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Marine Biology

, Volume 156, Issue 6, pp 1321–1333 | Cite as

Between introgression events and fragmentation, islands are the last refuge for the American crocodile in Caribbean Mexico

  • Salima Machkour-M’Rabet
  • Yann Hénaut
  • Pierre Charruau
  • Muriel Gevrey
  • Peter Winterton
  • Luc Legal
Original Paper

Abstract

Habitat loss and degradation in the Mexican Caribbean, caused by the development of tourism, have decreased the potential nesting area for the American crocodile (Crocodylus acutus) and have fragmented the populations of the Yucatan peninsula. Our study investigated five populations (three continental: North, South, Sian Ka’an, and two insular: Cozumel, Banco Chinchorro) of C. acutus in the Mexican Caribbean using seven different inter simple sequence repeat (ISSR) markers as tools for genetic variability and population differentiation. Three classification methods were tested and compared: distance analysis, self-organizing map, and Bayesian methods, to evaluate the resolution of each method with ISSR markers. The 77 loci selected revealed a high variability between populations (polymorphism from 17% for Sian Ka’an to 75% for Banco Chinchorro) with a total polymorphism of 84% and a global coefficient of gene differentiation (GST) of 0.296, but low values of Nei’s Gene diversity (from 0.065 for Sian Ka’an to 0.233 for Banco Chinchorro). Our results suggest elevated inbreeding in all local populations with higher indices for Banco Chinchorro and lower indices for Sian Ka’an. Three independent classification methods gave similar results, and suggested that most continental individuals are admixtures, with different levels of introgression, with the sympatric species Crocodylus moreletii. We propose that the islands/atolls remain the sole areas with genetically “pure” American crocodiles and we discuss these results for future conservation of this endangered crocodile species.

Keywords

Inter Simple Sequence Repeat Distance Analysis Yucatan Peninsula Hybrid Individual Inter Simple Sequence Repeat Marker 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Mauro Collí Orozco for his greatly appreciated help during the field work in Banco Chinchorro and Héctor González Cortés of the “Fundación de Parques y Museos de Cozumel” for providing logistic help and for animal capture during the campaign in Cozumel. Banco Chinchorro Biosphere Reserve provided important support for fieldwork. We thank Magdalena Hernández Chávez, of El Colegio de la Frontera Sur (ECOSUR), for helping in the preparation of samples. Many people provided precious technical help and advice for the study: Sophie Calmé, Rogelio Cedeño-Vázquez, Celine Pelissier, Gabriela Perez-Lachaud, Hervé Gryta, Jérome Albre. Finally, we would like to thank Janneth Adriana Padilla Saldivar of ECOSUR for drawing the map.

References

  1. Avise JC (2004) Molecular markers, natural history and evolution. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  2. Baker RJ, Bradley RD (2006) Speciation in mammals and the genetic species concept. J Mammal 87:643–662. doi: https://doi.org/10.1644/06-MAMM-F-038R2.1 CrossRefGoogle Scholar
  3. Barilani M, Sfougaris A, Giannakopoulos A, Mucci N, Tabarroni C, Randi E (2007) Detecting introgressive hybridisation in rock partridge populations (Alectoris graeca) in Greece through Bayesian admixture analyses of multilocus genotypes. Conserv Genet 8:343–354. doi: https://doi.org/10.1007/s10592-006-9174-1 CrossRefGoogle Scholar
  4. Behura SK (2006) Molecular marker systems in insects: current trends and future avenues. Mol Ecol 15:3087–3113. doi: https://doi.org/10.1111/j.1365-294X.2006.03014.x CrossRefGoogle Scholar
  5. Bonin A, Nicole F, Pompanon F, Miaud C, Taberlet P (2007) Population adaptive index: a new method to help measure intraspecific genetic diversity and prioritize populations for conservation. Conserv Biol 21:697–708. doi: https://doi.org/10.1111/j.1523-1739.2007.00685.x CrossRefGoogle Scholar
  6. Bouzid W, Lek S, Macé M et al (2008) Genetic diversity of Ligula intestinalis (L.) (Cestoda: Diphyllobothriidea) based on analysis of inter-simple sequence repeat (ISSR) markers. J Zoological Syst Evol Res 46:289–296CrossRefGoogle Scholar
  7. Cedeño-Vázquez JR, Rodríguez D, Calmé S et al (2008) Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan peninsula: I. Evidence from mitochondrial DNA and morphology. J Exp Zool 309(A):661–673CrossRefGoogle Scholar
  8. Charruau P, Cedeño-Vazquez JR, Calmé S (2005) Status and conservation of the American Crocodile (Crocodylus acutus) in Banco Chinchorro Biosphere Reserve, Quintana Roo, Mexico. Herpetol Rev 36:390–395Google Scholar
  9. Davis LM, Glenn TC, Elsey RM et al (2000) Genetic structure of six populations of American alligators: a microsatellite analysis. In: Grigg GC, Seebacher F, Franklin CE et al (eds) Crocodilian biology and evolution. Surrey Beatty & Sons, Chipping Norton, NSW, Australia, pp 38–50Google Scholar
  10. Dever JA, Strauss RE, Rainwater TR, McMurry ST, Densmore LD III (2002) Genetic diversity, population subdivision, and gene flow in Morelet’s Crocodile (Crocodylus moreletii) from Belize, Central America. Copeia 4:1078–1091. doi: https://doi.org/10.1643/0045-8511(2002)002[1078:GDPSAG]2.0.CO;2 CrossRefGoogle Scholar
  11. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction sites. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  12. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. doi: https://doi.org/10.1111/j.1471-8286.2007.01758.x CrossRefGoogle Scholar
  13. Farias IP, Da Silveira R, de Thoisy B et al (2004) Genetic diversity and population structure of Amazonian crocodilians. Anim Conserv 7:265–272. doi: https://doi.org/10.1017/S136794300400143X CrossRefGoogle Scholar
  14. FitzSimmons NN, Tanksley S, Forstner MRJ et al (2000) Microsatellite markers for Crocodylus: new genetic tools for population genetic mating system studies and forensics. In: Grigg GC, Seebacher F, Franklin CE et al (eds) Crocodilian biology and evolution. Surrey Beatty & Sons, Chipping Norton, NSW, Australia, pp 51–57Google Scholar
  15. FitzSimmons NN, Buchan JC, Lam PV et al (2002) Identification of purebred Crocodylus siamensis for reintroduction in Vietnam. J Exp Zool 294:373–381. Mol Dev Evol. doi: https://doi.org/10.1002/jez.10201 CrossRefGoogle Scholar
  16. Frankham R, Ballou JD, Briscoe DA (2005) Introduction to conservation genetics. Cambridge University Press, UKGoogle Scholar
  17. García-Grajales J, Aguirre-León G, Contreras-Hernández A (2007) Tamaño y estructura poblacional de Crocodylus acutus (Cuvier 1807) (Reptilia: Crocodylidae) en el estero La Ventanilla, Oaxaca, México. Acta Zool Mex 23:53–71Google Scholar
  18. Giraudel JL, Aurelle D, Berrebi P, Lek S (2000) Application of the self-organizing mapping and fuzzy clustering to microsatellite data: how to detect genetic structure in brown trout (Salmo trutta) populations. In: Lek S, Guégan JF (eds) Artificial Neuronal Networks. Springer-Verlag, Berlin, pp 187–202CrossRefGoogle Scholar
  19. Groombridge B (1987) The distribution and status of world crocodilians. In: Webb GJW, Manolis SC, Whitehead PJ (eds) Wildlife management: crocodiles and alligators. Surrey Beatty and Sons Pty Limited, Chipping Norton, Australia, pp 9–22Google Scholar
  20. Guicking D, Griffiths RA, Moore RD, Joger U, Wink M (2006) Introduced alien or persecuted native? resolving the origin of the viperine snake (Natrix maura) on Mallorca. Biodivers Conserv 15:3045–3054. doi: https://doi.org/10.1007/s10531-005-4878-y CrossRefGoogle Scholar
  21. Gyory J, Mariano AJ, Ryan EH (2001–2008a) Ocean surface currents: the Caribbean current. http://oceancurrents.rsmas.miami.edu/caribbean/caribbean.html. Accessed 18 Aug 2008
  22. Gyory J, Mariano AJ, Ryan EH (2001–2008b) Ocean surface currents: the Yucatan current. http://oceancurrents.rsmas.miami.edu/caribbean/yucatan.html. Accessed 18 Aug 2008
  23. Hekkala ER (2004) Conservation genetics at the species boundary: case studies from African and Caribbean Crocodiles (genus: Crocodylus). PhD thesis, Columbia University, New York, USAGoogle Scholar
  24. Hoffman EA, Schueler FW, Jones AG, Blouin MS (2006) An analysis of selection on a colour polymorphism in the northern leopard frog. Mol Ecol 15:2627–2641. doi: https://doi.org/10.1111/j.1365-294X.2006.02934.x CrossRefGoogle Scholar
  25. Huff DR, Peakall R, Smouse PE (1993) RAPD variation within and among natural populations of outcrossing buffalograss Buchloe dactyloides (Nutt) Engelm. Theor Appl Genet 86:927–934. doi: https://doi.org/10.1007/BF00211043 CrossRefGoogle Scholar
  26. Hundsdoerfer AK, Wink M (2006) Incongruence of morphology and genetic markers in Hyles tithymali (Lepidoptera: Sphingidae) from the Canary Islands. J Zoolog Syst Evol Res 44:316–322. doi: https://doi.org/10.1111/j.1439-0469.2006.00366.x CrossRefGoogle Scholar
  27. Hutton JM, Woodhouse ME (1989) Mark-recapture to assess factors affecting the proportion of Nile crocodile population seen during spotlight counts at Ngezi, Zimbabwe, and the use of spotlight counts to monitor crocodile abundance. J Appl Ecol 26:381–395. doi: https://doi.org/10.2307/2404068 CrossRefGoogle Scholar
  28. Joger U, Fritz U, Guicking D et al (2007) Phylogeography of western Palaearctic reptiles–spatial and temporal speciation patterns. J Comp Zool 246:293–313Google Scholar
  29. Kay WR (2004) Movements and home ranges of radio-tracked Crocodylus porosus in the Cambridge Gulf region of Western Australia. Wildl Res 31:495–508. doi: https://doi.org/10.1071/WR04037 CrossRefGoogle Scholar
  30. Kohonen T (2001) Self-organizing maps, 3rd edn. Springer-Verlag, Berlin, GermanyCrossRefGoogle Scholar
  31. Kothera L, Richards CM, Carney SE (2007) Genetic diversity and structure in the rare Colorado endemic plant Physaria bellii Mulligan (Brassicaceae). Conserv Genet 8:1043–1050. doi: https://doi.org/10.1007/s10592-006-9252-4 CrossRefGoogle Scholar
  32. Kushlan JA, Mazzotti F (1989) Population biology of the American crocodile. J Herpetol 23:7–21. doi: https://doi.org/10.2307/1564310 CrossRefGoogle Scholar
  33. Lawson R, Kofron CP, Dessauer HC (1989) Allozyme variation in a natural population of the Nile crocodile. Am Zool 29:863–871CrossRefGoogle Scholar
  34. Lek S, Guegan JF (2000) Artificial neuronal networks. Application to ecology and evolution. Springer-Verlag, HeidelbergCrossRefGoogle Scholar
  35. Lewontin RC (1972) The apportionment of human diversity. Evol Biol 6:381–398Google Scholar
  36. Luque C, Legal L, Staudter H, Gers C, Wink M (2002) ISSR (inter simple sequence repeats) as genetic markers in Noctuids (Lepidoptera). Hereditas 136:251–253. doi: https://doi.org/10.1034/j.1601-5223.2002.1360312.x CrossRefGoogle Scholar
  37. Luque C, Legal L, Machkour-M’Rabet S, Winterton P, Gers C, Wink M (2009) Apparent influences of host plant distribution on the structure and the genetic variability of local populations of the Purple Clay (Diarsia brunnea). Biochem Syst Ecol 37:6–15CrossRefGoogle Scholar
  38. Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99. doi: https://doi.org/10.1111/j.1365-294X.1994.tb00109.x CrossRefGoogle Scholar
  39. Magnusson WE (1982) Techniques of surveying for crocodiles. In: IUCN (eds) Proceedings of the 5th working meet. Croc. Spec. Group, Crocodiles. Morges, Switzerland, pp 389–403Google Scholar
  40. Maltagliati F, Lai T, Casu M, Valdesalici S, Castelli A (2006) Identification of endangered Mediterranean cyprinodontiform fish by means of DNA inter-simple sequence repeats (ISSRs). Biochem Syst Ecol 34:626–634. doi: https://doi.org/10.1016/j.bse.2006.02.003 CrossRefGoogle Scholar
  41. MathWorks (2001) Laboratory of Information and Computer Science, Helsinski University of Technology (Version 6.1.0.450 Release 12.1). The MathWorks, Inc. http://www.cis.hut.fi/projects/somtoolbox
  42. Mazzotti FJ, Brandt LA, Moler P, Cherkiss MS (2007) American crocodile (Crocodylus acutus) in Florida: recommendations for endangered species recovery and ecosystem restoration. J Herpetol 41:122–132. doi: https://doi.org/10.1670/0022-1511(2007)41[122:ACCAIF]2.0.CO;2 CrossRefGoogle Scholar
  43. McAliley LR, Willis RE, Ray DA et al (2006) Are crocodiles really monophyletic?—evidence for subdivisions from sequence and morphological data. Mol Phylogenet Evol 39:16–32. doi: https://doi.org/10.1016/j.ympev.2006.01.012 CrossRefGoogle Scholar
  44. Menzies RA, Kushlan J (1991) Genetic variation in populations of the American crocodile. J Herpetol 25:357–361. doi: https://doi.org/10.2307/1564598 CrossRefGoogle Scholar
  45. Nagy ZT, Glaw F, Andreone A, Wink M, Vences M (2007) Species boundaries in Malagasy snakes of the genus Madagascarophis (Serpentes: Colubridae sensu lato) assessed by nuclear and mitochondria markers. Org Divers Evol 7:241–251. doi: https://doi.org/10.1016/j.ode.2006.07.003 CrossRefGoogle Scholar
  46. Oaks JR (2007) Phylogenetics systematics, biogeography, and evolutionary ecology of the true crocodiles (Eusuchia: Crocodylidae: Crocodylus). PhD thesis, University of Wisconsin Oshkosh, USAGoogle Scholar
  47. Page RDM (1996) Treeview: an application to display phylogenetic trees on personal computers. Bioinformatics 12:357–358. doi: https://doi.org/10.1093/bioinformatics/12.4.357 CrossRefGoogle Scholar
  48. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi: https://doi.org/10.1111/j.1471-8286.2005.01155.x CrossRefGoogle Scholar
  49. Platt SG, Thorbjarnarson JB (1997) Status and life history of the American Crocodile in Belize. Belize coastal zone management project BZE/92/G31. Report to United Nations Development Program. Global Environmental Facility, Belize City, BelizeGoogle Scholar
  50. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. http://www.pritch.bsd.uchicago.edu PubMedPubMedCentralGoogle Scholar
  51. Ray DA, Dever JA, Platt SG et al (2004) Low levels of nucleotide diversity in Crocodylus moreletii and evidence of hybridization with C. acutus. Conserv Genet 5:449–462. doi: https://doi.org/10.1023/B:COGE.0000041024.96928.fe CrossRefGoogle Scholar
  52. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109. doi: https://doi.org/10.1146/annurev.ecolsys.27.1.83 CrossRefGoogle Scholar
  53. Rodriguez D (2007) Crocodilian evolution, systematics and population genetics: recovery and ecological interactions of the American Crocodile (Crocodylus acutus). PhD thesis, Texas Tech University, Lubboch, TexasGoogle Scholar
  54. Rodriguez D, Cedeño-Vázquez JR, Forstner MRJ, Densmore LD III (2008) Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan peninsula: II. Evidence from microsatellites. J Exp Zool 309(A):674–686CrossRefGoogle Scholar
  55. Ross JP (1998) Crocodiles: status survey and conservation action plan, 2nd edn. IUCN/SSC Crocodile Specialist Group Publ, Oxford Press, OxfordGoogle Scholar
  56. Roux O, Gevrey M, Arvanitakis L et al (2007) ISSR-PCR: tool for discrimination and genetic structure analysis of Plutella xylostella populations native to different geographical areas. Mol Phylogenet Evol 43:240–250. doi: https://doi.org/10.1016/j.ympev.2006.09.017 CrossRefGoogle Scholar
  57. Ruanet VV, Kochieva EZ, Ryzhova NN (2005) Kohonen network study of the results of RAPD and ISSR analyses of genomic polymorphism in the genus Capsicum L. Russ J Genet 4:202–210. doi: https://doi.org/10.1007/s11177-005-0045-5 CrossRefGoogle Scholar
  58. 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 8:777–787. doi: https://doi.org/10.1007/s10592-006-9225-7 CrossRefGoogle Scholar
  59. Swofford DL (2001) PAUP Phylogenetic analysis using parsimony. Sinauer, Sunderland, MA (Version 4.0b10)Google Scholar
  60. Thorbjarnarson J, Mazzotti F, Sanderson E et al (2006) Regional habitat conservation priorities for the American crocodile. Biol Conserv 128:25–36. doi: https://doi.org/10.1016/j.biocon.2005.09.013 CrossRefGoogle Scholar
  61. Wink M (2006) Use of DNA markers to study birds migration. J Ornithol 147:234–244. doi: https://doi.org/10.1007/s10336-006-0065-5 CrossRefGoogle Scholar
  62. Yeh FC, Yang R, Boyle TJB (1999) Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belg J Bot 129:157Google Scholar
  63. Zhao N, Ai W, Shao Z et al (2005) Microsatellites assessment of Chinese sturgeon (Acipenser sinensis Gray) genetic variability. J Appl Ichthyol 21:7–13. doi: https://doi.org/10.1111/j.1439-0426.2004.00630.x CrossRefGoogle Scholar
  64. Zhu B, Zhao N, Shao Z, Lek S, Chang J (2006) Genetic population structure of Chinese sturgeon (Acipenser sinensis) in the Yangtze River revealed by artificial neural network. J Appl Ichthyol 22:82–88. doi: https://doi.org/10.1111/j.1439-0426.2007.00932.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Salima Machkour-M’Rabet
    • 1
  • Yann Hénaut
    • 1
  • Pierre Charruau
    • 1
  • Muriel Gevrey
    • 2
  • Peter Winterton
    • 3
  • Luc Legal
    • 4
    • 5
  1. 1.Ecología y Conservación de Fauna SilvestreEl Colegio de la Frontera Sur (ECOSUR)ChetumalMexico
  2. 2.Laboratoire Evolution et Diversité Biologique, UMR 5174Université Paul SabatierToulouseFrance
  3. 3.Université Paul SabatierToulouse cedex 4France
  4. 4.Laboratoire d’Ecologie Fonctionnelle (EcoLab), UMR 5245Université Paul SabatierToulouseFrance
  5. 5.Departamento de Sistemática y EvoluciónCEAMISH-Universidad Autónoma del Estado de MorelosCuernavacaMexico

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