Simple Y-Autosomal Incompatibilities Cause Hybrid Male Sterility in Reciprocal Crosses Between Drosophila virilis and D. americana

Sweigart, Andrea L.

doi:10.1534/genetics.109.112896

Cited by 42 publications

(22 citation statements)

References 78 publications

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“…simulans hybrids lack the gene and are sterile. The finding of a gene involved in reproductive isolation in the ancestral Drosophila Y chromosome suggests a simple explanation for the key role of this chromosome in several cases of reproductive isolation between Drosophila species (e.g., Pantazidis et al 1993;Sweigart 2010), especially because sex-chromosomes are much more prone than autosomes to cause imbalances in hybrids (Long et al 2012). It will be interesting to verify whether gene movements to/from the Y chromosome occurred in these species.…”

Section: Discussionmentioning

confidence: 99%

Efficient identification of Y chromosome sequences in the human and Drosophila genomes

2013

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Notwithstanding their biological importance, Y chromosomes remain poorly known in most species. A major obstacle to their study is the identification of Y chromosome sequences; due to its high content of repetitive DNA, in most genome projects, the Y chromosome sequence is fragmented into a large number of small, unmapped scaffolds. Identification of Y-linked genes among these fragments has yielded important insights about the origin and evolution of Y chromosomes, but the process is labor intensive, restricting studies to a small number of species. Apart from these fragmentary assemblies, in a few mammalian species, the euchromatic sequence of the Y is essentially complete, owing to painstaking BAC mapping and sequencing. Here we use female short-read sequencing and k-mer comparison to identify Y-linked sequences in two very different genomes, Drosophila virilis and human. Using this method, essentially all D. virilis scaffolds were unambiguously classified as Y-linked or not Y-linked. We found 800 new scaffolds (totaling 8.5 Mbp), and four new genes in the Y chromosome of D. virilis, including JYalpha, a gene involved in hybrid male sterility. Our results also strongly support the preponderance of gene gains over gene losses in the evolution of the Drosophila Y. In the intensively studied human genome, used here as a positive control, we recovered all previously known genes or gene families, plus a small amount (283 kb) of new, unfinished sequence. Hence, this method works in large and complex genomes and can be applied to any species with sex chromosomes.

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Section: Discussionmentioning

confidence: 99%

Efficient identification of Y chromosome sequences in the human and Drosophila genomes

2013

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“…Finally, our model assumes that coevolving incompatibilities or BDM incompatibilities arising from adaptive evolution frequently occur between species. Accumulating evidence suggests that incompatibilities arising from coevolution may be common [30,36,[83][84][85][86]. For example, in marine copepods, coevolution between cytochrome c and cytochrome c oxidase results in a reciprocal breakdown of protein function in hybrids [86].…”

Section: Discussionmentioning

confidence: 99%

Reproductive isolation of hybrid populations driven by genetic incompatibilities

Schumer

Cui

Rosenthal

et al. 2014

Preprint

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Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model. Author SummaryUnderstanding the origin of species is one of the central challenges in evolutionary biology. It has been suggested that hybridization could generate new species because hybrids can display novel combinations of traits that induce reproductive isolation from their parental species (called "hybrid speciation"). Existing models predict that this should only occur in special cases, and indeed there have been only few well-supported examples. We describe a new model of hybrid reproductive isolation that results from selection against genetic incompatibilities in hybrids, which are predicted to be common. Simulations reveal that hybrid populations rapidly and frequently become isolated from parental species by fixing combinations of genes that hinder successful reproduction with parental species.

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“…Second, in taxa with XY males (e.g., Drosophila and mammals), the contribution of the X chromosome to hybrid male sterility is typically disproportionately large relative to that of the autosomes (the "large X effect" Coyne and Orr 1989;Coyne 1992;Masly and Presgraves 2007). While Y-linked effects are less prevalent, the Y chromosome is responsible for male sterility in multiple crosses between Drosophila species pairs (Coyne 1985;Sweigart 2010; reviewed in Turelli and Orr 2000;Coyne and Orr 2004). In mammals, however, the potential contribution of the Y to hybrid male sterility has received considerably less attention (but see Eicher et al 1982;Geraldes et al 2008).…”

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confidence: 99%

The Contribution of the Y Chromosome to Hybrid Male Sterility in House Mice

et al. 2012

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Hybrid sterility in the heterogametic sex is a common feature of speciation in animals. In house mice, the contribution of the Mus musculus musculus X chromosome to hybrid male sterility is large. It is not known, however, whether F 1 male sterility is caused by X-Y or X-autosome incompatibilities or a combination of both. We investigated the contribution of the M. musculus domesticus Y chromosome to hybrid male sterility in a cross between wild-derived strains in which males with a M. m. musculus X chromosome and M. m. domesticus Y chromosome are partially sterile, while males from the reciprocal cross are reproductively normal. We used eight X introgression lines to combine different X chromosome genotypes with different Y chromosomes on an F 1 autosomal background, and we measured a suite of male reproductive traits. Reproductive deficits were observed in most F 1 males, regardless of Y chromosome genotype. Nonetheless, we found evidence for a negative interaction between the M. m. domesticus Y and an interval on the M. m. musculus X that resulted in abnormal sperm morphology. Therefore, although F 1 male sterility appears to be caused mainly by Xautosome incompatibilities, X-Y incompatibilities contribute to some aspects of sterility.

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Simple Y-Autosomal Incompatibilities Cause Hybrid Male Sterility in Reciprocal Crosses Between Drosophila virilis and D. americana

Cited by 42 publications

References 78 publications

Efficient identification of Y chromosome sequences in the human and Drosophila genomes

Efficient identification of Y chromosome sequences in the human and Drosophila genomes

Reproductive isolation of hybrid populations driven by genetic incompatibilities

The Contribution of the Y Chromosome to Hybrid Male Sterility in House Mice

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