Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

ABSTRACT Reproductive isolation between species is often caused by deleterious interactions among loci in hybrids. Finding the genes involved in these incompatibilities provides insight into the mechanisms of speciation. With recently diverged subspecies, house mice provide a powerful system for understanding the genetics of reproductive isolation early in the speciation process. Although previous studies have yielded important clues about the genetics of hybrid male sterility in house mice, they have been restricted to F1 sterility or incompatibilities involving the X chromosome. To provide a more complete characterization of this key reproductive barrier, we conducted an F2 intercross between wild-derived inbred strains from two subspecies of house mice, Mus musculus musculus and Mus musculus domesticus. We identified a suite of autosomal and X-linked QTL that underlie measures of hybrid male sterility, including testis weight, sperm density, and sperm morphology. In many cases, the autosomal loci were unique to a specific sterility trait and exhibited an effect only when homozygous, underscoring the importance of examining reproductive barriers beyond the F1 generation. We also found novel two-locus incompatibilities between the M. m. musculus X chromosome and M. m. domesticus autosomal alleles. Our results reveal a complex genetic architecture for hybrid male sterility and suggest a prominent role for reproductive barriers in advanced generations in maintaining subspecies integrity in house mice.

EXPLAINING patterns of biodiversity requires a mechanistic understanding of how new species arise. Genetic dissection of reproductive barriers between nascent species is a powerful approach for revealing the causes of speciation. This strategy has been highly successful, particularly in Drosophila, where nine specific genes that cause reduced fitness in hybrids have been identified (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; Phadnis and Orr 2009; Tang and Presgraves 2009). Despite this progress, several factors motivate additional genetic studies of postzygotic isolation. Although other species have provided important insights (e.g., Sweigart et al. 2006; Bomblies et al. 2007; Moyle 2007; Chen et al. 2008; Lee et al. 2008; Long et al. 2008; Kao et al. 2010; Martin and Willis 2010), current knowledge of the genetics of postzygotic isolation remains highly biased toward Drosophila. In addition, some of the best-studied species hybridize rarely or not at all in the wild, complicating attempts to connect reproductive barriers examined in the lab with gene flow in nature. Finally, there is a dearth of information on taxa in the process of speciating, where it is possible to find genetic changes responsible for the initial development of reproductive isolation.

House mice provide a powerful system for studying the genetics of reproductive isolation. Three recognizable subspecies diverged from a common ancestor only 500,000 generations ago (She et al. 1990; Boursot et al. 1996; Suzuki et al. 2004; Salcedo et al. 2007; Geraldes et al. 2008). Despite this short divergence time, several lines of evidence indicate reproductive isolation between two of the subspecies, Mus musculus musculus and Mus musculus domesticus. The subspecies meet in a well-studied zone of secondary contact that stretches across central Europe (Boursot et al. 1993; Sage et al. 1993), where diagnostic allele frequencies shift rapidly over short geographic distances (Boursot et al. 1993; 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. 2007, 2008; Teeter et al. 2008, 2010), as expected for genomic regions involved in reproductive isolation (Payseur 2010). …

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