Inter‐species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil

Natural hybrid zones between distinct species have been reported for many taxa, but so far, few examples involve carnivores or Neotropical mammals in general. In this study, we employed mitochondrial DNA (mtDNA) sequences and nine microsatellite loci to identify and characterize a hybrid zone between two Neotropical felids, Leopardus geoffroyi and L. tigrinus, both of which are well‐established species having diverged from each other c. 1 million years ago. These two felids are mostly allopatric throughout their ranges in South America, with a narrow contact zone that includes southern Brazil. We present strong evidence for the occurrence of hybridization between these species and identify at least 14 individuals (most of them originating from the geographical contact zone) exhibiting signs of interspecific genomic introgression. The genetic structure of Brazilian L. tigrinus populations seems to be affected by this introgression process, showing a gradient of differentiation from L. geoffroyi correlated with distance from the contact zone. We also corroborate and extend previous findings of hybridization between L. tigrinus and a third related felid, L. colocolo, leading to an unusual situation for a mammal, in which the former species contains introgressed mtDNA lineages from two distinct taxa in addition to its own.

[1]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[2]  N. Ferrand,et al.  Molecular analysis of hybridisation between wild and domestic cats (Felis silvestris) in Portugal: implications for conservation , 2008, Conservation Genetics.

[3]  K. Hupe,et al.  The Near Eastern Origin of Cat Domestication , 2007, Science.

[4]  L. Waits,et al.  Taxonomic status and conservation strategy of the endangered red wolf: a response to Kyle et al. (2006) , 2007, Conservation Genetics.

[5]  E. Eizirik,et al.  Phylogeography and population history of the crab‐eating fox (Cerdocyon thous) , 2006, Molecular ecology.

[6]  N. Gemmell,et al.  Ménage à trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction , 2006, Molecular ecology.

[7]  E. Casanave,et al.  Body mass variation in the Geoffroy's cat (Oncifelis geoffroyi) , 2006 .

[8]  D. Tautz,et al.  When invaders meet locally adapted types: rapid moulding of hybrid zones between sculpins (Cottus, Pisces) in the Rhine system , 2006, Molecular ecology.

[9]  P. Wilson,et al.  Genetic nature of eastern wolves: Past, present and future , 2006, Conservation Genetics.

[10]  Agostinho Antunes,et al.  The Late Miocene Radiation of Modern Felidae: A Genetic Assessment , 2006, Science.

[11]  E. Randi,et al.  Bayesian analyses of admixture in wild and domestic cats (Felis silvestris) using linked microsatellite loci , 2005, Molecular ecology.

[12]  C. Primmer,et al.  Efficiency of model‐based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci , 2005, Molecular ecology.

[13]  S. O’Brien,et al.  An STR forensic typing system for genetic individualization of domestic cat (Felis catus) samples. , 2005, Journal of forensic sciences.

[14]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[15]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[16]  C. Oosterhout,et al.  Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data , 2004 .

[17]  Benjamin M. Fitzpatrick,et al.  RATES OF EVOLUTION OF HYBRID INVIABILITY IN BIRDS AND MAMMALS , 2004, Evolution; international journal of organic evolution.

[18]  Sudhir Kumar,et al.  MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment , 2004, Briefings Bioinform..

[19]  J. Mank,et al.  A Century of Hybridization: Decreasing Genetic Distance Between American Black Ducks and Mallards , 2004, Conservation Genetics.

[20]  L. Ruggiero,et al.  Hybridization Between Canada Lynx and Bobcats: Genetic Results and Management Implications , 2004, Conservation Genetics.

[21]  M. Nei,et al.  MEGA: Integrated software for molecular evolutionary genetics analysis and sequence alignment briefings in bioinformatics. , 2004 .

[22]  Xavier Messeguer,et al.  DnaSP, DNA polymorphism analyses by the coalescent and other methods , 2003, Bioinform..

[23]  Craig R. Miller,et al.  Pedigree‐based assignment tests for reversing coyote (Canis latrans) introgression into the wild red wolf (Canis rufus) population , 2003, Molecular ecology.

[24]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[25]  E. Nielsen,et al.  Evidence of a hybrid‐zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis , 2003, Molecular ecology.

[26]  L. Waits,et al.  Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern US coyotes , 2003, Molecular ecology.

[27]  Alexei J Drummond,et al.  Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. , 2002, Genetics.

[28]  V. Lucchini,et al.  Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation , 2002, Conservation Genetics.

[29]  F. Allendorf,et al.  The problems with hybrids: setting conservation guidelines , 2001 .

[30]  M. Beaumont,et al.  Genetic identification of wild and domestic cats (Felis silvestris) and their hybrids using Bayesian clustering methods. , 2001, Molecular biology and evolution.

[31]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[32]  M. Culver,et al.  Patterns of size homoplasy at 10 microsatellite loci in pumas (Puma concolor). , 2001, Molecular biology and evolution.

[33]  N. Barton The role of hybridization in evolution , 2001, Molecular ecology.

[34]  M W Bruford,et al.  Genetic diversity and introgression in the Scottish wildcat , 2001, Molecular ecology.

[35]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[36]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[37]  S. O’Brien,et al.  Disparate phylogeographic patterns of molecular genetic variation in four closely related South American small cat species , 1999, Molecular ecology.

[38]  A A Schäffer,et al.  A genetic linkage map of microsatellites in the domestic cat (Felis catus). , 1999, Genomics.

[39]  R. Wayne,et al.  Hybridization between Wolves and Dogs , 1999 .

[40]  D. Reich,et al.  Genetic evidence for a recent origin by hybridization of red wolves , 1999, Molecular ecology.

[41]  George R. Hughes,et al.  Wild Cats – Status Survey and Conservation Action Plan , 1998, Biodiversity & Conservation.

[42]  T. Dowling,et al.  The role of hybridization and introgression in the diversification of animals , 1997 .

[43]  P. Jarne,et al.  Microsatellites, from molecules to populations and back. , 1996, Trends in ecology & evolution.

[44]  F. Weissing,et al.  Constraints on allele size at microsatellite loci: implications for genetic differentiation. , 1996, Genetics.

[45]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[46]  D. Futuyma,et al.  Hybrid zones and the evolutionary process , 1995 .

[47]  E. Ostrander,et al.  Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis , 1994, Molecular ecology.

[48]  E. Ostrander,et al.  Patterns of differentiation and hybridization in North American wolflike canids, revealed by analysis of microsatellite loci. , 1994, Molecular biology and evolution.

[49]  E. Thompson,et al.  Performing the exact test of Hardy-Weinberg proportion for multiple alleles. , 1992, Biometrics.

[50]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[51]  R. Wayne,et al.  Mitochondrial DNA analysis implying extensive hybridization of the endangered red wolf Canis rufus , 1991, Nature.

[52]  A. Kitchener The Natural History of the Wild Cats , 1991 .

[53]  N. Lehman,et al.  INTROGRESSION OF COYOTE MITOCHONDRIAL DNA INTO SYMPATRIC NORTH AMERICAN GRAY WOLF POPULATIONS , 1991, Evolution; international journal of organic evolution.

[54]  W. Rice ANALYZING TABLES OF STATISTICAL TESTS , 1989, Evolution; international journal of organic evolution.

[55]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[56]  K. Mullis,et al.  Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. , 1985, Science.

[57]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[58]  C. Guggisberg,et al.  Wild Cats of the World , 1975 .

[59]  Andrew P. Martin,et al.  THE SIMPLE FOOL’S GUIDE TO PCR , 2004 .

[60]  H. Ellegren,et al.  Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf–dog hybrids , 2003, Heredity.

[61]  J. Huelsenbeck,et al.  MRBAYES : Bayesian inference of phylogeny , 2001 .

[62]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[63]  H. Bandelt,et al.  Median-joining networks for inferring intraspecific phylogenies. , 1999, Molecular biology and evolution.

[64]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[65]  D. Hillis Nucleic acids IV : Sequencing and cloning , 1996 .

[66]  T. Oliveira Neotropical cats: Ecology and conservation , 1994 .

[67]  A. Hoelzel,et al.  Detection of mitochondrial DNA fragments. , 1992 .

[68]  M. Arnold Natural Hybridization as an Evolutionary Process , 1992 .

[69]  J. Eisenberg Mammals of the Neotropics , 1989 .

[70]  N. Barton,et al.  Analysis of Hybrid Zones , 1985 .

[71]  rates of , 2006 .