Inferences of selection and migration in the Danish house mouse hybrid zone

Abstract

We analysed the patterns of allele frequency change for ten diagnostic autosomal allozyme loci in the hybrid zone between the house mouse subspecies Mus musculus domesticus and M. m. musculus in central Jutland. After determining the general orientation of the clines of allele frequencies, we analysed the cline shapes along the direction of maximum gradient. Eight of the ten clines are best described by steep central steps with coincident positions and an average width of 8.9 km (support limits 7.6-12.4) flanked by tails of introgression, indicating the existence of a barrier to gene flow and only weak selection on the loci studied. We derived estimates of migration from linkage disequilibrium in the centre of the zone, and by applying isolation by distance methods to microsatellite data from some of these populations. These give concordant estimates of s = 0.5-0.8 km generation -. The barrier to gene flow is of the order of 20 km (support limits 14-28), and could be explained by selection of a few per cent at 43-120 underdominant loci that reduces the mean fitness in the central populations to 0.45. Some of the clines appear symmetrical, whereas others are strongly asymmetrical, and two loci appear to have escaped the central barrier to gene flow, reflecting the differential action of selection on different parts of the genome. Asymmetry is always in the direction of more introgression into musculus , indicating either a general progression of domesticus into the musculus territory, possibly mediated by differential behaviour, or past movement of the hybrid zone in the opposite direction, impeded by potential geographical barriers to migration in domesticus territory.Barton NH, Gale KS. 1993. Genetic analysis of hybrid zones.In: Harrison RG, ed. Hybrid zones and the evolutionary process. Oxford: Oxford University Press, 13-45. Barton NH, Hewitt GM. 1985. Analysis of hybrid zones.

Empirical study of hybrid zone movement

“…In three of these, introgression of domesticus mtDNA was found in musculus populations, and in two, introgression of musculus mtDNA was found in domesticus populations (Božíková et al, 2005 and references therein). A study of ten allozyme loci showed asymmetry always in the direction of domesticus into musculus (Raufaste et al, 2005). Several studies have found that musculus females prefer musculus males, but domesticus females display no breeding preference (Smadja and Ganem, 2002;Smadja et al, 2004;Bimova et al, 2005;Ganem et al, 2005).…”

Haldane's rule in the 21st century

“…Studies include work on taxa with male heterogamety, where maternally inherited loci are seen to introgress further than autosomal and paternally inherited loci (for example, in the Mus musculus-M. domesticus hybrid zone, mitochondrial DNA introgresses to a greater degree than autosomal loci (Raufaste et al, 2005)), as well as taxa with female heterogamety (where biparentally inherited loci are seen to introgress deeper than maternally inherited ones; Jiggins et al, 1997;Helbig et al, 2001;Cianchi et al, 2003;Kronforst et al, 2006). As a particularly comprehensive example, Carling and Brumfield (2008) studied cline width in a (female-heterogametic) avian hybrid zone and found that Z-linked and mitochondrial genes introgressed less deeply than autosomal markers, which is consistent with HR.…”

Speciation through evolution of sex-linked genes

“…Furthermore, a balance between gene flow and selection against hybrids often leads to the formation of narrow hybrid zones, reducing recombination and therefore allowing divergence between populations either side of the zone to continue (parapatric speciation; Kondrashov, 2003). Clines of sex-linked loci are often narrower than those of autosomal loci, for example in the house mouse (Tucker et al, 1992;Dod et al, 1993Dod et al, , 2005Raufaste et al, 2005;Macholán et al, 2007), indicating either that selection against hybrids is more efficient on the X/Z chromosome or that it is more likely to contain genes selected against in hybrids. Either way, recombination in parapatry is lower for X/Z-linked loci than autosomal loci, increasing their potential for divergence.…”