Population genomics of the mostly thelytokous Diplolepis rosae (Linnaeus, 1758) (Hymenoptera: Cynipidae) reveals population-specific selection for sex

Abstract

In Hymenoptera, arrhenotokous parthenogenesis (arrhenotoky) is a common reproductive mode. Thelytokous parthenogenesis (thelytoky), when virgin females produce only females, is less common and is found in several taxa. In our study, we assessed the efficacy of recombination and the effect of thelytoky on the genome structure of Diplolepis rosae, a gall wasp producing bedeguars in dog roses. We assembled a high-quality reference genome using Oxford Nanopore long-read technology and sequenced 17 samples collected in France with high-coverage Illumina reads. We found two D. rosae peripatric lineages that differed in the level of recombination and homozygosity. The first D. rosae lineage showed a recombination rate that was 13.2 times higher and a per-individual heterozygosity that was 1.6 times higher. We inferred that genes under negative selection were enriched in functions related to male traits ( sperm competition, insemination, and copulation gene ontology terms) in the more recombining lineage, while in the less recombining form, the same lineage genes showed traces pointing towards balancing or relaxed selection. Thus, although D. rosae reproduces mainly by thelytoky, selection may act to maintain sexual reproduction. SignificanceMany organisms can alternate between sexual and asexual reproduction in different ways. Sexual reproduction is essential to creating genetic diversity for adaptation to changing environments, whereas asexual reproduction is important in the short term and in stable environments. Using genomic data, we demonstrated the existence of two lineages in the rose bedeguar wasp Diplolepis rosae previously shown to reproduce mainly by thelytokous parthenogenesis, giving almost only females. One of the lineages showed higher recombination, higher heterozygosity, and genes involved in male traits under negative selection. This could be linked to the expected advantages of maintaining sexual reproduction in natural populations.