Background PRDM9 is a key regulator of meiotic recombination in most metazoans, responsible for reshuffling parental genomes. During meiosis, the PRDM9 protein recognizes and binds specific target motifs via its array of C2H2 zinc-fingers encoded by a rapidly evolving minisatellite. The gene coding for PRDM9 is the only speciation gene identified in vertebrates to date and shows high variation, particularly in the DNA-recognizing positions of the zinc-finger array, within and between species. Across all vertebrate genomes studied for PRDM9 evolution, only one genome lacks variability between repeat types – that of the North Pacific minke whale. This study aims to understand the evolution and diversity of Prdm9 in minke whales, which display the most unusual genome reference allele of Prdm9 so far discovered in mammals. Results Minke whales possess all the features characteristic of PRDM9-directed recombination, including complete KRAB, SSXRD and SET domains and a rapidly evolving array of C2H2-type-Zincfingers (ZnF) with evidence of rapid evolution, particularly at DNA-recognizing positions that evolve under positive diversifying selection. Seventeen novel PRDM9 variants were identified within the Antarctic minke whale species, plus a single distinct PRDM9 variant in Common minke whales – shared across North Atlantic and North Pacific minke whale subspecies boundaries. Conclusion The PRDM9 ZnF array evolves rapidly, in minke whales, with at least one DNA-recognizing position under positive selection. Extensive PRDM9 diversity is observed, particularly in the Antarctic in minke whales. Common minke whales shared a specific Prdm9 allele across subspecies boundaries, suggesting incomplete speciation by the mechanisms associated with PRDM9 hybrid sterility.

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PRDM9-mediated reproductive isolation was first described in offspring ofMus musculus musculusstrain PWD/Ph andMus musculus domesticusstrain C57BL/6J. Male F1-hybrids do not complete chromosome synapsis and arrest meiosis at Prophase I. Currently, all data supports an oligogenic control of hybrid sterility based on incompatibilities between PRDM9 and hybrid-sterility locusHstx2inMus musculushybrids. Erosion of PRDM9 binding sites was proposed to result in asymmetric binding on diverged homologs of intersubspecific F1hybrids. Numerous alleles ofPrdm9have been characterized for different subspecies ofMus musculus, but only a few were analyzed for their impact on hybrid sterility. We analyzedPrdm9diversity in natural wild mouse populations from Europe, Asia, and the Middle East and identified several novelPrdm9alleles. We established that a singlePrdm9allele is associated witht-haplotype Chromosome 17 in all three subspecies ofMus musculusand characterized the phylogenetic relationships of novelPrdm9alleles with established sterility alleles. Novel wildPrdm9alleles produced F1-hybrid male offspring that were either fertile or showedPrdm9-dependent reduction of fertility and high levels of asynapsis. Fertility or sterility phenotypes segregated purely with thePrdm9genotype, although theMus musculus musculusbackground varied. Our data substantiate that hybrid sterility is under oligogenic control withPrdm9as the leading player but is consistent with a nonbinary regulation of hybrid sterility and gradual fertility decline when homologs diverge.

The PRDM9 protein controls the reshuffling of parental genomes in most metazoans. During meiosis the PRDM9 protein recognizes and binds specific target motifs via its zinc-finger array, which is encoded by a hypervariable minisatellite. To date, PRDM9 diversity has been little studied outside humans, wild mice and some domesticated species where evolutionary constraints may have been relaxed. Here we explore the structure and variability of PRDM9 in samples of the minke whales from the Atlantic, Pacific and Southern Oceans. We show that minke whales possess all the features characteristic of organisms with PRDM9-directed recombination initiation, including complete KRAB, SSXRD and SET domains and a rapidly evolving array of C2H2-type-Zincfingers (ZnF). We uncovered eighteen novel PRDM9 variants and evidence of rapid evolution, particularly of DNA-recognizing positions that evolve under positive selection. At different geographical scales, we observed extensive PRDM9 diversity in Antarctic minke whales (Balaenoptera bonarensis), that conversely lack observable population differentiation in mitochondrial DNA and microsatellites. In contrast, a single PRDM9 variant is shared between all Common Minke whales and even across subspecies boundaries of North Atlantic (B. a. acutorostrata) and North Pacific (B. a. scammoni) minke whale, which do show clear population differentiation. PRDM9 variation of whales predicts distinct recombination initiation landscapes genome wide, which has possible consequences for speciation.