Reproductive Isolation in Hybrid Mice Due to Spermatogenesis Defects at Three Meiotic Stages

Oka, Atsuhiro; Mita, Akihiko; Takada, Yuki; Koseki, Haruhiko; Shiroishi, Toshihiko

doi:10.1534/genetics.110.118976

Cited by 45 publications

(46 citation statements)

References 68 publications

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“…Severity of these phenotypes also varies widely among the classical inbred strains of house mice, where the incidence of abnormal sperm is negatively correlated with fertilization success (Kawai et al 2006). Consistent with observed defects in spermatogenesis, we also found a reduction in the area of seminiferous tubules, a change tied to decreases in the number of round spermatids in crosses between these subspecies (Britton-Davidian et al 2005) that likely reflects failure during meiosis (Oka et al 2010).…”

Section: Discussionsupporting

confidence: 83%

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

et al. 2011

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Reproductive isolation between species is often caused by deleterious interactions among loci in hybrids. Finding the genes involved in these incompatibilities provides insight into the mechanisms of speciation. With recently diverged subspecies, house mice provide a powerful system for understanding the genetics of reproductive isolation early in the speciation process. Although previous studies have yielded important clues about the genetics of hybrid male sterility in house mice, they have been restricted to F 1 sterility or incompatibilities involving the X chromosome. To provide a more complete characterization of this key reproductive barrier, we conducted an F 2 intercross between wild-derived inbred strains from two subspecies of house mice, Mus musculus musculus and Mus musculus domesticus. We identified a suite of autosomal and X-linked QTL that underlie measures of hybrid male sterility, including testis weight, sperm density, and sperm morphology. In many cases, the autosomal loci were unique to a specific sterility trait and exhibited an effect only when homozygous, underscoring the importance of examining reproductive barriers beyond the F 1 generation. We also found novel two-locus incompatibilities between the M. m. musculus X chromosome and M. m. domesticus autosomal alleles. Our results reveal a complex genetic architecture for hybrid male sterility and suggest a prominent role for reproductive barriers in advanced generations in maintaining subspecies integrity in house mice.

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Section: Discussionsupporting

confidence: 83%

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

et al. 2011

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“…One explanation for this result is that the X chromosome contains more shared incompatibilities than the autosomes, and the PhyloQTL approach offers higher power than the heuristic method to detect these loci. The X chromosome confers hybrid male sterility between domesticus and musculus through complex regulatory mechanisms that remain unclear (Storchová et al 2004;Good et al 2008bGood et al , 2010Oka et al 2010;Campbell et al 2013;Turner et al 2014;Bhattacharyya et al 2014;Oka and Shiroishi 2014). It is possible that incompatibilities involving the X chromosome differ from purely autosomal interactions in some way that affects the snowball prediction.…”

Section: Discussionmentioning

confidence: 99%

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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“…Hybrid male sterility between more divergent species, Mus spretus and M. m. domesticus (C57BL/6J) (She et al 1990;Suzuki et al 2004), has been mapped to the PAR (Guénet et al 1990). In this species pair, sterility was also limited to heterozygotes (Matsuda et al 1991;Hale et al 1993), in which high levels of dissociation among the X and Y chromosomes triggered meiotic arrest (Matsuda et al 1992;Oka et al 2010). We observed high frequencies of spermatocytes carrying unpaired X and Y chromosomes at late pachytene in F 1 hybrids between M. m. castaneus CAST and M. m. domesticus WSB , an effect likely caused by intersubspecific differences in the PAR region.…”

Section: Discussionmentioning

confidence: 99%

Genetics and Evolution of Hybrid Male Sterility in House Mice

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Dumont³

et al. 2012

Genetics

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Comparative genetic mapping provides insights into the evolution of the reproductive barriers that separate closely related species. This approach has been used to document the accumulation of reproductive incompatibilities over time, but has only been applied to a few taxa. House mice offer a powerful system to reconstruct the evolution of reproductive isolation between multiple subspecies pairs. However, studies of the primary reproductive barrier in house mice-hybrid male sterility-have been restricted to a single subspecies pair: Mus musculus musculus and Mus musculus domesticus. To provide a more complete characterization of reproductive isolation in house mice, we conducted an F 2 intercross between wild-derived inbred strains from Mus musculus castaneus and M. m. domesticus. We identified autosomal and X-linked QTL associated with a range of hybrid male sterility phenotypes, including testis weight, sperm density, and sperm morphology. The pseudoautosomal region (PAR) was strongly associated with hybrid sterility phenotypes when heterozygous. We compared QTL found in this cross with QTL identified in a previous F 2 intercross between M. m. musculus and M. m. domesticus and found three shared autosomal QTL. Most QTL were not shared, demonstrating that the genetic basis of hybrid male sterility largely differs between these closely related subspecies pairs. These results lay the groundwork for identifying genes responsible for the early stages of speciation in house mice.

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Reproductive Isolation in Hybrid Mice Due to Spermatogenesis Defects at Three Meiotic Stages

Cited by 45 publications

References 68 publications

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

The Pace of Hybrid Incompatibility Evolution in House Mice

Genetics and Evolution of Hybrid Male Sterility in House Mice

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