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Testing for hybridization and assessing genetic diversity in Morelet’s crocodile (Crocodylus moreletii) populations from central Veracruz

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Abstract

Among the loss of genetic diversity due to population declines, population fragmentation and habitat loss, hybridization also stands as a threat to Morelet’s crocodile (Crocodylus moreletii) populations. Genetic surveys in Belize and the Yucatan Peninsula have detected evidence of hybridization with the American crocodile (C. acutus). Admixture between these two species is most likely driven by human-mediated translocations. Along the central gulf coast of Mexico, C. moreletii populations are presumed to be purebred. To test this, we use nine microsatellite loci and sequence data from the mitochondrial control region to detect if C. acutus alleles have introgressed into populations of C. moreletii from central Veracruz. In 2010, C. moreletii was transferred from Appendix I to II of CITES based on a whole species demographic analysis, which indicated that populations had recovered across its range. Our study shows that populations in central Veracruz are purebred, although they exhibit low levels of genetic diversity most likely caused by inbreeding. Our data also suggest there is fragmentation among populations of C. moreletii, which may lead to further loss of genetic variation. Due the purity and low genetic diversity of C. moreletii populations from central Veracruz, we recommend increased protection and active management practices that take genetic data into account.

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References

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Oxford

    Google Scholar 

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  • Allendorf FW, Leary RF, Hitt NP, Knudsen KL, Lundquist LL, Spruell P (2004) Intercrosses and the U.S. endangered species act: should hybridized populations be included as westslope cutthroat trout? Conserv Biol 18:1203–1213

    Article  Google Scholar 

  • Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165

    Article  PubMed  Google Scholar 

  • Bishop JM, Leslie AJ, Bourquin SL, O’Ryan C (2009) Reduced effective population size in an overexploited population of the Nile crocodile (Crocodylus niloticus). Biol Conserv 142:2335–2341

    Article  Google Scholar 

  • Cedeño-Vázquez JR, Rodriguez D, Calme S, Ross JP, Densmore LD, Thorbjarnarson JB (2008) Hybridization between Crocodylus acutus and Crocodylus moreletii en the Yucatan Peninsula: I. Evidence from mitochondrial DNA and morphology. J Exp Zool 309A:661–673

    Article  Google Scholar 

  • Chunco AJ, Jobe T, Pfennig KS (2012) Why do species co-Occur? A test of alternative hypotheses describing abiotic differences in sympatry versus allopatry using spadefoot toads. PLOS One. doi:10.1371/journal.pone.0032748

    PubMed  Google Scholar 

  • CITES (2010) Fifteenth meeting of the conference of the parties Doha (Qatar), 13–25 March 2010. Consideration of proposals for amendment for appendices I and II

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Davis LM, Glenn TC, Elsey RM, Dessaeur HC, Sawyer RH (2001) Multiple paternity and mating patterns in the American alligator, Alligator mississippiensis. Mol Ecol 10:1011–1024

    Article  PubMed  CAS  Google Scholar 

  • Davis LM, Glenn TC, Strickland DC, Guillette LJ Jr, Elsey RM, Rhodes WE, Dessaeur HC, Sawyer RH (2002) Microsatellite DNA analyses support an east–west phylogeographic split of American alligator populations. J Exp Zool 294:352–372

    Article  PubMed  CAS  Google Scholar 

  • Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B Stat Methodol 39:1–38

    Google Scholar 

  • Dever JA, Densmore LD (2001) Microsatellites in Morelet’s crocodile (Crocodylus moreletii) and their utility in addressing crocodilian population genetics questions. J Herpetol 35:541–544

    Article  Google Scholar 

  • Dever JA, Strauss RE, Rainwater TR, McMurry ST, Densmore III LD (2002) Genetic diversity, population subdivision, and gene flow in Morelet′s crocodile (Crocodylus moreletii) from Belize, Central America. Copeia 4:1078–1091

    Article  Google Scholar 

  • Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Fitzsimmons NN, 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: Grigg G, Seebacher F, Franklin CE (eds) Crocodilian biology and evolution. Surrey Beatty & Sons, Chipping Norton, pp 51–57

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Glenn TC, Dessauer HC, Braun MJ (1998) Characterization of microsatellite DNA loci in American alligators. Copeia 3:591–601

    Article  Google Scholar 

  • Groombridge B (1987) The distribution and status of world Crocodilians. In: Webb GJW, Manolis CS, Whitehead PJ (eds) Wildlife management: crocodiles and alligators. Surrey Beatty & Sons, Sydney, pp 9–21

    Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hedrick PW (1986) Average inbreeding or equilibrium inbreeding? Am J Hum Genet 38:965–970

    PubMed  CAS  Google Scholar 

  • Hekkala ER (2004) Conservation genetics at the species boundary: case studies from African and Caribbean crocodiles (genus: Crocodylus). Dissertation, Columbia University

    Google Scholar 

  • Isberg SR, Chen Y, Barker SG, Moran C (2004) Analysis of microsatellites and parentage testing in saltwater crocodiles. J Hered 95:445–449

    Article  PubMed  CAS  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Lacy RC, Miller PS (2002) Incorporating human populations and activities into population viability analysis. In: Beissinger SR, McCullough DR (eds) Population viability analysis. University of Chicago Press, Chicago, pp 490–510

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Machkour-M’Rabet S, Hénaut Y, Charruau P, Gevrey M, Winterton P, Legal L (2009) Between introgression events and fragmentation, islands are the last refuge for the American crocodile in Caribbean Mexico. Mar Biol 156:1321–1333

    Article  Google Scholar 

  • McVay JD, Rodriguez D, Rainwater TR, Dever JA, Platt SG, McMurry MRJ, Forstner S, Densmore LD (2008) Evidence of multiple paternity in Morelet’s Crocodile (Crocodylus moreletii) in Belize, CA, inferred from microsatellite markers. J Exp Zool 309A:643–648

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Olden JD, Poff NL, Douglas MR, Douglas MD, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24

    Article  PubMed  Google Scholar 

  • Oosterhout CV, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Pacheco SGJ (2010) Caracterización genética de Crocodylus moreletii en la reserva de la biósfera Ría lagartos. Estructura genética poblacional y evidencia de hibridación entre C. moreletii y C. acutus. Tesis, Universidad Autónoma de Yucatán, Yucatán, México

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Ray DA, Dever JA, Platt SG, Rainwater TR, Finger AG, McMurry ST, Batzer MA, Barr B, Stafford PJ, McKnight J, Densmore III LD (2004) Low levels of nucleotide diversity in Crocodylus moreletii and evidence of hybridization with C. acutus. Conserv Genet 5:449–462

    Article  CAS  Google Scholar 

  • R Core Team (2012) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna. http://www.R-project.org

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rodriguez D, Cedeño-Vázquez JR, Forstner MRJ, Densmore LD (2008) Hybridization between Crocodylus acutus and Crocodylus moreletii in the Yucatan Peninsula: II. Evidence from microsatellites. J Exp Zool 309A:674–686

    Article  CAS  Google Scholar 

  • Rodriguez D, Forstner MRJ, Moler PE, Wasilewski JA, Cherkiss MS, Densmore LD III (2011) Effect of human-mediated migration and hybridization on the recovery of the American crocodile in Florida (USA). Conserv Genet 12:449–459

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Ryberg WA, Fitzgerald LA, Honeycutt RL, Cathey JC (2002) Genetic relationships of American alligator populations distributed across different ecological and geographic scales. J Exp Zool 294:325–333

    Article  PubMed  CAS  Google Scholar 

  • Sánchez HO, López SG, García NOA, Benítez DH (2011) Programa de monitoreo del cocodrilo de pantano (Crocodylus moreletii) México-Belice-Guatemala. México. Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México

    Google Scholar 

  • Schlaepfer MA, Hoover C, Dodd CK (2005) Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. Bioscience 55:256–264

    Article  Google Scholar 

  • SEMARNAT (2012) Ley General de vida silvestre. Diario oficial de la federación. http://www.diputados.gob.mx/LeyesBiblio/pdf/146.pdf

  • Shaddick K, Burridg CP, Jerry DR, Schwartz TS, Truong K, Gilligan DM, Beheregaray LB (2011) A hybrid zone and bidirectional introgression between two catadromous species: Australian bass Macquaria novemaculeata and estuary perch Macquaria colonorum. J Fish Biol 79:1214–1235

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Stafford PJ, McMurry ST, Rainwater TR, Ray DA, Densmore LD, Barr B (2003) Morelet’s crocodile (Crocodylus moreletii) in the Macal river watershed, Maya mountains, Belize. Herpetol Bull 85:15–23

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA). Software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Villegas A, Reynoso VH (2010) Fuga de cocodrilos en La Antigua, Veracruz. Diario del Istmo, 25 de Septiembre de 2010, p 2

  • Weaver JP, Rodriguez D, Venegas-Anaya M, Cedeño-Vázquez JR, Forstner MJR, Densmore LD (2008) Genetic characterization of captive cuban crocodiles (Crocodylus rhombifer) and evidence of hybridization with the American crocodile (Crocodylus acutus). J Exp Zool 309A:649–660

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Blanca Martínez-de León, Miguel Munguía, Roger Guevara and Christopher Guibal for their helpful comments and suggestions on an earlier version of this manuscript. We thank Jeremy Weaver and Michael Vandewege for lab assistance. This research was supported with partial funding by a Consejo Nacional de Ciencia y Tecnología (CONACYT) doctoral fellowship (No: 172256) (RGT) and Red de Biología y Conservación de Vertebrados del Instituto de Ecología, A.C. Field work was conducted under special collecting permit (SGPA/DGVS/02227 and SGPA/DGVS/05851/07 to AGR. Molecular analysis were performed in the Department of Biological Sciences, Texas Tech University, with funding provided by National Science Foundation grant BSR-0444133 (LDD). Samples were donated to the Texas Cooperative Wildlife Collection, Dept. of Wildlife and Fisheries Sciences, Texas A&M University, TX from the Colección Nacional de Anfibios y Reptiles, Instituto de Biología, Universidad Nacional Autónoma de México, MX (CITES MX-HR-007-MEX. Folio:001).

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Authors and Affiliations

  1. Red de Biología y Conservación de Vertebrados, Instituto de Ecología A.C., AP 63, 91070, Xalapa, Veracruz, Mexico

    Ricardo González-Trujillo & Alberto González-Romero

  2. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853-2701, USA

    David Rodriguez

  3. Department of Biology, Texas State University-San Marcos, San Marcos, TX, 78666, USA

    Michael R. J. Forstner

  4. Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409-3131, USA

    Llewellyn D. Densmore III

  5. Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, 04510, Mexico, DF, Mexico

    Víctor Hugo Reynoso

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  1. Ricardo González-Trujillo
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  2. David Rodriguez
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  3. Alberto González-Romero
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  4. Michael R. J. Forstner
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  5. Llewellyn D. Densmore III
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  6. Víctor Hugo Reynoso
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Correspondence to Víctor Hugo Reynoso.

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González-Trujillo, R., Rodriguez, D., González-Romero, A. et al. Testing for hybridization and assessing genetic diversity in Morelet’s crocodile (Crocodylus moreletii) populations from central Veracruz. Conserv Genet 13, 1677–1683 (2012). https://doi.org/10.1007/s10592-012-0406-2

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