Local dynamics of a fast‐evolving <i>sex‐ratio</i> system in <i><scp>D</scp>rosophila simulans</i>

Bastide, Héloïse; Gérard, P.; Ogereau, David; Cazemajor, Michel; Montchamp‐Moreau, Catherine

doi:10.1111/mec.12492

Cited by 28 publications

(35 citation statements)

References 73 publications

(96 reference statements)

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“…Consequently, individual selection should contribute relatively modestly to among‐population trait variation. Conversely, selfish elements with different transmission patterns have opposing fitness optima, and conflict can result in rapid shifts between these peaks (Bastide, Gerard, Ogereau, Cazemajor, & Montchamp‐Moreau, 2013). Interacting populations that are situated at different points in the adaptive landscape will differ significantly in traits related to the transmission of these elements, and these traits may contribute to the competitive ability of populations.…”

Section: Discussionmentioning

confidence: 99%

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Rood

Freedberg

2016

Ecology and Evolution

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Maternal sex ratio distorters (MSDs) are selfish elements that enhance their transmission by biasing their host's sex allocation in favor of females. While previous models have predicted that the female‐biased populations resulting from sex ratio distortion can benefit from enhanced productivity, these models neglect Fisherian selection for nuclear suppressors, an unrealistic assumption in most systems. We used individual‐based computer simulation modeling to explore the intragenomic conflict between sex ratio distorters and their suppressors and explored the impacts of these dynamics on population‐level competition between species characterized by MSDs and those lacking them. The conflict between distorters and suppressors was capable of producing large cyclical fluctuations in the population sex ratio and reproductive rate. Despite fitness costs associated with the distorters and suppressors, MSD populations often exhibited enhanced productivity and outcompeted non‐MSD populations in single and multiple‐population competition simulations. Notably, the conflict itself is beneficial to the success of populations, as sex ratio oscillations limit the competitive deficits associated with prolonged periods of male rarity. Although intragenomic conflict has been historically viewed as deleterious to populations, our results suggest that distorter–suppressor conflict can provide population‐level advantages, potentially helping to explain the persistence of sex ratio distorters in a range of taxa.

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Section: Discussionmentioning

confidence: 99%

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Rood

Freedberg

2016

Ecology and Evolution

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“…According to the estimated age of Dp SR (<500 y) (14), the spread of the Paris drivers is recent, and their evolution in populations is very fast (20,21). Through its own spreading, together with Dp SR , the HP1D2 SR allele carried by X SR4 (lacking CSD) became the most frequent allele in the Malagasy populations (based on the selective sweep studied in refs.…”

Section: Hp1d2 Ismentioning

confidence: 99%

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Helleu

Gérard

Dubruille

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-linked heterochromatin protein 1 (HP1) gene, HP1D2, plays a key role in the classical Paris sex-ratio (SR) meiotic drive occurring in Drosophila simulans. Driver HP1D2 alleles prevent the segregation of the Y chromatids during meiosis II, causing female-biased sex ratio in progeny. HP1D2 accumulates on the heterochromatic Y chromosome in male germ cells, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modification. We show that Paris SR drive is a consequence of dysfunctional HP1D2 alleles that fail to prepare the Y chromosome for meiosis, thus providing evidence that the rapid evolution of genes controlling the heterochromatin structure can be a significant source of intragenomic conflicts. meiotic drive | intragenomic conflict | heterochromatin | sex chromosomes

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“…There are hints that segregation distorters may be prevalent in natural populations (Jaenike 2001;Reed et al 2005;Bastide et al 2013), but few specific loci have been identified. Hybrid backgrounds may reveal these loci, if suppressors fail to function or are separated from their targets by segregation (Mercot et al 1995).…”

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confidence: 99%

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

et al. 2014

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The abundance and composition of heterochromatin changes rapidly between species and contributes to hybrid incompatibility and reproductive isolation. Heterochromatin differences may also destabilize chromosome segregation and cause meiotic drive, the non-Mendelian segregation of homologous chromosomes. Here we use a range of genetic and cytological assays to examine the meiotic properties of a Drosophila simulans chromosome 4 (sim-IV) introgressed into D. melanogaster. These two species differ by 12-13% at synonymous sites and several genes essential for chromosome segregation have experienced recurrent adaptive evolution since their divergence. Furthermore, their chromosome 4s are visibly different due to heterochromatin divergence, including in the AATAT pericentromeric satellite DNA. We find a visible imbalance in the positioning of the two chromosome 4s in sim-IV/mel-IV heterozygote and also replicate this finding with a D. melanogaster 4 containing a heterochromatic deletion. These results demonstrate that heterochromatin abundance can have a visible effect on chromosome positioning during meiosis. Despite this effect, however, we find that sim-IV segregates normally in both diplo and triplo 4 D. melanogaster females and does not experience elevated nondisjunction. We conclude that segregation abnormalities and a high level of meiotic drive are not inevitable byproducts of extensive heterochromatin divergence. Animal chromosomes typically contain large amounts of noncoding repetitive DNA that nevertheless varies widely between species. This variation may potentially induce non-Mendelian transmission of chromosomes. We have examined the meiotic properties and transmission of a highly diverged chromosome 4 from a foreign species within the fruitfly Drosophila melanogaster. This chromosome has substantially less of a simple sequence repeat than does D. melanogaster 4, and we find that this difference results in altered positioning when chromosomes align during meiosis. Yet this foreign chromosome segregates at normal frequencies, demonstrating that chromosome segregation can be robust to major differences in repetitive DNA abundance.H ETEROCHROMATIC repeats at and near telomeres and centromeres turn over rapidly at short evolutionary time scales (Charlesworth et al. 1994). A subset of genes involved in meiosis, chromosome and chromatin function, and transposable element defense also show high rates of divergence between sibling species, often with accompanying signatures of adaptive evolution Begun et al. 2007;Larracuente et al. 2008;Anderson et al. 2009;Obbard et al. 2009;Raffa et al. 2011;Langley et al. 2012). These patterns suggest that organisms need to mount a continual adaptive response to suppress deleterious consequences caused by heterochromatic repetitive DNAs. Satellite DNAs and transposable elements, the major components of heterochromatin, can increase their copy numbers by unequal crossing over and transposition. These expansions can reduce fitness by increasing genome size and rates of...

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Local dynamics of a fast‐evolving sex‐ratio system in Drosophila simulans

Cited by 28 publications

References 73 publications

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Intragenomic conflict produces sex ratio dynamics that favor maternal sex ratio distorters

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

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