A chromosome-level genome reveals the 3D architecture of odorant receptors and their role in the social behaviors of a parasitoid wasp
Abstract
The emergence of social behaviors in insects is closely linked to the evolution of olfactory systems, yet the genomic mechanisms that shape chemoreceptor expansion and their behavioral outputs remain poorly understood. The subsocial ectoparasitoid wasp Sclerodermus guani (Hymenoptera: Bethylidae), a widely employed biocontrol agent against wood-boring pests, relies on olfaction to coordinate host-seeking, reproduction, and cooperative maternal care, providing a tractable system to investigate these relationships in a transitional subsocial species.
Here, we present a chromosome-level genome assembly for S. guani and integrate chromatin conformation, transcriptomics, electrophysiology, and functional genetics to examine the organization and behavioral significance of odorant receptor (OR) expansion. We identify 182 chemosensory receptors, including 148 ORs marked by tandem expansion and sex-biased antennal expression. These OR loci preferentially occupy interaction-rich topologically associating domain (TAD) interiors characterized by elevated interaction frequency and reduced boundary insulation. While tandem arrays genome-wide are enriched in such permissive chromatin environments, OR singletons unexpectedly share similar positional bias, suggesting that OR loci are intrinsically embedded within chromatin neighborhoods poised for duplication and coordinated regulation.
To test the functional consequences of this expanded and structurally organized receptor family, we generated a heritable null mutation in the conserved OR co-receptor (Orco). Orco mutants displayed severe impairments in host localization, mating efficiency, and most strikingly, a collapse of oviposition fidelity and maternal care. Notably, mutants frequently laid eggs indiscriminately, including on conspecific larvae, indicating a loss of kin recognition and raising the possibility that OR-mediated olfaction contributes to the evolutionary transition from solitary parasitism to maternal care in this lineage.
Together, these findings suggest that three-dimensional genome organization may bias the diversification and regulation of chemosensory gene families, and that OR-mediated olfaction is necessary for coordinated reproduction, discriminative parasitism, and maternal care in a subsocial insect.
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