Steep clines within a highly permeable genome across a hybrid zone between two subspecies of the European rabbit

Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 marker...

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Published in	Molecular ecology Vol. 22; no. 9; pp. 2511 - 2525
Main Authors	Carneiro, Miguel, Baird, Stuart J. E, Afonso, Sandra, Ramirez, Esther, Tarroso, Pedro, Teotónio, Henrique, Villafuerte, Rafael, Nachman, Michael W, Ferrand, Nuno
Format	Journal Article
Language	English
Published	Oxford Blackwell Publishing Ltd 01.05.2013 Blackwell
Subjects	Animals Biological and medical sciences Biological evolution Classical genetics, quantitative genetics, hybrids cline theory DNA, Mitochondrial - genetics Europe Female Fundamental and applied biological sciences. Psychology Gene Flow Gene Frequency Genetic Loci Genetics of eukaryotes. Biological and molecular evolution Genome Genomics Genotype hybrid zone Hybridization, Genetic hybrids introgression Linkage Disequilibrium loci Male mitochondrial DNA Models, Genetic Molecular Sequence Data nucleotide sequences Polymorphism, Single Nucleotide Population genetics Population genetics, reproduction patterns Rabbits Rabbits - genetics reproductive isolation sex chromosomes Species Specificity X Chromosome - genetics Y Chromosome - genetics Europe Hybrid zone cline theory Reproductive isolation Theory Sex chromosome Lagomorpha sex chromosomes Population genetics Vertebrata Gene flow Oryctolagus cuniculus Mammalia Genome
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Abstract	Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X‐chromosome, Y‐chromosome and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines (w ≥ 300 km) relative to an estimated dispersal of 1.95–4.22 km/generation, others showed abrupt transitions (w ≈ 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co‐localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X‐ and Y‐chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow and anticipate that isolation factors should often localize to small genomic regions.
AbstractList	Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X-chromosome, Y-chromosome and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines (w ≥ 300 km) relative to an estimated dispersal of 1.95-4.22 km/generation, others showed abrupt transitions (w ≈ 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co-localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X- and Y-chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow and anticipate that isolation factors should often localize to small genomic regions. Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X-chromosome, Y-chromosome and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines (w greater than or equal to 300 km) relative to an estimated dispersal of 1.95-4.22 km/generation, others showed abrupt transitions (w approximately 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co-localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X- and Y-chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow and anticipate that isolation factors should often localize to small genomic regions. Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X‐chromosome, Y‐chromosome and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines (w ≥ 300 km) relative to an estimated dispersal of 1.95–4.22 km/generation, others showed abrupt transitions (w ≈ 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co‐localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X‐ and Y‐chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow and anticipate that isolation factors should often localize to small genomic regions. Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X-chromosome, Y-chromosome and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines (w ≥ 300 km) relative to an estimated dispersal of 1.95-4.22 km/generation, others showed abrupt transitions (w [asymptotically =] 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co-localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X- and Y-chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow and anticipate that isolation factors should often localize to small genomic regions. [PUBLICATION ABSTRACT] Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic characterization of a hybrid zone between two subspecies of the European rabbit. We examined patterns of allele frequency change for 22 markers located on the autosomes, X-chromosome, Y-chromosome, and mtDNA in 1078 individuals sampled across the hybrid zone. While some loci revealed extremely wide clines ( w >=300 km) relative to an estimated dispersal of 1.95–4.22 km/generation, others showed abrupt transitions ( w ≈ 10 km), indicating localized genomic regions of strong selection against introgression. The subset of loci showing steep clines had largely coincident centers and stepped changes in allele frequency that did not co-localize with any physical barrier or ecotone, suggesting that the rabbit hybrid zone is a tension zone. The steepest clines were for X and Y chromosome markers. Our results are consistent with previous inference based on DNA sequence variation of individuals sampled in allopatry in suggesting that a large proportion of each genome has escaped the overall barrier to gene flow in the middle of the hybrid zone. These results imply an old history of hybridization and high effective gene flow, and anticipate that isolation factors should often localize to small genomic regions.
Author	Tarroso, Pedro Afonso, Sandra Ramirez, Esther Ferrand, Nuno Nachman, Michael W. Baird, Stuart J. E. Carneiro, Miguel Villafuerte, Rafael Teotónio, Henrique
AuthorAffiliation	4 IREC, Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005, Ciudad Real, Spain 6 Instituto Gulbenkian de Ciência, Apartado 14, P-2781-901 Oeiras, Portugal 5 Université Montpellier 2, CNRS, Institut des Sciences de l'Evolution CC 061, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France 1 CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Campus Agrário de Vairão, Universidade do Porto, 4485-661, Vairão 2 Departamento de Biologia da Faculdade de Ciências, Universidade do Porto, 4099-002 Porto, Portugal 7 Instituto de Investigación en Recursos Cinegéticos (CSIC-UCLM-JCCM), Departamento de Zoología, Universidad de Córdoba, Campus de Rabanales, Edificio Darwin 3 a planta, Córdoba 14071 Spain 3 Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, 85721
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Keywords	Hybrid zone cline theory Reproductive isolation Theory Sex chromosome Lagomorpha sex chromosomes Population genetics Vertebrata Gene flow Oryctolagus cuniculus Mammalia Genome
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Notes	http://dx.doi.org/10.1111/mec.12272 ArticleID:MEC12272 National Science Foundation and National Institutes of Health European Social Fund and Portuguese MCTES - No. SFRH/BD/23786/2005; No. SFRH/BPD/72343/2010 Fundação para a Ciência e a Tecnologia - No. PTDC/BIA-BDE/72304/2006; No. PTDC/BIA-EVF/111368/2009; No. PTDC/CVT/122943/2010; No. CGL2009-11665; No. POII09-0099-2557 Fundação para a Ciência e a Tecnologia - No. PTDC/BIA-BEC/103440/2008 istex:34537B8DF138C84863CFB08005ACF49720042076 Table S1 Locality details and numbers of individuals sampled. Table S2 PCR and extension primers used in the Sequenom's iPlex genotyping. Table S3 Maximum likelihood estimates (MLE) for the two parameters of the non-geographic concordance analysis (α and β) and probability of non-concordant introgression patterns for each locus. Fig. S1 Likelihood profiles for monotonic change in allele frequencies across the sampling area. Fig. S2 A summary of clinal patterns for all individual loci without constraint to any particular model of monotonic change. Fig. S3 Likelihood profiles for cline center (c) and cline width (w) estimated under the cline model retained for each locus. Fig. S4 Consensus Hardy-Weinberg (FIS) values across the center of the rabbit hybrid zone (indicated by a solid vertical line). Fig. S5 Scatterplot of cline width (km) versus net nucleotide divergence (Da; A) and locus specific estimates of gene flow between Oryctolagus algirus and O. c. cuniculus individuals sampled away from the hybrid zone (data from Carneiro et al. , ). Fig. S6 Map of the study area with major topographic features. ark:/67375/WNG-H7R50LMF-M ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 ObjectType-Article-2 ObjectType-Feature-1
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Snippet	Maintenance of genetic distinction in the face of gene flow is an important aspect of the speciation process. Here, we provide a detailed spatial and genetic...
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SubjectTerms	Animals Biological and medical sciences Biological evolution Classical genetics, quantitative genetics, hybrids cline theory DNA, Mitochondrial - genetics Europe Female Fundamental and applied biological sciences. Psychology Gene Flow Gene Frequency Genetic Loci Genetics of eukaryotes. Biological and molecular evolution Genome Genomics Genotype hybrid zone Hybridization, Genetic hybrids introgression Linkage Disequilibrium loci Male mitochondrial DNA Models, Genetic Molecular Sequence Data nucleotide sequences Polymorphism, Single Nucleotide Population genetics Population genetics, reproduction patterns Rabbits Rabbits - genetics reproductive isolation sex chromosomes Species Specificity X Chromosome - genetics Y Chromosome - genetics
Title	Steep clines within a highly permeable genome across a hybrid zone between two subspecies of the European rabbit
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