The role of ecological speciation and selection in the divergence of shads Alosa spp

Elucidating the processes that underlie population divergence and ultimately speciation is key to understanding the origin and maintenance of biodiversity. An ecological shift in habitat use accompanied by phenotypic differentiation represents a specific case of divergence where deterministic forces, rather than random processes, are likely to be implicated. Ecologically important traits, in particular, are likely to converge across distinct lineages if they are repeatedly favored by natural selection in similar environments. Studying parallel evolution will therefore reveal much about adaptation to environmental shifts in natural populations [24]. Here we propose to investigate these processes using ecological modeling, landscape genetics and genome-scanning methods.\nSeveral lines of evidence confirm that shads (Alosa spp) represent a remarkably interesting model to investigate the evolutionary processes related to ecological speciation. Shads are representatives of the family Clupeidae where diadromy or even total adaptation to freshwater (landlocked) is frequently observed. Our (PA, RF) previous findings do not support the notion that diversification in European shads can be fully explained by neutral processes generally associated to allopatric or peripatric speciation [14]. Ecological shifts in habitat, especially those related to the capacity to live in lower salinity conditions, could have played a fundamental role in the diversification of the genus. Divergence between the two closely related and often sympatric species, A alosa and A. fallax, seems to be mainly driven by adaptation to different marine and freshwater habitats. These species are therefore an excellent model with which to study the role of adaptive divergence and disruptive selection in speciation\nThe objective of this project is to elucidate the genetic architecture of adaptive divergence in shads and to test if differences at trait loci were or are maintained by selection among natural populations. We hypothesize that the genus as a whole and particularly the European shads (A. alosa and A. fallax) diversified by adapting to novel habitats. We will test this hypothesis by answering the following questions: 1) Can the divergence between A. alosa and A. fallax be explained by adaptive processes and selection at particular loci associated with different ecological conditions? What is the signature of selection at the DNA sequence level? 2) What is/was the role of selection and adaptation to different ecological transitions and gradients in promoting speciation and divergence in shads? 3) Are there parallel patterns of divergence in the independent episodes of freshwater adaptation across the genus at different timescales?\nWe will begin this research with a bottom-up approach where loci that could be fitness-related under specific ecological conditions are studied. Genes having atypically high Fst values between species [7] [11] and associated with adaptation in other species such as ?-and ?-globin will be sequenced and analyzed in terms of molecular variation. Some of the authors (WE, NF, SS) have extensive experience using this approach in model and non-model organisms e.g. [12] [22] [30]. However, adaptation is, by nature, a complex phenomenon where many traits evolve in concert. As such, a strictly bottom-up approach risks missing the most relevant candidate genes and may preclude satisfactory explanations of adaptive divergence. A top-down approach of explaining adaptive divergence may be more effective, particularly in non-model organisms such as shads where the genomic information is severely limited. This will be achieved by conducting an Amplified Fragment Length Polymorphism (AFLP) genome scan to isolate genetic loci associated with ecological traits and using PCR-walking technology to sequence them.\n \nA particular strength of this study is the possibility of performing genomic scans on replicate sets of populations that span the same kinds of environmental gradients and transitions. These natural experiments have been run in different geographic locations and for different lengths of time (decades to millennia). Landscape genetics and ecological modeling using GIS-based environmental data will be used to characterize different habitats and identify ecological variation among populations. This will allow us to effectively identify genes under selection and their association to specific ecological factors. Ultimately this research will enable us to assess the relative importance of selective versus neutral processes in shaping patterns of genetic and phenotypic variation in the Eurasian shad species complex.