Genomics, transcriptomics and epigenomics of the host adaptation in Lepidoptera species (Ostrinia spp.) – Adapt-Ome

We combine experimental approaches (controlled moth infestations on plants in insect-proof cages, plant choices set-ups for egg laying), analyses in natural populations , and the use of new high-throughput sequencing technologies to identify - the mutations differentiating corn borers of those on wild plants - genes more or less expressed, depending on the host plant - and the mechanisms controlling the activity of these genes. The genes and regulators so identified will be analyzed in natural populations to reconstruct their history and those of the populations.

The first analyses in experimental populations verify the specialization of the corn borer moth and the mugwort borer moth to their respective host plants, as shown by a better survival and/or development on their native plant than on an alternative plant. Surprisingly, we also observed that the ECB refused mugwort as egg-laying site, while this plant could be the ancestral host. The analysis of genes differential expression according to the host plant gives us the first candidates to the relationship between these moths and their host plant for survival traits (detoxification) and development (digestion, structural genes). Our analyzes of natural populations also showed for the first time that there is a geographical variation of specialization and divergence between the borer species. All these data lead us to propose new hypotheses for the shift from wild ancestral plants to corn, and to identify better the underlying mechanisms.

The research of this project give new suggestions for the management of ECB populations, for example by specifying the geographic areas where the corn borer is a species clearly isolated from its congeners and strictly affiliated to corn, and geographical areas where the moth is less divergent from its sister species on mugwort. Fight against the ECB pest indeed presupposes to know its capacity to take refuge on other plants or to be introgressed by a related moth species, unaffiliated to maize. The first results of the project stress also the importance of the host recognition in the ECB specialization together with a strong rejection of other potential host plants. This gives new elements to explore the gustatory and olfactory mechanisms involved, which could lead to propose strategies based on the confusion of odours during the egg-laying phase, or on trap plants placed near the corn to protect.

The project partners produce scientific publications in journals of general ecology and evolution, as well as communications in national and international conferences.
The host specialization, in particular for pest species, is of growing interest in the scientist community and we participate to the understanding of the so-called ecological speciation process (species emergence due to specialization to new environments), as well as to the debated issues of the historical reasons and mechanisms involved in the emergence of new agricultural pests.

Insects provide spectacular examples of rapid diversification and high standing diversity. In particular, phytophagous insects often undergo remarkable radiations, making phytophagous lineages more diverse than their non-phytophagous counterparts. Diversification among phytophagous insects is likely to result from their tendency to specialize on certain host plant species. This specialization may induce host shifts and the evolution of new specialist races or species (through ‘ecological speciation’).
Three components are necessary to ecological speciation: 1) a source of divergent selection, 2) a form of reproductive isolation, and 3) a genetic mechanism linking selection to reproductive isolation. The genes under selection and those conferring reproductive isolation may be one and the same (pleiotropy) or physically different (but statistically associated via linkage disequilibrium, LD). Points 1 and 2 have been thoroughly studied in various models. Other studies tackled the individual genetic mechanisms involved in host adaptation or in reproductive isolation .Yet, a more comprehensive view of the link between adaptation and isolation (i.e. point 3) is still lacking.
Here we propose a study of the genomic mechanisms underlying the specialization of moth species (Ostrinia spp., Crambidae, Lepidoptera) to their host plants. The project will concern two closely related species, the European corn borer (ECB, Ostrinia nubilalis) and the Adzuki bean borer (ABB, Ostrinia scapulalis). The first feeds mainly on maize (Gramineae), while the latter develops on various dicotyledons. Gramineae feeders are scarce in the Ostrinia genus, and the maize was indeed introduced recently in Europe (500 years ago), i.e. in the native range of ECB, so that a host shift from dicotyledons to this gramineae is the most probable scenario.
We intend to combine various observation levels and methodological approaches for an ambitious and comprehensive survey of these mechanisms. On one hand, we will apply population genomics, phylogeography and phylogenetics in natural populations of ECB and ABB (and for some tasks of the project in the Ostrinia genus, more broadly), to identify the genomic pattern of host specialization. On another hand, we will settle experimental populations of ECB and ABB on various hosts, to isolate the host effects from other environmental effects. These experimental populations will be the support for studying both genetic and regulatory (e.g. epigenetic) factors. While the first have been favoured in Evolution theory, because genes have long been considered as the ultimate targets of the evolution, the latter appear more and more as facilitators (or by contrast, as constraints) for genetic novelties to occur.
These various observation levels and methodological approaches will be supported by the production of high-throughput genomic data owing to the recent advances in NGS (next generation sequencing) technologies. If these technologies induced a revolution for the study of non-model organism by giving access to up to now unimaginable amount of genomic data, we believe that they could also favor a shift in evolutionary concepts towards a more comprehensive view of the genetics of adaptation, including complex regulatory gene networks.
The originality of the project likes in this will of reciprocal feedback between mechanisms and evolution. It indeed results from the fruitful rising collaboration between genomicists, population biologists and geneticists who compose the consortium of the project.