Contrasting patterns of genetic differentiation among blackcaps (Sylvia atricapilla) with divergent migratory orientations in Europe

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Mettler, Raeann ^a   Martin Schaefer, H ^a   Chernetsov, Nikita ^b   Fiedler, Wolfgang ^c,d   Hobson, Keith A ^e   Ilieva, Mihaela ^f   Imhof, Elisabeth ^a   Johnsen, Arild ^g   Renner, Swen C ^h,i   Rolshausen, Gregor ^j   Serrano, David ^k   Wesołowski, Tomasz ^l   Segelbacher, Gernot ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b ZOOLOGICAL INSTITUTE   (Russian Federation)

^c MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^d UNIVERSITY OF KONSTANZ   (Germany)

^e ENVIRONMENT CANADA   (Canada)

^f INSTITUTE OF BIODIVERSITY AND ECOSYSTEM RESEARCH   (Bulgaria)

^g UNIVERSITY OF OSLO   (Norway)

^h UNIVERSITY OF ULM   (Germany)

ⁱ SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^j MCGILL UNIVERSITY   (Canada)

^k DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^l UNIVERSITY OF WROC AW   (Poland)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BLACKCAP; CONTROLLED STUDY; EUROPE; GENETIC ISOLATION BY DISTANCE; GENETIC VARIABILITY; GERMANY; GLACIATION; MIGRANT BIRD; NONHUMAN; POPULATION MIGRATION; SONGBIRD; SYMPATRY; WINTER; ANIMAL; EVOLUTION; FEMALE; GENETICS; GEOGRAPHY; MALE; POPULATION GENETICS;

ANIMAL MIGRATION; ANIMALS; BIOLOGICAL EVOLUTION; EUROPE; FEMALE; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; MALE; PASSERIFORMES;

EID: 84896698445     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081365     Document Type: Article

References (72)

1. Hewitt GM (1996) Some genetic consequences of ice ages, and their role, in divergence and speciation. Biol J Linn Soc Lond 58: 247-276. doi:10.1006/bijl.1996.0035.
2. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405: 907-913. doi:10.1038/35016000. PubMed: 10879524.
3. Neethling M, Matthee CA, Bowie RCK, von der Heyden S (2008) Evidence for panmixia despite barriers to gene flow in the southern African endemic, Caffrogobius caffer (Teleostei: Gobiidae). BMC Evol Biol 8: 325. PubMed: 19040766.
4. Oomen RA, Reudink MW, Nocera JJ, Somers CM, Green MC et al. (2011) Mitochondrial evidence for panmixia despite perceived barriers to gene flow in a widely distributed waterbird. J Hered 102: 584-592. doi:10.1093/jhered/esr055. PubMed: 21705489.
5. Reudink MW, Kyle CJ, Nocera JJ, Oomen RA, Green MC et al. (2011) Panmixia on a continental scale in a widely distributed colonial waterbird. Biol J Linn Soc Lond 102: 583-592. doi:10.1111/j.1095-8312.2010.01608.x.
6. Coyne JA, Orr JA (2004) Speciation. Sunderland, MA: Sinauer Associates Inc.
7. Newton I (2008) The Migration Ecology of Birds. London, UK: Academic Press.
8. Ruegg KC, Smith TB (2002) Not as the crow flies: a historical explanation for circuitous migration in Swainson's thrush (Catharus ustulatus). Proc R Soc Lond B Biol Sci 269: 1375-1381. doi:10.1098/rspb.2002.2032.
9. Lyons JI, Pierce AA, Barribeau SM, Sternberg ED, Mongue AJ et al. (2012) Lack of genetic differentiation between monarch butterflies with divergent migration destinations. Mol Ecol 21: 1-12. doi:10.1111/j.1365-294X.2011.05381.x. PubMed: 22574833.
10. Dallimer M, Jones PJ, Pemberton JM, Cheke RA (2003) Lack of genetic and plumage differentiation in the red-billed quelea Quelea quelea across a migratory divide in southern Africa. Mol Ecol 12: 345-353. doi:10.1046/j.1365- 294X.2003.01733.x. PubMed: 12535086.
11. McKay BD (2009) Evolutionary history suggests rapid differentiation in the yellow-throated warbler Dendroica dominica. J Avian Biol 40: 181-190.
12. Bensch S, Grahn M, Müller N, Gay L, Akesson S (2009) Genetic, morphological, and feather isotope variation of migratory willow warblers show gradual divergence in a ring. Mol Ecol 18: 3087-3096. doi:10.1111/j.1365-294X. 2009.04210.x. PubMed: 19457197.
13. Rohwer S, Irwin DE (2011) Molt, Orientation, and Avian Speciation. Auk 128: 419-425. doi:10.1525/auk.2011.10176.
14. Ruegg K (2008) Genetic, morphological, and ecological characterization of a hybrid zone that spans a migratory divide. Evolution 62: 452-466. doi:10.1111/j.1558-5646.2007.00263.x. PubMed: 18039327.
15. Pulido F, Berthold P (2010) Current selection for lower migratory activity will drive the evolution of residency in a migratory bird population. Proc Natl Acad Sci U S A 107: 7341-7346. doi:10.1073/pnas.0910361107. PubMed: 20368446.
16. Kovach RP, Gharrett AJ, Tallmon DA (2012) Genetic change for earlier migration timing in a pink salmon population. Proc R Soc Lond B Biol Sci 279: 3870-3878. doi:10.1098/rspb.2012.1158.
17. Bearhop S, Fiedler W, Furness RW, Votier SC, Waldron S et al. (2005) Assortative mating as a mechanism for rapid evolution of a migratory divide. Science 310: 502-504. doi:10.1126/science.1115661. PubMed: 16239479.
18. Rolshausen G, Hobson KA, Schaefer HM (2010) Spring arrival along a migratory divide of sympatric blackcaps (Sylvia atricapilla). Oecologia 162: 175-183. doi:10.1007/s00442-009-1445-3. PubMed: 19711103.
19. Ruegg K, Anderson EC, Slabbekoorn H (2012) Differences in timing of migration and response to sexual signalling drive asymmetric hybridization across a migratory divide. J Evol Biol 9: 1741-1750. PubMed: 22747896.
20. Rolshausen G, Segelbacher G, Hobson KA, Schaefer HM (2009) Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Curr Biol 19: 2097-2101. doi:10.1016/j.cub.2009.10.061. PubMed: 19962309.
21. Helbig A (1991) Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE-and SW-migrating blackcaps (Sylvia atricapilla). Behav Ecol Sociobiol 28: 9-12.
22. Pulido F, Berthold P (2003) Quantitative genetic analysis of migratory behavior. In: P BertholdE GwinnerE Sonnenschein. Avian Migration. Berlin: Springer-Verlag. pp. 53-77.
23. Helbig AJ, Berthold P, Mohr G, Querner U (1994) Inheritance of a novel migratory direction in central European Blackcaps. Naturwissenschaften 81: 184-186. doi:10.1007/BF01134540.
24. Helbig AJ (1996) Genetic basis, mode of inheritance and evolutionary changes of migratory directions in palaearctic warblers (Aves: Sylviidae). Exp Biol 199: 49-55. PubMed: 9317319.
25. Zink G (1985) Der Zug europäischer Singvögel. Ein Atlas der Wiederfunde beringter Vögel. Vogelwarte Radolfzell: Max-Planck-Institute für Verhaltensphysiologie.
26. Møller a P, Garamszegi LZ, Peralta-Sánchez JM, Soler JJ (2011) Migratory divides and their consequences for dispersal, population size and parasite-host interactions. Evol Biol 24: 1744-1755
27. Helbig J (1991) SE- and SW-migrating blackcap (Sylvia atricapilla) populations in Central Europe: Orientation of birds in the contact zone. Journal of Evolutionary Biology 4: 657-670. doi:10.1046/j.1420-9101.1991.4040657.x.
28. Pérez-Tris J, Bensch S, Carbonell R, Helbig AJ, Tellería JL (2004) Historical diversification of migration patterns in a passerine bird. Evolution 58: 1819-1832. doi:10.1111/j.0014-3820.2004.tb00464.x. PubMed: 15446433.
29. Berthold P, Helbig A, Mohr G, Querner U (1992) Rapid microevolution of migratory behaviour in a wild bird species. Nature 360: 668-670. doi: 10.1038/360668a0.
30. Terrill Scott B, Berthold P (1990) Ecophysiological aspects of rapid population growth in a novel migratory Blackcap (Sylvia atricapilla) population: an experimental approach. Oecologia 85: 266-270. doi: 10.1007/BF00319412.
31. Procházka P, Stokke BG, Jensen H, Fainová D, Bellinvia E et al. (2011) Low genetic differentiation among reed warbler Acrocephalus scirpaceus populations across Europe. J Avian Biol 42: 103-113. doi: 10.1111/j.1600-048X.2010.05161.x.
32. Hobson KA, Bowen GJ, Wassenaar LI, Ferrand Y, Lormee H (2004) Using stable hydrogen and oxygen isotope measurements of feathers to infer geographical origins of migrating European birds. Oecologia 141: 477-488. PubMed: 15375691.
33. Wassenaar LI, Hobson KA (2003) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isotopes Environ Health Stud 39: 211-217. doi:10.1080/1025601031000096781. PubMed: 14521282.
34. Csörgo{combining double acute accent} T, Gyurácz J (2009) Barátposzáta Sylvia atricapilla. In: T Csörgo{combining double acute accent}Z KarczaH Gergo{combining double acute accent}M GáborJ Gyurácz. Magyar madárvonulási atlasz. Budapest.: Kossuth Kaidó. pp. 504-508.
35. Klvaňa P (2008) Pěnice černohlavá Sylvia atricapilla. In: J CepákP KlvaňaJ FormánekD HorákM Jelínek. Czech and Slovak Bird Migration Atlas. Prague: Aventinum. pp. 436-439.
36. Fransson T, Hall-Karlsson S (2008) Svensk ringmärkningsatlas. Vol. 3. Stockholm: Naturhistoriska riksmuseet and Sveriges Ornitologiska Förening
37. Kopiec K, Ozarowska A (2012) The origin of Blackcaps Sylvia atricapilla wintering on the British Isles. Ornis Fenn 89: 254-263.
38. Molecular Ecology Resources Primer Development Consortium, Aksoy S, Almeida-Val VMF, Azevedo VCR, Baucom R et al. (2013) Permanent Genetic Resources added to Molecular Ecology Resources Database 1 October 2012-30 November 2012. Mol Ecol Resour 13: 341-343. doi:10.1111/1755-0998.12061. PubMed: 23356940.
39. Segelbacher G, Rolshausen G, Weis-Dootz T, Serrano D, Schaefer HM (2008) Isolation of 10 tetranucleotide microsatellite loci in the blackcap (Sylvia atricapilla). Mol Ecol Resour 8: 1108-1110. doi:10.1111/j.1755-0998.2008.02171. x. PubMed: 21585986.
40. Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25: 1982-1983. doi:10.1093/bioinformatics/btp303. PubMed: 19420055.
41. Peakall R, Smouse P (2006) GENALEX 6□?: genetic analysis in Excel . Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295. doi:10.1111/j.1471-8286.2005.01155.x.
42. Rousset F (2008) genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103-106. doi:10.1111/j.1471-8286.2007.01931.x. PubMed: 21585727.
43. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc Series B Stat Methodol 64: 479-498. doi: 10.1111/1467-9868.00346.
44. Jost L (2008) G ST and its relatives do not measure differentiation. Mol Ecol 17: 4015-4026. doi:10.1111/j.1365-294X.2008.03887.x. PubMed: 19238703.
45. Gerlach G, Jueterbock A, Kraemer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Mol Ecol 19: 3845-3852. doi: 10.1111/j.1365-294X.2010. 04784.x. PubMed: 20735737.
46. 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. doi:10.1111/j.1755-0998.2010.02847.x. PubMed: 21565059.
47. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6: 13 v 3.23 http://ibdws.sdsu.edu/.
48. Vavrek MJ (2011) fossil: palaeoecological and palaeogeographical analysis tools. Palaeontol Electronica: 14: 1T.
49. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462. PubMed: 7705646.
50. Cramp S (1992) Handbook of the birds of Europe, the Middle East and North Africa: The birds of the Western Palearctic, Vol. 6. Oxford: Oxford University Press.
51. R Development Core Team (2013) R: A language and environment for statistical computing. Available: http://www.r-project.org/.
52. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959. PubMed: 10835412.
53. Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F -statistics. Mol Ecol Notes 2: 184-186.
54. Hewitt G (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc Lond 68: 87-112. doi:10.1111/j.1095-8312.1999.tb01160.x.
55. Davis LA, Roalson EH, Cornell KL, McClanahan KD, Webster MS (2006) Genetic divergence and migration patterns in a North American passerine bird: implications for evolution and conservation. Mol Ecol 15: 2141-2152. doi:10.1111/j.1365-294X.2006.02914.x. PubMed: 16780431.
56. Neto JM, Arroyo JL, Bargain B, Monrós JS, Mátrai N et al. (2012) Phylogeography of a habitat specialist with high dispersal capability: the Savi's Warbler Locustella luscinioides. PLOS ONE 7: e38497. doi: 10.1371/journal.pone.0038497. PubMed: 22701653.
57. Helbig AJ (1992) Population differentiation of migratory directions in birds: comparison between ringing results and orientation behaviour of hand-raised migrants. Oecologia 90: 483-488. doi:10.1007/BF01875441.
58. Wesołowski T (2011) Blackcap Sylvia atricapilla numbers, phenology and reproduction in a primeval forest - a 33-year study. J Ornithol 152: 319-329. doi:10.1007/s10336-010-0585-x.
59. Barton NH, Hewitt GM (1985) Analysis of Hybrid Zones. Annu Rev Ecol Syst 16: 113-148. doi:10.1146/annurev.es.16.110185.000553.
60. Buggs RJ (2007) Empirical study of hybrid zone movement. Heredity (Edinb) 99: 301-312. doi:10.1038/sj.hdy.6800997. PubMed: 17611495.
61. Stutchbury BJM, Tarof SA, Done T, Gow E, Kramer PM et al. (2009) Tracking long-distance songbird migration by using geolocators. Science 323: 896. doi:10.1126/science.1166664. PubMed: 19213909.
62. Tøttrup AP, Klaassen RHG, Strandberg R, Thorup K, Kristensen MW et al. (2012) The annual cycle of a trans-equatorial Eurasian-African passerine migrant: different spatio-temporal strategies for autumn and spring migration. Proc Biol Sci 279: 1008-1016. doi:10.1098/rspb.2011.1323. PubMed: 21900322.
63. Delmore KE, Fox JW, Irwin DE (2012) Dramatic intraspecific differences in migratory routes, stopover sites and wintering areas, revealed using light-level geolocators. P Proc Biol Sci 279: 4582-4589
64. Helbig AJ (1991) Inheritance of migratory direction in a bird species: a cross-breeding experiment with SE- and SW-migrating blackcaps (Sylvia atricapilla). Behav Ecol Sociobiol 28: 9-12.
65. Payevsky V (1999) Breeding biology, morphometrics, and population dynamics of Sylvia warblers in the Eastern Baltic. Avian Ecol Behav 2: 19-50.
66. Sokolov LV (2006) Effect of global warming on the timing of migration and breeding of passerine birds in the 20th century. Entomol Rev 86: S59-S81. doi:10.1134/S0013873806100058.
67. Dingle H (2006) Animal migration: is there a common migratory syndrome? J Ornithol 147: 212-220. doi:10.1007/s10336-005-0052-2.
68. Pulido F (2007) The genetics and evolution of avian migration. BioScience 57: 165-174.
69. Liedvogel M, Akesson S, Bensch S (2011) The genetics of migration on the move. Trends Ecol Evol 26: 561-569. doi:10.1016/j.tree. 2011.07.009. PubMed: 21862171.
70. Piersma T, Pérez-Tris J, Mouritsen H, Bauchinger U, Bairlein F (2005) Is there a "migratory syndrome" common to all migrant birds? Ann N Y Acad Sci 1046: 282-293. doi:10.1196/annals.1343.026. PubMed: 16055861.
71. Rheindt FE, Edwards SV (2011) Genetic introgression?□: an integral but neglected component of speciation in birds. Auk 128: 620-632. doi: 10.1525/auk.2011.128.4.620.
72. Chabot AA, Hobson KA, Van Wilgenburg SL, McQuat GJ, Lougheed SC (2012) Advances in linking wintering migrant birds to their breeding-ground origins using combined analyses of genetic and stable isotope markers. PLOS ONE 7: e43627. doi:10.1371/journal.pone.0043627. PubMed: 22916285.