Abstract
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.
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Abercrombie CL, Davidson D, Hope CA, Scott DE (1980) Status of Morelet's crocodile (Crocodylus moreletii ) in Belize. Biol. Cons., 17, 103–113.
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.
Adams SE, Smith MH, Baccus R (1980) Biochemical variation in the American alligator. Herpetologica, 36, 289–296.
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.
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.
Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspeci c phylogenies. Mol. Biol. Evol., 16, 37–48.
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.
Brazaitis P (1973) The identification of living crocodilians. Zoologica, 58, 59–88.
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.
Brochu CA (2000) Phylogenetic relationships and divergence timing of Crocodylus based on morphology and the fossil record. Copeia, 2000, 657–673.
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.
Charnock-Wilson J (1970) Manatees and crocodiles. Oryx, 10, 236–238.
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.
Crochet P-A, Desmarais E (2000) Slow rate of evolution in the mitochondrial control region of gulls. Mol. Biol. Evol., 17, 1797–1806
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.
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.
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.
Dawson MN, Staton JL, Jacobs DK (2001) Phylogeography of the tidewater goby, Eucyclogobius newberryi (Teleostei, Gobiidae), in coastal California. Evolution, 55, 1167–1179.
Densmore LD, Owen RD (1989) Molecular systematics of the order Crocodilia. Am. Zool., 29, 831–841.
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.
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.
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.
Donovan MF, Semlitsch RD, Routman EJ (2000) Biogeogra-phy of the southeastern United States: A comparison of salamander phylogeographic studies. Evolution, 54, 1449–1456.
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.
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.
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.
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.
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.
Gartside DF, Dessauer HC, Joanen T (1977) Genic homozygosity in an ancient reptile (Alligator mississippiensis ). Biochem. Genet., 15, 655–663.
Gatesy J, Amato GD (1992) Sequence similarity of 12S ribosomal segment of mitochondrial DNAs of Gharial and False Gharial. Copeia, 1992, 241–243.
Glenn TC, Dessauer HD, Braun MJ (1998) Characterization of microsatellite DNA loci in American alligators. Copeia, 1998, 591–601.
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.
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.
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.
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.
Jensen-Seaman MI, Kidd KK (2001) Mitochondrial DNA variation and biogeography of eastern gorillas. Mol. Ecol., 10, 2241–2247.
Kotlik P, Berrebi P (2001) Phylogeography of the barbell Barbus barbus assessed by mitochondrial DNA variation. Mol. Ecol., 10, 2177–2185.
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.
McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in Pacific butterflyshes Chaetodontidae. J. Mol. Evol., 45, 473–484.
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res., 27, 209–220.
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.
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.
Menzies RA, Kushlan J, Dessauer HC (1979) Low degree of genetic variability in the American alligator (Alligator mississippiensis ). Isozyme Bull., 12, 61.
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.
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.
Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York.
Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci., 12, 357–358.
Platt S (1996) The Ecology and Status of Morelet's Crocodile in Belize. Ph. D. thesis, Clemson University.
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.
Platt SG, Thorbjarnarson JB (2000a) Population status and conservation of Morelet's crocodile, Crocodylus acutus, in northern Belize. Biol. Cons., 96, 13–20.
Platt SG, Thorbjarnarson JB (2000b) Population status and conservation of Morelet's crocodile, Crocodylus moreletii, in northern Belize. Biol. Cons., 96, 21–29.
Posada D, Crandall KA (1998) MODELTEST: Testing the model of DNA substitution. Bioinformatics, 14, 817–818.
Powell J (1972) The Morelet's crocodile: An unknown quantity. Animal Kingdom, 1972 (2), 21–26.
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.
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.
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.
Ray DA, Densmore LD (2002) The crocodilian mitochondrial control region: General structure, conserved sequences and evolutionary implications. J. Exp. Zool., 294, 334–345.
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol., 9, 552–569.
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.
Rooney AP, Honeycutt RL, Derr JN (2001) Historical population size change of bowhead whales inferred from DNA sequence polymorphism data. Evolution, 55, 1678–1685.
Ross CA, Ross FD (1974) Caudal scalation of Central American Crocodylus. Proc. Biol. Soc. Wash., 87, 231–234.
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.
Ross JP (1998) Crocodiles: An Action Plan for their Conservation, IUCN/SSC Crocodile Specialist Group Publ., Oxford Press, Oxford.
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York.
Schmidt KP (1924) Notes on Central American crocodiles. Fieldiana, 12, 79–92.
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.
Sigler L (1998) A Crocodylus acutus with the appearance of a C. moreletii. Crocodile Specialist Group Newsletter, 173, 9–11.
Swofford DL (1998) PAUP Phylogenetic Analysis Using Parsimony, version 4. 01b.
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.
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.
Wright S (1978) Evolution and the genetics of populations. Vol. 4. Variability within and among natural populations. University of Chicago Press, Chicago.
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Ray, D.A., Dever, J.A., Platt, S.G. et al. Low Levels of Nucleotide Diversity in Crocodylus moreletii and Evidence of Hybridization with C. acutus . Conservation Genetics 5, 449–462 (2004). https://doi.org/10.1023/B:COGE.0000041024.96928.fe
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DOI: https://doi.org/10.1023/B:COGE.0000041024.96928.fe