Abstract
Interspecific hybrid lethality and sterility are a consequence of divergent evolution between species and serve to maintain the discrete identities of species. The evolution of hybrid incompatibilities has been described in widely accepted models by Dobzhansky and Muller where lineage-specific functional divergence is the essential characteristic of hybrid incompatibility genes. Experimentally tractable models are required to identify and test candidate hybrid incompatibility genes. Several Drosophila melanogaster genes involved in hybrid incompatibility have been identified but none has yet been shown to have functionally diverged in accordance with the Dobzhansky-Muller model. By introducing transgenic copies of the X-linked Hybrid male rescue (Hmr) gene into D. melanogaster from its sibling species D. simulans and D. mauritiana, we demonstrate that Hmr has functionally diverged to cause F1 hybrid incompatibility between these species. Consistent with the Dobzhansky-Muller model, we find that Hmr has diverged extensively in the D. melanogaster lineage, but we also find extensive divergence in the sibling-species lineage. Together, these findings implicate over 13% of the amino acids encoded by Hmr as candidates for causing hybrid incompatibility. The exceptional level of divergence at Hmr cannot be explained by neutral processes because we use phylogenetic methods and population genetic analyses to show that the elevated amino-acid divergence in both lineages is due to positive selection in the distant past—at least one million generations ago. Our findings suggest that multiple substitutions driven by natural selection may be a general phenomenon required to generate hybrid incompatibility alleles.
Highlights
Reproductive isolation is the most commonly used criterion to define species
We detected accelerated divergence along the sibling-species lineages, but because of the trichotomy for divergence per synonymous site (Ds). simulans, D. sechellia, and D. mauritiana, these branch lengths have little confidence. This divergence appears to be irrelevant with respect to the hybrid incompatibility (HI) phenotype because we showed above that transgenic copies of Hmrþ from both D. simulans and D. mauritiana have no effect on hybrid viability (Table 1)
We have shown here that transgenes carrying D. simulans or D. mauritiana Hmrþ have no effect on hybrid fitness, in contrast to the strong deleterious effects previously observed with D. melanogaster Hmrþ
Summary
Reproductive isolation is the most commonly used criterion to define species. Hybrid incompatibilities (HIs) such as hybrid sterility and lethality are widely observed examples of reproductive isolation. The essential criterion for defining HI genes, is that the alleles from the two species have distinct phenotypic properties in hybrids: for example, in Figure 1A the derived allele A from one species causes the incompatibility while the ancestral allele a from the other species does not This model makes clear and testable genetic predictions, namely, that experimental manipulation of allele A (or X) but not allele a (or x) will affect the HI phenotype. Downstream effector genes such as d1 in Figure 1A contribute to the phenotype of HI but are not expected to have functionally diverged alleles in the two hybridizing species; in other words, experimental manipulation of downstream effector alleles from either species will have equivalent effects on the HI phenotype These alternative possibilities can only be addressed by genetically manipulating each species allele in a controlled hybrid background, but this has yet to be achieved in model organisms such as Drosophila melanogaster
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