Conservation Genetics

, Volume 5, Issue 4, pp 449–462 | Cite as

Low Levels of Nucleotide Diversity in Crocodylus moreletii and Evidence of Hybridization with C. acutus

  • David A. Ray
  • Jennifer A. Dever
  • Steven G. Platt
  • Thomas R. Rainwater
  • Adam G. Finger
  • Scott T. McMurry
  • Mark A. Batzer
  • Brady Barr
  • Peter J. Stafford
  • Jenna McKnight
  • Llewellyn D. Densmore


Examinations of both population genetic structure and the processes that lead to such structure in crocodilians have been initiated in several species in response to a call by the IUCN Crocodile Specialist Group. A recent study used microsatellite markers to characterize Morelet's crocodile (Crocodylus moreletii) populations in north-central Belize and presented evidence for isolation by distance. To further investigate this hypothesis, we sequenced a portion of the mitochondrial control region for representative animals after including samples from additional locales in Belize, Guatemala and Mexico. While there is limited evidence of subdivision involving other locales, we found that most of the differentiation among populations of C. moreletiican be attributed to animals collected from a single locale in Belize, Banana Bank Lagoon. Furthermore, mitochondrial DNA sequence analysis showed that animals from this and certain other locales display a haplotype characteristic of the American crocodile, C. acutus, rather than C. moreletii. We interpret this as evidence of hybridization between the two species and comment on how these new data have influenced our interpretation of previous findings. We also find very low levels of nucleotide diversity in C. moreletiihaplotypes and provide evidence for a low rate of substitution in the crocodilian mitochondrial control region. Finally, the conservation implications of these findings are discussed.

Crocodylus D-loop hybridization mtDNA phylogeography 


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  1. Abercrombie CL, Davidson D, Hope CA, Scott DE (1980) Status of Morelet's crocodile (Crocodylus moreletii ) in Belize. Biol. Cons., 17, 103–113.Google Scholar
  2. Abercrombie CL, Davidson D, Hope CA, Scott DE, Lane JE (1982) Investigations into the status of Morelet's crocodile Crocodylus moreletii in Belize, 1980. In: Crocodiles, Proceedings 5th Working Meeting of the Crocodile Specialist Group, pp. 11–30. IUCN –The World Conservation Union, Morges, Switzerland.Google Scholar
  3. Adams SE, Smith MH, Baccus R (1980) Biochemical variation in the American alligator. Herpetologica, 36, 289–296.Google Scholar
  4. Avise JC, Bowen BW, Lamb T, Meylan AB, Bermingham E (1992) Mitochondrial DNA evolution at a turtle's pace: Evidence for low genetic variability and reduced microevolutionary rate in the Testudines. Mol. Biol. Evol., 9, 457–473.PubMedGoogle Scholar
  5. Baker AJ, Marshall HD (1997) Mitochondrial control region sequences as tools for understanding evolution. In: Avian Molecular Evolution and Systematics (ed. Mindell D), pp. 51–82. Academic Press, San Diego.Google Scholar
  6. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspeci c phylogenies. Mol. Biol. Evol., 16, 37–48.PubMedGoogle Scholar
  7. Barrowclough GF, Gutierrez RJ, Groth JG (1999) Phyloge-ography of spotted owl (Strix occidentalis) populations based on mitochondrial sequences: Gene flow, genetic structure, and a novel biogeographic pattern. Evolution, 53, 919–931.Google Scholar
  8. Brazaitis P (1973) The identification of living crocodilians. Zoologica, 58, 59–88.Google Scholar
  9. Brochu C, Densmore LD (2001) Crocodile phylogenetics: A review of current progress. In: Crocodilian Biology and Evolution (eds. Grigg G, Seebacher F, Franklin C), pp. 3–8. Surrey Beatty and Sons, Chipping Norton.Google Scholar
  10. Brochu CA (2000) Phylogenetic relationships and divergence timing of Crocodylus based on morphology and the fossil record. Copeia, 2000, 657–673.Google Scholar
  11. Brown WM, Prager EM, Wang A, Wilson AC (1982) Mitochondrial DNA sequences of primates: Tempo and mode of evolution. Proc. Natl. Acad. Sci, USA, 76, 1976–1971.Google Scholar
  12. Charnock-Wilson J (1970) Manatees and crocodiles. Oryx, 10, 236–238.Google Scholar
  13. Cicero C, Johnson NK (1998) Molecular phylogeography and ecological diversi cation in a clade of New World songbirds (genus Vireo ). Mol. Ecol., 7, 1359–1370.PubMedGoogle Scholar
  14. Crochet P-A, Desmarais E (2000) Slow rate of evolution in the mitochondrial control region of gulls. Mol. Biol. Evol., 17, 1797–1806PubMedGoogle Scholar
  15. Davis LM, Glenn TC, Elsey RM, Brisbin IL, Dessauer HC, Sawyer RH (2001a) Genetic structure of six populations of American alligators: A microsatellite analysis. In: Crocodilian Biology and Evolution (eds. Grigg G, Seebacher F, Franklin C), pp. 38–50. Surrey Beatty and Sons, Chipping Norton.Google Scholar
  16. Davis LM, Glenn TC, Elsey RM, Dessauer HC, Sawyer RH (2001b) Multiple paternity and mating patterns in the American alligator, Alligator mississippiensis. Mol. Ecol., 10, 1011–1024.PubMedGoogle Scholar
  17. Davis LM, Glenn TC, Strickland DC, Guillette LJ, Elsey RM, Rhodes WE, Dessauer HC, Sawyer RH (2002) Microsatellite DNA analyses support an east –west phylogeographic split of American alligator populations. J. Exp. Zool., 294, 352–372.PubMedGoogle Scholar
  18. Dawson MN, Staton JL, Jacobs DK (2001) Phylogeography of the tidewater goby, Eucyclogobius newberryi (Teleostei, Gobiidae), in coastal California. Evolution, 55, 1167–1179.PubMedGoogle Scholar
  19. Densmore LD, Owen RD (1989) Molecular systematics of the order Crocodilia. Am. Zool., 29, 831–841.Google Scholar
  20. Densmore LD, White PS (1991) The systematics and evolution of the Crocodilia as suggested by restriction endonuclease analysis of mitochondrial and nuclear ribosomal DNA. Copeia, 1991, 602–615.Google Scholar
  21. Dever JA, Densmore LD (2001) Microsatellites in Morelet's crocodile Crocodylus moreletii and their utility in addressing crocodilian population genetics questions. J. Herp., 35, 542–544.Google Scholar
  22. Dever JA, Strauss RE, Rainwater TR, McMurry ST, Densmore LD (2002) Genetic diversity, population structure and gene flow in Morelet 's crocodile (Crocodylus moreletii ) from Belize, Central America. Copeia, 2002 (4), 1078–1091.Google Scholar
  23. Donovan MF, Semlitsch RD, Routman EJ (2000) Biogeogra-phy of the southeastern United States: A comparison of salamander phylogeographic studies. Evolution, 54, 1449–1456.PubMedGoogle Scholar
  24. Encalada SE, Lahanas PN, Bjorndal KA, Bolten AB, Miyamoto MM, Bowen BW (1996) Phylogeography and population structure of the Atlantic and Mediterranean green turtle Chelonia mydas: A mitochondrial DNA control region assessment. Mol. Ecol., 5, 473–483.PubMedGoogle Scholar
  25. FitzSimmons N, Tanksley S, Forstner MR, Louis EE, Daglish R, Gratten J, Davis S (2001) Microsatellite markers for Crocodylus: New genetic tools for population genetics, mating system studies and forensics. In: Crocodilian Biology and Evolution (eds. Grigg G, Seebacher F, Franklin C), pp. 51–57. Surrey Beatty and Sons, Chipping Norton.Google Scholar
  26. FitzSimmons NN, Buchan JC, Lam PV, Polet G, Hung TT, Thang NQ, Gratten J (2002) Identification of purebred Crocodylus siamensis for reintroduction in Vietnam. J. Exp. Zool., 294,373–381.PubMedGoogle Scholar
  27. Fleischer RC, Perry EA, Muralidharan K, Stevens EE, Wemmer CM (2001) Phylogeography of the Asian elephant Elaphas maximus based on mitochondrial DNA. Evolution, 55, 1882–1892.PubMedGoogle Scholar
  28. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: Frequency, causes, and consequence, with insights from animal mitochondrial DNA. Annu. Rev. Ecol. Evol. Syst., 34, 397–423.Google Scholar
  29. Gartside DF, Dessauer HC, Joanen T (1977) Genic homozygosity in an ancient reptile (Alligator mississippiensis ). Biochem. Genet., 15, 655–663.PubMedGoogle Scholar
  30. Gatesy J, Amato GD (1992) Sequence similarity of 12S ribosomal segment of mitochondrial DNAs of Gharial and False Gharial. Copeia, 1992, 241–243.Google Scholar
  31. Glenn TC, Dessauer HD, Braun MJ (1998) Characterization of microsatellite DNA loci in American alligators. Copeia, 1998, 591–601.Google Scholar
  32. Glenn TC, Staton JL, Vu AT, Davis LM, Alvarado Bremer JR, Rhodes WE, Brisbin Jr IL, Sawyer RH (2002) Low mitochondrial DNA variation among American alligators and a novel non-coding region in crocodilians. J. Exp. Zool., 294, 312–324.PubMedGoogle Scholar
  33. Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symp. Ser., 41, 95–98.Google Scholar
  34. Hasegawa M, Kishino H, Yano T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. J. Mol. Evol.,22, 160–174.PubMedGoogle Scholar
  35. Hoffmann FG, Baker RJ (2001) Systematics of the genus Glossophaga Chiroptera: Phyllostomidae and phylogeography in G. soricina based on the cytochrome b gene. J. Mamm., 82, 1092–1101.Google Scholar
  36. Jensen-Seaman MI, Kidd KK (2001) Mitochondrial DNA variation and biogeography of eastern gorillas. Mol. Ecol., 10, 2241–2247.PubMedGoogle Scholar
  37. Kotlik P, Berrebi P (2001) Phylogeography of the barbell Barbus barbus assessed by mitochondrial DNA variation. Mol. Ecol., 10, 2177–2185.PubMedGoogle Scholar
  38. Lahanas PN, Miyamoto MM, Bjorndal KA, Bolten AB (1994) Molecular evolution and population genetics of greater Caribbean green turtles (Chelonia mydas ) as inferred from mitochondrial control region sequences. Genetica 94, 57–67.PubMedGoogle Scholar
  39. McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in Pacific butterflyshes Chaetodontidae. J. Mol. Evol., 45, 473–484.PubMedGoogle Scholar
  40. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res., 27, 209–220.PubMedGoogle Scholar
  41. Maruyama T, Fuerst PA (1984) Populations bottlenecks and nonequilibrium models in population genetics I. Allele numbers when populations evolve from zero variability. Genetics, 108, 745–763.PubMedGoogle Scholar
  42. Maruyama T, Fuerst PA (1985) Populations bottlenecks and nonequilibrium models in population genetics II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics, 111, 675–689.PubMedGoogle Scholar
  43. Menzies RA, Kushlan J, Dessauer HC (1979) Low degree of genetic variability in the American alligator (Alligator mississippiensis ). Isozyme Bull., 12, 61.Google Scholar
  44. Milot E, Gibbs HL, Hobson KA (2000) Phylogeography and genetic structure of northern populations of the yellow warbler (Dendroica petechia). Mol. Ecol., 9, 667–681.PubMedGoogle Scholar
  45. Nielson M, Lohman K, Sullivan J (2001) Phylogeography of the tailed frog Ascaphus truei: Implications for the biogeography of the Pacific Northwest. Evolution, 55, 147–160.PubMedGoogle Scholar
  46. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.Google Scholar
  47. Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci., 12, 357–358.PubMedGoogle Scholar
  48. Platt S (1996) The Ecology and Status of Morelet's Crocodile in Belize. Ph. D. thesis, Clemson University.Google 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 Programme, Global Environmental Facility, Belize City, Belize. 163 pp.Google Scholar
  50. Platt SG, Thorbjarnarson JB (2000a) Population status and conservation of Morelet's crocodile, Crocodylus acutus, in northern Belize. Biol. Cons., 96, 13–20.Google Scholar
  51. Platt SG, Thorbjarnarson JB (2000b) Population status and conservation of Morelet's crocodile, Crocodylus moreletii, in northern Belize. Biol. Cons., 96, 21–29.Google Scholar
  52. Posada D, Crandall KA (1998) MODELTEST: Testing the model of DNA substitution. Bioinformatics, 14, 817–818.CrossRefPubMedGoogle Scholar
  53. Powell J (1972) The Morelet's crocodile: An unknown quantity. Animal Kingdom, 1972 (2), 21–26.Google Scholar
  54. Ramos R, de Buffrenil V, Ross JP (1994) Current status of the Cuban crocodile, Crocodylus rhombifer, in the wild. In: Crocodiles, Proceedings of the 12th Working Meeting of the Crocodile Specialist Group, pp. 113–140. IUCN, Gland, Switzerland.Google Scholar
  55. Randi E, Lucchini V (1998) Organization and evolution of the mitochondrial DNA control region in the avian genus Alectoris. J. Mol. Evol., 47, 449–162.PubMedGoogle Scholar
  56. Ray DA, White PS, Duong HV, Cullen T, Densmore LD (2001) High levels of variation in the African dwarf crocodile Osteolaemus tetraspis. In: Crocodilian Biology and Evolution (eds. Grigg G, Seebacher F, Franklin C), pp. 58–69. Surrey Beatty and Sons, Chipping Norton.Google Scholar
  57. Ray DA, Densmore LD (2002) The crocodilian mitochondrial control region: General structure, conserved sequences and evolutionary implications. J. Exp. Zool., 294, 334–345.PubMedGoogle Scholar
  58. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol., 9, 552–569.Google Scholar
  59. Roman J, Santhuff SD, Moler PE, Bowen BW (1999) Population structure and cryptic evolutionary units in the alligator snapping turtle. Conserv. Biol., 13, 135–142.Google Scholar
  60. Rooney AP, Honeycutt RL, Derr JN (2001) Historical population size change of bowhead whales inferred from DNA sequence polymorphism data. Evolution, 55, 1678–1685.PubMedGoogle Scholar
  61. Ross CA, Ross FD (1974) Caudal scalation of Central American Crocodylus. Proc. Biol. Soc. Wash., 87, 231–234.Google Scholar
  62. Ross FD, Mayer GC (1983) On the dorsal armor of the Crocodilia. In: Advances in Herpetology and Evolutionary Biology (eds. Rhodin AGJ, Miyata K), pp. 305–331. Museum Comp. Zool., Cambridge.Google Scholar
  63. Ross JP (1998) Crocodiles: An Action Plan for their Conservation, IUCN/SSC Crocodile Specialist Group Publ., Oxford Press, Oxford.Google Scholar
  64. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York.Google Scholar
  65. Schmidt KP (1924) Notes on Central American crocodiles. Fieldiana, 12, 79–92.Google Scholar
  66. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2000: A software for population genetics data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland.Google Scholar
  67. Sigler L (1998) A Crocodylus acutus with the appearance of a C. moreletii. Crocodile Specialist Group Newsletter, 173, 9–11.Google Scholar
  68. Swofford DL (1998) PAUP Phylogenetic Analysis Using Parsimony, version 4. 01b.Google Scholar
  69. VilàC, Amorim IR, Leonard JA, Posada D, Castroviejo J, Petrucci –Fonseca F, Crandall KA, Ellegren H, Wayne RK (1999) Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol. Ecol., 8, 2089–2103.PubMedGoogle Scholar
  70. Walker D, Avise JC (1998) Principles of phylogeography as illustrated by freshwater and terrestrial turtles in the south-eastern United States. Ann. Rev. Ecol. Syst., 29, 23–58.Google Scholar
  71. Wright S (1978) Evolution and the genetics of populations. Vol. 4. Variability within and among natural populations. University of Chicago Press, Chicago.Google Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • David A. Ray
    • 1
    • 2
  • Jennifer A. Dever
    • 3
  • Steven G. Platt
    • 4
    • 4
  • Thomas R. Rainwater
    • 5
  • Adam G. Finger
    • 1
  • Scott T. McMurry
    • 1
  • Mark A. Batzer
    • 2
  • Brady Barr
    • 6
  • Peter J. Stafford
    • 7
  • Jenna McKnight
    • 8
  • Llewellyn D. Densmore
    • 1
  1. 1.Department of Biological Sciences, MS 3131Texas Tech UniversityLubbockUSA
  2. 2.Department of Biological SciencesLouisiana State UniversityBaton RougeUSA
  3. 3.University of San FranciscoHarney Science CenterSan FranciscoUSA
  4. 4.Wildlife Conservation SocietyBronxUS
  5. 5.The Institute of Environmental and Human HealthTexas Tech UniversityLubbockUSA
  6. 6.National Geographic SocietyWashingtonUSA
  7. 7.The Natural History MuseumLondonUK
  8. 8.Department of BiologyUniversity of MiamiCoral GablesUSA

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