Chromosome fusions repatterned recombination rate and facilitated reproductive isolation during Pristionchus nematode speciation

Abstract

AbstractLarge-scale genome-structural evolution is common in various organisms. Recent developments in speciation genomics revealed the importance of inversions, whereas the role of other genome-structural rearrangements, including chromosome fusions, have not been well characterized. We study genomic divergence and reproductive isolation of closely related nematodes: the androdioecious (hermaphroditic) modelPristionchus pacificusand its dioecious sister speciesPristionchus exspectatus. A chromosome-level genome assembly ofP. exspectatususing single-molecule and Hi-C sequencing revealed a chromosome-wide rearrangement relative toP. pacificus. Strikingly, genomic characterization and cytogenetic studies including outgroup speciesPristionchus occultusindicated two independent fusions involving the same chromosome, ChrIR, between these related species. Genetic linkage analysis indicated that these fusions altered the chromosome-wide pattern of recombination, resulting in large low-recombination regions that probably facilitated the coevolution between some of the ~14.8% of genes across the entire genomes. Quantitative trait locus analyses for hybrid sterility in all three sexes revealed that major quantitative trait loci mapped to the fused chromosome ChrIR. While abnormal chromosome segregations of the fused chromosome partially explain hybrid female sterility, hybrid-specific recombination that breaks linkage of genes in the low-recombination region was associated with hybrid male sterility. Thus, recent chromosome fusions repatterned recombination rate and drove reproductive isolation duringPristionchusspeciation.