Large-scale genomic rearrangements are a potential explanation for reproductive isolation in the Pogonomyrmex dependent-lineage system

Abstract

Genetic variation is the raw material for evolution. One source of variation is chromosomal rearrangements, which can bring genes together and form genetic linkage. Rearrangements can also suppress recombination and gene flow, as in the case of sex chromosome evolution. We conducted the first population genomic study of the red harvester ant Pogonomyrmex barbatus to investigate genomic rearrangements that differentiate the lineages J1 and J2 in the "dependent-lineage system" (also known as "social hybridogenesis"). In this unusual reproductive system, males and females from different lineages mate to create hybrids, yet these hybrids develop into sterile offspring (workers), and so the two lineages remain reproductively isolated. We sequenced high-quality reference genomes for the two lineages to search for a potential explanation of the suppression of gene flow between them. Comparison of the two genome assemblies revealed multiple large-scale genomic rearrangements, all of which occurred in the J1 lineage. The rearrangements formed some of the largest J1 chromosomes, including the largest scaffold in the assembly that was formed by at least two translocation events and additional intra-chromosomal rearrangements. The translocations brought together 118 odorant receptor (OR) genes on this rearranged chromosome, 44 of which are 9-exon ORs, which are implicated in chemical communication in ants. We also identified an enrichment of transposable elements in a large synteny gap between the translocated segments. The discovery of multiple translocations that formed large rearranged chromosomes provides a potential explanation for the reproductive isolation between the pair of dependent lineages in this system, and opens the way for the study of the molecular genetic basis of an intriguing evolutionary phenomenon in these and in other ant lineages.