Genome evolution in a putatively asexual wasp

Abstract

Asexual lineages are destined for extinction--a result predicted by theory and revealed in practice. Short-term benefits of asexuality are eventually outstripped by their fitness costs: losses of sex and recombination are together expected to reduce efficacy of selection, increase mutation load, and thus, lower fitness. We characterized genomic patterns of accumulating mutations in Diachasma muliebre, a parasitic wasp that has apparently lost sex, an inference supported by many decades of field collections of 1000s of individuals in which only females were found. The split between D. muliebre and its closest sexual relative, Diachasma ferrugineum, is quite recent, allowing us to observe initial events in the evolution of this putative asexual species. First, we find a faster rate of molecular evolution across the D. muliebre genome. In addition, we observed a marked excess of replacement nucleotide substitutions in orthologous genes in the putatively asexual D. muliebre when compared to D. ferrugineum. This pattern directly indicates genome-wide relaxed selection in this young, putatively asexual species, the resulting mutational load from which is expected to ultimately lead to extinction. However, these genomic effects occur in the presence of genomic recombination initially detected by a previous study and also supported by analyses of genome-wide substitution rates within codons. In addition, following completion of the genome sequence and its analysis, we discovered two D. muliebre males, suggesting the possibility of rare sex in this species. Haplodiploid animals, including the sexual ancestors of D. muliebre, bear small genetic loads, likely making their initial transitions to asexuality relatively benign. Paradoxically, an elevated rate of mutation accumulation resulting from asexuality, when accompanied by retention of recombination and/or rare sex, could actually be beneficial: we hypothesize that the novel variation introduced by mutation along with limited shuffling of genes may facilitate initial adaptation and extend persistence of such lineages.