Host-Associated Differentiation in a Parasitoid Wasp Connected to Venom-Related but Not Chemosensory Genes

The mechanisms driving the megadiversity of parasitic wasps remain a central question in evolutionary ecology. To investigate the genomic architecture underlying host-associated differentiation in parasitic wasps, we generated a de novo genome assembly and performed whole-genome re-sequencing of 17 populations of the parasitoid wasp Asecodes parviclava (Eulophidae) across a latitudinal gradient and multiple Galerucella host species. Despite panmixia in host populations, we identified three genetically differentiated wasp lineages, with the most profound divergence separating Galerucella tenella-associated wasps from other populations. Locus-specific scans revealed that selection acts highly asymmetrically. We detected significant differentiation and copy-number expansion clustered within venom-related gene families, contrasting sharply with a near-complete lack of divergence in chemosensory genes. This decoupled evolution suggests that host finding may rely on behavioural plasticity, whereas physiological compatibility is genetically hard-wired via multi-layered immune-suppression mechanisms. Finally, asymmetrical gene flow in northern populations demonstrates that fine-scale habitat overlap creates ecological connectivity without eroding specialized lineages, as intense host-mediated selection purges maladapted hybrids. Ultimately, our study demonstrates that physiological barriers, rather than behavioural recognition, may maintain specialized parasitoid lineages, providing new insights into the genomic basis of speciation with gene flow in specialized natural enemies.