Les séminaires de l'ISYEB - Amir Yassin, ISYEB

Host plant shift is a major diversification process in herbivorous insects, which constitute one fourth of the Earth’s biodiversity. However, the underlying genetic and evolutionary mechanisms remain unclear. Of particular interest is the degree of genomic modularity between loci controlling different fitness attributes on the new host, such as chemical perception and tolerance to defensive toxins. While positive pleiotropy should enhance the pace of host shifts, modularity could constrain its path, whereas negative pleiotropy might abort the process. In spite of significant progress in QTL mapping and candidate gene approaches in a few herbivorous insects, the lack of powerful genetic and genomic tools in such « non-model » organisms hindered the resolution of the modularity question at a genome-wide scale. In the family Drosophilidae, a continuum between generalist detritivorous flies such as Drosophila melanogaster and strictly herbivorous leaf-mining flies such as Scaptomyza flava exists, offering the opportunity to genetically dissect insect-plant relationships. We have recently described an interesting case of the subspecies Drosophila yakuba mayottensis which became strictly-associated to the toxic fruits of noni (Morinda citrifolia) on the island of Mayotte. This case is reminiscent to the specialization on the same host in the Seychelles archipelago by another species, D. sechellia, which is closely-related to the generalist D. melanogaster. Population genomics analyses identified a number of loci strongly differentiating the specialist D. y. mayottensis from its generalist relative subspecies D. y. yakuba, but the implication of these loci in noni specialization traits remains unknown. Building up on these results, we leveraged the crossability between the two subspecies and generated through laboratory experimental admixture a number of recombinant populations. Following 10 generations of admixture with no selection, we tested recombinant adults for two traits : preference for noni and survival on it. We found that both traits respectively localize to 3 and 10 major loci in agreement with the genomic modularity hypothesis. We also provide evidence for positive and negative pleiotropy at a few minor loci indicating that the prevalence of modularity may still be partially constrained by minor pleiotropic effects. Interestingly, the major loci contained a small set of candidate genes for chemosensory perception or resistance against plant toxins with some having been associated with host shift not only in the noni-specialist D. sechellia, but also in the herbivorous Scaptomyza as well as in a number of « non-model » herbivores belonging to other insect orders. These results highlight the relevance of studies in model organisms in elucidating general mechanisms underlying host plant shift beyond specific insect-plant systems, and open new doors to understand one of the most important questions in evolutionary biology : the « inordinate fondness » (or great diversity) of herbivorous insects.