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Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila

Abstract

Speciation—the splitting of one species into two—occurs by the evolution of any of several forms of reproductive isolation between taxa, including the intrinsic sterility and inviability of hybrids. Abundant evidence shows that these hybrid fitness problems are caused by incompatible interactions between loci: new alleles that become established in one species are sometimes functionally incompatible with alleles at interacting loci from another species. However, almost nothing is known about the genes involved in such hybrid incompatibilities or the evolutionary forces that drive their divergence. Here we identify a gene that causes epistatic inviability in hybrids between two fruitfly species, Drosophila melanogaster and D. simulans. Our population genetic analysis reveals that this gene—which encodes a nuclear pore protein—evolved by positive natural selection in both species' lineages. These results show that a lethal hybrid incompatibility has evolved as a by-product of adaptive protein evolution.

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Figure 1: Deficiency mapping hybrid lethality.
Figure 2: Nup98-Nup96 structure and evolution.
Figure 3: Evolutionary history of Nup96 with ratios of replacement to silent substitutions mapped onto the known phylogeny of the D. melanogaster group species.

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Acknowledgements

We thank J. Coyne for providing the D. yakuba stock, and C. Aquadro for the Zimbabwe strains of D. melanogaster and D. simulans. We acknowledge the contribution of M. Erickson in preliminary molecular analysis of the nucleoporin locus. We thank A. Betancourt, A. Clark, J. Coyne, W. Stephan and J. Werren for helpful discussion and comments. This work was supported by funds from a Caspari Fellowship, a Messermith Fellowship, and a Dissertation Improvement Grant from the National Science Foundation to D.C.P.; from the National Institutes of Health and National Science Foundation to S.M.A.; and from the National Institutes of Health to H.A.O.

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Correspondence to Daven C. Presgraves.

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Presgraves, D., Balagopalan, L., Abmayr, S. et al. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423, 715–719 (2003). https://doi.org/10.1038/nature01679

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