Abstract
Hybrid male sterility (HMS) contributes to reproductive isolation commonly observed among house mouse (Mus musculus) subspecies, both in the wild and in laboratory crosses. Incompatibilities involving specific Prdm9 alleles and certain Chromosome (Chr) X genotypes are known determinants of fertility and HMS, and previous work in the field has demonstrated that genetic background modifies these two major loci. We constructed hybrids that have identical genotypes at Prdm9 and identical X chromosomes, but differ widely across the rest of the genome. In each case, we crossed female PWK/PhJ mice representative of the M. m. musculus subspecies to males from a classical inbred strain representative of M. m. domesticus: 129S1/SvImJ, A/J, C57BL/6J, or DBA/2J. We detected three distinct trajectories of fertility among the hybrids using breeding experiments. The PWK129S1 males were always infertile. PWKDBA2 males were fertile, despite their genotypes at the major HMS loci. We also observed age-dependent changes in fertility parameters across multiple genetic backgrounds. The PWKB6 and PWKAJ males were always infertile before 12 weeks and after 35 weeks. However, some PWKB6 and PWKAJ males were transiently fertile between 12 and 35 weeks. This observation could resolve previous contradictory reports about the fertility of PWKB6. Taken together, these results point to multiple segregating HMS modifier alleles, some of which have age-related modes of action. The ultimate identification of these alleles and their age-related mechanisms will advance understanding both of the genetic architecture of HMS and of how reproductive barriers are maintained between house mouse subspecies.
Highlights
Hybrid male sterility (HMS) is the phenomenon in which matings between genetically distinct parents produce viable yet infertile male offspring
We demonstrate that undiscovered HMS alleles segregate among these strains and present a novel observation of age-dependent HMS in the mouse
All eight types were identically heterozygous at the Prdm9 gene
Summary
Hybrid male sterility (HMS) is the phenomenon in which matings between genetically distinct parents produce viable yet infertile male offspring. Muller model (Dobzhansky 1937; Muller 1942; Orr 1995) proposes an evolutionary genetic mechanism for the development of reproductive incompatibilities. With restriction to gene flow, diverging populations accumulate and fix new mutations. These derived alleles are neutral within each population, but act deleteriously in hybrids through epistatic interactions that cause HMS. An important extension of Haldane’s rule is that, sometimes, reciprocal interspecies crosses produce sterile hybrid offspring in one cross direction, but not the other, if incompatibilities evolve at different rates in each species (Turelli and Moyle 2007)
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