Fruitless mating with the exes: the irreversible parthenogenesis in a stick insect

Abstract

Parthenogenetic lineages, common in many animals, have sparked debate about their evolutionary persistence. While asexuality is expected to ensure reproductive assurance and provide a demographic advantage, parthenogens should suffer from the lack of gene shuffling with other individuals. On the other hand, occasional sexual reproduction has been theoretically predicted to be enough to mitigate the long-term costs of parthenogenesis. Recent studies have revealed instances of cryptic sex in some old parthenogenetic lineages, which is most likely mediated by rarely occurring males. Unlike female traits that rapidly become vestigial under asexuality, traits in males have been predicted to slowly decay due to the accumulation of neutral mutations over long evolutionary times. In fact, rare males often retain sexual functions, raising questions about the asexuality of these long-standing parthenogenetic lineages. Here, we intensively examined the possibility of sexual reproduction in the Japanese common stick insect, Ramulus mikado, which was also suggested to be an old parthenogen in our previous work. While asexual female reproduction appears to be quite predominant throughout Japan, we fortunately obtained the rare males from the field. These males exhibited typical stick insect male morphology and engaged in mating behaviors with conspecific females. However, no paternal-specific alleles were detected in the offspring; all embryos showed genotypes identical to their mothers. Our histological observations on a few males revealed that they had no sperm in their reproductive organs, although the degree of decay may be different among the lineages. We also found that females have sexual organs with signs of degeneration. All these results demonstrate the irreversible asexual reproduction of R. mikado and indicate their long history as a parthenogenetic species. Our present study provides unique insights into the maintenance of parthenogenesis and degenerative evolution of sexual traits in ancient asexual lineages.