Evidence for cryptic sex in parthenogenetic stick insects of the genus Timema

Abstract

Obligately parthenogenetic species are expected to be short lived since the lack of sex and recombination should translate into a slower adaptation rate and increased accumulation of deleterious alleles. Some, however, are thought to have been reproducing without males for millions of years. It is not clear how these old parthenogens can escape the predicted long-term costs of parthenogenesis, but an obvious explanation is cryptic sex. In this study, we screen for signatures of cryptic sex in eight populations of four parthenogenetic species of Timema stick insects, some estimated to be older than 1 Myr. Low genotype diversity, homozygosity of individuals and high linkage disequilibrium (LD) unaffected by marker distances support exclusively parthenogenetic reproduction in six populations. However, in two populations (namely, of the species Timema douglasi and T. monikensis ) we find strong evidence for cryptic sex, most likely mediated by rare males. These populations had comparatively high genotype diversities, lower LD, and a clear LD decay with genetic distance. Rare sex in species that are otherwise largely parthenogenetic could help explain the unusual success of parthenogenesis in the Timema genus and raises the question whether episodes of rare sex are in fact the simplest explanation for the persistence of many old parthenogens in nature.

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

“…The evolutionary persistence of parthenogenesis has long been discussed (Judson & Normark 1996, Schurko et al 2009), and recent studies have shown evidence of occasional sexual reproduction in the parthenogenetic species that were thought to have reproduced solely parthenogenetically for millions of years (Vakhrusheva et al 2020, Boyer et al 2021, Freitas et al 2023) (but see [Kearney et al 2022]). Therefore, obligately parthenogenetic species with a long history may still have the possibility of utilizing or returning to sexual reproduction.…”

“…All these results strongly suggest that R. mikado could no longer return to sexual reproduction. Although not easy to verify, the plasticity of reproductive modes is critical to explain how old or ancient parthenogenetic lineages can avoid the long-term costs of asexuality (Boyer et al 2021, Freitas et al 2023). In this mean, the present study provided unique insights into the evolution and the consequence of the loss of sex.…”

“…The existence of ancient parthenogens challenges the idea that obligately parthenogenetic species should be short-lived due to the lack of sex and recombination, resulting in a reduced rate of adaptation and increased accumulation of deleterious mutations (Judson & Normark 1996). However, rare sex, which is theoretically predicted to be sufficient to mitigate the long-term costs of parthenogenesis (reviewed in D’Souza & Michiels 2010), has been recently detected in several species with obligate parthenogenesis (Vakhrusheva et al 2020, Boyer et al 2021, Freitas et al 2023, but see Kearney et al 2022). Therefore, variation in the reproductive modes, including occasional sex rather than the classical bimodal obligate sex and obligate parthenogenesis pattern, should be considered to improve our understanding of the evolutionary persistence of parthenogenesis.…”

“…Even after the loss of male individuals, males can often survive in the genomes; in fact, rarely occurring males have been described in many asexual lineages (van der Kooi & Schwander 2014) and are suspected to mediate the rare sex events (Vakhrusheva et al 2020, Boyer et al 2021, Freitas et al 2023). In predominantly parthenogenetic species, females have substantially reduced opportunities for mating with males and have ultimately lost it during evolution (van der Kooi & Schwander 2014, Rayner et al 2022).…”

“…Schwander et al (2013) reported functional males in ancient asexual species of Timema , and that such males can copulate with the females of sister sexual species and successfully produce offspring. Furthermore, a recent study detected evidence of rare sex in asexual Timema , which is most likely mediated by rare males (Freitas et al 2023). In a parthenogenetic strain of the laboratory stick insect, Carausius morosus , with a history of about 100 years, rare males have normal sperm as well as abnormal spermatids in their testis (Pehani 1925, Pijnacker 1964).…”