The evolution of genetic information underlies the dynamics of biodiversity, and among the avatars generated by this information at higher levels of organisation, species are considered an important unit of evolution. The pertinence of this level of organisation depends on our understanding of the relationship between the process of speciation and that of adaptation to the environment and the level of coupling/uncoupling between the two, a major challenge of modern evolutionary theory. This can be addressed at the early stages of the speciation process by determining how genetic information is partitioned among incipient species that continue to exchange part of it. We will apply the approach to two well studied mammalian models (hares and house mice) for which we have gathered evidence of extensive but differential genetic exchanges between closely related taxa in the recent past, at the favour of changes in the environment, presumably range shifts linked to climatic fluctuations during the last glaciation. The Iberian hare, Lepus granatensis, shows traces of past introgression from a boreal species, L. timidus. Patterns of geographic and frequency distribution of alien alleles vary a lot across the species range (the Iberian Peninsula) between the few markers tested, and suggest the possible combined action of drift during range changes and selection favouring introgression. In a region of contact between three subspecies of the house mouse (Mus musculus, in the Middle East), the few genomic regions tested display extremely contrasted and discordant phylogeographic partitioning of diversity between three parapatric subspecies (M. m. domesticus, M. m. musculus and M. m. castaneus). Despite being highly involved in reproductive isolation, sex chromosomes appear to participate in important genetic exchanges or phylogeographic discordances between taxa in both biological models. In this project we will extend these observations of the apportionment and exchange of genetic diversity between taxa genome-wide, thanks to the recent progress of high throughput sequencing technologies. With this extensive dataset we will infer the historical conditions of the genetic exchanges between the taxa since their initial divergence, and determine their variations along the genome. We will also study the population genetics of genomic regions with varying patterns of introgression/phylogeographic discordance, in order to take apart the influence of demographic/range expansion processes from that of selection in promoting introgression.
The project builds on an ancient collaboration between the French and Portuguese teams that has led to several common publications. Each team is specialist of one of the biological models (mice and hare respectively), holds important sample collections necessary for the project, and has good knowledge of the natural history and population genetics of its organism. Because the same approach and questions apply to both models in the project, the collaboration will allow sharing the important technical and methodological developments needed to conduct the project. In particular, some specific necessary data analyses methods will be developed and tested, based on intensive population genetics simulations and model fitting by Approximate Bayesian Computation.
The project is expected to deliver unprecedented understanding, on two biological models, of the genetic architecture of reproductive isolation, the role of species range shifts and natural selection in promoting introgression, and will contribute to elucidate the possible dual role of sex chromosomes and genetic conflicts in driving reproductive isolation vs. promoting gene flow. Questions specific to each model will also be addressed such as the adaptive nature of mtDNA introgression in hare, in relation to cold adaptation, and the role of introgression in the adaptation of the three mouse subspecies to commensalism with Human.