A macroevolutionary role for chromosomal fusion and fission inErebiabutterflies

Abstract

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 and 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 employed state-dependent birth-death models to infer trajectories of karyotype evolution across this genus. We demonstrate 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. Moreover, we found that the relative importance of fusion and fission differs among Erebia clades of different ages, where especially in younger, more karyotypically diverse clades, speciation is more frequently associated with 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.

Living on the edge—Genomic and ecological delineation of cryptic lineages in the high‐elevation specialist Erebia nivalis

“…We excluded monomorphic sites and sites with missing data for a resulting dataset containing about 33k SNPs. We set up SNAPP as in Stange et al (2018) with a strict clock model and used the divergence between E. cassioides and E. nivalis in Augustijnen et al (2023) as a dating constraint. The age of this node was previously estimated to be 1.4783 Mya (95% highest posterior density interval (HPD): 0.8606-2.6302), which was approximated in our new inference by a lognormal distribution with offset 0, mean 1.4783 and standard deviation 0.1: lognormal (0,1.4783,0.1).…”

“…The butterfly genus Erebia Dalman, 1816 (Lepidoptera: Nymphalidae, and Satyrinae) comprises approximately 100 described species that occur across the Northern Hemisphere, with a hotspot in central Europe (Peña et al, 2015). The diversity of Erebia is a result of repeated range shifts during glacial cycles, associated with isolation in different refugia (Peña et al, 2015), ecological differentiation (Klečková et al, 2014) and chromosomal rearrangements that likely promoted reproductive isolation (Augustijnen et al, 2023). As Erebia species are often restricted to mountainous or otherwise cold environments and often have geographically isolated populations, they have been considered model species to study biodiversity loss in mountain butterflies (e.g., De Groot et al, 2009; Minter et al, 2020; Romo et al, 2023; Scalercio et al, 2014; Sistri et al, 2022).…”

Meiotic drive against chromosome fusions in butterfly hybrids

“…Most lepidopteran species have a chromosome number close to n = 31, but substantial variation exists (Lorković 1941; Lukhtanov 2014; de Vos et al 2020). Macroevolutionary studies have shown that chromosome number variation is positively associated with the rate of speciation in some specific butterfly genera that have extensive karyotype differences between species (de Vos et al 2020; Augustijnen et al 2023). However, it is still unclear if the interspecific difference in karyotype is a result of genetic drift, natural selection, or some other fixation bias, such as meiotic drive.…”

Evolution of hybrid inviability associated with chromosome fusions

“…While L. sinapis has extreme intraspecific karyotype variation, several other groups of butterflies show extensive interspecific chromosome number variation. For example between species in the Leptidea ( 37 ), Polyommatus ( 38 ) and Erebia ( 39 ) genera, and the tribe Ithomiini ( 40 ). Chromosome number variation in some of these groups are associated with increased diversification rates ( 41 ), indicating that rearrangements may have been involved in the establishment of reproductive barriers.…”