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The Dobzhansky and Muller (D-M) model explains the evolution of hybrid incompatibility (HI) through the interaction between lineage-specific derived alleles at two or more loci. In agreement with the expectation that HI results from functional divergence, many protein-coding genes that contribute to incompatibilities between species show signatures of adaptive evolution, including  Lhr , which encodes a heterochromatin protein whose amino acid sequence has diverged extensively between  Drosophila melanogaster  and  D. simulans  by natural selection. The lethality of  D. melanogaster / D. simulans  F1 hybrid sons is rescued by removing  D. simulans Lhr , but not  D. melanogaster Lhr , suggesting that the lethal effect results from adaptive evolution in the  D. simulans  lineage. It has been proposed that adaptive protein divergence in  Lhr  reflects antagonistic coevolution with species-specific heterochromatin sequences and that defects in LHR protein localization cause hybrid lethality. Here we present surprising results that are inconsistent with this coding-sequence-based model. Using  Lhr  transgenes expressed under native conditions, we find no evidence that LHR localization differs between  D. melanogaster  and  D. simulans , nor do we find evidence that it mislocalizes in their interspecific hybrids. Rather, we demonstrate that  Lhr  orthologs are differentially expressed in the hybrid background, with the levels of  D. simulans Lhr  double that of  D. melanogaster Lhr . We further show that this asymmetric expression is caused by  cis -by- trans  regulatory divergence of  Lhr . Therefore, the non-equivalent hybrid lethal effects of  Lhr  orthologs can be explained by asymmetric expression of a molecular function that is shared by both orthologs and thus was presumably inherited from the ancestral allele of  Lhr . We present a model whereby hybrid lethality occurs by the interaction between evolutionarily ancestral and derived alleles.

Cis-by-Trans Regulatory Divergence Causes the Asymmetric Lethal Effects of an Ancestral Hybrid Incompatibility Gene