Polymorphism in hybrid male sterility in wild-derived Mus musculus musculus strains on proximal chromosome 17

Abstract

The hybrid sterility-1 (Hst1) locus at Chr 17 causes male sterility in crosses between the house mouse subspecies Mus musculus domesticus (Mmd) and M. m. musculus (Mmm). This locus has been defined by its polymorphic variants in two laboratory strains (Mmd genome) when mated to PWD/Ph mice (Mmm genome): C57BL/10 (carrying the sterile allele) and C3H (fertile allele). The occurrence of sterile and/or fertile (wild Mmm x C57BL)F1 males is evidence that polymorphism for this trait also exists in natural populations of Mmm; however, the nature of this polymorphism remains unclear. Therefore, we derived two wild-origin Mmm strains, STUS and STUF, that produce sterile and fertile males, respectively, in crosses with C57BL mice. To determine the genetic basis underlying male fertility, the (STUS x STUF)F1 females were mated to C57BL/10 J males. About one-third of resulting hybrid males (33.8%) had a significantly smaller epididymis and testes than parental animals and lacked spermatozoa due to meiotic arrest. A further one-fifth of males (20.3%) also had anomalous reproductive traits but produced some spermatozoa. The remaining fertile males (45.9%) displayed no deviation from values found in parental individuals. QTL analysis of the progeny revealed strong associations of male fitness components with the proximal end of Chr 17, and a significant effect of the central section of Chr X on testes mass. The data suggest that genetic incompatibilities associated with male sterility have evolved independently at the proximal end of Chr 17 and are polymorphic within both Mmd and Mmm genomes.

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

“…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.…”

“…In addition, M. m. musculus and M. m. domesticus exhibit prezygotic isolation, including preferences for mates from the same subspecies (Laukaitis et al 1997;Talley et al 2001;Ganem 2002, 2005;Smadja et al 2004;Ganem et al 2008) and higher fertilization rates by sperm from the same subspecies when females are multiply mated (Dean and Nachman 2009). The most direct evidence for reproductive isolation comes from laboratory crosses involving wild-derived inbred strains, where F 1 hybrid male sterility is routinely observed, usually without hybrid female sterility (Iványi et al 1969;Forejt and Iványi 1974;Storchová et al 2004;BrittonDavidian et al 2005;Vyskočilová et al 2005Vyskočilová et al , 2009Good et al 2008a,b).…”

“…Substantial effort directed toward finding the incompatibilities that underlie hybrid male sterility between M. m. domesticus and M. m. musculus has revealed some genetic patterns. First, the X chromosome is an important contributor (Oka et al 2004;Storchová et al 2004;Britton-Davidian et al 2005;Good et al 2008aGood et al ,b, 2010Vyskočilová et al 2009). F 1 's from most crosses follow Haldane's rule (Haldane 1922), with hybrid females showing few signs of sterility.…”

“…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).…”

Is the control of recombination conserved among diverse eukaryotes?

“…Once hotspots become substantially depleted, new Prdm9 alleles with altered DNA-binding specificity will be favoured, redirecting recombination to newly 'hot' sites, and thus ensuring a necessary number of crossover events to support disjunction. These rapid changes, however, come with an evolutionary cost, as combinations of incompatible Prdm9 alleles apparently result in male infertility (Vyskocilova et al, 2009). This, presumably, is the basis for why Prdm9 is a species-incompatibility gene (Mihola et al, 2009).…”