A macroevolutionary role for chromosomal fusion and fission in Erebia butterflies.

The impact of large-scale chromosomal rearrangements, such as fusions and fissions, on speciation is a long-standing conundrum. We assessed whether bursts of change in chromosome numbers resulting from chromosomal fusion or fission are related to increased speciation rates in Erebia, one of the most species-rich and karyotypically variable butterfly groups. We established a genome-based phylogeny and used state-dependent birth-death models to infer trajectories of karyotype evolution. We demonstrated that rates of anagenetic chromosomal changes (i.e., along phylogenetic branches) exceed cladogenetic changes (i.e., at speciation events), but, when cladogenetic changes occur, they are mostly associated with chromosomal fissions rather than fusions. We found that the relative importance of fusion and fission differs among Erebia clades of different ages and that especially in younger, more karyotypically diverse clades, speciation is more frequently associated with cladogenetic chromosomal changes. Overall, our results imply that chromosomal fusions and fissions have contrasting macroevolutionary roles and that large-scale chromosomal rearrangements are associated with bursts of species diversification.

Speciation through chromosomal fusion and fission in Lepidoptera.

Changes in chromosome numbers may strongly affect reproductive barriers, because individuals heterozygous for distinct karyotypes are typically expected to be at least partially sterile or to show reduced recombination. Therefore, several classic speciation models are based on chromosomal changes. One import mechanism generating variation in chromosome numbers is fusion and fission of existing chromosomes, which is particularly likely in species with holocentric chromosomes, i.e. chromosomes that lack a single centromere. Holocentric chromosomes evolved repeatedly across the tree of life, including in Lepidoptera. Although changes in chromosome numbers are hypothesized to be an important driver of the spectacular diversification of Lepidoptera, comparative studies across the order are lacking. We performed the first comprehensive literature survey of karyotypes for Lepidoptera species since the 1970s and tested if, and how, chromosomal variation might affect speciation. Even though a meta-analysis of karyological differences between closely related taxa did not reveal an effect on the degree of reproductive isolation, phylogenetic diversification rate analyses across the 16 best-covered genera indicated a strong, positive association of rates of chromosome number evolution and speciation. These findings suggest a macroevolutionary impact of varying chromosome numbers in Lepidoptera and likely apply to other taxonomic groups, especially to those with holocentric chromosomes. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.