Genetics and Evolution of Hybrid Male Sterility in House Mice

White, Michael A.; Stubbings, Maria; Dumont, Beth L.; Payseur, Bret A.

doi:10.1534/genetics.112.140251

Cited by 74 publications

(114 citation statements)

References 157 publications

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“…We used data from two studies that mapped QTL for hybrid male sterility between wild-derived inbred strains from the three subspecies of house mice: M. m. musculus (PWD/PhJ) and M. m. domesticus (WSB/EiJ) ) and M. m. castaneus (CAST/EiJ) and M. m. domesticus (WSB/EiJ) (White et al 2012a). These studies quantified five morphological traits strongly correlated with male fertility: testis weight, sperm density, proportion of abnormal sperm, sperm head shape, and stage VII seminiferous tubule area.…”

Section: Identifying Shared and Unique Incompatibilitiesmentioning

confidence: 99%

“…In the first approach, we considered single QTL identified by standard interval mapping in White et al (2011White et al ( , 2012a. For each QTL peak, we examined the physical positions of the maximum LOD score and the 1.5-LOD interval.…”

Section: Identifying Shared and Unique Incompatibilitiesmentioning

confidence: 99%

“…Our QTL analysis used data from previously published studies (White et al , 2012a. Sequences used to estimate the subspecies trees and branch length are from Keane et al (2011).…”

Section: Data Availabilitymentioning

confidence: 99%

“…The three subspecies diverged recently (Geraldes et al 2008(Geraldes et al , 2011White et al 2009;Duvaux et al 2011), perhaps ,350,000 years ago (Geraldes et al 2011). Two pairs of subspecies show partial reproductive isolation, particularly in the form of hybrid male sterility (Forejt and Iványi 1974;Britton-Davidian et al 2005;Vyskočilová et al 2005;Good et al 2008a;White et al 2012a), indicating speciation is in progress. House mouse subspecies also hybridize in the wild (Boursot et al 1993;Sage et al 1993;Duvaux et al 2011;Jing et al 2014), providing opportunities to connect the genetics of reproductive isolation phenotypes in the laboratory with gene flow in nature.…”

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The Pace of Hybrid Incompatibility Evolution in House Mice

2015

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Hybrids between species are often sterile or inviable. This form of reproductive isolation is thought to evolve via the accumulation of mutations that interact to reduce fitness when combined in hybrids. Mathematical formulations of this "DobzhanskyMuller model" predict an accelerating buildup of hybrid incompatibilities with divergence time (the "snowball effect"). Although the Dobzhansky-Muller model is widely accepted, the snowball effect has only been tested in two species groups. We evaluated evidence for the snowball effect in the evolution of hybrid male sterility among subspecies of house mice, a recently diverged group that shows partial reproductive isolation. We compared the history of subspecies divergence with patterns of quantitative trait loci (QTL) detected in F 2 intercrosses between two pairs of subspecies (Mus musculus domesticus with M. m. musculus and M. m. domesticus with M. m. castaneus). We used a recently developed phylogenetic comparative method to statistically measure the fit of these data to the snowball prediction. To apply this method, QTL were partitioned as either shared or unshared in the two crosses. A heuristic partitioning based on the overlap of QTL confidence intervals produced unambiguous support for the snowball effect. An alternative approach combining data among crosses favored the snowball effect for the autosomes, but a linear accumulation of incompatibilities for the X chromosome. Reasoning that the X chromosome analyses are complicated by low mapping resolution, we conclude that hybrid male sterility loci have snowballed in house mice. Our study illustrates the power of comparative genetic mapping for understanding mechanisms of speciation.

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Section: Identifying Shared and Unique Incompatibilitiesmentioning

confidence: 99%

Section: Identifying Shared and Unique Incompatibilitiesmentioning

confidence: 99%

“…Our QTL analysis used data from previously published studies (White et al , 2012a. Sequences used to estimate the subspecies trees and branch length are from Keane et al (2011).…”

Section: Data Availabilitymentioning

confidence: 99%

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The Pace of Hybrid Incompatibility Evolution in House Mice

2015

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“…Genetic studies of hybrid male sterility-the primary reproductive barrier between house mouse subspecies-support this prediction. Loci that cause F 2 sterility in crosses between M. musculus castaneus (the subspecies studied by Kousathanas et al (2014)) and M. musculus domesticus map differentially to the X chromosome (White et al 2012) and multiple X-linked loci shape F 1 and F 2 sterility in crosses between M. musculus domesticus and M. musculus musculus (Storchova et al 2004;Good et al 2008;White et al 2011). Interestingly, disruptions in MSCI are also connected to hybrid male sterility in house mice (Campbell et al 2013).…”

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Disproportionate Roles for the X Chromosome and Proteins in Adaptive Evolution

Payseur

2014

Genetics

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A daptation requires genetic variation. A complete understanding of this key evolutionary process includes identification of the mutations that confer adaptive change. High-resolution genetic dissection of particular adaptive phenotypes can pinpoint these mutations, but this is a challenging task and the resulting conclusions are restricted to the traits under consideration.An alternative approach is to examine characteristics of adaptive mutations through the powerful lens of population genetics. By measuring intraspecific polymorphism and interspecific divergence across genomes, evolutionary properties of those mutations targeted by natural selection can be discovered. Under this framework as well, generalities are widely sought and difficult to identify. A useful way to make progress is to compare patterns of adaptive evolution among different categories of loci. Two contrasts are based on the genomic location of mutations: X linked vs. autosomal and protein coding vs. cis-regulatory (i.e., noncoding sequences that affect local gene expression). These contrasts have generated substantial interest because they are tied directly to basic questions about adaptive evolution.The fate of a beneficial mutation should depend on its mode of inheritance. This idea motivates comparisons between rates of adaptive evolution on the X chromosome and the autosomes. Recent, low-frequency recessive mutations are immediately exposed to selection in males when X-linked and are mostly hidden from selection (in heterozygotes) when autosomal. If beneficial mutations are at least partially recessive on average, they will fix faster on the X chromosome (Avery 1984), elevating the rate of evolution relative to autosomal loci. In an influential theoretical article, Charlesworth et al. (1987) quantified this connection between dominance and "faster X" evolution and identified the biological conditions under which it applies. With several assumptions, the relative rates of molecular evolution at X-linked and autosomal loci can even be used to estimate the average dominance of new advantageous mutations, an important quantity in evolutionary biology.The study of faster X evolution is also motivated by a desire to explain the outsized role of the X chromosome in speciation. In a wide variety of species pairs, the sterility and/or inviability of hybrids created by interspecific crosses maps differentially to the X chromosome (Coyne and Orr 2004). This bias seems to reflect a higher density of hybrid incompatibilities involving the X chromosome (Masly and Presgraves 2007).The prediction of faster X evolution has been tested repeatedly by comparing between-species divergence at X-linked and autosomal genes (Meisel and Connallon 2013). The most popular approach calculates the relative rate of substitution at nonsynonymous and synonymous sites, reasoning that nonsynonymous changes will often be targeted by selection. A flurry of studies featuring Drosophila revealed a range of support for faster X evolution (Betancourt et al. 2002;Thornton and ...

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Hybrid Incompatibility inDrosophila: An Updated Genetic and Evolutionary Analysis

Fontdevila

2016

Encyclopedia of Life Sciences

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Negative interactions between independently evolved genes in two species are responsible of incompatibility of their hybrid, manifested by sterility and inviability. The heterogametic sex (XY males in Drosophila ) is the most affected and the X chromosome has the largest effect on hybrid incompatibility (HI). These rules of speciation depend on the genetic architecture of HI. Albeit some speciation genes have a major effect, this architecture shows a complex polygenic structure of multiple interactions. HI genes are frequently associated to genetic factors that evolved selfishly by favouring their preferential transmission. Genetic analyses show signatures of positive selection in speciation genes that may favour the role of adaptive evolution. Whether these signatures are compatible with evolution of selfish factors – an idea that is gaining support – still remains a contentious issue. Finally, there is also a current upsurge of evidences in favour of the importance of genetic regulation in the evolution of hybrid incompatibilities. Key Concepts Species must maintain their identity by isolation mechanisms that prevent gene flow among them. In sexual species, hybrid incompatibility, evidenced by sterility and/or inviability, is an isolation mechanism of great importance. The negative interaction in the hybrid between at least two genes that each evolved independently in two species (the BDM model) has been proved by multiple studies. Several genes of major effect (speciation genes) are highly implicated, albeit interacting with other genetic factors, in hybrid incompatibilities. A complex architecture of many genes with multiple interactions among them underlies the hybrid incompatibility. The heterogametic sex is generally more affected by the hybrid incompatibility through interactions between X‐linked recessive genes and partially dominant autosomal genes (the dominant theory). When substituted in a foreign genome, the X chromosome has a larger effect than any autosomal substitution, due to the greater density of speciation genes in the X chromosome. Many speciation genes show signatures of positive selection in their DNA, which suggests, but not always, adaptive evolution. Some speciation genes are associated to genetic factors evolved by genetic conflict, for example, meiotic drive, suggesting that a kind of evolutionary arms race between drivers and suppressors underlies the evolution of hybrid incompatibility. Recently, regulatory divergence rather than divergence in coding sequences is gaining support as a main actor in hybrid incompatibilities.

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Genetics and Evolution of Hybrid Male Sterility in House Mice

Cited by 74 publications

References 157 publications

The Pace of Hybrid Incompatibility Evolution in House Mice

The Pace of Hybrid Incompatibility Evolution in House Mice

Disproportionate Roles for the X Chromosome and Proteins in Adaptive Evolution

Hybrid Incompatibility inDrosophila: An Updated Genetic and Evolutionary Analysis

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