Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods

Why and how sexual reproduction is maintained in natural populations, the so-called "queen of problems," is a key unanswered question in evolutionary biology. Recent efforts to solve the problem of sex have often emphasized results generated from laboratory settings. Here, we use a survey of representative "sex in the wild" literature to review and synthesize the outcomes of empirical studies focused on natural populations. Especially notable results included relatively strong support for mechanisms involving niche differentiation and a near absence of attention to adaptive evolution. Support for a major role of parasites is largely confined to a single study system, and only three systems contribute most of the support for mutation accumulation hypotheses. This evidence for taxon specificity suggests that outcomes of particular studies should not be more broadly extrapolated without extreme caution. We conclude by suggesting steps forward, highlighting tests of niche differentiation mechanisms in both laboratory and nature, and empirical evaluation of adaptive evolution-focused hypotheses in the wild. We also emphasize the value of leveraging the growing body of genomic resources for nonmodel taxa to address whether the clearance of harmful mutations and spread of beneficial variants in natural populations proceeds as expected under various hypotheses for sex.

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“…; van der Kooi et al. ) to detect associations with, or consequences of, reproductive mode variation that apply across taxa.…”

Section: Resultsmentioning

confidence: 99%

Sex in the wild: How and why field-based studies contribute to solving the problem of sex*

et al. 2018

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“…One explanation is that social hybridogenesis was selected for in populations with clonal queens because of the fitness payoff of outbreeding in workers. Obligate crossing between divergent gene pools results in very high worker heterozygosity, which may improve colony fitness, possibly through heterosis (Burke & Arnold, 2001;Cahan, Julian, Schwander, & Keller, 2006;Umphrey, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…Pure lineage queens arise either from mating between partners from the same genetic lineage or from thelytokous parthenogenesis, while males are pure lineage sons produced by arrhenotokous parthenogenesis as is typical for hymenopterans. Interestingly, this system may allow colonies to benefit from superior hybrid workers due to hybrid vigour without the negative consequences of hybridization on reproduction as both queens and males are nonhybrids (Burke & Arnold, 2001;Umphrey, 2006). Several ant species have independently evolved such a mode of reproduction, called "social hybridogenesis".…”

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confidence: 99%

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

et al. 2019

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Over the last decade, genetic studies on social insects have revealed a remarkable diversity of unusual reproductive strategies, such as male clonality, female clonality, and social hybridogenesis. In this context, Cataglyphis desert ants are useful models because of their unique reproductive systems. In several species, queens conditionally use sexual reproduction and parthenogenesis to produce sterile workers and reproductive queens, respectively. In social hybridogenesis, two distinct genetic lineages coexist within a population, and workers result from mating between partners of different lineages; in contrast, queens and males are both produced asexually by parthenogenesis. Consequently, nonreproductive workers are all interlineage hybrids, whereas reproductives are all pure lineage individuals. Here, we characterized the reproductive systems of 11 species to investigate the distribution of the conditional use of sex and social hybridogenesis in Cataglyphis. We identified one new case in which sexual reproduction was conditionally used in the absence of dependent‐lineage reproduction. We also discovered five new instances of social hybridogenesis. Based on our phylogenetic analyses, we inferred that both the conditional use of sex and social hybridogenesis independently evolved multiple times in the genus Cataglyphis.

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“…Wolbachia, 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).…”

Section: Endosymbiont Infection Infection With Intracellular Endosymmentioning

confidence: 99%

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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Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods

Cited by 62 publications

References 57 publications

Sex in the wild: How and why field-based studies contribute to solving the problem of sex*

Sex in the wild: How and why field-based studies contribute to solving the problem of sex*

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

Genomic features of parthenogenetic animals

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