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Accelerated Evolution of the Prdm9 Speciation Gene across Diverse Metazoan Taxa

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      Abstract

      The onset of prezygotic and postzygotic barriers to gene flow between populations is a hallmark of speciation. One of the earliest postzygotic isolating barriers to arise between incipient species is the sterility of the heterogametic sex in interspecies' hybrids. Four genes that underlie hybrid sterility have been identified in animals: Odysseus, JYalpha, and Overdrive in Drosophila and Prdm9 ( Meisetz) in mice. Mouse Prdm9 encodes a protein with a KRAB motif, a histone methyltransferase domain and several zinc fingers. The difference of a single zinc finger distinguishes Prdm9 alleles that cause hybrid sterility from those that do not. We find that concerted evolution and positive selection have rapidly altered the number and sequence of Prdm9 zinc fingers across 13 rodent genomes. The patterns of positive selection in Prdm9 zinc fingers imply that rapid evolution has acted on the interface between the Prdm9 protein and the DNA sequences to which it binds. Similar patterns are apparent for Prdm9 zinc fingers for diverse metazoans, including primates. Indeed, allelic variation at the DNA–binding positions of human PRDM9 zinc fingers show significant association with decreased risk of infertility. Prdm9 thus plays a role in determining male sterility both between species (mouse) and within species (human). The recurrent episodes of positive selection acting on Prdm9 suggest that the DNA sequences to which it binds must also be evolving rapidly. Our findings do not identify the nature of the underlying DNA sequences, but argue against the proposed role of Prdm9 as an essential transcription factor in mouse meiosis. We propose a hypothetical model in which incompatibilities between Prdm9-binding specificity and satellite DNAs provide the molecular basis for Prdm9-mediated hybrid sterility. We suggest that Prdm9 should be investigated as a candidate gene in other instances of hybrid sterility in metazoans.

      Author Summary

      Speciation, the process by which one species splits into two, involves reproductive barriers between previously interbreeding populations. The question of how speciation occurs has rightly occupied the attention of biologists since before Darwin's “On the Origin of Species.” Studies of recently diverged species have revealed the presence of hybrid sterility genes (colloquially referred to as “speciation genes”), alleles of which are associated with sterility of interspecies hybrids. Mouse Prdm9 is the only known such gene in vertebrate animals. Here we report that the Prdm9 protein has evolved extremely rapidly in its DNA-binding domain, comprising an array of “zinc fingers.” This suggests that hybrid sterility may arise from a mismatch between the DNA-binding specificity of Prdm9 and rapidly evolving DNA. We propose that Prdm9 binds to satellite-DNA repeats evolving rapidly within and between different species. Prdm9 evolution is unusual because other hybrid sterility genes appear only to evolve rapidly in isolated bursts, whereas Prdm9 has evolved rapidly over 700 million years, in many rodent species, diverse primates and other metazoans. This leads to the tantalizing possibility that Prdm9 may have served as a “speciation gene” on other occasions in metazoan evolution, a possibility that will now need to be investigated.

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      Most cited references 70

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            Author and article information

            Affiliations
            [1 ]Medical Research Council Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
            [2 ]Department of Molecular and Cell Biology, University of California Berkeley, Berkeley, California, United States of America
            [3 ]Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
            [4 ]Department of Genome Sciences, University of Washington, Seattle, Washington, United States of America
            [5 ]School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, Queensland, Australia
            [6 ]Howard Hughes Medical Institute, Fred Hutchinson Cancer Research Center, Seattle, Washington, United States of America
            University of Arizona, United States of America
            Author notes

            Conceived and designed the experiments: PLO LG JJB GL HSM CPP. Performed the experiments: PLO LG ZB KCR GL HSM. Analyzed the data: LG. Contributed reagents/materials/analysis tools: SAB. Wrote the paper: PLO LG JJB KCR NP GL HSM CPP.

            Contributors
            Role: Editor
            Journal
            PLoS Genet
            plos
            plosgen
            PLoS Genetics
            Public Library of Science (San Francisco, USA )
            1553-7390
            1553-7404
            December 2009
            December 2009
            4 December 2009
            : 5
            : 12
            2779102
            19997497
            09-PLGE-RA-0852R3
            10.1371/journal.pgen.1000753
            (Editor)
            Oliver et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
            Counts
            Pages: 14
            Categories
            Research Article
            Evolutionary Biology
            Evolutionary Biology/Evolutionary and Comparative Genetics
            Evolutionary Biology/Human Evolution
            Genetics and Genomics/Bioinformatics
            Genetics and Genomics/Gene Function
            Molecular Biology/Bioinformatics
            Molecular Biology/Molecular Evolution

            Genetics

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