Asymmetry and Polymorphism of Hybrid Male Sterility During the Early Stages of Speciation in House Mice

Good, Jeffrey M.; Handel, Mary Ann; Nachman, Michael W.

doi:10.1111/j.1558-5646.2007.00257.x

Cited by 147 publications

(269 citation statements)

References 101 publications

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“…F 1 hybrid sterility F 1 hybrid male sterility is polymorphic among strains of M. m. musculus and M. m. domesticus (Vyskočilová et al 2005(Vyskočilová et al , 2009Good et al 2008b;Piálek et al 2008) and has not been evaluated in crosses between the wild-derived inbred strains PWD/PhJ (M. m. musculus PWD ) and WSB/EiJ (M. m. domesticus WSB ). To determine if F 1 males were sterile in crosses between these strains, we quantified a range of phenotypes in 70-day-old F 1 and parental males.…”

Section: Resultsmentioning

confidence: 99%

“…Some of the QTL that we identified might not be fixed differences between subspecies; under this scenario, the resulting incompatibilities would only have the potential to contribute to reproductive barriers in part of the subspecies range. Intra-subspecific variation in inter-subspecific hybrid male sterility has been documented in both M. m. musculus and M. m. domesticus (Good et al 2008b). In addition, the large effective population size and short divergence time among subspecies have left a clear signature of incomplete lineage sorting across the genome (Geraldes et al 2008;White et al 2009).…”

Section: Dobzhansky-muller Incompatibilities With the X Chromosomementioning

confidence: 99%

“…F 1 's from most crosses follow Haldane's rule (Haldane 1922), with hybrid females showing few signs of sterility. In hybrid males, sterility is more common when M. m. musculus is the mother (Britton-Davidian et al 2005;Good et al 2008b;Vyskočilová et al 2009). The role for the M. m. musculus X chromosome suggested by these observations has been confirmed through backcrosses (Storchová et al 2004) and chromosomal introgression studies (Good et al 2008a;Gregorová et al 2008).…”

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confidence: 99%

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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: Resultsmentioning

confidence: 99%

Section: Dobzhansky-muller Incompatibilities With the X Chromosomementioning

confidence: 99%

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confidence: 99%

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

et al. 2011

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“…C T values were normalized relative to Ubc or beta-actin values for each plate (DC T ). Because postmeiotic cells are depleted in the testes of sterile males (Good et al 2008a), whole-testis expression was normalized a second time relative to two postmeiotic autosomal genes, Acrv1 and Protamine 1.…”

Section: Qrt-pcrmentioning

confidence: 99%

Meiotic Sex Chromosome Inactivation Is Disrupted in Sterile Hybrid Male House Mice

2013

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In male mammals, the X and Y chromosomes are transcriptionally silenced in primary spermatocytes by meiotic sex chromosome inactivation (MSCI) and remain repressed for the duration of spermatogenesis. Here, we test the longstanding hypothesis that disrupted MSCI might contribute to the preferential sterility of heterogametic hybrid males. We studied a cross between wildderived inbred strains of Mus musculus musculus and M. m. domesticus in which sterility is asymmetric: F 1 males with a M. m. musculus mother are sterile or nearly so while F 1 males with a M. m. domesticus mother are normal. In previous work, we discovered widespread overexpression of X-linked genes in the testes of sterile but not fertile F 1 males. Here, we ask whether this overexpression is specifically a result of disrupted MSCI. To do this, we isolated cells from different stages of spermatogenesis and measured the expression of several genes using quantitative PCR. We found that X overexpression in sterile F 1 primary spermatocytes is coincident with the onset of MSCI and persists in postmeiotic spermatids. Using a series of recombinant X genotypes, we then asked whether X overexpression in hybrids is controlled by cis-acting loci across the X chromosome. We found that it is not. Instead, one large interval in the proximal portion of the M. m. musculus X chromosome is associated with both overexpression and the severity of sterility phenotypes in hybrids. These results demonstrate a strong association between X-linked hybrid male sterility and disruption of MSCI and suggest that transacting loci on the X are important for the transcriptional regulation of the X chromosome during spermatogenesis. FORTY years ago, Lifschytz and Lindsley (1972) proposed the provocative hypothesis that the X chromosome is inactivated during male meiosis and that disruption of this process could lead to sterility. The idea that failure of meiotic sex chromosome inactivation (MSCI) might cause sterility is significant in speciation genetics since it provides a possible explanation for the widespread observation that in crosses between species, sterility typically appears first in the heterogametic sex (Haldane 1922;Forejt 1996;Presgraves 2008).Whether MSCI takes place in Drosophila has been debated for several decades (Kremer et al. 1986;McKee and Handel 1993;Hense et al. 2007;Vibranovski et al. 2009). Current evidence suggests that expression on the X chromosome is suppressed relative to the autosomes during spermatogenesis but that this suppression precedes meiosis and thus does not reflect MSCI (Meiklejohn et al. 2011; but see Vibranovski et al. 2012). Likewise, the sex chromosomes are not differentially silenced in chicken oocytes (Guioli et al. 2012). Therefore, failed MSCI cannot explain hybrid sterility in all female-heterogametic taxa. In therian mammals, however, MSCI is well established (Solari 1974;McKee and Handel 1993;Namekawa et al. 2007). Although no MSCI-essential loci have been found on the sex chromosomes, many of the autosomal genes t...

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“…The observation of male sterility combined with the detection of abrupt Y-and X-chromosome marker clines (Dod et al, 1993;Macholan et al, 2007; relative to other markers across the hybrid zone are consistent with the hypothesis that sex chromosomes and in particular factors on the X-chromosome have an important role in causing genetic incompatibilities in mouse hybrids (Coyne and Orr, 2004). Nevertheless, there is extensive geographical and individual variation in male sterility (BrittonDavidian et al, 2005;Good et al, 2008;Turner et al, 2012), and sex-chromosomal marker clines may be not coincident with other genetic markers in particular geographical regions, potentially due to asymmetrical processes (Macholan et al, 2008;Jones et al, 2010). For example, the Y-chromosome was found non-coincident with other markers in an area of about 330 km 2 in the Czech-Bavarian part of the mouse hybrid zone (Macholan et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Sex-specific clines support incipient speciation in a common European mammal

2013

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Hybrid zones provide excellent opportunities to study processes and mechanisms underlying reproductive isolation and speciation. Here we investigated sex-specific clines of molecular markers in hybrid zones of morphologically cryptic yet genetically highly-diverged evolutionary lineages of the European common vole (Microtus arvalis). We analyzed the position and width of four secondary contact zones along three independent transects in the region of the Alps using maternally (mitochondrial DNA) and paternally (Y-chromosome) inherited genetic markers. Given male-biased dispersal in the common vole, a selectively neutral secondary contact would show broader paternal marker clines than maternal ones. In a selective case, for example, involving a form of Haldane's rule, Y-chromosomal clines would not be expected to be broader than maternal markers because they are transmitted by the heterogametic sex and thus gene flow would be restricted. Consistent with the selective case, paternal clines were significantly narrower or at most equal in width to maternal clines in all contact zones. In addition, analyses using maximum likelihood cline-fitting detected a shift of paternal relative to maternal clines in three of four contact zones. These patterns suggest that processes at the contact zones in the common vole are not selectively neutral, and that partial reproductive isolation is already established between these evolutionary lineages. We conclude that hybrid zone movement, sexual selection and/or genetic incompatibilities are likely associated with an unusual unidirectional manifestation of Haldane's rule in this common European mammal.

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Asymmetry and Polymorphism of Hybrid Male Sterility During the Early Stages of Speciation in House Mice

Cited by 147 publications

References 101 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

Meiotic Sex Chromosome Inactivation Is Disrupted in Sterile Hybrid Male House Mice

Sex-specific clines support incipient speciation in a common European mammal

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