Evidence for cryptic gene flow in parthenogenetic stick insects of the genus<i>Timema</i>

Freitas, Susana; Parker, Darren J.; Labédan, Marjorie; Dumas, Zoé; Schwander, Tanja

doi:10.1101/2023.01.21.525009

Cited by 9 publications

(13 citation statements)

References 66 publications

(144 reference statements)

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“…Our SSR analysis shows high heterozygosity in five loci and zero or near-zero in the remaining eight loci in R. mikado (electronic supplementary material, table S3). 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].…”

Section: Discussionsupporting

confidence: 76%

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

Suetsugu,

Nozaki,

Hirota

et al. 2023

Proc. R. Soc. B.

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Exploring how organisms overcome geographical barriers to dispersal is a fundamental question in biology. Passive long-distance dispersal events, although infrequent and unpredictable, have a considerable impact on species range expansions. Despite limited active dispersal capabilities, many stick insect species have vast geographical ranges, indicating that passive long-distance dispersal is vital for their distribution. A potential mode of passive dispersal in stick insects is via the egg stage within avian digestive tracts, as suggested by experimental evidence. However, detecting such events under natural conditions is challenging due to their rarity. Therefore, to indirectly assess the potential of historical avian-mediated dispersal, we examined the population genetic structure of the flightless stick insect Ramulus mikado across Japan, based on a multifaceted molecular approach [cytochrome oxidase subunit I (COI) haplotypes, nuclear simple sequence repeat markers and genome-wide single nucleotide polymorphisms]. Subsequently, we identified unique phylogeographic patterns, including the discovery of identical COI genotypes spanning considerable distances, which substantiates the notion of passive long-distance genotypic dispersal. Overall, all the molecular data revealed the low and mostly non-significant genetic differentiation among populations, with identical or very similar genotypes across distant populations. We propose that long-distance dispersal facilitated by birds is the plausible explanation for the unique phylogeographic pattern observed in this flightless stick insect.

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Section: Discussionsupporting

confidence: 76%

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

Suetsugu,

Nozaki,

Hirota

et al. 2023

Proc. R. Soc. B.

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“…Occasional male production and re-expression of the sexual pathway in otherwise obligate parthenogens paves the way for cryptic sex, which could contribute to explaining their long-term persistence (Freitas et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?

Larose

Lavanchy

Freitas

et al. 2022

Preprint

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Transitions from obligate sex to obligate parthenogenesis have occurred repeatedly across the tree of life. Whether these transitions occur abruptly or via a transient phase of facultative parthenogenesis is rarely known. We discovered and characterised facultatively parthenogenetic populations of the North American stick insect Timema douglasi, a species in which only obligately parthenogenetic populations were known so far. These populations comprised three genetic lineages. Females from all lineages were capable of parthenogenesis (with variable efficiency) but their propensity to reproduce sexually after mating varied extensively. In all three lineages, parthenogenesis resulted in the complete loss of heterozygosity in a single generation. Obligately parthenogenetic Timema have also lost all heterozygosity, suggesting that parthenogenesis evolved via a gradual capacity increase while conserving the proximate mechanism. It is unclear whether the populations we discovered have re-evolved sex (via re-expression of existing pathways), or whether they are vestigial sexual populations in a species where all other lineages have evolved obligate parthenogenesis already. We speculate that facultative parthenogenesis may often be transient and be replaced by obligate strategies (either sex or parthenogenesis) because of a trade-off between the efficiency of the two reproductive modes.

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“…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.…”

Section: Introductionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Nozaki

Chikami

Yano

et al. 2023

Preprint

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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.

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Evidence for cryptic gene flow in parthenogenetic stick insects of the genusTimema

Cited by 9 publications

References 66 publications

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

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

Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?

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

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