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Genetic analysis of genome-scale recombination rate evolution in house mice.

Dumont BL, Payseur BA - PLoS Genet. (2011)

Bottom Line: Much of the F2 variance for recombination rate and a substantial portion of the difference in recombination rate between the parental strains is explained by eight moderate- to large-effect quantitative trait loci, including two transgressive loci on the X chromosome.In contrast to the rapid evolution observed in males, female CAST/EiJ and PWD/PhJ animals show minimal divergence in recombination rate (∼5%).The existence of loci on the X chromosome suggests a genetic mechanism to explain this male-biased evolution.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin, United States of America.

ABSTRACT
The rate of meiotic recombination varies markedly between species and among individuals. Classical genetic experiments demonstrated a heritable component to population variation in recombination rate, and specific sequence variants that contribute to recombination rate differences between individuals have recently been identified. Despite these advances, the genetic basis of species divergence in recombination rate remains unexplored. Using a cytological assay that allows direct in situ imaging of recombination events in spermatocytes, we report a large (∼30%) difference in global recombination rate between males of two closely related house mouse subspecies (Mus musculus musculus and M. m. castaneus). To characterize the genetic basis of this recombination rate divergence, we generated an F2 panel of inter-subspecific hybrid males (n = 276) from an intercross between wild-derived inbred strains CAST/EiJ (M. m. castaneus) and PWD/PhJ (M. m. musculus). We uncover considerable heritable variation for recombination rate among males from this mapping population. Much of the F2 variance for recombination rate and a substantial portion of the difference in recombination rate between the parental strains is explained by eight moderate- to large-effect quantitative trait loci, including two transgressive loci on the X chromosome. In contrast to the rapid evolution observed in males, female CAST/EiJ and PWD/PhJ animals show minimal divergence in recombination rate (∼5%). The existence of loci on the X chromosome suggests a genetic mechanism to explain this male-biased evolution. Our results provide an initial map of the genetic changes underlying subspecies differences in genome-scale recombination rate and underscore the power of the house mouse system for understanding the evolution of this trait.

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Variation in mean MLH1 foci counts (±2 standard errors) between males (blue) and females (green) of inbred CAST, PWD, and inter-subspecific CASTxPWD (CxP) and PWDxCAST (PxC) F1 origin.Strain means were calculated by pooling MLH1 foci counts over multiple animals (CAST females: data from [62]; PWD females: 3 animals; CASTxPWD F1 females: 2 animals; PWD males: 10 animals; CAST males: 3 animals; PWD×CAST F1 males: 1 animal; CAST×PWD F1 males: 11 animals).
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pgen-1002116-g006: Variation in mean MLH1 foci counts (±2 standard errors) between males (blue) and females (green) of inbred CAST, PWD, and inter-subspecific CASTxPWD (CxP) and PWDxCAST (PxC) F1 origin.Strain means were calculated by pooling MLH1 foci counts over multiple animals (CAST females: data from [62]; PWD females: 3 animals; CASTxPWD F1 females: 2 animals; PWD males: 10 animals; CAST males: 3 animals; PWD×CAST F1 males: 1 animal; CAST×PWD F1 males: 11 animals).

Mentions: Interestingly, the allele from the low recombination rate CAST parent confers the increase in recombination rate at this X-linked locus, opposite the pattern seen at the chromosome 7 QTL (Table 1). Consistent with this result, we uncover a striking difference in genomic recombination rate between reciprocal F1 males (Figure 6). Male F1 animals that receive their X chromosome from a CAST mother (CASTxPWD F1s) have ∼5 more MLH1 foci per meiosis than F1 males carrying the PWD X chromosome (PWDxCAST F1s).


Genetic analysis of genome-scale recombination rate evolution in house mice.

Dumont BL, Payseur BA - PLoS Genet. (2011)

Variation in mean MLH1 foci counts (±2 standard errors) between males (blue) and females (green) of inbred CAST, PWD, and inter-subspecific CASTxPWD (CxP) and PWDxCAST (PxC) F1 origin.Strain means were calculated by pooling MLH1 foci counts over multiple animals (CAST females: data from [62]; PWD females: 3 animals; CASTxPWD F1 females: 2 animals; PWD males: 10 animals; CAST males: 3 animals; PWD×CAST F1 males: 1 animal; CAST×PWD F1 males: 11 animals).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3111479&req=5

pgen-1002116-g006: Variation in mean MLH1 foci counts (±2 standard errors) between males (blue) and females (green) of inbred CAST, PWD, and inter-subspecific CASTxPWD (CxP) and PWDxCAST (PxC) F1 origin.Strain means were calculated by pooling MLH1 foci counts over multiple animals (CAST females: data from [62]; PWD females: 3 animals; CASTxPWD F1 females: 2 animals; PWD males: 10 animals; CAST males: 3 animals; PWD×CAST F1 males: 1 animal; CAST×PWD F1 males: 11 animals).
Mentions: Interestingly, the allele from the low recombination rate CAST parent confers the increase in recombination rate at this X-linked locus, opposite the pattern seen at the chromosome 7 QTL (Table 1). Consistent with this result, we uncover a striking difference in genomic recombination rate between reciprocal F1 males (Figure 6). Male F1 animals that receive their X chromosome from a CAST mother (CASTxPWD F1s) have ∼5 more MLH1 foci per meiosis than F1 males carrying the PWD X chromosome (PWDxCAST F1s).

Bottom Line: Much of the F2 variance for recombination rate and a substantial portion of the difference in recombination rate between the parental strains is explained by eight moderate- to large-effect quantitative trait loci, including two transgressive loci on the X chromosome.In contrast to the rapid evolution observed in males, female CAST/EiJ and PWD/PhJ animals show minimal divergence in recombination rate (∼5%).The existence of loci on the X chromosome suggests a genetic mechanism to explain this male-biased evolution.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genetics, University of Wisconsin, Madison, Wisconsin, United States of America.

ABSTRACT
The rate of meiotic recombination varies markedly between species and among individuals. Classical genetic experiments demonstrated a heritable component to population variation in recombination rate, and specific sequence variants that contribute to recombination rate differences between individuals have recently been identified. Despite these advances, the genetic basis of species divergence in recombination rate remains unexplored. Using a cytological assay that allows direct in situ imaging of recombination events in spermatocytes, we report a large (∼30%) difference in global recombination rate between males of two closely related house mouse subspecies (Mus musculus musculus and M. m. castaneus). To characterize the genetic basis of this recombination rate divergence, we generated an F2 panel of inter-subspecific hybrid males (n = 276) from an intercross between wild-derived inbred strains CAST/EiJ (M. m. castaneus) and PWD/PhJ (M. m. musculus). We uncover considerable heritable variation for recombination rate among males from this mapping population. Much of the F2 variance for recombination rate and a substantial portion of the difference in recombination rate between the parental strains is explained by eight moderate- to large-effect quantitative trait loci, including two transgressive loci on the X chromosome. In contrast to the rapid evolution observed in males, female CAST/EiJ and PWD/PhJ animals show minimal divergence in recombination rate (∼5%). The existence of loci on the X chromosome suggests a genetic mechanism to explain this male-biased evolution. Our results provide an initial map of the genetic changes underlying subspecies differences in genome-scale recombination rate and underscore the power of the house mouse system for understanding the evolution of this trait.

Show MeSH