Non-random sorting of parental chemical compounds during hybrid speciation

Abstract

The role of hybridization during speciation remains partially understood, yet introgression among lineages may trigger reproductive isolation (RI). Hybrid speciation may reveal how specific traits drive RI and how characters are sorted following admixture. Here, we study hybrid speciation in a complex of butterfly species (Coenonympha spp.) in which 2 hybrid lineages (C. darwiniana and C. cephalidarwiniana) received about 75% of their genomes from C. arcania, and 25% from C. gardetta. By contrast with their genomic ancestry compositions, hybrid lineages mate readily with their minor parent in contact zones, while the major parent shows nearly complete isolation from all lineages. To test whether hybrid speciation operated via the non-random sorting of traits acting as pre-zygotic barriers, we assessed chemical profile similarity between species using gas chromatography-mass spectrometry and contrasted it to genomic composition and natural patterns of hybridization. Both hybrid species exhibited profiles strikingly similar to their minor parent despite the genomic contribution of the major parent, matching predictions for isolating traits. This suggests that chemical traits were sorted non-randomly during hybrid speciation and that they contributed to RI from the major parent. Our results reveal how hybridization may trigger rapid speciation and underscore the significance of chemical signalling in shaping barriers among emerging species.