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. Even after the loss of male individuals, males can survive on the genomes; in fact, rarely occurring males were described in many asexual lineages. Theoretical predictions suggest that genes related to male sexual traits in parthenogenetic lineages will decay over long evolutionary times free from the pressure of stabilizing selection. However, in many cases, such rare males are potentially functional. In this study, we investigated the functionality of rare males in the Japanese parthenogenetic stick insect,Ramulus mikado. Rarely occurring males in the species exhibited the external and anatomical morphology typical in stick insect males, and vigorously and successfully performed mating behaviors with conspecific females; nevertheless, no paternal genotypes were detected in the offspring; all embryos were genetically identical to their mothers. Our histological observation demonstrated that females received a spermatophore without sperms in their copulatory pouch, and revealed that in a male, spermatogenesis was completely deformed. These results suggest the irreversible clonal reproduction ofR. mikadodue to compromised male function. Our present study provides the first case of evident dysfunction in rare males of stick insects, illuminating the degenerative evolution of sexual traits in asexual lineages.

Phylogeographical evidence for historical long-distance dispersal in the flightless stick insect Ramulus mikado

“…This pattern, also observed in genome-wide SNP data (electronic supplementary material, figure S2), suggests the predominance of asexual reproduction, though historical cryptic gene flow cannot be excluded [ 61 ]. This assumption is consistent with not only the female predominance in R. mikado [ 22 ] but also the non-functionality of the rare males [ 62 ]. The pattern of heterozygosity contrasts with terminal fusion automixis or gamete duplication, causing tremendous heterozygosity loss [ 63 , 64 ].…”

“…The pattern of heterozygosity contrasts with terminal fusion automixis or gamete duplication, causing tremendous heterozygosity loss [ 63 , 64 ]. Automixis with central fusion seems most plausible, as SSR analysis revealed mothers and offspring (embryos) mostly shared genotypes, with rare heterozygous to homozygous transitions due to recombination [ 62 ]. The mixture of highly heterozygous and homozygous loci probably results from varying recombination probabilities by loci [ 64 ].…”