  Google Scholar 

  • Van der Winden J, Hagemeijer W, Terlouw R (1996) Heeft de Zwarte Stern Chlidonias niger een toekomst als broedvogel in Nederland? Limosa 69:149–164

    Google Scholar 

  • Van der Winden J, Nyame SK, Ntiamoa-Baidu Y, Gordon C (2000) Black Terns in Ghana, October 2000. Bureau Waardenburg, Ghana Wildlife Society, Centre for African Wetlands, Bureau Waardenburg report, 1052

  • Verkuil YI, Piersma T, Jukema J, Hooijmeijer JC, Zwarts L, Baker AJ (2012) The interplay between habitat availability and population differentiation: a case study on genetic and morphological structure in an inland wader (Charadriiformes). Biol J Linnean Soc 106:641–656

    Article  Google Scholar 

  • Waser PM, Strobeck C (1998) Genetic signatures of interpopulation dispersal. Trends Ecol Evol 13:43–44

    Article  CAS  PubMed  Google Scholar 

  • Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17:2321–2328

    Article  CAS  PubMed  Google Scholar 

  • Wetlands International (2006) Waterbird population estimates, 4th edn. Wetlands International, Wageningen

    Google Scholar 

  • Whittier JB, Leslie DM, Van Den Bussche RA (2006) Genetic variation among subspecies of Least Tern (Sterna antillarum): implications for conservation. Waterbirds 29:176–184

    Article  Google Scholar 

  • Wickham H (2009) Ggplot2: elegant graphics for data analysis. Springer, New York

    Book  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zink RM, Pavlova A, Drovetski S, Rohwer S (2008) Mitochondrial phylogeographies of five widespread Eurasian bird species. J Ornithol 149:399–413

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in ecology and evolution. Methods Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgements

We thank Phillip Elliott and Matthew Graham and two anonymous reviewers whose evaluation improved the manuscript. Funding was supplied by CSU-AAUP Research Grants and a Nisbet Research Grant from The Waterbird Society to P. Szczys, a Jean H. Thoreson ECSU-AAUP Scholarship to K.A. Lamothe, and The Rufford Foundation, Wetlands International and the Erasmus MC, Rotterdam to J. van der Winden. Data collection in Siberia, Russia was supported by the Russian Science Foundation Grant N 14-14-00603. Marcis Leja, Janis Viksne, Petro Gorlov, Josif Chernichko, Vladimir Shilo, and Jean-Marc Paillisson are thanked for field support of this project. This study complied with the current laws of the relevant countries

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Authors and Affiliations

  1. Eastern Connecticut State University, Willimantic, CT, 06226, USA

    Patricia Szczys & Karl A. Lamothe

  2. University of Toronto, Toronto, ON, M5S 3B2, Canada

    Karl A. Lamothe

  3. Institute of Systematic and Ecology of Animals, SB RAS, Novosibirsk, Russia

    Alexey Druzyaka

  4. Novosibirsk State University, Novosibirsk, Russia

    Alexey Druzyaka

  5. Statistics Netherlands, P.O. Box 24500, 2490 HA, The Hague, The Netherlands

    Martin J. M. Poot

  6. Azov-Black Sea Ornithological Station, Lenin Street 20, Melitopol, Ukraine

    Valeri Siokhin

  7. Ecology, Research and Consultancy, Dantelaan 115, 3533 VC, Utrecht, The Netherlands

    Jan van der Winden

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  1. Patricia Szczys
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  3. Alexey Druzyaka
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Correspondence to Patricia Szczys.

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Communicated by M. Wink.

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Szczys, P., Lamothe, K.A., Druzyaka, A. et al. Range-wide patterns of population differentiation of Eurasian Black Terns (Chlidonias niger niger) related to use of discrete post-nuptial staging sites. J Ornithol 158, 365–378 (2017). https://doi.org/10.1007/s10336-016-1408-5

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