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Journal of Ornithology

, Volume 160, Issue 4, pp 965–972 | Cite as

Shallow genetic population structure in an expanding migratory bird with high breeding site fidelity, the Western Eurasian Crane Grus grus grus

  • Martin HaaseEmail author
  • Henriette Höltje
  • Beate Blahy
  • Damon Bridge
  • Eberhard Henne
  • Ulf S. Johansson
  • Katrin Kaldma
  • Ekaterina A. Khudyakova
  • Amy King
  • Aivar Leito
  • Wolfgang Mewes
  • Elena A. Mudrik
  • Ivar Ojaste
  • Dmitry V. Politov
  • Ronald Popken
  • Juhani Rinne
  • Andrew Stanbury
  • Jesper Tofft
  • Ülo Väli
  • Angela Schmitz Ornés
Original Article

Abstract

For more than half a century, the Western Eurasian Crane (Grus grus grus) has been expanding its range toward western Europe, recolonizing areas where it had been previously driven to extinction, including the UK, the Netherlands and Denmark. The Western Eurasian Crane is, on the one hand, a very mobile, migratory species, but on the other, is territorial and shows high breeding site fidelity. Hence, its genetic population structure is subject to antagonizing forces, which have different consequences. Based on the genotyping of six highly variable microsatellite loci, we inferred the population structure of the Western Eurasian Crane from samples from eight regions. We integrated classic F-statistics including analyses of molecular variance with a priori designation of structure and divisive clustering approaches, i.e. a Bayesian procedure (STRUCTURE) and discriminant analysis of principal components, which infer structure a posteriori. According to the F-statistics, populations were only weakly differentiated, and the majority of the genetic variance (> 90%) was attributed to individuals. At first glance, the divisive approaches appeared to agree in finding four clusters. Yet, there was no correspondence regarding the composition of the clusters and none of the results were biologically meaningful. However, STRUCTURE delivered an alternative interpretation, designating the highest likelihood to a scenario without subdivision, in clear agreement with the findings based on the F-statistics. In conclusion, the Western Eurasian Crane is genetically largely homogeneous, probably as a consequence of the rapid growth and range expansion of its population.

Keywords

Analyses of molecular variance Bayesian clustering Gruiformes Population expansion Population genetics Population growth 

Zusammenfassung

Geringe genetische Populationsstruktur eines sich ausbreitenden Zugvogels mit hoher Brutortreue, des Westlichen Eurasischen Kranichs, Grus grus grus

Seit mehr als einem halben Jahrhundert breitet sich der Eurasische Kranich (Grus grus grus) wieder nach Westeuropa bis hin nach Großbritannien, den Niederlanden und Dänemark aus, wo er ausgerottet war. Der Eurasische Kranich ist einerseits eine sehr mobile, ziehende Art. Andererseits ist er territorial und zeichnet sich durch eine hohe Brutplatztreue aus. Die genetische Populationsstruktur ist somit von gegensätzlichen Kräften mit unterschiedlichen Konsequenzen geprägt. Wir ermittelten die Populationsstruktur der Westeuropäischen Population (WEP) des Eurasischen Kranichs basierend auf sechs hochvariablen Mikrosatelliten-Loci und Samples aus acht Regionen. Wir kombinierten klassische F-Statistik einschließlich molekularer Varianzanzanalysen mit a priori festgelegter Struktur mit divisiven Clusteranalysen—einer Bayes’schen Methode (STRUCTURE) und einer Diskriminanzanalyse von Hauptkomponenten (DAPC)–, die die Struktur a posteriori schätzen. Die F-Statistik zeigte, dass die Populationen nur gering differenziert waren. Der Großteil der genetischen Varianz (> 90%) lag auf Ebene der Individuen. Auf den ersten Blick schienen die divisiven Ansätze ein übereinstimmendes Bild zu zeichnen. Beide fanden vier Cluster. Allerdings gab es keinerlei Übereinstimmung in der Zusammensetzung der Cluster und keines der Resultate war biologisch sinnvoll. STRUCTURE wies allerdings die höchste Wahrscheinlichkeit einem Szenario ohne Populationsunterteilung zu und lieferte somit eine alternative Interpretation, die mit der F-Statistik übereinstimmte. Daher schließen wir, dass die WEP des Eurasischen Kranichs weitestgehend homogen ist.

Notes

Acknowledgements

Completely unexpectedly, our co-author Aivar Leito passed away a few days before finalizing the manuscript. We dedicate this study to his memory. We are grateful to Christel Meibauer and Silke Fregin, technicians in the lab in Greifswald, for their support. Pekka Mustakallio is particularly acknowledged for organising the Finnish crane ringing scheme. We are thankful to Uko Bleive, Trinus Haitjema, Mati Martinson, Indrek Põder, Urmas Sellis and Ainar Unus for collecting the samples in Estonia. This work was supported by institutional research funding (IUT21-1) of the Estonian Ministry of Education and Research. E. A. M. and D. V. P. were supported by the Russian state (contract no. 0112-2019-0001).

Supplementary material

10336_2019_1688_MOESM1_ESM.docx (56 kb)
Supplementary material 1 (DOCX 56 kb)

References

  1. Barton N, Slatkin M (1986) A quasi-equilibrium theory of the distribution of rare alleles in a subdivided population. Heredity 56:409–415PubMedGoogle Scholar
  2. Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons Gen Resour 4:359–361Google Scholar
  3. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedPubMedCentralGoogle Scholar
  4. Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864PubMedGoogle Scholar
  5. 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 10:564–567PubMedPubMedCentralGoogle Scholar
  6. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501Google Scholar
  7. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578PubMedPubMedCentralGoogle Scholar
  8. Fourcade Y, Richardson DS, Keišs O, Budka M, Green RE, Fokin S, Secondi J (2016) Corncrake conservation genetics at a European scale: the impact of biogeographical and anthropological processes. Biol Cons 198:210–219Google Scholar
  9. Garnier J, Lewis MA (2016) Expansion under climate change: the genetic consequences. Bull Math Biol 78:2165–2185PubMedGoogle Scholar
  10. Goldberg J, Trewick SA, Powlesland RG (2011) Population structure and biogeography of Hemiphaga pigeons (Aves: Columbidae) on islands in the New Zealand region. J Biogeogr 38:285–298Google Scholar
  11. Goodsman DW, Cooke B, Coltman DW, Lewis MA (2014) The genetic signature of rapid range expansions: how dispersal, growth and invasion speed impact heterozygosity and allele surfing. Theor Pop Biol 98:1–10Google Scholar
  12. Haase M, Ilyashenko V (2012) A glimpse on mitochondrial differentiation of four currently recognized subspecies of Common Crane (Grus grus). Ardeola 59:131–136Google Scholar
  13. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedPubMedCentralGoogle Scholar
  14. Höltje H, Mewes W, Haase M, Schmitz A (2016) Genetic evidence of female specific eggshell colouration in the Common Crane (Grus grus). J Ornithol 157:609–617Google Scholar
  15. Horváth MBB, Martinez-Cruz JJ, Negro L, Kalm R, Godoy JA (2005) An overlooked DNA source for non-invasive genetic analysis in birds. J Avian Biol 36:84–88Google Scholar
  16. Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291Google Scholar
  17. Jahner JP, Gibson D, Weitzman CL, Blomberg EJ, Selinger JS, Parchman TL (2016) Fine-scale genetic structure among Greater Sage-grouse leks in central Nevada. BMC Evol Biol 16:127PubMedPubMedCentralGoogle Scholar
  18. Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071PubMedPubMedCentralGoogle Scholar
  19. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94PubMedPubMedCentralGoogle Scholar
  20. Joosten H, Couwenberg J (2001) Zur Anthropogenen Veränderung der Moore: Bilanzen zum Moorverslust, das Beispiel Europa. In: Succow M, Joosten H (eds) Landschaftsökologische Moorkunde. Schweizerbart’sche, Stuttgart, pp 406–409Google Scholar
  21. Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedGoogle Scholar
  22. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191PubMedPubMedCentralGoogle Scholar
  23. Leito A, Keskpaik J, Ojaste I, Truu J (2006) The Eurasian Crane in Estonia. Estonian University of Life Sciences, TartuGoogle Scholar
  24. Leito A, Ojaste I, Põder I (2013) Monitoring of the Eurasian Crane in Estonia: methods and last results. In: Nowald G, Weber A, Fanke J, Weinhardt E, Donner N (eds) Proceedings of the VIIth European Crane Conference, Stralsund. Groß Mohrdorf, pp 141–145Google Scholar
  25. Leito A, Külvik M, Bunce RGH, Ojaste I, Raet J, Villoslada M, Leivits M, Kull A, Kuusemets V, Kull T, Metzger MJ, Sepp K (2015) The potential impacts of changes in ecological networks, land use and climate on the Eurasian Crane population in Estonia. Landscape Ecol 30:887–904Google Scholar
  26. Meirmans PG, Hedrick PW (2011) Assessing population structure: F ST and related measures. Mol Ecol Resour 11:5–18PubMedGoogle Scholar
  27. Meirmans PG, van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794Google Scholar
  28. Mewes W (2017) Die Brutorttreue von Kranichen Grus grus in Nordostdeutschland. Vogelwelt 137:249–260Google Scholar
  29. Mills LS, Allendorf FW (1996) The one-migrant-per-generation-rule in conservation and management. Cons Biol 6:1509–1518Google Scholar
  30. Morinha F, Dávila JA, Bastos E, Cabral JA, Frías O, Gonzalez JL, Travassos P, Carvalho D, Milá B, Blanco G (2017) Extreme genetic structure in a social bird species despite high dispersal capacity. Mol Ecol 26:2812–2825PubMedGoogle Scholar
  31. Mudrik EA, Kashentseva TA, Redchuk PS, Politov DV (2015) Microsatellite variability data confirm low genetic differentiation of western and eastern subspecies of Common Crane Grus grus L. (Gruidae, Aves). Mol Biol 49:260–266Google Scholar
  32. Nowald G, Alonso JC (2016) Beringung und Datenverarbeitung. In: Prange H (ed) Die Welt der Kraniche. MediaNatur, Minden, pp 183–194Google Scholar
  33. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. Population genetic software for teaching and research: an update. Bioinformatics 28:2537–2539PubMedPubMedCentralGoogle Scholar
  34. Prange H (2016) Die Welt der Kraniche. MediaNatur, MindenGoogle Scholar
  35. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  36. Pritchard JK, Wen X, Falush D (2007) Documentation for STRUCTURE software: version 2.2Google Scholar
  37. Proctor NS, Lynch PJ (1993) Manual of ornithology: avian structure and function. Yale University Press, YaleGoogle Scholar
  38. Pulgarín-R PC, Burg TM (2012) Genetic signals of demographic expansion in Downy Woodpecker (Picoides pubescens) after the last North American Glacial Maximum. PLOS ONE 7:e40412PubMedPubMedCentralGoogle Scholar
  39. Quillfeldt P, Moodley Y, Weimerskirch H, Cherel Y, Delord K, Phillips RA, Navarro J, Calderon L, Masello JF (2017) Does genetic structure reflect differences in non-breeding movements? A case study in small, highly mobile seabirds. BMC Evol Biol 17:160PubMedPubMedCentralGoogle Scholar
  40. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  41. Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10:263–284Google Scholar
  42. Rousset F (2007) Inferences from spatial population genetics. In: Balding D, Bishop M, Cannings C (eds) Handbook of statistical genetics. Wiley, Chichester, pp 945–979Google Scholar
  43. Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedPubMedCentralGoogle Scholar
  44. Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the “landscape” in landscape genetics. Heredity 98:128–142PubMedGoogle Scholar
  45. Tofft J (2016) Dänemark. In: Prange H (ed) Die Welt der Kraniche. MediaNatur, Minden, pp 462–465Google Scholar
  46. Van Andel J, Aronson J (2006) Restoration ecology. Blackwell, MaldenGoogle Scholar
  47. Wang J (2004) Application of the one-migrant-per-generation rule to conservation and management. Cons Biol 18:332–343Google Scholar
  48. Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: F ST not equal to 1/(4N m + 1). Heredity 82:117–125PubMedGoogle Scholar
  49. Wright S (1978) Evolution and the genetics of populations. Variability within and among natural populations, vol 4. University of Chicago Press, ChicagoGoogle Scholar
  50. Zaccara S, Crosa G, Vanetti I, Binelli G, Childress B, McCulloch G, Harper DM (2011) Lesser Flamingo Phoeniconaias minor as a nomadic species in African shallow alkaline lakes and pans: genetic structure and future perspectives. Ostrich 82:95–100Google Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  • Martin Haase
    • 1
    Email author
  • Henriette Höltje
    • 1
  • Beate Blahy
    • 2
  • Damon Bridge
    • 3
  • Eberhard Henne
    • 2
  • Ulf S. Johansson
    • 4
  • Katrin Kaldma
    • 5
  • Ekaterina A. Khudyakova
    • 6
  • Amy King
    • 3
  • Aivar Leito
    • 5
  • Wolfgang Mewes
    • 7
  • Elena A. Mudrik
    • 8
  • Ivar Ojaste
    • 5
  • Dmitry V. Politov
    • 8
  • Ronald Popken
    • 9
  • Juhani Rinne
    • 10
  • Andrew Stanbury
    • 3
  • Jesper Tofft
    • 11
  • Ülo Väli
    • 5
  • Angela Schmitz Ornés
    • 1
  1. 1.Vogelwarte Zoological Institute and MuseumUniversity of GreifswaldGreifswaldGermany
  2. 2.Koppel 1SteinhöfelGermany
  3. 3.RSPB Centre for Conservation ScienceRoyal Society for the Protection of BirdsSandyUK
  4. 4.Department of ZoologySwedish Museum of Natural HistoryStockholmSweden
  5. 5.Institute of Agricultural and Environmental SciencesEstonian University of Life SciencesTartuEstonia
  6. 6.Faculty of Biology and ChemistryIvanovo State UniversityIvanovoRussia
  7. 7.Grüner Weg 3KarowGermany
  8. 8.Vavilov Institute of General Genetics Russian Academy of SciencesMoscowRussia
  9. 9.NatuurmonumentenRuinenNetherlands
  10. 10.MasalaFinland
  11. 11.AabenraaDenmark

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