Abstract
Genealogical records of animals (studbook) are created to avoid reproduction between closely related individuals, which could cause inbreeding, particularly for such endangered species as the Panthera onca (Linnaeus, 1758). Jaguar is the largest felid in the Americas and is considered an important ecological key species. In Mexico, wild jaguar populations have been significantly reduced in recent decades, and population decline typically accompany decreases in genetic variation. There is no current census of captive jaguars in Mexico, and zoos do not follow a standardized protocol in breeding programs based on genetic studies. Here, we emphasise the importance of maintaining an adequate level of genetic variation and propose the implementation of standardised studbooks for jaguars in Mexico, mainly to avoid inbreeding. In addition, achieving the aims of studbook registration would provide a population genetic characterisation that could serve as a basis for ex situ conservation programmes.
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References
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Met 57(1):289–300
Boakes EH, Wang J, Amos W (2007) An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity 98:172–182. doi:10.1038/sj.hdy.6800923
Boecklen WJ (1986) Optimal design of nature reserves: consequences of genetic drift. Biol Conserv 38(4):323–338. doi:10.1016/0006-3207(86)90058-3
Briscoe DA, Malpica JM, Robertson A, Smith GJ, Frankham R, Banks RG, Barker JSF (1992) Rapid loss of genetic variation in large captive populations of Drosophila flies: implications for the genetic management of captive populations. Conserv Biol 6(3):416–425. doi:10.1046/j.1523-1739.1992.06030416.x
Campos Fernández-Fígares MM (2002) El caballo y el jaguar: sobre la historia verdadera de la conquista de la Nueva España. Comares Editores, España
Cartín-Núñez M, Carrillo E (2009) New record of black jaguar, Panthera onca (Carnivora: Felidae) in Costa Rica. Brenesia 71–72:67–68
Caso A, Lopez-Gonzalez C, Payan E, Eizirik E, de Oliveira T, Leite-Pitman R, Kelly M, Valderrama C (2008) Panthera onca-The IUCN Red List of Threatened Species. Version 2014.3. www.iucnredlist.org. Downloaded on 29 April 2015
Ceballos G, Chávez C, Zarza H (2011a) El Jaguar en México. Alianza WWF/Telcel CONANP, UNAM. Servicios Ecológicos y Científicos, México, Distrito Federal
Ceballos G, Chávez C, List R, Zarza H, Medellín RA (2011b) Jaguar Conservation and Management in Mexico: case studies and perspectives, Alianza WWF/Telcel CONANP, UNAM. Servicios Ecológicos y Científicos, México, Distrito Federal
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631. doi:10.1093/molbev/msl191
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796. doi:10.1038/nrg2664
Chávez C, Zarza H (2009) Distribución potencial del hábitat del jaguar y áreas de conflicto humano-jaguar en la península de Yucatán. Rev Mex Mastozool 13:46–62
Chirhart SE, Honeycutt RL, Greenbaum IF (2000) Microsatellite markers for the deer mouse P. maniculatus. Mol Ecol 9:1669–1672
CITES (2015) Convention on international trade in endangered species of wild fauna and flora appendices I, II and III. http://www.cites.org/eng/app/appendices.php. Accessed 10 April 2015
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014
Dutta T, Sharma S, Maldonado JE, Wood TC, Panwar HS, Seidensticker J (2013) Fine-scale population genetic structure in a wide-ranging carnivore, the leopard (Panthera pardus fusca) in central India. Divers Distrib 19(7):760–771. doi:10.1111/ddi.12024
Dyer RJ (2009) Genetic studio: a suit of programs from spatial analysis of genetic-marker data. Mol Ecol Resour 9:110–113
Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7
Eizirik E, Heup KJ, Menotti-Raymond M, Crawshaw PG, O’Brien SJ, Johnson WE (2001) Phylogeography, population history and conservation genetics of jaguars (Panthera onca, Mammalia, Felidae). Mol Ecol 10:65–79. doi:10.1046/j.1365-294X.2001.01144.x
Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS, O’Brien SJ (2003) Molecular genetics and evolution of melanism in the cat family. Curr Biol 13:448–453. doi:10.1016/S0960-9822(03)00128-3
Eizirik E, Haag T, Santos AS, Salzano FM, Silveira L, Azevedo FCC, Furtado MM (2008) Jaguar Conserv Genet. CAT News 4:31–34
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x
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 Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x
Falush D, Stephens M, Pritchard J (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587
Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327. doi:10.1146/annurev.ge.29.120195.001513
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol Early View. doi:10.1111/mec.13139
Fredrickson R, Hedrick P (2002) Body sizes in endangered Mexican wolves: effects of inbreeding and cross-lineage matings. Anim Conserv 5:39–43. doi:10.1017/S1367943002001051
Fredrickson RJ, Siminski P, Woolf M, Hedrick PW (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proc R Soc Lond B Bio 274:2365–2371. doi:10.1098/rspb.2007.0785
Haag T, Santos AS, Sana DA, Morato RG, Cullen L Jr, Crawshaw PG, De Angelo C, Di Bitetti MS, Salzano FM, Eizirik E (2010) The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of Atlantic Forest jaguars (Panthera onca). Mol Ecol 19:4906–4921. doi:10.1111/j.1365-294X.2010.04856.x
Hedrick PW (1994) Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73:363–372. doi:10.1038/hdy.1994.183
Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636. doi:10.1016/S0169-5347(01)02282-0
Hedrick PW, Fredrickson R (2008) Captive breeding and the reintroduction of Mexican and red wolves. Mol Ecol 17:344–350. doi:10.1111/j.1365-294X.2007.03400.x
Hedrick PW, Fredrickson R (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet 11:615–626. doi:10.1007/s10592-009-9999-5
Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162
Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38(03):209–216. doi:10.1017/S0016672300020553
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9(5):1322–1332. doi:10.1111/j.1755-0998.2009.02591.x
Jiménez JA, Hughes KA, Alaks G, Graham L, Lacy RC (1994) An experimental study of inbreeding depression in a natural habitat. Science 266(5183):271–273. doi:10.1126/science.7939661
Kalinowski ST, Wagner AP, Taper ML (2006) ML-Relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6(2):576–579. doi:10.1111/j.1471-8286.2006.01256.x
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17(5):230–241. doi:10.1016/S0169-5347(02)02489-8
Kitchener AC (1997) The role of museums and zoos in conservation biology. Int Zoo Yb 35:325–336. doi:10.1111/j.1748-1090.1997.tb01228.x
Laikre L (1999) Hereditary defects and conservation genetic management of captive populations. Zoo Biol 18:81–99. doi:10.1002/(SICI)1098-2361(1999)18:2<81:AID-ZOO1>3.0.CO;2-2
Langella O (2002) Populations 1230 Copyright (C) 1999 Olivier Langella CNRS-UPR9034. http://bioinformatics.org/~tryphon/populations/
Luo SJ, Kim JH, Johnson WE, van der Walt J, Martenson J, Yuhki N, Miquelle DG, Uphyrkina O, Goodrich JM, Quigley HB, Tilson R, Brady G, Martelli P, Subramaniam V, McDougal C, Hean S, Huang SQ, Pan W, Karanth UK, Sunquist M, Smith JLD, O’Brien SJ (2004) Phylogeography and genetic ancestry of tigers (Panthera tigris). PLoS Biol 2(12):2275–2293. doi:10.1371/journal.pbio.0020442
Luo SJ, Johnson WE, Martenson J, Antunes A, Martelli P, Uphyrkina O, Traylor-Holzer K, Smith JLD, O’Brien SJ (2008) Subspecies genetic assignments of worldwide captive tigers increase conservation value of captive populations. Curr Biol 18(8):592–596. doi:10.1016/j.cub.2008.03.053
Marker LL, Wilkerson AJP, Sarno RJ, Martenson J, Breitenmoser-Würsten C, O’Brien SJ, Johnson WE (2008) Molecular genetic insights on cheetah (Acinonyx jubatus) ecology and conservation in Namibia. J Hered 99(1):2–13. doi:10.1093/jhered/esm081
Martínez-Cruz B, Godoy JA, Negro JJ (2004) Population genetics after fragmentation: the case of the endangered Spanish imperial eagle (Aquila adalberti). Mol Ecol 13(8):2243–2255. doi:10.1111/j.1365-294X.2004.02220.x
Menotti-Raymond M, David VA, Lyons LA, Schäffer AA, Tomlin JF, Hutton MK, O’Brien SJ (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57(1):9–23. doi:10.1006/geno.1999.5743
Meretsky VJ, Snyder NF, Beissinger SR, Clendenen DA, Wiley JW (2000) Demography of the California Condor: implications for reestablishment. Conserv Biol 14:957–967. doi:10.1046/j.1523-1739.2000.99113.x
Meyer JR (1994) Black jaguars in Belize? A survey of melanism in the jaguar, Panthera onca. http://biological-diversity.info/Black_Jaguar.htm
Moreno VR, Grisolia AB, Campagnari F, Milazzotto M, Adania CH, Garcia JF, Souza EBD (2006) Genetic variability of Herpailurus yagouaroundi, Puma concolor and Panthera onca (Mammalia, Felidae) studied using Felis catus microsatellites. Genet Mol Biol 29(2):290–293. doi:10.1590/S1415-47572006000200017
Nei M (1972) Genetic distance between populations. Am Nat 106:283–292
O’Brien SJ (1994) Genetic and phylogenetic analyses of endangered species. Annu Rev Genet 28(1):467–489. doi:10.1146/annurev.ge.28.120194.002343
O’Brien SJ, Johnson WE (2005) Big Cat Genomics. Annu Rev Genom Hum Genet 6:407–429. doi:10.1146/annurev.genom.6.080604.162151
Olech W, Perzanowski K (2002) A genetic background for reintroduction program of the European bison (Bison bonasus) in the Carpathians. Biol Conserv 108:221–228. doi:10.1016/S0006-3207(02)00108-8
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:10.1111/j.1471-8286.2005.01155.x
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 90:502–503
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Quigley HB, Crawshaw PG (1992) A conservation plan for the jaguar Panthera onca in the Pantanal region of Brazil. Biol Conserv 61(3):149–157. doi:10.1016/0006-3207(92)91111-5
R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol 2(2):185–193. doi:10.1111/j.1523-1739.1988.tb00169.x
Rambaut A, Drummond A (2010) FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, UK. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 2013 Apr 25
Raymond M, Rousset F (1995) GENEPOP v 12: population genetics software for exact test and ecumenicism. J Hered 86:248–249
Rodríguez-Soto C, Monroy-Vilchis O, Maiorano L, Boitani L, Faller JC, Briones MA, Núñez R, Rosas-Rosas O, Ceballos G, Falcucci A (2011) Predicting potential distribution of the jaguar (Panthera onca) in Mexico: identification of priority areas for conservation. Divers Distrib 17:350–361. doi:10.1111/j.1472-4642.2010.00740.x
Roques S, Furtado M, Jácomo AT, Silveira L, Sollmann R, Tôrres NM, Godoy JA, Palomares F (2014) Monitoring jaguar populations Panthera onca with non-invasive genetics: a pilot study in Brazilian ecosystems. Oryx 48(03):361–369. doi:10.1017/S0030605312001640
Roques S, Sollman R, Jácomo A, Tôrres N, Silveira L, Chávez C, Keller C, Mello do Prado D, Carignano Torres P, Jorge dos Santos C, Bernardes Garcia da Luz X, Magnusson WE, Godoy JA, Ceballos G, Palomares F (2015) Effects of habitat deterioration on the population genetics and conservation of the jaguar. Conserv Genet. doi:10.1007/s10592-015-0766-5
Ruiz-García M (2013) Jaguar, genes y conservación: La historia poblacional del gran félido americano revelada por el ADN. Investigación y ciencia 441:24–31
Ruiz-García M, Payán E, Murillo A, Álvarez D (2006) DNA microsatellite characterization of the jaguar (Panthera onca) in Colombia. Genes Genet Syst 81:115–127. doi:10.1266/ggs.81.115
Sambrook J, Russell WD (2001) Molecular cloning: a laboratory manual, Vol 2. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, New York, pp 47–53
SEMARNAT-Secretaría de Medio Ambiente y Recursos Naturales (2010) Norma Oficial Mexicana NOM-059-ECOL-2010, Protección ambiental de especies nativas de México de flora y fauna silvestres en categorías de riesgo y especificaciones para su inclusión, exclusión o cambio en la lista de especies en riesgo. Diario Oficial de la Federación 1–56
Silver SC, Ostro LET, Marsh LK, Maffei L, Noss AJ, Kelly MJ, Wallace RB, Gómez H, Ayala G (2004) The use of camera traps for estimating jaguar Panthera onca abundance and density using capture/recapture analysis. Oryx 38(02):148–154. doi:10.1017/S0030605304000286
Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc B 64(3):479–498. doi:10.1111/1467-9868.00346
Swindell WR, Bouzat JL (2006) Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 60(5):1014–1022. doi:10.1111/j.0014-3820.2006.tb01179.x
Templeton AR, Read B (1998) Elimination of inbreeding depression from a captive population of Speke’s gazelle: validity of the original statistical analysis and confirmation by permutation testing. Zoo Biol 17:77–94. doi:10.1002/(SICI)1098-2361(1998)17:2<77:AID-ZOO4>3.0.CO;2-6
Van Oosterhout C, 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. doi:10.1111/j.1471-8286.2004.00684.x
Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184. doi:10.1007/s10592-005-9100-y
Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8(4):753–756. doi:10.1111/j.1755-0998.2007.02061.x
Whittaker DG, Ostermann SD, Boyce WM (2004) Genetic variability of reintroduced California bighorn sheep in Oregon. J Wildl Manag 68:850–859. doi:10.2193/0022-541X(2004)068[0850:GVORCB]2.0.CO;2
Willis K, Wiese RJ (1997) Elimination of inbreeding depression from captive populations: Speke’s gazelle revisited. Zoo Biol 16:9–16. doi:10.1002/(SICI)1098-2361(1997)16:1<9:AID-ZOO3>3.0.CO;2-E
Willoughby JR, Fernandez NB, Lamb MC, Ivy JA, Lacy RC, DeWoody JA (2015) The impacts of inbreeding, drift and selection on genetic diversity in captive breeding populations. Mol Ecol 24(1):98–110. doi:10.1111/mec.13020
Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20(9):1843–1861. doi:10.1007/s10531-011-0074-4
Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2002) Rapid genetic deterioration in captive populations: causes and conservation implications. Conserv Genet 3(3):277–288. doi:10.1023/A:1019954801089
Acknowledgments
The first author acknowledges CONACYT (No. 212653) for the scholarship, and all the support obtained as a Ph.D. student in the programme of Doctorado en Ciencias Biológicas y de la Salud from the Universidad Autónoma Metropolitana-Xochimilco. One phase of the project was done at Estación Biológica de Doñana in Seville, Spain. The authors would like to thank Begoña Adrados, María Méndez and María Lucena for the invaluable help in analysis and laboratory procedures. Also they would like to thank to all the zoos that provided blood samples, with a special mention to Dirección General de Zoológicos y Vida Silvestre in Mexico City.
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Rueda-Zozaya, P., Mendoza-Martínez, G.D., Martínez-Gómez, D. et al. Genetic variability and structure of jaguar (Panthera onca) in Mexican zoos. Genetica 144, 59–69 (2016). https://doi.org/10.1007/s10709-015-9878-6
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DOI: https://doi.org/10.1007/s10709-015-9878-6