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

Larose, Chloé; Lavanchy, Guillaume; Freitas, Susana; Parker, Darren J.; Schwander, Tanja

doi:10.1101/2022.03.25.485836

Cited by 3 publications

(6 citation statements)

References 70 publications

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“…There was also no evidence of LD decay (Figure 3 - B, Figures S6-9), consistent with linkage between polymorphic positions and absence of recombination. Finally, individuals from all six obligately parthenogenetic populations (including the two for which LD estimates are not informative due to low polymorphism) presented consistently low heterozygosity (Figure 6), as previously shown for Timema individuals produced via parthenogenesis (Jaron et al 2022; Larose et al 2022).…”

Section: Resultssupporting

confidence: 75%

“…Given the evidence for cryptic gene flow in the T. douglasi – Manchester and T. monikensis – FS populations, we investigated whether we could identify sexually produced individuals. Parthenogenetically produced Timema individuals are largely or completely homozygous (Jaron et al 2022; Larose et al 2022). By contrast, sex between different clones would manifest as elevated heterozygosity in the resulting offspring.…”

Section: Resultsmentioning

confidence: 99%

“…These lineages vary in age, and the oldest parthenogenetic Timema is thought to have been reproducing via parthenogenesis for over 1 million years (Schwander et al 2011). Parthenogenetic Timema are very homozygous as they most likely reproduce via a form of automictic parthenogenesis where heterozygosity is completely lost each generation (Jaron et al 2022; Larose et al 2022). Rare males have been found in four of the five described parthenogenetic Timema species (Vickery and Sandoval 1999, 2001; Schwander et al 2013), and these rare “parthenogenetic” males present normal male reproductive organs, and can mate and produce offspring with sexual sister-species females, although with reduced fertility (Schwander et al 2013).…”

Section: Introductionmentioning

confidence: 99%

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

Freitas

Parker

Labédan

et al. 2023

Preprint

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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 ofTimemastick insects, some estimated to be older than 1M yrs. 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 speciesTimema douglasiandT. 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 theTimemagenus and raises the question whether episodes of rare sex are in fact the simplest explanation for the persistence of many old parthenogens in nature.

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Section: Resultssupporting

confidence: 75%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Freitas

Parker

Labédan

et al. 2023

Preprint

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“…On the flip side, that these males produce sperm that have strikingly aberrant morphology compared to sexual counterparts (Jalinsky et al, 2020) suggests that such recombination within asexual lineages might be extremely rare. Similarly, taxa thought to be obligate sexuals that give rise to asexuals may have cryptic asexual reproductive capabilities (i.e., facultative asexuality 10.3389/fevo.2022.845640 rather than obligate sexuality) and gradually transition to obligate asexuality, as had been hypothesized in Timema stick insects (Schwander and Crespi, 2009) and more recently supported with genetic evidence (Larose et al, 2022). There is nevertheless no evidence to date for facultative asexuality in P. antipodarum.…”

Section: Evidence For Little Overall Difference In Sexual Vs Asexual ...mentioning

confidence: 91%

Patterns of gene expression in ovaries of sexual vs. asexual lineages of a freshwater snail

McElroy

Soper²,

Hehman³

et al. 2022

Front. Ecol. Evol.

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Why sexual reproduction is so common when asexual reproduction should be much more efficient and less costly remains an open question in evolutionary biology. Comparisons between otherwise similar sexual and asexual taxa allow us to characterize the genetic architecture underlying asexuality, which can, in turn, illuminate how this reproductive mode transition occurred and the mechanisms by which it is maintained or disrupted. Here, we used transcriptome sequencing to compare patterns of ovarian gene expression between actively reproducing obligately sexual and obligately asexual females from multiple lineages of Potamopyrgus antipodarum, a freshwater New Zealand snail characterized by frequent separate transitions to asexuality and coexistence of otherwise similar sexual and asexual lineages. We also used these sequence data to evaluate whether population history accounts for variation in patterns of gene expression. We found that source population was a major source of gene expression variation, and likely more influential than reproductive mode. This outcome for these common garden-raised snails is strikingly similar to earlier results from field-collected snails. While we did not identify a likely set of candidate genes from expression profiles that could plausibly explain how transitions to asexuality occurred, we identified around 1,000 genes with evidence of differential expression between sexual and asexual reproductive modes, and 21 genes that appear to exhibit consistent expression differences between sexuals and asexuals across genetic backgrounds. This second smaller set of genes provides a good starting point for further exploration regarding a potential role in the transition to asexual reproduction. These results mark the first effort to characterize the causes of asexuality in P. antipodarum, demonstrate the apparently high heritability of gene expression patterns in this species, and hint that for P. antipodarum, transitions to asexuality might not necessarily be strongly associated with broad changes in gene expression.

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“…Thus, meiotic parthenogens may be on a much steeper trajectory towards extinction than mitotic ones. Parthenogenetic Panagrolaimus nematodes are obligate asexual species, unlike other parthenogenetic taxa such as stick insects where facultative parthenogenetic species occur (Larose et al , 2022).…”

Section: Introductionmentioning

confidence: 99%

Parthenogenomics: insights on mutation rates and nucleotide diversity in parthenogeneticPanagrolaimusnematodes

Villegas

Ferretti

Wiehe

et al. 2022

Preprint

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Asexual reproduction is assumed to lead to the accumulation of deleterious mutations (Mullers ratchet), and reduced heterozygosity due to the absence of recombination. Panagrolaimid nematodes display different modes of reproduction. Sexual reproduction through distinct males and females, asexual reproduction through parthenogenesis found in the genus Panagrolaimus, and hermaphroditism, found in Propanagrolaimus. Here, we compared genomic features of free-living nematode populations with different reproduction modes isolated from geographically distant regions to study genomic diversity and genome-wide differentiation. We firstly estimated genome-wide spontaneous mutation rates per genome for a polyploid parthenogenetic Panagrolaimus strain and a diploid hermaphroditic Propanagrolaimus species via mutation-accumulation-lines. Secondly, we calculated population genomic parameters including nucleotide diversity and fixation index FST between populations of asexually and sexually reproducing nematodes. Thirdly, we used phylogenetic network methods on sexually and asexually reproducing Panagrolaimus strains to understand evolutionary relationships between them. The estimated mutation rate was slightly lower for the asexual strain, as expected for taxa with this reproductive mode. Natural polyploid asexual strains revealed higher nucleotide diversity. Despite their common ancestor, a gene network revealed a high level of genetic differentiation among asexual strains. The elevated heterozygosity found in the triploid parthenogens could be explained by the third genome copy. Given their tendentially lower mutation rates it can be hypothesized that this is part of the mechanism to evade Mullers ratchet. Our findings in parthenogenetic triploid nematode populations seem to challenge common expectations of evolution under asexuality.

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

Cited by 3 publications

References 70 publications

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

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

Patterns of gene expression in ovaries of sexual vs. asexual lineages of a freshwater snail

Parthenogenomics: insights on mutation rates and nucleotide diversity in parthenogeneticPanagrolaimusnematodes

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