Hybridization may often be an important source of adaptive variation, but the extent and long-term impacts of introgression have seldom been evaluated in the phylogenetic context of a radiation. Hares (Lepus) represent a widespread... more
Hybridization may often be an important source of adaptive variation, but the extent and long-term impacts of introgression have seldom been evaluated in the phylogenetic context of a radiation. Hares (Lepus) represent a widespread mammalian radiation of 32 extant species characterized by striking ecological adaptations and recurrent admixture. To understand the relevance of introgressive hybridization during the diversification of Lepus, we analyzed whole exome sequences (61.7 Mb) from 15 species of hares (1- 4 individuals per species), spanning the global distribution of the genus, and two outgroups. We used a coalescent framework to infer species relationships and divergence times, despite extensive genealogical discordance. We found high levels of allele sharing among species and show that this reflects extensive incomplete lineage sorting and temporally layered hybridization. Our results revealed recurrent introgression at all stages along the Lepus radiation, including recent ...
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Expression divergence, rather than sequence divergence, has been shown to be important in speciation, particularly in the early stages of divergence of traits involved in reproductive isolation. In the two European subspecies of house... more
Expression divergence, rather than sequence divergence, has been shown to be important in speciation, particularly in the early stages of divergence of traits involved in reproductive isolation. In the two European subspecies of house mice, Mus musculus musculus and Mus musculus domesticus, earlier studies have demonstrated olfactory-based assortative mate preference in populations close to their hybrid zone. It has been suggested that this behaviour evolved following the recent secondary contact between the two taxa (~3,000 years ago) in response to selection against hybridization. To test for a role of changes in gene expression in the observed behavioural shift, we conducted a RNA sequencing experiment on mouse vomeronasal organs. Key candidate genes for pheromone-based subspecies recognition, the vomeronasal receptors, are expressed in these organs. Overall patterns of gene expression varied significantly between samples from the two subspecies, with a large number of differenti...
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The house mouse is a powerful model to dissect the genetic basis of phenotypic variation, and serves as a model to study human diseases. Despite a wealth of discoveries, most classical laboratory strains have captured only a small... more
The house mouse is a powerful model to dissect the genetic basis of phenotypic variation, and serves as a model to study human diseases. Despite a wealth of discoveries, most classical laboratory strains have captured only a small fraction of genetic variation known to segregate in their wild progenitors, and existing strains are often related to each other in complex ways. Inbred strains of mice independently derived from natural populations have the potential to increase power in genetic studies with the addition of novel genetic variation. Here, we perform exome-enrichment and high-throughput sequencing (~8× coverage) of 26 wild-derived strains known in the mouse research community as the "Montpellier strains." We identified 1.46 million SNPs in our dataset, approximately 19% of which have not been detected from other inbred strains. This novel genetic variation is expected to contribute to phenotypic variation, as they include 18,496 nonsynonymous variants and 262 earl...
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Introgressive hybridization is an important and widespread evolutionary process, but the relative roles of neutral demography and natural selection in promoting massive introgression are difficult to assess and an important matter of... more
Introgressive hybridization is an important and widespread evolutionary process, but the relative roles of neutral demography and natural selection in promoting massive introgression are difficult to assess and an important matter of debate. Hares from the Iberian Peninsula provide an appropriate system to study this question. In its northern range, the Iberian hare, Lepus granatensis, shows a northwards gradient of increasing mitochondrial DNA (mtDNA) introgression from the arctic/boreal L. timidus, which it presumably replaced after the last glacial maximum. Here, we asked whether a south-north expansion wave of L. granatensis into L. timidus territory could underlie mtDNA introgression, and whether nuclear genes interacting with mitochondria ("mitonuc" genes) were affected. We extended previous RNA-sequencing and produced a comprehensive annotated transcriptome assembly for L. granatensis. We then genotyped 100 discovered nuclear SNPs in 317 specimens spanning the speci...
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Using protein loci and DNA markers, we show by a multilocus genetic analysis that certain populations of the two sympatric mouse species Mus musculus domesticus and Mus spretus show clear signs of partial introgression. Given the... more
Using protein loci and DNA markers, we show by a multilocus genetic analysis that certain populations of the two sympatric mouse species Mus musculus domesticus and Mus spretus show clear signs of partial introgression. Given the sterility of F1 males and the known partial genetic incompatibilities between the genomes of the two species, our finding does not invalidate the biological species complex, but allows to think that very limited genetic exchanges remain possible even long after the divergence of taxa. This may have some consequences on the dynamics of certain kinds of invasive or advantageous DNAs like transposable elements or pathogen resistance genes.
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Mitochondrial DNA (mtDNA) variation among specimens of the northwestern African hare (Lepus capensis schlumbergeri) and three European hares sampled in Spain (L. castroviejoi and L. granatensis, which are endemic to the Iberian Peninsula,... more
Mitochondrial DNA (mtDNA) variation among specimens of the northwestern African hare (Lepus capensis schlumbergeri) and three European hares sampled in Spain (L. castroviejoi and L. granatensis, which are endemic to the Iberian Peninsula, and L. europaeus) was analyzed using seven restriction endonucleases. Fourteen haplotypes were found among the 34 animals examined. Restriction site maps were constructed and the phylogeny of the haplotypes was inferred. mtDNA of L. capensis was the most divergent, which is consistent with its allopatric African distribution and with an African origin of European hares. We estimated that mtDNA in hares diverges at a rate of 1.5-1.8% per MY assuming that the European and African populations separated 5-6 MYBP. Maximum intraspecies nucleotides divergences were 1.3% in L. capensis, 2.7% in L. castroviejoi, and 2.3% in L. granatensis but 13.0% in L. europaeus. The latter species contained two main mtDNA lineages, one on the branch leading to L. castroviejoi and the other on that leading to L. granatensis. The separation of these two lineages from the L. castroviejoi or L. granatensis lineages appears to be much older than the first paleontological record of L. europaeus in the Iberian peninsula. This suggests that the apparent polyphyly of L. europaeus is due not to secondary introgression, but to the retention of ancestral polymorphism in L. europaeus. The results suggest that L. europaeus either has evolved as a very large population for a long time or has been fractionated. Such a pattern of persistence of very divergent lineages has also been reported in other species of highly mobile terrestrial mammals. As far as mtDNA is concerned. L. europaeus appears to be the common phylogenetic trunk which has diversified during dispersion over the European continent and from which L. castroviejoi and L. granatensis speciated separately in southwest Europe.
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ABSTRACT Climatic oscillations during the glaciations forced dramatic changes in species distributions, such that some presently temperate regions were alternately occupied by temperate and arctic species. These species could have met and... more
ABSTRACT Climatic oscillations during the glaciations forced dramatic changes in species distributions, such that some presently temperate regions were alternately occupied by temperate and arctic species. These species could have met and hybridized during climatic transitions. This phenomenon happened for three hare species present in Iberia (Lepus granatensis, Lepus europaeus and Lepus castroviejoi), which display high frequencies of mitochondrial DNA (mtDNA) from Lepus timidus, an arctic/boreal species presently extinct in Iberia. Here, we extend our previous geographical survey to determine whether the distribution of this mtDNA lineage extends beyond the northern half of the Iberian Peninsula, where it is found at high frequencies. We also review the taxonomy, distribution and molecular phylogeny of the genus Lepus. The phylogenetic inference reveals the presence of L. timidus-like mtDNA in several other hare species in Asia and North America, suggesting that the mitochondrial introgression observed in Iberia might be generalized. Comparison with the available nuclear gene phylogenies suggests that introgression could have happened repeatedly, possibly during different climatic transitions. We discuss demographic and adaptive scenarios that could account for the repetition in time and space of this spectacular phenomenon and suggest ways to improve our understanding of its determinants and consequences. Such high levels of introgressive hybridization should discourage attempts to revise hare taxonomy based solely on mtDNA.
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ABSTRACT
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Reinforcement is the process by which prezygotic isolation is strengthened as a response to selection against hybridisation. Most empirical support for reinforcement comes from the observation of its possible phenotypic signature: an... more
Reinforcement is the process by which prezygotic isolation is strengthened as a response to selection against hybridisation. Most empirical support for reinforcement comes from the observation of its possible phenotypic signature: an accentuated degree of prezygotic isolation in the hybrid zone as compared to allopatry. Here, we implemented a novel approach to this question by seeking for the signature of reinforcement at the genetic level. In the house mouse, selection against hybrids and enhanced olfactory-based assortative mate preferences are observed in a hybrid zone between the two European subspecies Mus musculus musculus and M. m. domesticus, suggesting a possible recent reinforcement event. To test for the genetic signature of reinforcing selection and identify genes involved in sexual isolation, we adopted a hitchhiking mapping approach targeting genomic regions containing candidate genes for assortative mating in mice. We densely scanned these genomic regions in hybrid zo...
Research Interests: Genomics, Population Genetics, Molecular Ecology, Biological Sciences, Denmark, and 8 moreMice, Female, Animals, Male, Genome, Austria, Phenotype, and Odors
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A new, model-based method was devised to locate nucleotide changes in a given phylogenetic tree. For each site, the posterior probability of any possible change in each branch of the tree is computed. This probabilistic method is a... more
A new, model-based method was devised to locate nucleotide changes in a given phylogenetic tree. For each site, the posterior probability of any possible change in each branch of the tree is computed. This probabilistic method is a valuable alternative to the maximum parsimony method when base composition is skewed (i.e., different from 25% A, 25% C, 25% G, 25% T): computer simulations showed that parsimony misses more rare --> common than common --> rare changes, resulting in biased inferred change matrices, whereas the new method appeared unbiased. The probabilistic method was applied to the analysis of the mutation and substitution processes in the mitochondrial control region of mouse. Distinct change patterns were found at the polymorphism (within species) and divergence (between species) levels, rejecting the hypothesis of a neutral evolution of base composition in mitochondrial DNA.
Research Interests: Evolutionary Biology, Genetics, Polymorphism, Molecular Evolution, Probability, and 14 morePhylogeny, Mitochondrial DNA, Mice, Animals, Molecular Phylogenetics and Evolution, Neutral Evolution, Probabilistic Method, Genetic Polymorphism, Phylogenetic Tree, Genetic variation, Maximum Parsimony, Likelihood Functions, Nucleotide Polymorphism, and Biochemistry and cell biology
We have compared patterns of geographic variation and molecular divergence of mitochondrial DNA (mtDNA) and Y chromosome over the range of the different subspecies of Mus musculus. MtDNA was typed for 305 nucleotides in the control... more
We have compared patterns of geographic variation and molecular divergence of mitochondrial DNA (mtDNA) and Y chromosome over the range of the different subspecies of Mus musculus. MtDNA was typed for 305 nucleotides in the control region, the Y chromosome for 834 base pairs (bp) in Zfy introns and 242 bp in Sry, a Zfy2 18-bp deletion, and two microsatellites. Apparent discrepancies exist between the distributions of the lineages of mtDNA and of the two major Y-chromosome lineages thus defined: some subspecies share the same mtDNA lineage but have different Y-chromosome lineages or vice versa. One microsatellite reveals a geographically clustered variation inside the distribution of each Y-chromosome lineage, showing that new Y-chromosome variants can rapidly spread locally. The two major Y-chromosome lineages have a divergence time only about one fourth of that between mtDNA lineages. Although this recent coalescence of the Y chromosomes between subspecies could partly be due to a ...
Research Interests: Genetics, Polymorphism, Molecular Evolution, Phylogeny, Mitochondrial DNA, and 15 moreMice, Animals, Male, Biological evolution, Introns, Geographic Variation, Control Region, Genetic variation, Base Sequence, House Mouse, Divergence Time, DNA binding proteins, Mus Musculus, Nucleotides, and Molecular Sequence Data
It has been suggested that the house mouse, Mus musculus, is a polytypic species that originated in the northern part of the Indian sub-continent. Its subspecies have established secondary contact zones in east-centre China and in western... more
It has been suggested that the house mouse, Mus musculus, is a polytypic species that originated in the northern part of the Indian sub-continent. Its subspecies have established secondary contact zones in east-centre China and in western Europe. However, the exact colonization routes taken by these subtaxa and their regions of primary differentiation have not yet been identified. We analyzed 89 mice from Transcaucasia at 35 enzyme loci and for polymorphism of the mitochondrial control region and a deletion of the Y chromosome. The various samples analyzed are a mosaic of populations intermediates between M. m. domesticus and M. m. musculus. Trancaucasia appears thus as a broad secondary contact zone, a fact which reinforces the idea that the species has retained large possibilities of remixing.
Research Interests: Biological Sciences, DNA, Animals, Y chromosome, Genotype, and 3 moreIsoenzymes, Transcaucasia, and Muridae
We have examined the phylogenetic distribution of two t-specific markers among representatives of various taxa belonging to the genus Mus. The centromeric TCP-1a marker (a testicular protein variant specific for all t-haplotypes so far... more
We have examined the phylogenetic distribution of two t-specific markers among representatives of various taxa belonging to the genus Mus. The centromeric TCP-1a marker (a testicular protein variant specific for all t-haplotypes so far studied) has also been apparently detected in several non-t representatives of the Mus IVA, Mus IVB, and probably M. cervicolor species. By contrast, a t-specific restriction-fragment-length polymorphism allele (RFLP) of the telomeric alpha-globin pseudogene DNA marker alpha-psi-4 was found only in animals belonging to the M. musculus-complex species either bearing genuine t-haplotypes or, like the M. m. bactrianus specimen studied here, likely to do so. This t-specific alpha-psi-4 RFLP allele was found to be as divergent from the RFLP alleles of the latter, non-t, taxonomical groups as it is from Mus 4A, Mus 4B, or M. spretus ones. These results suggest the presence of t-haplotypes and of t-specific markers in populations other than those belonging t...
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Polymorphism of animal mitochondrial DNA (mtDNA) has been shown to involve point mutations and limited length variations affecting essentially noncoding regions. In two wild mice of the European subspecies Mus mus musculus we found a... more
Polymorphism of animal mitochondrial DNA (mtDNA) has been shown to involve point mutations and limited length variations affecting essentially noncoding regions. In two wild mice of the European subspecies Mus mus musculus we found a mitochondrial mutant with a very large deletion in a coding region. The deletion is 5 kbp long (31% of the mitochondrial chromosome) and encompasses six tRNA genes and seven protein genes. The two mice were heteroplasmic: they contained a mixture of normal mtDNA and the deletion mutant. Although the latter is functionally defective, it represents 78%-79% of the mtDNA molecules in our preparations from each animal.
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Research Interests: Population Genetics, Molecular Evolution, Hybridization, Population genetics (Biology), Molecular Ecology, and 14 moreBiological Sciences, Molecular, mtDNA, Mitochondrial DNA, Europe, Female, Animals, Male, Sex chromosomes, Molecular Phylogenetics and Evolution, Introgression, Hares, Genetic Markers, and Sex Chromosome
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Sexual selection may hinder gene flow across contact zones when hybrid recognition signals are discriminated against. We tested this hypothesis in a unimodal hybrid zone between Mus musculus musculus and Mus musculus domesticus where a... more
Sexual selection may hinder gene flow across contact zones when hybrid recognition signals are discriminated against. We tested this hypothesis in a unimodal hybrid zone between Mus musculus musculus and Mus musculus domesticus where a pattern of reinforcement was described and lower hybrid fitness documented. We presented mice from the border of the hybrid zone with a choice between opposite sex urine from the same subspecies versus hybrids sampled in different locations across the zone. While no preference was evidenced in domesticus mice, musculus males discriminated in favour of musculus signals and against hybrid signals. Remarkably, the pattern of hybrid unattractiveness did not vary across the hybrid zone. Moreover, allopatric populations tested in the same conditions did not discriminate against hybrid signals, indicating character displacement for signal perception or preference. Finally, habituation–discrimination tests assessing similarities between signals pointed out th...
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Climatic oscillations during the glaciations forced dramatic changes in species distributions, such that some presently temperate regions were alternately occupied by temperate and arctic species. These species could have met and... more
Climatic oscillations during the glaciations forced dramatic changes in species distributions, such that some presently temperate regions were alternately occupied by temperate and arctic species. These species could have met and hybridized during climatic transitions. This phenomenon happened for three hare species present in Iberia ( Lepus granatensis , Lepus europaeus and Lepus castroviejoi ), which display high frequencies of mitochondrial DNA (mtDNA) from Lepus timidus , an arctic/boreal species presently extinct in Iberia. Here, we extend our previous geographical survey to determine whether the distribution of this mtDNA lineage extends beyond the northern half of the Iberian Peninsula, where it is found at high frequencies. We also review the taxonomy, distribution and molecular phylogeny of the genus Lepus . The phylogenetic inference reveals the presence of L. timidus -like mtDNA in several other hare species in Asia and North America, suggesting that the mitochondrial int...
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New technologies for detecting variation in DNA complement traditional methods in biodiversity. Better information on the degree and distribution of genetic variation is essential for developing more efficient ways of evaluating and... more
New technologies for detecting variation in DNA complement traditional methods in biodiversity. Better information on the degree and distribution of genetic variation is essential for developing more efficient ways of evaluating and conserving biodiversity. At present, ...
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Inferring the history of isolation and gene flow during species differentiation can inform us on the processes underlying their formation. Following their recent expansion in Europe, two subspecies of the house mouse (Mus musculus... more
Inferring the history of isolation and gene flow during species differentiation can inform us on the processes underlying their formation. Following their recent expansion in Europe, two subspecies of the house mouse (Mus musculus domesticus and Mus musculus musculus) have formed a hybrid zone maintained by hybrid incompatibilities and possibly behavioural reinforcement, offering a good model of incipient speciation. We reconstruct the history of their divergence using an approximate Bayesian computation framework and sequence variation at 57 autosomal loci. We find support for a long isolation period preceding the advent of gene flow around 200,000 generations ago, much before the formation of the European hybrid zone a few thousand years ago. The duration of the allopatric episode appears long enough (74% of divergence time) to explain the accumulation of many post-zygotic incompatibilities expressed in the present hybrid zone. The ancient contact inferred could have played a role in mating behaviour divergence and laid the ground for further reinforcement. We suggest that both subspecies originally colonized the Middle East from the northern Indian subcontinent, domesticus settling on the shores of the Persian Gulf and musculus on those of the Caspian Sea. Range expansions during interglacials would have induced secondary contacts, presumably in Iran, where they must have also interacted with Mus musculus castaneus. Future studies should incorporate this possibility, and we point to Iran and its surroundings as a hot spot for house mouse diversity and speciation studies.