Genomic basis of convergent specialization on a toxic plant in two Drosophila species – TOXIPHILA

The project combines different approaches to understand the genetic mechanisms of insects’ adaptation to their host plants. This adaptation is complex and includes both behavioral traits (such as attraction to chemical components of the plant) and physiological traits (such as tolerance to toxins and the plant's defensive mechanisms). The first part of the project concerns the precise quantification under controlled laboratory conditions of the divergence of these characters between specialist species and their closest generalist species. The second part seeks to compare the genetic diversity in natural populations of these species as well as in an experimental population resulting from crosses between the subspecies of D. yakuba, in order to identify the most divergent regions of the genome that are also associated with traits allowing adaptation to noni. The genetic analysis of the genes contained in these regions will then be pursued through their direct editing by CRISPR\Cas9 in the genome of specialist species.

Our primary results indicate that important behavioral and physiological differences exist between specialist species and their closest generalist species. In particular, specialist species are attracted to the toxic substances found in noni fruits. This surprising result had already been shown in D. sechellia but its replication in D. yakuba, whose specialization on noni is more recent, confirms its generality and suggests a potential link between neuronal evolution and detoxification pathways in herbivorous insects.
Preliminary genomic analyzes have also made it possible to identify the regions of the genome that are most differentiated between specialist and generalist species. However, the parallel between D. sechellia and D. yakuba remains less clear even though common genes seem to have been targeted by selection in these two species. These genes will be the subjects of genome editing studies.

Drosophila shares with humans ~ 60% of its genetic makeup and certainly much more with herbivorous insects. Identifying the genes involved in the recurrent specialization of the two Drosophila species studied here could reveal neural circuits and metabolic pathways common to herbivorous insects. This will have practical impact on the study and planning of biological control programs against crop pests that pose a major economic threat, but will also touch on a fundamental question in evolutionary biology: how abrupt environmental change, like a host plant shift following colonization of an island, could lead to the appearance of new species. In a context of global and rapid degradation of biodiversity, understanding how different genomes respond to common selective pressures becomes a great necessity.

The project is financing a doctoral thesis started in 2019. An article on the first results is being written.

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 are: (1) the degree of genomic modularity controlling different fitness attributes on the new host, (2) the genetic linkage between host use and reproductive isolation traits, and (3) the repeatability of genetic changes underlying the convergent specialization on the same host. In spite of significant progress, the lack of powerful genetic and genomic tools capable to identify genes underlying host plant use and/or reproductive isolation in classical herbivorous insect models has hindered the resolution of these questions. Here, we propose to investigate an interesting case, where two species, Drosophila sechellia and D. yakuba mayottensis have independently become specialists on the toxic fruits of noni (Morinda citrifolia) in the Seychelles and Mayotte islands, respectively. In both cases, noni specialization was accompanied by partial reproductive isolation. We will combine precise phenotypic analyses with population and quantitative genomics in D. yakuba to identify genes potentially underlying noni use and reproductive isolation in D. y. mayottensis. We will then leverage advanced genome editing and transgenesis tools (e.g., CRISPR\Cas9) that have recently been developed in both species, to functionally dissect those candidate genes. The expected results will improve our understanding of the genetic and evolutionary mechanisms underlying convergent host shift and ecological speciation, which could go beyond the Drosophila-noni relationship towards the identification of neuronal circuits or detoxification pathways that are common among herbivorous insects.