Abstract
Hybrid sterility is one of the reproductive isolation mechanisms leading to speciation. Prdm9, the only known vertebrate hybrid-sterility gene, causes failure of meiotic chromosome synapsis and infertility in male hybrids that are the offspring of two mouse subspecies. Within species, Prdm9 determines the sites of programmed DNA double-strand breaks (DSBs) and meiotic recombination hotspots. To investigate the relation between Prdm9-controlled meiotic arrest and asynapsis, we inserted random stretches of consubspecific homology on several autosomal pairs in sterile hybrids, and analyzed their ability to form synaptonemal complexes and to rescue male fertility. Twenty-seven or more megabases of consubspecific (belonging to the same subspecies) homology fully restored synapsis in a given autosomal pair, and we predicted that two or more DSBs within symmetric hotspots per chromosome are necessary for successful meiosis. We hypothesize that impaired recombination between evolutionarily diverged chromosomes could function as one of the mechanisms of hybrid sterility occurring in various sexually reproducing species.
Highlights
Hybrid sterility (HS) is a postzygotic reproductive isolation mechanism that enforces speciation by restricting gene flow between related taxa
All autosomes of hybrid males displayed a certain degree of asynapsis, classified as complete, partial, or intermingled, with frequencies ranging from 2.6% (Chr 1) to 42.2% (Chr 19) (Figure 2—source data 1)
The chromosomal length does not add any additional explanation of the asynapsis rate to that provided by symmetric double-strand breaks (DSBs) (p=0.709, comparison of GLMM models)
Summary
Hybrid sterility (HS) is a postzygotic reproductive isolation mechanism that enforces speciation by restricting gene flow between related taxa. The Bateson–Dobzhansky–Muller incompatibility (BDMI) hypothesis (Muller and Pontecorvo, 1942; Dobzhansky, 1951; Orr, 1996) explicated HS, and more generally any hybrid incompatibility, as a consequence of the independent divergence of mutually interacting genes resulting in aberrant interaction of the new alleles that have not been tested by natural selection. Haldane’s rule posits that if one sex of the F1 offspring of two different animal races is absent, rare, or sterile, it is the heterogametic sex (XY or ZW) (Haldane, 1922). Another common feature refers to the disproportionately large role of Chr X compared to that of autosomes in reproductive isolation (Presgraves, 2008). The asynapsis rate decreased from the maximal value
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