Clines, Hybrids, and Duplicates: Genome Scanning Shows Pathways to Intragenomic Adaptation

Whole genome duplication (WGD) is evident in the evolutionary histories of plants, vertebrates, insects, and fungi. In addition, natural WGD events have been dated to recent centuries, providing opportunities to study WGD in contemporary contexts. Doubling the number of gene homologs, WGD engenders adaptive flexibility, but also presents a serious threat to proper chromosome segregation, an essential conserved process. Nevertheless, early difficulties can be overcome. To understand the basis of adaptation to WGD, we measured signatures of selection in natural diploids and tetraploids from several species groups, including Arabidopsis arenosa, an outcrossing relative of A. thaliana. We first show that A. arenosa diploids are not preadapted to tetraploid meiosis, indicating that the meiotic machinery in fact faces a challenge upon WGD. We then resequenced 16 tetraploid and eight diploid individuals and calculated genome-wide measures of differentiation. An overlap of multiple differentiation metrics shows clear ploidy-specific differentiation in 39 regions spanning 44 genes; most regions contain a single gene, with rapid flanking decay. Among these are eight genes whose encoded proteins coordinate a subset of early meiotic functions: all are important for alignment and synapsis of homologous chromosomes and controlled formation of meiotic crossovers. This suggests that selection acted on unlinked loci to reorchestrate the events of early prophase I. We are currently investigating whether similar polygenic solutions to WGD are common by performing genome scans in other species, each with multiple recent WGD events. Our work indicates that even conserved meiotic processes are capable of nimble evolutionary shifts when required.