Faster rates of molecular sequence evolution in reproduction-related genes and in species with hypodermic sperm morphologies

Abstract Sexual selection is expected to drive the evolution of many striking behaviours and morphologies, leaving signatures of selection at loci underlying these phenotypes. However, relatively few studies have contrasted molecular sequence evolution at such loci across lineages that differ in their sexual selection context. Our comparative genomics study of Macrostomum, a large genus of free-living simultaneously hermaphroditic flatworms, takes advantage of functional annotations from the model species, M. lignano, and transcriptome assemblies of 97 congeners. We compare molecular sequence evolution in species with contrasting sperm morphologies, which are strongly associated with multiple convergent shifts in the mating strategy and thus reflect the sexual selection context in Macrostomum. The sperm of most reciprocally mating species carry lateral bristles, likely functioning as anchoring mechanisms against post-copulatory sperm removal. Hypodermically mating species lack these bristles, potentially as adaptations to a different environment experienced by hypodermic sperm. We document faster molecular sequence evolution in reproduction-related, compared to ubiquitously-expressed, genes across all sperm morphologies, consistent with more intense selection acting on the former. Furthermore, we observed faster molecular sequence evolution in species with hypodermic sperm morphologies, in both reproduction-related and ubiquitously-expressed genes. These genome-wide patterns suggest that shifts to hypodermic mating reduce the efficiency of selection, possibly due to higher selfing rates in hypodermically mating species. Moreover, we find little evidence for convergent amino acid changes across species. We provide the first comprehensive comparative analysis of molecular sequence evolution in a group of simultaneously hermaphroditic animals, across well-replicated contrasts of lineages with divergent sperm morphologies.