Genetics and Evolution of Hybrid Male Sterility in House Mice
White, Michael A., Stubbings, Maria, Dumont, Beth L., Payseur, Bret A., Genetics
ABSTRACT Comparative genetic mapping provides insights into the evolution of the reproductive barriers that separate closely related species. This approach has been used to document the accumulation of reproductive incompatibilities over time, but has only been applied to a few taxa. House mice offer a powerful system to reconstruct the evolution of reproductive isolation between multiple subspecies pairs. However, studies of the primary reproductive barrier in house mice-hybrid male sterility-have been restricted to a single subspecies pair: Mus musculus musculus and Mus musculus domesticus. To provide a more complete characterization of reproductive isolation in house mice, we conducted an F^sub 2^ intercross between wild-derived inbred strains from Mus musculus castaneus and M. m. domesticus. We identified autosomal and X-linked QTL associated with a range of hybrid male sterility phenotypes, including testis weight, sperm density, and sperm morphology. The pseudoautosomal region (PAR) was strongly associated with hybrid sterility phenotypes when heterozygous. We compared QTL found in this cross with QTL identified in a previous F^sub 2^ intercross between M. m. musculus and M. m. domesticus and found three shared autosomal QTL. Most QTL were not shared, demonstrating that the genetic basis of hybrid male sterility largely differs between these closely related subspecies pairs. These results lay the groundwork for identifying genes responsible for the early stages of speciation in house mice.
THE genetic dissection of reproductive barriers between species is a powerful approach to understanding speciation. In some cases, genetic mapping has revealed the identities and functions of the gene networks responsible for reproductive isolation (Sawamura and Yamamoto 1997; Ting et al. 1998; Barbash et al. 2003; Presgraves et al. 2003; Brideau et al. 2006; Bayes and Malik 2009; Ferree and Barbash 2009; Mihola et al. 2009; Phadnis and Orr 2009; Tang and Presgraves 2009). By providing a list of genomic locations that contribute to reproductive barriers, mapping also allows investigation of the role of genomic context, including local recombination rate (Noor et al. 2001; Rieseberg 2001; Butlin 2005; Nachman and Payseur 2012), in speciation. Phenotypes associated with reproductive isolation have been mapped in a variety of species, with an emphasis on hybrid sterility and hybrid inviability (Hollocher and Wu 1996; True et al. 1996; Tao et al. 2003; Sweigart et al. 2006; Bomblies et al. 2007; Masly and Presgraves 2007; Moyle 2007; Chen et al. 2008; Lee et al. 2008; Long et al. 2008; Kao et al. 2010; Martin and Willis 2010).
The comparison of reproductive isolation among species pairs has revealed general patterns that characterize speciation. For example, hybrid sterility tends to evolve before hybrid inviability (Coyne and Orr 1989). A worthwhile extension of this comparative framework focuses on the loci responsible for reproductive barriers (Moyle and Payseur 2009). By comparing loci mapped in different species pairs, genetic changes that increase reproductive isolation can be assigned to specific phylogenetic lineages, revealing the evolutionary history of reproductive barriers (Moyle and Nakazato 2008). This information enables the evaluation of models that describe the accumulation of reproductive isolating mutations (Orr 1995), the distinction between classes of incompatibilities (e.g., "derived- derived" and "ancestral-derived"; Orr 1995; Cattani and Presgraves 2009), and the temporal ordering of genetic changes that contribute to different reproductive barriers.
Recent applications of this comparative genetics approach have produced new insights into the evolution of reproductive isolation. Overlapping quantitative trait loci (QTL) control hybrid pollen/seed sterility in two species pairs of Solanum, suggesting common evolutionary origins for the underlying mutations (Moyle and Graham 2005; Moyle and Nakazato 2008). …