Biological Invasions

, Volume 14, Issue 10, pp 2101–2116 | Cite as

Genetic evidence of a recent successful colonization of introduced species on islands: Boa constrictorimperator on Cozumel Island

  • Ella Vázquez-Domínguez
  • Marco Suárez-Atilano
  • Warren Booth
  • Cristopher González-Baca
  • Alfredo D. Cuarón
Original Paper

Abstract

Only one study has described the population genetic structure of Boa constrictor imperator and only in a single naturally colonized island. B.c. imperator, a snake with a naturally wide distribution across the Neotropics, was introduced to Cozumel Island, Mexico, in 1971. At present, it is one of the most abundant, widely distributed, terrestrial vertebrate on the island. We analysed the genetic diversity and structure, based on seven microsatellite loci, of 76 individuals of B.c. imperator from Cozumel. We also included 96 samples from different localities across mainland Mexico, to review the potential origin of the founder individuals. We identified two genetically differentiated populations on Cozumel that showed moderate levels of genetic diversity (Ho = 0.590–0.620), with a low but significant level of genetic structure (FST = 0.032). Individuals were highly unrelated (71 %) and the majority of genetic variation was distributed within individuals (84 %). We detected a signal of reduction in population size and evidence of genetic bottleneck. The genetically closest mainland populations, indicating potential source of island founders, are localities from the Gulf of Mexico and Yucatan peninsula. Results are in agreement with a recently introduced population, founded by a few individuals originating from several sources, which has been successful. B.c. imperator is jeopardizing a highly vulnerable insular ecosystem, hence its eradication from Cozumel is urgently needed. Our information is also valuable for other introduced-boa cases or as a basis for its conservation elsewhere given its classification as a threatened species.

Keywords

Boidae Genetic diversity Genetic structure Mexico Microsatellites Invasive species 

Supplementary material

10530_2012_217_MOESM1_ESM.pdf (59 kb)
Supplementary material 1 (PDF 58 kb)
10530_2012_217_MOESM2_ESM.jpg (341 kb)
Supplementary material 2 (JPG 341 kb)

References

  1. Abdelkrim J, Pascal M, Clamet C, Samadi S (2005) Importance of assessing population genetic structure before eradication of invasive species: examples from insular Norway rat populations. Conserv Biol 19:1509–1518CrossRefGoogle Scholar
  2. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Wiley-Blackwell Publishing, USAGoogle Scholar
  3. Belkhir, KP, Borsa L, Chikhi N, Arrufaste N, Bonhomme F (2004) GENETIX 4.05: logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions. CNRS UMR 500, Université de Montpellier II, Montepellier, FranceGoogle Scholar
  4. Berglund H, Jaremo J, Bengtsson G (2009) Endemism predicts intrinsic vulnerability to nonindigenous species on islands. Am Nat 174:94–101PubMedCrossRefGoogle Scholar
  5. Bertona M, Chiaraviglio M (2003) Reproductive biology, mating aggregations and sexual dimorphism of the argentine Boa constrictor (Boa constrictor occidentalis). J Herpetol 37:510–516CrossRefGoogle Scholar
  6. Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511CrossRefGoogle Scholar
  7. Bomford M, Kraus F, Barry S, Lawrence E (2009) Determinants of establishment success in introduced reptiles and amphibians: a role for climate matching. Biol Invasions 11:713–724CrossRefGoogle Scholar
  8. Booth W, Schuett GW (2011) Molecular genetic evidence for alternate reproductive strategies in North American pitvipers (Serpentes, Viperidae): long-term sperm storage and facultative parthenogenesis. Biol J Linn Soc 104:934–942CrossRefGoogle Scholar
  9. Booth W, Johnson DH, Moore S, Schal C, Vargo EL (2011a) Evidence for viable, non-clonal but fatherless Boa constrictors. Biol Lett 7:253–257PubMedCrossRefGoogle Scholar
  10. Booth W, Million L, Reynolds RG, Burghardt GM, Vargo EL, Schal C, Tzika AC, Schuett GW (2011b) Consecutive virgin births in the new world boid snake, the Colombian rainbow boa, Epicrates maurus. J Hered. doi:10.1093/jhered/esr080
  11. Castañeda-Rico S, León-Paniagua L, Ruedas LA, Vázquez-Domínguez E (2011) High genetic diversity and extreme differentiation in the two remaining populations of Habromys simulatus. J Mamm 92:963–973CrossRefGoogle Scholar
  12. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedGoogle Scholar
  13. Chapuis M, Estoup PA (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631PubMedCrossRefGoogle Scholar
  14. Christy MT, Savidge JA, Rodda GH (2007) Multiple pathways for invasion of anurans on a Pacific island. Divers Distrib 13:598–607CrossRefGoogle Scholar
  15. Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted dispersal, and genetic diversity in Timber rattlesnakes. Conserv Biol 24:1059–1069PubMedCrossRefGoogle Scholar
  16. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  17. Cuarón AD (2009) Cozumel. In: Gillespie RG, Clague DA (eds) Encyclopedia of Islands. University of California Press, Berkeley, pp 203–206Google Scholar
  18. Cuarón AD, Martínez-Morales MA, McFadden KW, Valenzuela D, Gompper ME (2004) The status of dwarf carnivores on Cozumel Island, Mexico. Biodivers Conserv 13:317–331CrossRefGoogle Scholar
  19. Cuarón AD, Valenzuela-Galván D, García-Vasco D, Copa ME, Bautista S et al (2009) Conservation of the endemic dwarf carnivores of Cozumel Island, Mexico. Small Carniv Conserv 41:15–21Google Scholar
  20. Degner JF, Stout IJ, Roth JD, Parkinson CL (2007) Population genetics and conservation of the threatened southeastern beach mouse (Peromyscus polionotus niveiventris): subspecies and evolutionary units. Conserv Genet 8:1441–1452CrossRefGoogle Scholar
  21. Dlugosh KM, Parker M (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefGoogle Scholar
  22. Eales J, Thorpe RS, Malhotra A (2008) Weak founder effect signal in a recent introduction of Caribbean Anolis. Mol Ecol 17:1416–1426PubMedCrossRefGoogle Scholar
  23. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, LondonGoogle Scholar
  24. 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 Res 10:564–567CrossRefGoogle Scholar
  25. Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and numbers of founders in a biological invasion. Mol Ecol 17:773–782PubMedCrossRefGoogle Scholar
  26. Frankham R, Ballou J, Briscoe D (2005) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  27. Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29:113–140CrossRefGoogle Scholar
  28. Fuentes-Montemayor E, Cuarón AD, Vázquez-Domínguez E, Benítez-Malvido J, Valenzuela D, Andresen E (2009) Living on the edge: roads and edge effects on small mammal populations. J Anim Ecol 78:857–865PubMedCrossRefGoogle Scholar
  29. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  30. Goldstein DB, Ruiz-Linares BA, Cavalli-Sforza LL, Feldman MW (1995a) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723–6727PubMedCrossRefGoogle Scholar
  31. Goldstein DB, Ruiz-Linares A, Cavalli-Sforza LL, Feldman MW (1995b) An evaluation of genetic distances for use with microsatellite data. Genetics 140:679–695Google Scholar
  32. González-Baca CA (2006) Ecología de forrajeo de Boa constrictor. Un depredador introducido a la Isla Cozumel. MSc thesis, Universidad Nacional Autónoma de México, MéxicoGoogle Scholar
  33. Green S (2010) Ecology, conservation and commercial exploitation of the ‘Hog Island’ Boa contrictor in the Cayos Cochinos, Honduras. PhD Dissertation, University of Kent, KentGoogle Scholar
  34. Guicking DA, Griffiths RA, Moore RD, Joger U, Wonk M (2006) Introduced alien or persecuted native? Resolving the origin of the viperine snake (Natrix maura) on Mallorca. Biodiv Conserv 15:3045–3054CrossRefGoogle Scholar
  35. Guillot G (2009) On the inference of spatial structure from population genetics data using population genetics data. Bioinformatics 25:1796–1801PubMedCrossRefGoogle Scholar
  36. Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Not 5:712–715CrossRefGoogle Scholar
  37. Guillot G, Leblois R, Coulon A, Frantz AC (2009) Statistical methods in spatial genetics. Mol Ecol 18:4734–4756PubMedCrossRefGoogle Scholar
  38. Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  39. Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–477PubMedCrossRefGoogle Scholar
  40. Hamblin NL (1984) Animal use by the Cozumel Maya. University of Arizona Press, TucsonGoogle Scholar
  41. Henderson RW, Micucci TWP, Puorto G, Bourgeois RW (1995) Ecological correlates and patterns in the distribution of Neotropical boines (Serpentes: Boidae): a preliminary assessment. Herpetol Nat Hist 3:15–27Google Scholar
  42. Hille A, Janssen IAW, Menken SBJ, Schlegel M, Thorpe RS (2002) Heterologous amplification of microsatellite markers from colubroid snakes in European Natricinaes. J Hered 93:63–66PubMedCrossRefGoogle Scholar
  43. Jansen KP, Mushinsky HR, Karl SA (2008) Population genetics of the mangrove salt marsh snake, Nerodia clarkii compressicauda, in a linear fragmented habitat. Conserv Genet 9:401–410CrossRefGoogle Scholar
  44. Kaeuffer R, Coltman DW, Chapuis J-L, Pontier D, Réale D (2007) Unexpected heterozygosity in an island mouflon population founded by a single pair of individuals. Proc R Soc Lond Ser B 274:527–533CrossRefGoogle Scholar
  45. Kalinowski ST, Wagner AP, Taper ML (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579CrossRefGoogle Scholar
  46. Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis. Springer, USAGoogle Scholar
  47. Kraus F (2010) Global trends in alien reptiles and amphibians. Aliens 27:13–18Google Scholar
  48. Langella O (2002) Populations 1.2.30. Copyright (C) 1999, Olivier Langella, CNRS-UPR9034. Available at http://bioinformatics.org/;tryphon/populations/
  49. Loew SS, Williams DF, Ralls K, Pilgrim K, Fleischer RC (2005) Population structure and genetic variation in the endangered giant kangaroo rat (Dipodomys ingens). Conserv Genet 6:495–510CrossRefGoogle Scholar
  50. Long JL (2003) Introduced mammals of the world. Their history, distribution and influence. Csiro Publishing, AustraliaGoogle Scholar
  51. Longmire JL, Maltbie M, Caker RJ (1997) Use of “lysis buffer” in DNA isolation and its implication for museum collections. Occas Pap Mus Tex Tech Univ 163:1–4Google Scholar
  52. Lowe S, Browne M, Boudjelas S, De Poorter M (2001) 100 of the world’s worst invasive alien species: a selection from the global invasive database. Species Survival Comission, World Conservation Union, AucklandGoogle Scholar
  53. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  54. Martínez-Morales MA, Cuarón AD (1999) Boa constrictor, an introduced predator threatening the endemic fauna on Cozumel Island, México. Biodiv Conserv 8:957–963CrossRefGoogle Scholar
  55. Martínez-Morales MA, Cruz PC, Cuarón AD (2009) Predicted population trends for Cozumel Curassows (Crax rubra griscomi): empirical evidence and predictive models in the face of climate change. J Field Ornithol 80:317–327CrossRefGoogle Scholar
  56. McFadden KW, García-Vasco D, Cuarón AD, Valenzuela D, Medellín RA, Gompper ME (2010) Vulnerable island carnivores: the endangered endemic dwarf procyonids from Cozumel Island. Biodiv Conserv 19:491–502CrossRefGoogle Scholar
  57. Mena H (2007) Presencia de Leptospira spp. y moquillo canino en poblaciones de perros y carnívoros silvestres en la Isla Cozumel. MSc thesis, Universidad Nacional Autónoma de México, MéxicoGoogle Scholar
  58. Nei M (1972) Genetic distance between populations. Am Nat 106:283–292CrossRefGoogle Scholar
  59. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New YorkGoogle Scholar
  60. Oppel S, Beaven BM, Bolton M, Vickery J, Bodey TW (2011) Eradication of invasive mammals on islands inhabited by humans and domestic animals. Conserv Biol 25:232–240PubMedGoogle Scholar
  61. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Not 6:288–295CrossRefGoogle Scholar
  62. Perdomo H (2006) Caminos como barreras para el movimiento de aves y efectos del huracán Wilma, en una comunidad de aves de sotobosque de la selva mediana subcaducifolia de la Isla Cozumel. MSc thesis, Universidad Nacional Autónoma de México, MéxicoGoogle Scholar
  63. 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
  64. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS 2: a software for genetics assignment and first-generation migrant detections. J Hered 95:536–539PubMedCrossRefGoogle Scholar
  65. Porras LW (1999) Island boa constrictors (Boa constrictor). Reptiles 7:48–61Google Scholar
  66. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  67. Prosser ML, Gibbs HL, Weatherhead PJ (1999) Microgeographic population structure in the northern water snake, Nerodia sipedon sipedon detected using microsatellite DNA loci. Mol Ecol 8:329–333PubMedCrossRefGoogle Scholar
  68. Prosser ML, Gibbs HL, Weatherhead PJ, Brown GP (2000) Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon). Behav Ecol 13:800–807CrossRefGoogle Scholar
  69. Queller DC, Goodnight KF (1989) Estimation of genetic relatedness using allozyme data. Evolution 43:258–275CrossRefGoogle Scholar
  70. Quick J, Reinert SHK, de Cuba ER, Odum RA (2005) Recent occurrence and dietary habits of Boa constrictor on Aruba, Dutch West Indies. J Herpetol 39:304–307CrossRefGoogle Scholar
  71. Raymond M, Rousset F (1995) GenePop v1.2: population genetics software for exact test and ecumenicism. J Hered 86:248–249Google Scholar
  72. Reaser JK, Meyerson LA, Cronk Q et al (2007) Ecological and socioeconomic impacts of invasive alien species in island ecosystems. Environ Conserv 34:1–14CrossRefGoogle Scholar
  73. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  74. Rivera PC, Gardenal CN, Chiaraviglio M (2006) Sex-biased dispersal and high levels of gene flow among local populations in the argentine boa constrictor, Boa constrictor occidentalis. Austral Ecol 31:948–955CrossRefGoogle Scholar
  75. Rodda GH, Fritts TH, Campbell EW III, Dean-Bradley K, Perry G, Qualls CP (2002) Practical concerns in the eradication of island snakes. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN SSC Invasive Species Specialist Group, Aukland, pp 260–265Google Scholar
  76. Roemer GW, Donian CJ, Courchamp F (2002) Golden eagles, feral pigs, and insular carnivores: How exotic species turn native predators into prey. Proc Natl Acad Sci USA 99:791–796PubMedCrossRefGoogle Scholar
  77. Romero-Nájera I, Cuarón AD, González-Baca C (2007) Distribution, abundance, and habitat use of introduced Boa constrictor threatening the native biota of Cozumel Island, Mexico. Biodiv Conserv 16:1183–1195CrossRefGoogle Scholar
  78. Sax DF, Gaines SD (2008) Species invasions and extinction: the future of native biodiversity on islands. Proc Natl Acad Sci USA 105:11490–11497PubMedCrossRefGoogle Scholar
  79. Sax DF, Stachowicz JJ, Gaines SD (2005) Species invasions: insights into ecology, evolution and biogeography. Sinauer, SunderlandGoogle Scholar
  80. Semarnat (2010) Norma Oficial Mexicana NOM-059-SEMARNAT-2010, Protección ambiental-Especies nativas de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio-Lista de especies en riesgo. Diario Oficial de la Federación, 10 diciembre 2010, MéxicoGoogle Scholar
  81. Sever DM, Hamlett WC (2002) Female sperm storage in reptiles. J Exp Zool 292:187–199PubMedCrossRefGoogle Scholar
  82. Shriver MD, Jin L, Boerwinkle E, Deka R, Ferrel RE, Chakraborty R (1995) A novel measure of genetic distance for highly polymorphic tandem repeat loci. Mol Biol Evol 12:914–920PubMedGoogle Scholar
  83. Sotomayor JJ (2009) Asociación de Leptospira y los ratones endémicos y exóticos en la Isla Cozumel, México. Advanced BSc thesis, Universidad Nacional Autónoma de México, MéxicoGoogle Scholar
  84. Spear SF, Storfer A (2010) Anthropogenic and natural disturbance lead to differing patterns of gene flow in the Rocky Mountain tailed frog, Ascaphus montanus. Biol Conserv 143:778–786CrossRefGoogle Scholar
  85. Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360PubMedCrossRefGoogle Scholar
  86. Torres Villegas CP (2006) Distribución, abundancia y comportamiento de perros y gatos en la Isla de Cozumel. MSc thesis, Universidad Nacional Autónoma de México, MéxicoGoogle Scholar
  87. Tzika AC, Koening S, Miller R, García G, Remy C, Milinkovitch M (2008a) Population structure of an endemic vulnerable species, the Jamaican boa (Epicrates subflavus). Mol Ecol 17:533–544PubMedCrossRefGoogle Scholar
  88. Tzika AC, Rosa SFP, Fabiani A, Snell HL et al (2008b) Population genetics of Galapagos land iguana (genus Colophus) remnant populations. Mol Ecol 17:4943–4952PubMedCrossRefGoogle Scholar
  89. Tzika AC, Remy C, Gibson MR, Milinkovitch M (2009) Molecular genetic analysis of a captive-breeding program: the vulnerable endemic Jamaican yellow boa. Conserv Genet 10:69–77CrossRefGoogle Scholar
  90. Uller T, Olsson M (2008) Multiple paternity in reptiles: patterns and processes. Mol Ecol 17:2566–2580PubMedCrossRefGoogle Scholar
  91. van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping error in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  92. Vázquez-Domínguez E, Ceballos G, Cruzado J (2004) Extirpation of an insular subspecies by a single introduced cat: the case of the endemic deer mouse Peromyscus guardia on Estanque Island, Mexico. Oryx 38:347–350CrossRefGoogle Scholar
  93. Vega R, Vázquez-Domínguez E, Mejía-Puente A, Cuarón AD (2007) Unexpected high levels of genetic variability and the population structure of an island endemic rodent (Oryzomys couesi cozumelae). Biol Conserv 137:210–222CrossRefGoogle Scholar
  94. Wahlund S (1928) Zusammensetzung von populationen und korrelation-serscheinungen von standpunkt der verebungslehre aus betrachtet. Hereditas 11:65–106CrossRefGoogle Scholar
  95. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked loci. Conserv Gene 7:167–184CrossRefGoogle Scholar
  96. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8:753–756CrossRefGoogle Scholar
  97. Weidie AE (1985) Geology of the Yucatan platform, part 1. In: Ward WC, Weidie AE, Back W (eds) Geology and hydrogeology of the Yucatan and quaternary geology of northeastern Yucatan peninsula. New Orleans Geological Society, New Orleans, pp 1–19Google Scholar
  98. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  99. Wilson BS, Koening SE, van Veen R, Miersma E, Rudolph DC (2011) Cane toads a threat to West Indian wildlife: mortality of Jamaican boas attributable to toad ingestion. Biol Invasions 13:55–60CrossRefGoogle Scholar
  100. Zeiseet I, Beebee TJC (2003) Population genetics of a successful invader: the marsh frog Rana ridibunda in Britain. Mol Ecol 12:639–646CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Ella Vázquez-Domínguez
    • 1
  • Marco Suárez-Atilano
    • 1
  • Warren Booth
    • 2
  • Cristopher González-Baca
    • 3
  • Alfredo D. Cuarón
    • 3
    • 4
  1. 1.Departamento de Ecología de la Biodiversidad, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexicoMexico
  2. 2.Department of Entomology and W. M. Keck Center for Behavioral BiologyNorth Carolina State UniversityRaleighUSA
  3. 3.SACBÉ – Servicios Ambientales, Conservación Biológica y EducaciónCozumelMexico
  4. 4.Multicriteria SCMexicoMexico

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