Skip to main content
SpringerLink
Log in

Contrasted patterns of genetic differentiation across eight bird species in the Lesser Antilles

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Archipelagoes are considered as “natural laboratories” for studying processes that shape the distribution of diversity. The Lesser Antilles provide a favorable geographical context for divergence to occur. However, although morphological subspecies have been described across this archipelago in numerous avian species, the potential for the Lesser Antilles in driving intra-specific genetic divergence in highly mobile organisms such as birds remains understudied. Here, we assessed level of intra-specific genetic diversity and differentiation between three islands of the Lesser Antilles (Guadeloupe, Dominica and Martinique) using a multi-species approach on eight bird species. For each species, we built a set of microsatellite markers from cross-species amplifications. Significant patterns of inter-island and/or within-island genetic differentiation were detected in all species. However, levels of intra-specific genetic differentiation among the eight bird species were not always consistent with the boundaries of subspecies previously described in the sampled islands. These results suggest different histories of colonization/expansion and/or different species-specific ecological traits affecting gene flow, advocating for multi-species studies of historical and contemporary factors shaping the distribution of diversity on islands.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arguedas N, Parker PG (2000) Seasonal migration and genetic population structure in house wrens. The Condor 102:517–528

    Article  Google Scholar 

  • Arnoux E, Eraud C, Thomas A et al (2013) Phenotypic variation of Forest Thrushes Turdus lherminieri in Guadeloupe: evidence for geographic differentiation at fine spatial scale. J Ornithol 154:977–985

    Article  Google Scholar 

  • Arnoux E, Eraud C, Navarro N et al (2014) Morphology and genetics reveal an intriguing pattern of differentiation at a very small geographic scale in a bird species, the forest thrush Turdus lherminieri. Heredity 113:514–525

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barr KR, Lindsay DL, Athrey G et al (2008) Population structure in an endangered songbird: maintenance of genetic differentiation despite high vagility and significant population recovery. Mol Ecol 17:3628–3639

    Article  PubMed  Google Scholar 

  • Bates JM (2002) The genetic effects of forest fragmentation on five species of amazonian birds. J Avian Biol 33:276–294

    Article  Google Scholar 

  • Belisle M, Desrochers A, Fortin M-J (2001) Influence of forest cover on the movements of forest birds: a homing experiment. Ecology 82:1893

    Article  Google Scholar 

  • Belkhir KBP, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier (France) http://www.univ-montp2.fr/~genetix/genet?ix/genetix.htm

  • Bellemain E, Bermingham E, Ricklefs RE (2008) The dynamic evolutionary history of the bananaquit (Coereba flaveola) in the Caribbean revealed by a multigene analysis. BMC Evol Biol 8:240

    Article  PubMed Central  PubMed  Google Scholar 

  • Bertrand JAM, Bourgeois YXC, Delahaie B et al (2014) Extremely reduced dispersal and gene flow in an island bird. Heredity 112:190–196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bouzat JL, Johnson K (2004) Genetic structure among closely spaced leks in a peripheral population of lesser prairie-chickens. Mol Ecol 13:499–505

    Article  PubMed  Google Scholar 

  • Brewer D (2016a) Black-whiskered Vireo (Vireo altiloquus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

    Google Scholar 

  • Brewer D (2016b) Lesser antillean saltator (Saltator albicollis). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

    Google Scholar 

  • Burney CW, Brumfield RT (2009) Ecology predicts levels of genetic differentiation in Neotropical birds. Am Nat 174:358–368

    Article  PubMed  Google Scholar 

  • Clegg SM, Degnan SM, Moritz C et al (2002) Microevolution in island forms: the roles of drift and directional selection in morphological divergence of a passerine bird. Evolution 56:2090–2099

    Article  PubMed  Google Scholar 

  • Clegg SM, Kelly JF, Kimura M, Smith TB (2003) Combining genetic markers and stable isotopes to reveal population connectivity and migration patterns in a Neotropical migrant, Wilson’s warbler (Wilsonia pusilla). Mol Ecol 12:819–830

    Article  CAS  PubMed  Google Scholar 

  • Cody M (2016) Scaly-breasted Thrasher (Margarops fuscus). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

    Google Scholar 

  • Coyne JA, Price TD (2000) Little evidence for sympatric speciation in island birds. Evolution 54:2166–2171

    CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Curson J (2016) Plumbeous Warbler (Dendroica plumbea). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

    Google Scholar 

  • Darwin C (1859) On the origins of species by means of natural selection. Watts, London

    Google Scholar 

  • Davies KF, Margules CR, Lawrence JF (2000) Which traits of species predict population declines in experimental forest fragments? Ecology 81:1450–1461

    Article  Google Scholar 

  • Dawson DA, Horsburgh GJ, KüPper C et al (2010) New methods to identify conserved microsatellite loci and develop primer sets of high cross-species utility—as demonstrated for birds. Mol Ecol Resour 10:475–494

    Article  CAS  PubMed  Google Scholar 

  • Dawson DA, Ball AD, Spurgin LG et al (2013) High-utility conserved avian microsatellite markers enable parentage and population studies across a wide range of species. BMC Genom 14:176

    Article  CAS  Google Scholar 

  • del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (2014) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

    Google Scholar 

  • Desrochers A, Bélisle M, Morand-Ferron J, Bourque J (2011) Integrating GIS and homing experiments to study avian movement costs. Landsc Ecol 26:47–58

    Article  Google Scholar 

  • Doebeli M, Dieckmann U (2003) Speciation along environmental gradients. Nature 421:259–264

    Article  CAS  PubMed  Google Scholar 

  • Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966

    Article  CAS  PubMed  Google Scholar 

  • Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, Princeton

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed Central  CAS  PubMed  Google Scholar 

  • Francisco MR, Gibbs HL, Galetti M et al (2007) Genetic structure in a tropical lek-breeding bird, the blue manakin (Chiroxiphia caudata) in the Brazilian Atlantic Forest. Mol Ecol 16:4908–4918

    Article  PubMed  Google Scholar 

  • Freeman-Gallant CR (1996) Microgeographic patterns of genetic and morphological variation Savannah Sparrows (Passerculus sandwichensis). Evolution 50:1631–1637

    Article  Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Ann Rev Ecol Evol Syst 34:397–423

    Article  Google Scholar 

  • Garnier S, Alibert P, Audiot P et al (2004) Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus solieri. Mol Ecol 13:1883–1897

    Article  CAS  PubMed  Google Scholar 

  • Gillespie R (2004) Community assembly through adaptive radiation in Hawaiian spiders. Science 303:356–359

    Article  CAS  PubMed  Google Scholar 

  • Grant PR, Grant BR (2002) Adaptive radiation of Darwin’s finches. Am Sci 90:130–139

    Article  Google Scholar 

  • Greenberg R, Cordero PJ, Droege S, Fleischer RC (1998) Morphological adaptation with no mitochondrial DNA differentiation in the coastal plain swamp sparrow. The Auk 115:706–712

    Article  Google Scholar 

  • Harris RJ, Reed JM (2002) Behavioral barriers to non-migratory movements of birds. Ann Zool Fenn 39:275–290

    Google Scholar 

  • Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638

    Article  CAS  PubMed  Google Scholar 

  • Henle K, Davies KF, Kleyer M et al (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Article  Google Scholar 

  • Hillis DM, Moritz C, Mable BK (1996) Molecular systematics, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed Central  PubMed  Google Scholar 

  • Hunt JS, Bermingham E, Ricklefs RE (2001) Molecular systematics and biogeography of Antillean thrashers, tremblers, and mockingbirds (Aves: Mimidae). The Auk 118:35–55

    Article  Google Scholar 

  • Kisel Y, Barraclough TG (2010) Speciation has a spatial scale that depends on levels of gene flow. Am Nat 175:316–334

    Article  PubMed  Google Scholar 

  • Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836

    Article  CAS  PubMed  Google Scholar 

  • Lovette IJ, Bermingham E, Seutin G, Ricklefs RE (1998) Evolutionary differentiation in three endemic West Indian warblers. Auk 115:890–903

    Article  Google Scholar 

  • Lovette IJ, Bermingham E, Ricklefs RE (1999) Mitochondrial DNA phylogeography and the conservation of endangered Lesser Antillean Icterus orioles. Conserv Biol 13:1088–1096

    Article  Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • McGuire JA, Witt CC, Altshuler DL, Remsen JV Jr (2007) Phylogenetic systematics and biogeography of hummingbirds: bayesian and maximum likelihood analyses of partitioned data and selection of a appropriate partitioning strategy. Syst Biol 56:837–856

    Article  CAS  PubMed  Google Scholar 

  • McKay BD, Zink RM (2010) The causes of mitochondrial DNA gene tree paraphyly in birds. Mol Phyl Evol 54:647–650

    Article  Google Scholar 

  • Molecular Ecology Resources Primer Development Consortium, Arranz SE, Avarre J-C et al (2013) Permanent genetic resources added to molecular ecology resources database 1 December 2012–31 January 2013. Mol Ecol Resour 13:546–549

    Article  Google Scholar 

  • Moore RP, Robinson WD, Lovette IJ, Robinson TR (2008) Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol Lett 11:960–968

    Article  CAS  PubMed  Google Scholar 

  • Nice CC, Shapiro AM (1999) Molecular and morphological divergence in the butterfly genus Lycaeides (Lepidoptera: Lycaenidae) in North America: evidence of recent speciation. JEB 12:936–950

    CAS  Google Scholar 

  • Omland KE, Lanyon SM, Fritz SJ (1999) A molecular phylogeny of the New World orioles (Icterus): the importance of dense taxon sampling. Mol Phylogenet Evol 12:224–239

    Article  CAS  PubMed  Google Scholar 

  • Painter JN, Crozier RH, Poiani A et al (2000) Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys. Mol Ecol 9:1339–1347

    Article  CAS  PubMed  Google Scholar 

  • Parent CE, Crespi BJ (2006) Sequential colonization and diversification of Galapagos endemic land snail genus Bulimulus (Gastropoda, Stylommatophora). Evolution 60:2311–2328

    CAS  PubMed  Google Scholar 

  • Porlier M, Garant D, Perret P, Charmantier A (2012) Habitat-linked population genetic differentiation in the blue tit Cyanistes caeruleus. J Hered 103:781–791

    Article  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ricklefs RE (2010) Colonization of the Lesser Antilles by land birds. Ecology 91:1811–1821

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Bermingham E (2001) Nonequilibrium diversity dynamics of the Lesser Antillean avifauna. Science 294:1522–1524

    Article  CAS  PubMed  Google Scholar 

  • Ricklefs RE, Bermingham E (2004) History and the species-area relationship in Lesser Antillean birds. Am Nat 163:227–239

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Bermingham E (2007) The causes of evolutionary radiations in archipelagoes: passerine birds in the Lesser Antilles. Am Nat 169:285–297

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Bermingham E (2008) The West Indies as a laboratory of biogeography and evolution. Philos Trans R Soc B Biol Sci 363:2393–2413

    Article  Google Scholar 

  • Rising J, Jaramillo A (2016) Lesser Antillean Bullfinch (Loxigilla noctis). In: del Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive. Lynx Edicions, Barcelona

    Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

    Book  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ryan PG, Bloomer P, Moloney CL et al (2007) Ecological speciation in South Atlantic island Finches. Science 315:1420–1423

    Article  CAS  PubMed  Google Scholar 

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proc R Soc Lond B Biol Sci 273:1987–1998

    Article  Google Scholar 

  • Seutin G, Brauwn J, Ricklefs R, Bermingham E (1993) Genetic divergence among populations of a tropical passerine, the streaked saltator (Saltator albicolis). The Auk 110:117–126

  • Seutin G, Klein NK, Ricklefs RE, Bermingham E (1994) Historical biogeography of the Bananaquit (Coereba flaveola) in the Caribbean region: a mitchondrial DNA assessment. Evolution 48:1041

    Article  CAS  Google Scholar 

  • Slatkin M (1973) Gene flow and selection in a cline. Genetics 75:733–756

    PubMed Central  CAS  PubMed  Google Scholar 

  • Szpiech ZA, Jakobsson M, Rosenberg NA (2008) ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinform Oxf Engl 24:2498–2504

    Article  CAS  Google Scholar 

  • 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 4:535–538

    Article  Google Scholar 

  • Veit ML, Robertson RJ, Hamel PB, Friesen VL (2005) Population genetic structure and dispersal across a fragmented landscape in cerulean warblers (Dendroica cerulea). Conserv Genet 6:159–174

    Article  Google Scholar 

  • Villard M-A, Haché S (2012) Conifer plantations consistently act as barriers to movement in a deciduous forest songbird: a translocation experiment. Biol Conserv 155:33–37

    Article  Google Scholar 

  • Wallace AR (1880) Island life, or the phenomena and causes of insular faunas and floras, including a revision and attempted solution of the problem of geological climates. Macmillan Press, London

    Book  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whittaker RJ, Fernandez-Palacios JM (2007) Island biogeography. Oxford University Press, Oxford

    Google Scholar 

  • Woxvold IA, Adcock GJ, Mulder RA (2006) Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds. Mol Ecol 15:3139–3146

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the editor and three anonymous referees for their constructive comments on previous versions of the manuscript. This project was supported by the ERA-Net Net-Biome 2010, the Agence Nationale de la Recherche, the Fundação para a Ciência e a Tecnologia, the Conseil Régional de la Martinique, the Conseil Régional de Bourgogne. Bird sampling has been done with permits from several organizations: the Direction de l’Environnement, de l’Aménagement et du Logement (DEAL) from Guadeloupe, the DEAL from Martinique, the Forestry of the Commonwealth of Dominica, the Parc National de la Guadeloupe, the Direction Régionale de l’Office National des Forêts (ONF) de Guadeloupe, the Direction Régionale de l’ONF de Martinique. We thank, M Bely, ML Carpentier, F Cavallo, S Chauvin, M Delpuech, G Leblond, M Leblond, E Lefol, V Rocheteau for their help with fieldwork. We also thank J Arlington, J. Cornuault, A Lévesque and D Rozet for their advices and help.

Author information

Authors and Affiliations

  1. CNRS, Biogéosciences UMR6282, Univ. Bourgogne Franche-Comté, 21000, Dijon, France

    Aurélie Khimoun, Emilie Arnoux, Guillaume Martel, Alexandre Pot, Maxime Loubon, Franck Théron, Bruno Faivre & Stéphane Garnier

  2. CNERA Avifaune migratrice, Office National de la Chasse et de la Faune Sauvage, Station biologique de Chizé, Carrefour de la Canauderie, 79360, Villiers en Bois, France

    Cyril Eraud

  3. Cellule Technique des Antilles Françaises, Office National de la Chasse et de la Faune Sauvage, 5 rue de la Dorade, 79229, Les Trois-Ilets, Martinique, France

    Béatriz Condé

  4. Research Centre in Biodiversity and Genetic Resources, CIBIO, Campus Agrário de Vairão, Rua Padre Armando Quintas, 4485-661, Vairão, Portugal

    Maxime Loubon, Franck Théron & Rita Covas

Authors
  1. Aurélie Khimoun
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emilie Arnoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillaume Martel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandre Pot
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cyril Eraud
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Béatriz Condé
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maxime Loubon
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Franck Théron
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rita Covas
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bruno Faivre
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Stéphane Garnier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aurélie Khimoun.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khimoun, A., Arnoux, E., Martel, G. et al. Contrasted patterns of genetic differentiation across eight bird species in the Lesser Antilles. Genetica 144, 125–138 (2016). https://doi.org/10.1007/s10709-016-9883-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-016-9883-4

Keywords

Search

Navigation