Genetics and Lineage-Specific Evolution of a Lethal Hybrid Incompatibility between Drosophila Mauritiana and Its Sibling Species

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The Dobzhansky-Muller model posits that intrinsic postzygotic reproductive isolation-the sterility or lethality of species hybrids-results from the evolution of incompatible epistatic interactions between species: favorable or neutral alleles that become fixed in the genetic background of one species can cause sterility or lethality in the genetic background of another species. The kind of hybrid incompatibility that evolves between two species, however, depends on the particular evolutionary history of the causative substitutions. An allele that is functionally derived in one species can be incompatible with an allele that is functionally derived in the other species (a derived-derived hybrid incompatibility). But an allele that is functionally derived in one species can also be incompatible with an allele that has retained the ancestral state in the other species (a derived-ancestral hybrid incompatibility). The relative abundance of such derived-derived vs. derived-ancestral hybrid incompatibilities is unknown. Here, we characterize the genetics and evolutionary history of a lethal hybrid incompatibility between Drosophila mauritiana and its two sibling species, D. sechellia and D. simulans. We show that a hybrid lethality factor(s) in the pericentric heterochromatin of the D. mauritiana X chromosome, hybrid lethal on the X (hlx), is incompatible with a factor(s) in the same small autosomal region from both D. sechellia and D. simulans, Suppressor of hlx [Su(hlx)]. By combining genetic and phylogenetic information, we infer that hlx-Su(hlx) hybrid lethality is likely caused by a derived-ancestral incompatibility, a hypothesis that can be tested directly when the genes are identified.

SPECIATION often involves the evolution of intrinsic postzygotic reproductive barriers-including the sterility and inviability of hybrids-that limit the potential for genetic exchange between populations or species (Dobzhansky 1937; Coyne and Orr 2004). Hybrid sterility and inviability in animals are usually caused by incompatible gene interactions: often functionally divergent genes from one species are incompatible with interacting genes from another species. Many studies have mapped such hybrid incompatibility genes to small chromosomal regions (Naveira and Fontdevila 1986; Pantazidis et al. 1993;Carvajal et al. 1996;Hollocher andWu1996;Trueet al. 1996; SawamuraandYamamoto 1997; Naisbit et al. 2002; Presgraves 2003; Tao et al. 2003; Slotman et al. 2004; Moyle and Graham 2005; Sweigartet al. 2006;MaslyandPresgraves2007;Good et al. 2008) and, in several cases, identified the causative genes. These studies reveal that hybrid incompatibilities can involve functionally divergent protein-coding genes (Ting et al. 1998; Barbash et al. 2003; Presgraves et al. 2003; Brideau et al. 2006; Mihola et al. 2009; Phadnis and Orr 2009; Tang and Presgraves 2009), chimeric duplicate genes (Wittbrodt et al. 1989), repetitive DNA (Sawamura and Yamamoto 1997), and gene movement (Masly et al. 2006).

However, none of these individual hybrid incompatibility loci causes sterility or inviability on its own. Rather, as Dobzhansky (1937) and Muller (1940, 1942) first explained, hybrid fitness problems must involve deleterious epistatic interactions that evolve as incidental by-products of divergence (seeOrr 1996). In the usual depiction of the so-called Dobzhansky-Muller model, an ancestral population with the two-locus genotype aabb splits into two geographically isolated lineages and each fixes new and different substitutions (yielding AAbb and aaBB lineages, respectively); when brought together in hybrids (AaBb), an incompatibility between these substitutions causes hybrid sterility or hybrid inviability (Figure 1A). Recent theory shows that the evolution of hybrid incompatibilities should follow some simple rules. For example, hybrid incompatibilities should be asymmetric (i.e., A is incompatible with B, but a should be compatible with b), should often be complex (i. …