Transcriptomic basis underlying the evolution of female horn plasticity in scarab beetles

Exaggerated traits in insects often evolve through nutrition-sensitive growth, yet studies have focused largely on male exaggeration widespread in nature, leaving the developmental and evolutionary basis of female exaggeration and the extent to which plasticity differs between sexes poorly understood.

Here, we investigated the transcriptomic basis of female horn plasticity in three Onthophagus beetles that differ in horn morphology and nutritional responsiveness. Phylogenetic analyses indicate that rudimentary female horns represent the ancestral condition, with exaggerated, nutrition-sensitive horns evolving in derived lineages. Comparative transcriptomics reveal that enhanced female horn plasticity arises primarily through the recruitment and modulation of conserved regulatory networks, with limited contributions from taxon-restricted genes. Despite the shared reliance on conserved modules in two species with enhanced female horn plasticity, the transcriptional repertoires underlying horn plasticity are largely lineage-specific. In O. rectecornutus, where both sexes bear exaggerated horns, sex comparisons demonstrate that males and females rely on the expression of largely distinct gene sets, with only a small fraction of shared nutrition-responsive genes.

Together, our results show that exaggerated female horns arise through a mosaic of conserved and lineage-specific regulatory mechanisms, with strong sex bias in transcriptional control. More generally, our findings highlight how conserved developmental toolkits can be rewired in lineage- and sex-specific ways to evolve novel, plastic, and exaggerated traits.