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.
Highlights
The question of how two species originate from one has fascinated biologists since before Darwin’s iconic treatise on the subject [1]
Twelve of the 13 rodent species we examined possess at least one pair of Prdm9 zinc fingers that were so recently duplicated that they have identical nucleotide sequences
3 out of 4 non-synonymous single nucleotide polymorphisms (SNPs) associated with fertility are found at zinc finger position 6, a site predicted to determine DNA-binding specificity and which we show has evolved under positive selection in human PRDM9 (Figure 4 and Figure 5A)
Summary
The question of how two species originate from one has fascinated biologists since before Darwin’s iconic treatise on the subject [1]. Postzygotic reproductive barriers between species are thought to result from the acquisition of genetic incompatibilities as an incidental by-product of divergence between two populations. In its simplest form, this Dobzhansky-Muller model involves genetic interactions between two loci (e.g. a and b) [2]. A negative epistatic interaction between the two new alleles (A with B) in hybrids might result in sterility or inviability, a hallmark of postzygotic isolation in hybrids between two species [3]. One of the earliest postzygotic isolating barriers in interspecies hybrids is the sterility of the heterogametic sex (XY males or ZW females), a pattern referred to as Haldane’s rule that holds almost universally across animal taxa [3,5]. Examination of early events in speciation that lead to hybrid sterility (for example [6,7]) is vital to gain insight into this mysterious process
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