Do chromosome rearrangements fix by genetic drift or natural selection? Insights from Brenthis butterflies

• Published in: Molecular ecology 2024-12, Vol.33 (24), p.e17146-n/a
• Main Authors: Mackintosh, Alexander, Vila, Roger, Martin, Simon H., Setter, Derek, Lohse, Konrad
• Format: Article
• Language: English
• Subjects: Animals; Butterflies - genetics; Chromosome rearrangements; Chromosomes; Gene Rearrangement - genetics; Genetic Drift; Genetics, Population; Genome, Insect; Genomes; genomics/proteomics; inbreeding; insects; molecular evolution; Natural selection; natural selection and contemporary evolution; Original; ORIGINAL ARTICLE; Population genetics; population genetics ‐ empirical; Populations; Reproductive fitness; Selection, Genetic
• ISSN: 0962-1083; 1365-294X; 1365-294X
• DOI: 10.1111/mec.17146

Large‐scale chromosome rearrangements, such as fissions and fusions, are a common feature of eukaryote evolution. They can have considerable influence on the evolution of populations, yet it remains unclear exactly how rearrangements become established and eventually fix. Rearrangements could fix by genetic drift if they are weakly deleterious or neutral, or they may instead be favoured by positive natural selection. Here, we compare genome assemblies of three closely related Brenthis butterfly species and characterize a complex history of fission and fusion rearrangements. An inferred demographic history of these species suggests that rearrangements became fixed in populations with large long‐term effective size (N e), consistent with rearrangements being selectively neutral or only very weakly underdominant. Using a recently developed analytic framework for characterizing hard selective sweeps, we find that chromosome fusions are not enriched for evidence of past sweeps compared to other regions of the genome. Nonetheless, we do infer a strong and recent selective sweep around one chromosome fusion in the B. daphne genome. Our results suggest that rearrangements in these species likely have weak absolute fitness effects and fix by genetic drift. However, one putative selective sweep raises the possibility that natural selection may sometimes play a role in the fixation of chromosome fusions.