Abstract
Speciation is the evolutionary process of species formation through the progressive establishment of reproductive isolation barriers between diverging populations. Understanding what kind of loci constitute these barriers, which evolutionary forces underlie their formation and how they impact the fitness of hybrids are fundamental questions in evolutionary biology. However, studying true biological species that do not interact through genetic exchanges do not help answering these questions as many reproductive isolation barriers potentially exist, making the identification of the initial barriers a difficult task. This is why we here focus our study of speciation on the European sea bass (Dicentrarchus labrax), a marine fish species subdivided into two incipient species, which are represented by the Atlantic and Mediterranean evolutionary lineages. In order to understand how divergence built up and maintained between these two lineages, we combined several complementary approaches. First, a population genomic study of wild individuals allowed us to specify the demographic context in which divergence took place and to identify the evolutionary mechanisms that allowed genetic differentiation to unfold at the genome level. We found that chromosomal variations in recombination rate have influenced the establishment of reproductive isolation. Furthermore, genomic regions involved in reproductive isolation showed particularly high levels of sequence divergence, that we related to the presence of anciently introgressed alleles. Our findings indicate that past genetic exchanges between D. labrax Atlantic lineage and a closely related species, the spotted sea bass (Dicentrarchus punctatus), have facilitated the establishment of reproductive isolation between the two extent D. labrax lineages. Secondly, we studied molecular evolution patterns of genes involved in reproductive isolation. We showed that these genes mainly display strong evolutionary constraints and thus undergo strong purifying selection. Thirdly, we used experimental crossings to determine if backcrossed individuals have a reduced fitness, which could be expected if there is hybrid depression. We observed that backcrossed individuals had the same fitness than non-backcross Mediterranean relatives. On the contrary, Atlantic alleles are even favored for these hybrids, and this occurs at the same loci where negative selection operates against Atlantic alleles over the long-term. These results thus reveal a complex temporal dynamic of selection on foreign Atlantic haplotypes. Overall, this work challenges the classical view of allopatric speciation which is generally thought as the progressive accumulation of barriers as the by-product of divergence between two populations, facilitated by the absence of gene flow. Here, we showed that on the contrary, genetic exchanges between D. labrax Atlantic population and a third lineage have probably accelerated the emergence of reproductive isolation between the two European sea bass lineages. Furthermore, reproductive isolation is generally assumed to rely on strong selection against first-generations hybrids. However, we showed that this is probably not the case for the European sea bass in which the dynamics of selection on foreign genetic material could be more complex, involving an inversion of selective effect over generations. This thesis shows that linked selection, in interaction with local recombination rate, plays a fundamental role in the establishment and maintenance of reproductive isolation.