Reduced effectiveness of purifying selection on new mutations in a parthenogenic terrestrial isopod (Trichoniscus pusillus)

Abstract

The "paradox of sex" refers to the question of why sexual reproduction is maintained in the wild, despite how costly it is compared to asexual reproduction. Because of these costs, one would suspect nature would select for asexual reproduction, yet sex seems to be continually selected for. Multiple hypotheses have been proposed to explain this incongruence, including the niche differentiation hypothesis, the Red Queen hypothesis, and accumulation of harmful mutations in asexual species due to inefficient purifying selection. This study focuses on the accumulation of mutations in the closely related terrestrial isopod species Trichoniscus pusillus, which has sexual diploid and parthenogenic triploid forms, and Hyloniscus riparius, an obligately sexual relative. We surveyed sex ratios of both species in an upstate New York population and obtained RNA-seq data from wild-caught individuals of both species to examine within- and between-species patterns of molecular evolution in protein-coding genes. The sex ratio and RNA-seq data together provide strong evidence that this T. pusillus population is entirely asexual and triploid, while the H. riparius population is sexual and diploid. Although all wild-caught T. pusillus individuals used for sequencing shared identical genotypes at nearly all SNPs, supporting a clonal origin for this population, heterozygosity and SNP density were much higher in T. pusillus than in the sexually reproducing H. riparius, suggesting this parthenogenic lineage may have arisen via mating between two divergent diploid lineages. Between-species sequence comparisons showed no evidence of ineffective purifying selection in the asexual T. pusillus lineage, as measured by the ratio of nonsynonymous to synonymous substitutions (dN/dS ratios). Likewise, there was no difference between T. pusillus and H. riparius in the ratios of nonsynonyous to synonymous SNPs overall (pN/pS). However, pN/pS ratios in T. pusillus were significantly higher when considering only SNPs that may have arisen via recent mutation after the transition to parthenogenesis. Thus, these recent SNPs support the hypothesis that purifying selection is less effective against new mutations in asexual lineages, but that this only becomes apparent over long time scales. This system provides a useful model for future studies on the evolutionary tradeoffs between sexual and asexual reproduction in nature. SignificanceAsexual organisms are expected to have several key evolutionary advantages, most multicellular organisms reproduce sexually. One hypothesis to explain why sex is so common despite its costs proposes that recombination allows selection to remove harmful mutations from sexual populations more efficiently. We tested this hypothesis by looking at sequence variants in expressed genes in a novel study system, an asexual terrestrial isopod crustacean and a close sexual relative. Our results support the hypothesis that selection is less effective at filtering out harmful mutations in asexual organisms, but that longer time scales may be needed for this cost of asexual reproduction to become substantial.