Genetic conflict outweighs heterogametic incompatibility in the mouse hybrid zone?

Abstract

BackgroundThe Mus musculus musculus/M. m. domesticus contact zone in Europe is characterised by sharp frequency discontinuities for sex chromosome markers at the centre of wider clines in allozyme frequencies.ResultsWe identify a triangular area (approximately 330 km2) where the musculus Y chromosome introgresses across this front for up to 22 km into domesticus territory. Introgression of the Y chromosome is accompanied by a perturbation of the census sex ratio: the sex ratio is significantly female biased in musculus localities and domesticus localities lacking Y chromosome introgression. In contrast, where the musculus Y is detected in domesticus localities, the sex ratio is close to parity, and significantly different from both classes of female biased localities. The geographic position of an abrupt cline in an X chromosome marker, and autosomal clines centred on the same position, seem unaffected by the musculus Y introgression.ConclusionWe conclude that sex ratio distortion is playing a role in the geographic separation of speciation genes in this section of the mouse hybrid zone. We suggest that clines for genes involved in sex-ratio distortion have escaped from the centre of the mouse hybrid zone, causing a decay in the barrier to gene flow between the two house mouse taxa.

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

“…Noncoincident marker clines similar to the ones in M. arvalis in a particular region of the European house mouse hybrid zone are compatible with such a process as well (Macholan et al, 2008). The M. m. musculus Y-chromosome and to a lesser extent X-chromosomal markers and mtDNA are here more introgressed into the M. m. domesticus territory than the rest of the genome (Macholan et al, 2008;. The authors suggested that this unusual pattern resulted from genetic conflict between the sexes, which may promote unidirectional sex-specific gene flow between subspecies.…”

“…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).…”

“…This may be explained by two non-mutually exclusive scenarios: first, the hybrid zone may have moved and left the M. m. musculus Y-chromosome in the M. m. domesticus territory or second, the M. m. musculus Y-chromosome might have escaped from a static hybrid zone centre comprising autosomal and X-chromosomal markers and advanced up to 22 km into the M. m. domesticus territory (Macholan et al, 2008). It was proposed that a genetic conflict between the sexes may act together with a distortion of the sex-ratio to promote unidirectional sex-specific gene flow between the subspecies (Macholan et al, 2008). The variability in marker cline patterns stresses the importance of replicated analyses for hybrid zone analyses.…”

“…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). This may be explained by two non-mutually exclusive scenarios: first, the hybrid zone may have moved and left the M. m. musculus Y-chromosome in the M. m. domesticus territory or second, the M. m. musculus Y-chromosome might have escaped from a static hybrid zone centre comprising autosomal and X-chromosomal markers and advanced up to 22 km into the M. m. domesticus territory (Macholan et al, 2008).…”

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

“…The subspecies meet in a well-studied zone of secondary contact that stretches across central Europe Sage et al 1993), where diagnostic allele frequencies shift rapidly over short geographic distances Sage et al 1993). Individual loci often exhibit marked reductions in gene flow (Vanlerberghe et al 1986;Dod et al 1993;Munclinger et al 2002;Payseur et al 2004;Dod et al 2005;Payseur and Nachman 2005;Raufaste et al 2005;Macholán et al 2007Macholán et al , 2008Teeter et al 2008Teeter et al , 2010, as expected for genomic regions involved in reproductive isolation (Payseur 2010). Hybrids sampled from this zone show signs of reduced fitness, including increased parasite loads (Sage et al 1986;Moulia et al 1991Moulia et al , 1993.…”