Conservation Genetics

, Volume 11, Issue 5, pp 1809–1821

Cryptic diversity and conservation units in the Bahama parrot

  • M. A. Russello
  • C. Stahala
  • D. Lalonde
  • K. L. Schmidt
  • G. Amato
Research Article

Abstract

Wide application of genetic approaches has enhanced the detection of cryptic diversity, even in historically well-studied organisms. In addition to improving our knowledge of biodiversity, detection of cryptic diversity can have important management implications within imperiled groups, such as the Cuban parrot complex (Amazona leucocephala). Bahama parrots (A. l. bahamensis) were once widespread throughout the archipelago, but are now restricted to the two largest islands (Abaco and Inagua). Mitochondrial DNA-based population genetic and phylogenetic analyses revealed the distinctiveness of the Abaco, Inagua and now extirpated Acklins populations, detecting diagnostic character support and reciprocal monophyly indicative of three phylogenetic species. Congruent results were obtained for the Abaco and Inagua populations based on Bayesian clustering analyses of microsatellite genotypic data. Genetic signatures of demographic contraction were identified on Abaco, but not Inagua. These findings were consistent with lower genetics-based estimates of effective population size on Abaco, as well as the disproportionate human impacts reported on the island relative to Inagua. Overall, our results suggest that the taxonomy of the Cuban parrot complex requires revision and that the conservation status of the Abaco phylogenetic species should be immediately elevated to reflect its historical isolation, recent population decline and continued threats to its persistence.

Keywords

Amazona leucocephala bahamensis Cuban Amazon parrot Population genetic Phylogenetic species Historical DNA Museum specimen Subspecies dilemma 

Supplementary material

10592_2010_74_MOESM1_ESM.xls (22 kb)
Supplementary material 1 (XLS 21 kb)

References

  1. Attrill R (1980) The status and conservation of the Bahamas Amazon (Amazona leucocephala bahamensis). In: Pasquier RF (ed) Conservation of new world parrots. Smithsonian Institution Press, Washington, DC, pp 81–88Google Scholar
  2. Barrowclough GF, Flesness NR (1996) Species, subspecies, and races: the problem of units of management in conversation. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, Harris H (eds) Wild mammals in captivity: principles and techniques. University of Chicago Press, Chicago, pp 247–254Google Scholar
  3. Beheregaray LB, Caccone A (2007) Cryptic biodiversity in a changing world. J Biol 6:1–5CrossRefGoogle Scholar
  4. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2001) Genetix, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UPR 9060, Université de Montpellier II, Montpellier, FranceGoogle Scholar
  5. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155CrossRefPubMedGoogle Scholar
  6. Brightsmith DJ (2005a) Competition, predation and nest niche shifts among tropical cavity nesters: phylogeny and natural history evolution of parrots (Psittaciformes) and trogons (Trogoniformes). J Avian Biol 36:64–73CrossRefGoogle Scholar
  7. Brightsmith DJ (2005b) Parrot nesting in southeastern Peru: seasonal patterns and keystone trees. Wilson Bull 117:296–305CrossRefGoogle Scholar
  8. Brown DM, Brenneman RA, Koepfli KP, Pollinger JP, Mila B, Georgiadis NJ, Louis EE, Grether GF, Jacobs DK, Wayne RK (2007) Extensive population genetic structure in the giraffe. BMC Biol 5:57Google Scholar
  9. Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by tag DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1010PubMedGoogle Scholar
  10. Ceballos G, Ehrlich PR (2009) Discoveries of new mammal species and their implications for conservation and ecosystem services. Proc Natl Acad Sci USA 106:3841–3846CrossRefPubMedGoogle Scholar
  11. Clark AH (1905) The West Indian parrots. Auk 22:337–344Google Scholar
  12. Cory CB (1891) Descriptions of thirteen new species of birds from the island of Grand Cayman, West Indies. Auk 3:497–501Google Scholar
  13. Cracraft J (1983) Species concepts and speciation analysis. Curr Ornithol 1:159–187Google Scholar
  14. Davis JI, Nixon KC (1992) Populations, genetic-variation, and the delimitation of phylogenetic species. Syst Biol 41:421–435Google Scholar
  15. Eberhard JR, Bermingham E (2004) Phylogeny and biogeography of the Amazona ochrocephala (Aves: Psittacidae) complex. Auk 121:318–332CrossRefGoogle Scholar
  16. Eberhard JR, Wright TF, Bermingham E (2001) Duplication and concerted evolution of the mitochondrial control region in the parrot genus Amazona. Mol Biol Evol 18:1330–1342PubMedGoogle Scholar
  17. Enkerlin-Hoeflich EC, Snyder NFR, Wiley JW (2006) Behavior of wild Amazona and Rhynchopsitta parrots, with comparative insights from other psittacines. In: Luescher AU (ed) Manual of parrot behavior. Blackwell Publishing, OxfordGoogle Scholar
  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  19. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  20. Frankham R (1995) Effective population size adult population size ratios in wildlife—a review. Genet Res 66:95–107CrossRefGoogle Scholar
  21. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  22. Gaunt AS, Oring LW (1997) Guidelines to the use of wild birds in research. The Ornithological Council, Washington, DCGoogle Scholar
  23. Gentile G, Fabiani A, Marquez C, Snell HL, Snell HM, Tapia W, Sbordoni V (2009) An overlooked pink species of land iguana in the Galápagos. Proc Natl Acad Sci USA 106:507–511CrossRefPubMedGoogle Scholar
  24. Gnam RS, Burchsted A (1991) Population estimates for the Bahamas Parrot on Abaco Island. Bahamas, J Field Ornithol, p 62Google Scholar
  25. Goldstein PZ, DeSalle R, Amato G, Vogler AP (2000) Conservation genetics at the species boundary. Conserv Biol 14:120–131CrossRefGoogle Scholar
  26. Guo SW, Thompson EA (1992) A Monte-Carlo method for combined segregation and linkage analysis. Am J Hum Genet 51:1111–1126PubMedGoogle Scholar
  27. Haig SM, Beever EA, Chambers SM, Draheim HM, Dugger BD, Dunham S, Elliott-Smith E, Fontaine JB, Kesler DC, Knaus BJ, Lopes IF, Loschl P, Mullins TD, Sheffield LM (2006) Taxonomic considerations in listing subspecies under the US Endangered Species Act. Conserv Biol 20:1584–1594CrossRefPubMedGoogle Scholar
  28. Hale EE (1891) The life of Christopher Columbus: from his own letters and journals and other documents of his time. G. L. Howe and Co., ChicagoGoogle Scholar
  29. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  30. Isaac NJB, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19:464–469CrossRefPubMedGoogle Scholar
  31. Johnson JA, Watson RT, Minde DP (2005) Prioritizing species conservation: does the Cape Verde kite exist? Proc R Soc B 272:1365–1371CrossRefPubMedGoogle Scholar
  32. Keegan WF (1992) Beachhead in the Bahamas—Columbus encounters a new world. Archaeology 45:44–50Google Scholar
  33. Leite KCE, Seixas GHF, Berkunsky I, Collevatti RG, Caparroz R (2008) Population genetic structure of the blue-fronted Amazon (Amazona aestiva, Psittacidae: Aves) based on nuclear microsatellite loci: implications for conservation. Genet Mol Res 7:819–829CrossRefPubMedGoogle Scholar
  34. Li WH (1977) Distribution of nucleotide differences between 2 randomly chosen cistrons in a finite population. Genetics 85:331–337PubMedGoogle Scholar
  35. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  36. Longmire JL, Maltbie M, Baker RJ (1997) Use of ‘lysis buffer’ in DNA isolation and its implication for museum collections. Occas Pap Mus Texas Tech Univ 163:1–3Google Scholar
  37. Matuzak GD, Bezy MB, Brightsmith DJ (2008) Foraging ecology of parrots in a modified landscape: seasonal trends and introduced species. Wilson J Ornithol 120:353–365CrossRefGoogle Scholar
  38. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  39. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeGoogle Scholar
  40. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  41. Ottens-Wainright P, Halanych KM, Eberhard JR, Burke RI, Wiley JW, Gnam RS, Aquilera XG (2004) Independent geographic origin of the genus Amazona in the West Indies. J Caribb Ornithol 17:23–49Google Scholar
  42. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447CrossRefPubMedGoogle Scholar
  43. Peters J (1928) The races of Amazona leucocephala. Auk 45:342–344Google Scholar
  44. Pfenninger M, Schwenk K (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol Biol 7:121Google Scholar
  45. Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology? Proc R Soc B 273:1049–1053CrossRefPubMedGoogle Scholar
  46. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  47. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  48. Poulakakis N, Glaberman S, Russello MA, Beheregaray LB, Ciofi C, Powell JR, Caccone A (2008) Historical DNA analysis reveals living descendants of an extinct species of Galápagos tortoise. Proc Natl Acad Sci USA 105:15464–15469CrossRefPubMedGoogle Scholar
  49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  50. Raymond M, Rousset F (1995) Genepop (version-1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  51. Reynolds MBJ (2006) Conservation taxonomy of the Cuban parrot: morphological, plumage and flight call variation. Loma Linda University, Loma LindaGoogle Scholar
  52. Reynolds MBJ, Hayes WK (2009) Conservation taxonomy of the Cuban parrot (Amazona leucocephala): I. variation in morphology and plumage. J Caribb Ornithol 22:1–18Google Scholar
  53. Ribas CC, Tavares ES, Yoshihara C, Miyaki CY (2007) Phylogeny and biogeography of Yellow-headed and Blue-fronted Parrots (Amazona ochrocephala and Amazona aestiva) with special reference to the South American taxa. Ibis 149:564–574CrossRefGoogle Scholar
  54. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  55. Rivera-Milan FF, Collazo JA, Stahala C, Moore WJ, Davis A, Herring G, Pagliaro R, Thompson JL, Bracey W (2005) Estimation of density and population size and recommendations for monitoring trends of Bahama parrots on Great Abaco and Great Inagua. Wildl Soc Bull 33:823–834CrossRefGoogle Scholar
  56. Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615CrossRefGoogle Scholar
  57. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  58. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  59. Russello MA, Amato G (2004) A molecular phylogeny of Amazona: implications for Neotropical parrot biogeography, taxonomy, and conservation. Mol Phylogenet Evol 30:421–437CrossRefPubMedGoogle Scholar
  60. Russello M, Calcagnotto D, DeSalle R, Amato G (2001) Characterization of microsatellite loci in the endangered St. Vincent Parrot, Amazona guildingii. Mol Ecol Notes 1:162–164CrossRefGoogle Scholar
  61. Russello MA, Glaberman S, Gibbs JP, Marquez C, Powell JR, Caccone A (2005a) A cryptic taxon of Galápagos tortoise in conservation peril. Biol Lett 1:287–290CrossRefPubMedGoogle Scholar
  62. Russello MA, Lin K, Amato G, Caccone A (2005b) Additional microsatellite loci for the endangered St. Vincent Parrot, Amazona guildingii. Conserv Genet 6:643–645CrossRefGoogle Scholar
  63. Russello MA, Brazaitis P, Gratten J, Watkins-Colwell GJ, Caccone A (2007) Molecular assessment of the genetic integrity, distinctiveness and phylogeographic context of the Saltwater crocodile (Crocodylus porosus) on Palau. Conserv Genet 8:777–787CrossRefGoogle Scholar
  64. Ryder OA (1986) Species conservation and systematics—the dilemma of subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  65. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics 152:1079–1089PubMedGoogle Scholar
  66. Schneider S, Roessli D, Excoffier L (2000) Arlequin v2.000: a software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, SwiterlandGoogle Scholar
  67. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234CrossRefPubMedGoogle Scholar
  68. Snyder NFR, McGowan P, Gilardi J, Grajal A (eds) (2000) Parrots: status, survey, and conservation action plan 2000–2004. International Union for Conservation of Nature, GlandGoogle Scholar
  69. Swofford D (2002) PAUP*: phylogenetic analysis using parsimony, v.4.0b10. Illinois Natural History Survey, ChampaignGoogle Scholar
  70. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  71. Trontelj P, Fiser C (2009) Cryptic species diversity should not be trivialised. System Biodivers 7:1–3CrossRefGoogle Scholar
  72. 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 4:535–538CrossRefGoogle Scholar
  73. Vogler AP, Desalle R (1994) Diagnosing units of conservation management. Conserv Biol 8:354–363CrossRefGoogle Scholar
  74. Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642CrossRefPubMedGoogle Scholar
  75. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184CrossRefGoogle Scholar
  76. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756CrossRefGoogle Scholar
  77. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  78. Wiley JW, Gnam RS, Koenig SE, Dornelly A, Galvez X, Bradley PE, White T, Zamore M, Reillo PR, Anthony D (2004) Status and conservation of the family Psittacidae in the West Indies. J Caribb Ornithol 17:94–154Google Scholar
  79. Wilson E, Brown W (1953) The subspecies concept and its taxonomic application. Syst Zool 2:97–111CrossRefGoogle Scholar
  80. Wright TF, Dahlin CR, Salinas-Melgoza A (2008) Stability and change in vocal dialects of the yellow-naped Amazon. Anim Behav 76:1017–1027CrossRefPubMedGoogle Scholar
  81. Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc Lond B 271:561–564CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • M. A. Russello
    • 1
    • 2
  • C. Stahala
    • 3
  • D. Lalonde
    • 1
    • 2
  • K. L. Schmidt
    • 4
  • G. Amato
    • 4
  1. 1.Department of BiologyUniversity of British Columbia OkanaganKelownaCanada
  2. 2.Centre for Species at Risk and Habitat StudiesUniversity of British Columbia OkanaganKelownaCanada
  3. 3.Department of Biological ScienceFlorida State UniversityTallahasseeUSA
  4. 4.Sackler Institute for Comparative Genomics, American Museum of Natural HistoryNew YorkUSA

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