Consequences of Asexuality in Natural Populations: Insights from Stick Insects

Bast, Jens; Parker, Darren J.; Dumas, Zoé; Jalvingh, Kirsten M.; Van, Patrick Tran; Jaroň, Kamil S.; Figuet, Emeric; Brandt, Alexander; Galtier, Nicolas; Schwander, Tanja

doi:10.1093/molbev/msy058

Cited by 67 publications

(91 citation statements)

References 64 publications

(83 reference statements)

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“…It was therefore not possible to analyze these genome features in the present study. However, the prediction that deleterious mutations accumulate more rapidly in asexual than sexual lineages has been tested in over twenty different groups of asexual species (reviewed in [51], plus four additional studies published since [17,23,52,53]), with results generally supporting the prediction.…”

Section: Mutation Accumulation and Positive Selectionmentioning

confidence: 99%

“…However, in only eight studies were the tests conducted genome-wide, while tests in the remaining studies were based on only one or a few genes. Note that four [52,[54][55][56] of the genome-wide studies were based on transcriptomes and are therefore not included in our systematic reanalysis. Among the genome-wide tests, results are much more mixed than among the studies on few genes, raising the question whether the latter are representative of the genome as a whole.…”

Section: Mutation Accumulation and Positive Selectionmentioning

confidence: 99%

“…Among the genome-wide tests, results are much more mixed than among the studies on few genes, raising the question whether the latter are representative of the genome as a whole. Specifically, only two of the eight genomewide studies support deleterious mutation accumulation in asexuals (stick insects and evening-primroses) [52,54]. Moreover, two studies found more deleterious mutation accumulation in sexual than asexual taxa (parasitoid wasps and oribatid mites) [21,55], while the four remaining ones found no differences between sexual and asexual taxa [17,23,27,56].…”

Section: Mutation Accumulation and Positive Selectionmentioning

confidence: 99%

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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: Mutation Accumulation and Positive Selectionmentioning

confidence: 99%

Section: Mutation Accumulation and Positive Selectionmentioning

confidence: 99%

Section: Mutation Accumulation and Positive Selectionmentioning

confidence: 99%

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Genomic features of parthenogenetic animals

Jaroň

Bast²,

Nowell

et al. 2018

Preprint

Self Cite

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“…However, when Ne for neutral sites is greatly reduced by selection at linked sites, the extent of randomly generated LD between neutral and selected sites will be considerably enhanced, and LD is the driving force for AOD [5]. The properties of genomes or genomic regions with low rates of genetic recombination are of considerable interest for a range of biological questions, including evolution and variation in bacteria [38,39], asexual higher organisms [40,41], organisms with high rates of self-fertilisation [42,43], and Y and W chromosomes [44][45][46][47]. There is a general expectation that genetic diversity and molecular signatures of adaptive evolution should be greatly reduced in such systems, as a result of selection at linked sites.…”

Section: Linkage Disequilibrium Patterns and A Further Test For Aodmentioning

confidence: 99%

Patterns of genetic variability in genomic regions with low rates of recombination

Becher

Jackson

Charlesworth

2019

Preprint

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Surveys of DNA sequence variation have shown that the level of genetic variability in a genomic region is often strongly positively correlated with its rate of crossing over (CO) [1][2][3]. This pattern is caused by selection acting on linked sites, which reduces genetic variability and can also cause the frequency distribution of segregating variants to contain more rare variants than expected without selection (skew). These effects of selection may involve the spread of beneficial mutations (selective sweeps, SSWs), the elimination of deleterious mutations (background selection, BGS) or both together, and are expected to be stronger with lower rates of crossing over [1][2][3]. However, in a recent study of human populations, the skew was reduced in the lowest CO regions compared with regions with somewhat higher CO rates [4]. A similar pattern is seen in the population genomic studies of Drosophila simulans described here. We propose an explanation for this paradoxical observation, and validate it using computer simulations. This explanation is based on the finding that partially recessive, linked deleterious mutations can increase rather than reduce neutral variability when the product of the effective population size (N e ) and the selection coefficient against homozygous carriers of mutations (s) is ≤ 1, i.e. there is associative overdominance (AOD) rather than BGS [5]. We show that AOD can operate in a genomic region with a low rate of CO, opening up a new perspective on how selection affects patterns of variability at linked sites. Results and Discussion Diversity Statistics in Relation to CO Rates in Drosophila simulansThe top two panels of Figure 1 show the relations between the rate of crossing over and mean pairwise diversity at four-fold degenerate nucleotide sites (π 4 ), for two populations of Drosophila simulans. Consistent with previous studies of many species [1-3, 6], there is a significant positive relation between CO rate and nucleotide site diversity for both X chromosome (X) and autosomes (A). As reported previously [7], X has much lower diversity than A for all bins of CO rates. Diversity is higher for the Madagascan than the Kenyan population, consistent with the latter having been founded as a relatively small population by flies descended from the putatively ancestral Madagascan population [7].The bottom panels of Figure 1 show the relations between CO rate and a measure of the skew of the site frequency spectrum (SFS) towards rare variants, Δθwhere π 4 and θw4 are the estimates of diversity based on the mean pairwise difference between alleles [8] and the number of segregating sites [9], respectively. Other measures of skew behave similarly (Supplemental Figure S1). As was also found in a Rwandan population of D. melanogaster [10], there is much greater skew on X than A, although the absolute level of skew for both X and A is much higher than in D. melanogaster, suggesting a more intense recent population expansion in D. simulans. The skew is also larger in the Madagascan than the Kenya...

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“…The maintenance of sexual reproduction in nature has been addressed by contrasting the traits of sexual and related asexual lineages, and ideal study systems have natural replication, with independently derived populations displaying contrasting reproductive strategies (see reviews; Neiman et al, 2018;Neiman & Schwander, 2011). Examples of this circumstance include the snail Potamopyrgus antipodarum whose different clonal lineages are derived from the same sexual species (Gibson et al, 2016;Jokela et al, 2009), and Timema stick insects that contain multiple species pairs of sexual/ asexual lineages (Bast et al, 2018;Schwander & Crespi, 2009;Schwander, Henry, & Crespi, 2011). An optimal study system would provide replication but lack the confounding effects of ploidy variation and hybridisation that exist in many study systems (Kearney, 2005).…”

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confidence: 99%

Loss and gain of sexual reproduction in the same stick insect

2019

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The outcome of competition between different reproductive strategies within a single species can be used to infer selective advantage of the winning strategy. Where multiple populations have independently lost or gained sexual reproduction it is possible to investigate whether the advantage is contingent on local conditions. In the New Zealand stick insect Clitarchus hookeri, three populations are distinguished by recent change in reproductive strategy and we determine their likely origins. One parthenogenetic population has established in the United Kingdom and we provide evidence that sexual reproduction has been lost in this population. We identify the sexual population from which the parthenogenetic population was derived, but show that the UK females have a post‐mating barrier to fertilisation. We also demonstrate that two sexual populations have recently arisen in New Zealand within the natural range of the mtDNA lineage that otherwise characterizes parthenogenesis in this species. We infer independent origins of males at these two locations using microsatellite genotypes. In one population, a mixture of local and nonlocal alleles suggested males were the result of invasion. Males in another population were most probably the result of loss of an X chromosome that produced a male phenotype in situ. Two successful switches in reproductive strategy suggest local competitive advantage for outcrossing over parthenogenetic reproduction. Clitarchus hookeri provides remarkable evidence of repeated and rapid changes in reproductive strategy, with competitive outcomes dependent on local conditions.

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Consequences of Asexuality in Natural Populations: Insights from Stick Insects

Cited by 67 publications

References 64 publications

Genomic features of parthenogenetic animals

Genomic features of parthenogenetic animals

Patterns of genetic variability in genomic regions with low rates of recombination

Loss and gain of sexual reproduction in the same stick insect

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