Neutral and selection-driven decay of sexual traits in asexual stick insects

Schwander, Tanja; Crespi, Bernard J.; Gries, Regine

doi:10.1098/rspb.2013.0823

Cited by 56 publications

(81 citation statements)

References 53 publications

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“…male-specific organs, spermatogenesis), as well as female traits involved in sexual reproduction (e.g., pheromone production, sperm storage organs) [95]. In the absence of pleiotropic effects, gene loss is expected due to mutation accumulation in the absence of purifying selection maintaining sexual traits, as well as to directional selection to reduce costly sexual traits [96]. Some gene loss consistent with these predictions is documented.…”

Section: Gene Lossmentioning

confidence: 88%

Genomic features of parthenogenetic animals

Jaroň

Bast²,

Nowell

et al. 2018

Preprint

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Evolution under asexuality is predicted to impact genomes in numerous ways, but empirical evidence remains unclear. Case studies of individual asexual animals have reported peculiar genomic features which were suggested to be caused by asexuality, including high heterozygosity, a high abundance of horizontally acquired genes, a low transposable element load, or the presence of palindromes. We systematically characterized these genomic features in published genomes of 26 asexual animals representing at least 18 independent transitions to asexuality. Surprisingly, not a single feature is systematically replicated across a majority of these transitions, suggesting that no genomic feature is characteristic of asexuality and that previously reported patterns were lineage specific rather than caused by asexuality. We found that only asexuals of hybrid origin were characterized by high heterozygosity levels. Asexuals that were not of hybrid origin appeared to be largely homozygous, independently of the cellular mechanism underlying asexuality. Overall, despite the importance of recombination rate variation for the evolution of sexual animal genomes, the genome-wide absence of recombination does not appear to have had the dramatic effects which are expected from classical theoretical models. The reasons for this are probably a combination of lineage-specific patterns, impact of the origin of asexuality, and a survivorship bias of asexual lineages. Box 1: Transitions to asexualityMeiotic sex and recombination evolved once in the common ancestor of eukaryotes [41].Asexual animals therefore derive from a sexual ancestor, but how transitions from sexual to asexual reproduction occur can vary and have different expected consequences for the genome [13]. Hybrid origin:Hybridization between sexual species can generate hybrid females that reproduce asexually [13,42]. Asexuality caused by hybridization can generate a highly heterozygous genome, depending on the divergence between the parental sexual species prior to hybridization. Hybridization can also result in a burst of transposable element activity [12]. Intraspecific origins: Endosymbiont infection. Infection with intracellular endosymbionts (such asWolbachia, Cardinium or Rickettsia) can cause asexuality, a pattern that is frequent in species with haplodiploid sex determination [43]. This type of transition often (but not always) results in fully homozygous lineages because induction of asexuality frequently occurs via gamete duplication (see Box 2). Spontaneous mutations/Contagious asexuality. Spontaneous mutations can alsounderlie transitions from sexual to asexual reproduction. In addition, asexual females of some species produce males that mate with females of sexual lineages, and thereby generate new asexual strains (contagious asexuality). In both cases, the genomes of incipient asexual lineages are expected to be very similar to those of their sexual relatives and subsequent changes should be largely driven by the cellular mechanism underlying asexuality (Box 2). an...

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Section: Gene Lossmentioning

confidence: 88%

Genomic features of parthenogenetic animals

Jaroň

Bast²,

Nowell

et al. 2018

Preprint

Self Cite

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“…Stronger rejection behaviours in obligate parthenogens compared to sexual relatives, or sharper selection‐driven decay in traits facilitating courtship, copulation and/or fertilization, would be suggestive of this link. Such patterns already appear to occur in a number of obligately asexual taxa (van der Kooi & Schwander, ; Schwander, Crespi, Gries, & Gries, ), but further investigations would be highly valuable.…”

Section: Discussionmentioning

confidence: 99%

The paradox of obligate sex: The roles of sexual conflict and mate scarcity in transitions to facultative and obligate asexuality

Burke

Bonduriansky

2019

J of Evolutionary Biology

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The maintenance of obligate sex in animals is a long‐standing evolutionary paradox. To solve this puzzle, evolutionary models need to explain why obligately sexual populations consistently resist invasion by facultative strategies that combine the benefits of both sexual and asexual reproduction. Sexual antagonism and mate availability are thought to shape the occurrence of reproductive modes in facultative systems. But it is unclear how such factors interact with each other to influence facultative invasions and transitions to obligate asexuality. Using individual‐based models, we clarify how sexually antagonistic coevolution and mate availability affect the likelihood that a mutant allele that gives virgin females the ability to reproduce parthenogenetically will invade an obligately sexual population. We show that male coercion cannot stop the allele from spreading because mutants generally benefit by producing at least some offspring asexually prior to encountering males. We find that effects of sexual conflict can lead to positive frequency‐dependent dynamics, where the spread of the allele is promoted by effective (no‐cost) resistance when males are common, and by mate limitation when sex ratios are female‐biased. However, once the mutant allele fixes, effective coercion prevents the complete loss of sex unless linkage disequilibrium can build up between the allele and alleles for effective resistance. Our findings clarify how limitations of female resistance imposed by the genetic architecture of sexual antagonism can promote the maintenance of sexual reproduction. At the same time, our finding of widespread obligate sex when costs of parthenogenesis are high suggests that developmental constraints could contribute to the rarity of facultative reproductive strategies in nature.

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“…Stick insects have XX‐X0 sex‐determination system, and males are developing via spontaneous loss of an X chromosome during oogenesis (Schwander and Crespi ; for details, see Schwander et al. ). Karyotypes of bisexual and unisexual Timema species are well studied with no evidence for polyploidy or hybridization in both bisexual and unisexual species, except for T. shepardi (Schwander and Crespi ).…”

Section: Insecta (=Ectognatha)mentioning

confidence: 99%

“…Despite the fact, that they have extremely low fitness in natural populations, rare males were fertile and fathered offspring with bisexual sister species. Stick insects have XX-X0 sex-determination system, and males are developing via spontaneous loss of an X chromosome during oogenesis (Schwander and Crespi 2009; for details, see Schwander et al 2013).…”

Section: Orthoptera (Ensifera)mentioning

confidence: 99%

Parthenogenesis in Hexapoda: Entognatha and non-holometabolous insects

Vershinina

Kuznetsova

2016

J Zoolog Syst Evol Res

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In hexapods, unlike the majority of animals, development without fertilization is a common phenomenon. They evolved a striking diversity of unisexual reproductive types that include a variety of modes starting from spontaneous parthenogenesis in females to the production of impaternate males with different variants in between. Many reports about parthenogenetic species have accumulated over time. Here, we present a review of various parthenogenetic hexapod groups with a particular focus on their chromosome systems and ploidy level. We show that conclusions about the reproductive mode often lack solid evidence and sometimes inefficiently demonstrate how parthenogenesis is maintained in corresponding groups. In this review, basal hexapods (Protura, Collembola, Diplura), primarily wingless insect groups (‘Apterygota’) and non‐holometabolous insects are listed with references to a variety of their unisexual reproductive modes.

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Neutral and selection-driven decay of sexual traits in asexual stick insects

Cited by 56 publications

References 53 publications

Genomic features of parthenogenetic animals

Genomic features of parthenogenetic animals

The paradox of obligate sex: The roles of sexual conflict and mate scarcity in transitions to facultative and obligate asexuality

Parthenogenesis in Hexapoda: Entognatha and non-holometabolous insects

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