Genome-scale evidence for host-associated lineage divergence in the parasitoid, Microctonus aethiopoides.

Abstract

Parasitoids closely rely on their hosts for successful reproduction and development. This dependence, combined with exposure to different environmental conditions, can lead to ecological specialisation and divergent selection. The parasitoid Microctonus aethiopoides serves as a valuable model for investigating such processes, as its use as a biocontrol agent against weevils of the genera Hypera and Sitona has revealed clear intraspecific divergence largely driven by different host pressures. This study examined M. aethiopoides strains from three different host species (Hypera postica, Sitona discoideus, Sitona obsoletus) and 10 geographic regions. We generated eight high-quality genome assemblies and compared them with each other and to two publicly available genomes. Comparative analyses revealed a strong host-associated phylogenetic structure separating the H. postica-associated strain from those associated with Sitona species. This separation was accompanied by distinct heterozygosity patterns, with the H. postica strain showing the highest heterozygosity, followed by S. discoideus and S. obsoletus-associated strains, and the lowest heterozygosity observed in the S. obsoletus-associated Irish strain, most likely due to its asexual reproductive mode. Further comparisons indicated that most gene families were conserved across strains, with rapid evolution of transposable element-related genes suggesting ongoing genomic diversification among strains. Chemosensory gene family classification showed broad conservation of these genes across strains, with modest variation in odourant receptor copy numbers. Overall, our study suggests that host associations may be key drivers of genomic divergence within M. aethiopoides strains, with this primarily driven by genome-level variation and limited evidence for major changes at the gene family level.