Phenotypic and genetic adaptations to a new host plant: Ecological divergence of a specialist insect

Divergent ecological adaptation resulting from selection is common, but how often it results in differentiation that can last in the face of gene flow is debated. Reproductive barriers persistent to stochastic environmental change are key for species to form. Hence, how ecological adaptation is coupled to reproductive isolation is key for understanding ecological speciation. Lineages that are both adapted to different ecological niches and reproductively isolated in sympatry are prime candidates for studying how ecological selection can result in speciation. Such a niche change has occurred in the highly specialized, phytophagous fly Tephritis conura, which has recently shifted onto a novel thistle host plant, resulting in two host races with different host plant use. Examining phenotypic and genetic differences enabling divergence in T. conura reveals how ephemeral ecological adaptation can result in persistent species. This thesis shows that a large inversion is the primary region of divergence between the two host races. Moreover, the inversion consistently co-segregates in the derived host race despite signals of introgression across the genome. The inversion is enriched for gene functions likely involved in divergent host use, such as phenology and metabolism, physically coupling intrinsic genetic differences with the divergent environments. I also document findings consistent with divergent morphological adaptation in length of the ovipositor, solidifying the ovipositor as a key trait enabling adaptation to different host use. The putatively strong directional selection on ovipositor length to match a new host plant in the derived host race could have depleted available variation. Yet, analyses of evolvability showed it imposing less constraint on other traits than expected, possibly facilitating rapid evolution of ovipositor length. Finally, I uncovered several barriers to reproductive isolation between host races, both pre- and postzygotic. The three most impactful barriers were phenology, host plant preference and extrinsic postzygotic viability. In concert, these strong isolation barriers reached very high levels of total reproductive isolation between host races. However, findings of introgression at a genomic level suggest some degree of permeability to gene flow. With this thesis, I establish Tephritis conura as a promising study system for unravelling the genomic features and evolutionary processes leading to ecological speciation.