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 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.

[1]  U. Dieckmann,et al.  Hybridization and speciation , 2013, Journal of evolutionary biology.

[2]  P. Tucker,et al.  Sperm-related phenotypes implicated in both maintenance and breakdown of a natural species barrier in the house mouse , 2012, Proceedings of the Royal Society B: Biological Sciences.

[3]  M. Nachman,et al.  Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  D. Schwahn,et al.  REDUCED MALE FERTILITY IS COMMON BUT HIGHLY VARIABLE IN FORM AND SEVERITY IN A NATURAL HOUSE MOUSE HYBRID ZONE , 2012, Evolution; international journal of organic evolution.

[5]  N. Barton,et al.  Genetic Drift Widens the Expected Cline but Narrows the Expected Cline Width , 2011, Genetics.

[6]  A. Fijarczyk,et al.  Nuclear and mitochondrial phylogeography of the European fire‐bellied toads Bombina bombina and Bombina variegata supports their independent histories , 2011, Molecular ecology.

[7]  J. Pool,et al.  Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone , 2011, Molecular ecology.

[8]  P. Tucker,et al.  Reinforcement selection acting on the European house mouse hybrid zone , 2011, Molecular ecology.

[9]  J. Piálek,et al.  ASSESSING MULTILOCUS INTROGRESSION PATTERNS: A CASE STUDY ON THE MOUSE X CHROMOSOME IN CENTRAL EUROPE , 2011, Evolution; international journal of organic evolution.

[10]  P. David,et al.  The coupling hypothesis: why genome scans may fail to map local adaptation genes , 2011, Molecular ecology.

[11]  J. Piálek,et al.  INFERENCE OF SELECTION AND STOCHASTIC EFFECTS IN THE HOUSE MOUSE HYBRID ZONE , 2011, Evolution; international journal of organic evolution.

[12]  M. Nachman,et al.  SPECIATION IN THE EUROPEAN RABBIT (ORYCTOLAGUS CUNICULUS): ISLANDS OF DIFFERENTIATION ON THE X CHROMOSOME AND AUTOSOMES , 2010, Evolution; international journal of organic evolution.

[13]  R. Faria,et al.  Chromosomal speciation revisited: rearranging theory with pieces of evidence. , 2010, Trends in ecology & evolution.

[14]  Filipe Santos,et al.  Monte Carlo integration over stepping stone models for spatial genetic inference using approximate Bayesian computation , 2010, Molecular ecology resources.

[15]  M. Nachman,et al.  FEMALE HETEROGAMETY AND SPECIATION: REDUCED INTROGRESSION OF THE Z CHROMOSOME BETWEEN TWO SPECIES OF NIGHTINGALES , 2010, Evolution; international journal of organic evolution.

[16]  Michael S. Barker,et al.  Comparative Genomic and Population Genetic Analyses Indicate Highly Porous Genomes and High Levels of Gene Flow between Divergent Helianthus Species , 2009, Evolution; international journal of organic evolution.

[17]  P. Boursot,et al.  The genomic legacy from the extinct Lepus timidus to the three hare species of Iberia: contrast between mtDNA, sex chromosomes and autosomes , 2009, Molecular ecology.

[18]  M. Nachman,et al.  Recombination and Speciation: Loci Near Centromeres Are More Differentiated Than Loci Near Telomeres Between Subspecies of the European Rabbit (Oryctolagus cuniculus) , 2009, Genetics.

[19]  J. Piálek,et al.  Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone? , 2008, BMC Evolutionary Biology.

[20]  Montgomery Slatkin,et al.  Subdivision in an ancestral species creates asymmetry in gene trees. , 2008, Molecular biology and evolution.

[21]  M. Nachman,et al.  Reduced introgression of the Y chromosome between subspecies of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula , 2008, Molecular ecology.

[22]  J. Good,et al.  Ancient hybridization and mitochondrial capture between two species of chipmunks , 2008, Molecular ecology.

[23]  J. Piálek,et al.  GENETIC ANALYSIS OF AUTOSOMAL AND X-LINKED MARKERS ACROSS A MOUSE HYBRID ZONE , 2007, Evolution; international journal of organic evolution.

[24]  N. Perrin,et al.  Advances in our understanding of mammalian sex‐biased dispersal , 2007, Molecular ecology.

[25]  P. Andolfatto,et al.  DISCORDANT DIVERGENCE TIMES AMONG Z-CHROMOSOME REGIONS BETWEEN TWO ECOLOGICALLY DISTINCT SWALLOWTAIL BUTTERFLY SPECIES , 2007, Evolution; international journal of organic evolution.

[26]  M. Nachman,et al.  Contrasting Patterns of Introgression at X-Linked Loci Across the Hybrid Zone Between Subspecies of the European Rabbit (Oryctolagus cuniculus) , 2006, Genetics.

[27]  C. Rogel-Gaillard,et al.  Expanded comparative mapping between man and rabbit and detection of a new conserved segment between HSA22 and OCU4 , 2005, Cytogenetic and Genome Research.

[28]  C. Rogel-Gaillard,et al.  High levels of nucleotide diversity in the European rabbit (Oryctolagus cuniculus) SRY gene. , 2005, Animal genetics.

[29]  F. Bonhomme,et al.  Inferences of selection and migration in the Danish house mouse hybrid zone , 2005 .

[30]  J. Piálek,et al.  The role of salivary androgen-binding protein in reproductive isolation between two subspecies of house mouse: Mus musculus musculus and Mus musculus domesticus , 2005 .

[31]  N. Ferrand,et al.  Genetic exchange across a hybrid zone within the Iberian endemic golden‐striped salamander, Chioglossa lusitanica , 2004, Molecular ecology.

[32]  M. Nachman,et al.  DIFFERENTIAL PATTERNS OF INTROGRESSION ACROSS THE X CHROMOSOME IN A HYBRID ZONE BETWEEN TWO SPECIES OF HOUSE MICE , 2004, Evolution; international journal of organic evolution.

[33]  C. Moritz,et al.  WHEN VICARS MEET: A NARROW CONTACT ZONE BETWEEN MORPHOLOGICALLY CRYPTIC PHYLOGEOGRAPHIC LINEAGES OF THE RAINFOREST SKINK, CARLIA RUBRIGULARIS , 2004, Evolution; international journal of organic evolution.

[34]  R. Villafuerte,et al.  Wild rabbit restocking for predator conservation in Spain , 2004 .

[35]  R. Nielsen,et al.  Multilocus Methods for Estimating Population Sizes, Migration Rates and Divergence Time, With Applications to the Divergence of Drosophila pseudoobscura and D. persimilis , 2004, Genetics.

[36]  L. Rieseberg,et al.  Major Ecological Transitions in Wild Sunflowers Facilitated by Hybridization , 2003, Science.

[37]  A. Templeton,et al.  POSTGLACIAL DISPERSAL OF THE EUROPEAN RABBIT (ORYCTOLAGUS CUNICULUS) ON THE IBERIAN PENINSULA RECONSTRUCTED FROM NESTED CLADE AND MISMATCH ANALYSES OF MITOCHONDRIAL DNA GENETIC VARIATION , 2002, Evolution; international journal of organic evolution.

[38]  N. Ferrand,et al.  Phylogeography of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula inferred from RFLP analysis of the cytochrome b gene , 2000, Heredity.

[39]  G. Hewitt The genetic legacy of the Quaternary ice ages , 2000, Nature.

[40]  L. Kruuk,et al.  A comparison of multilocus clines maintained by environmental adaptation or by selection against hybrids. , 1999, Genetics.

[41]  S. Gavrilets HYBRID ZONES WITH DOBZHANSKY‐TYPE EPISTATIC SELECTION , 1997, Evolution; international journal of organic evolution.

[42]  N. Barton,et al.  The spread of an advantageous allele across a barrier: the effects of random drift and selection against heterozygotes. , 1997, Genetics.

[43]  M. Arnold Natural Hybridization and Evolution , 1997 .

[44]  D. Bell,et al.  Geographical variation in size in the European rabbit Oryctolagus cuniculus (Lagomorpha: Leporidae) in western Europe and North Africa , 1996 .

[45]  D. Holst,et al.  Natal dispersal in the European wild rabbit , 1996, Animal Behaviour.

[46]  S. Baird A SIMULATION STUDY OF MULTILOCUS CLINES , 1995, Evolution; international journal of organic evolution.

[47]  G. Hewitt,et al.  Natal dispersal and genetic structure in a population of the European wild rabbit (Oryctolagus cuniculus) , 1995, Molecular ecology.

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

[49]  W. Atchley,et al.  House Mice as Models in Systematic Biology , 1993 .

[50]  P. Tucker,et al.  ABRUPT CLINE FOR SEX CHROMOSOMES IN A HYBRID ZONE BETWEEN TWO SPECIES OF MICE , 1992, Evolution; international journal of organic evolution.

[51]  Lawrence S. Kroll Mathematica--A System for Doing Mathematics by Computer. , 1989 .

[52]  M. Nei Molecular Evolutionary Genetics , 1987 .

[53]  N. Barton,et al.  The barrier to genetic exchange between hybridising populations , 1986, Heredity.

[54]  N. Barton,et al.  GENETIC ANALYSIS OF A HYBRID ZONE BETWEEN THE FIRE‐BELLIED TOADS, BOMBINA BOMBINA AND B. VARIEGATA, NEAR CRACOW IN SOUTHERN POLAND , 1986, Evolution; international journal of organic evolution.

[55]  N. Barton MULTILOCUS CLINES , 1983, Evolution; international journal of organic evolution.

[56]  N. Barton Gene flow past a cline , 1979, Heredity.

[57]  J. Endler Geographic variation, speciation, and clines. , 1977, Monographs in population biology.

[58]  R. Selander,et al.  Biochemical genetics of hybridisation in european house mice , 1973, Heredity.

[59]  A. D. Bazykin,et al.  HYPOTHETICAL MECHANISM OF SPECIATION , 1969, Evolution; international journal of organic evolution.

[60]  H. D. Brunk Maximum Likelihood Estimates of Monotone Parameters , 1955 .

[61]  S. Baird,et al.  Evolution of the House Mouse: What can the Mus musculus musculus/M. m. domesticus hybrid zone tell us about speciation? , 2012 .

[62]  N. Ferrand,et al.  The evolutionary history of the European rabbit ( Oryctolagus cuniculus ): major patterns of population differentiation and geographic expansion inferred from protein polymorphism , 2007 .

[63]  T. Dobzhansky,et al.  Studies on hybrid sterility , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[64]  Emilio Jurado Herramientas de gestión , 2004 .

[65]  STUDIES ON HYBRID STERILITY. 11. LOCALIZATION OF STERILITY FACTORS I N DROSOPHILA PSEUDOOBSCURA HYBRIDS , 2003 .

[66]  B. Richardson,et al.  Social structures, genetic structures and dispersal strategies in Australian rabbit (Oryctolagus cuniculus) populations , 2001, Behavioral Ecology and Sociobiology.

[67]  Nicholas H. Barton,et al.  Genetic analysis of hybrid zones , 1993 .

[68]  J. Szymura Genetic analysis of a hybrid zone between the fire-bellied toads, Bombina bombina and Bombina variegata, near Krakow in southern Poland. , 1986 .

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