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.

Holocentric repeat landscapes: From micro-evolutionary patterns to macro-evolutionary associations with karyotype evolution.

Repetitive elements can cause large-scale chromosomal rearrangements, for example through ectopic recombination, potentially promoting reproductive isolation and speciation. Species with holocentric chromosomes, that lack a localized centromere, might be more likely to retain chromosomal rearrangements that lead to karyotype changes such as fusions and fissions. This is because chromosome segregation during cell division should be less affected than in organisms with a localized centromere. The relationships between repetitive elements and chromosomal rearrangements and how they may translate to patterns of speciation in holocentric organisms are though poorly understood. Here, we use a reference-free approach based on low-coverage short-read sequencing data to characterize the repeat landscape of two independently evolved holocentric groups: Erebia butterflies and Carex sedges. We consider both micro- and macro-evolutionary scales to investigate the repeat landscape differentiation between Erebia populations and the association between repeats and karyotype changes in a phylogenetic framework for both Erebia and Carex. At a micro-evolutionary scale, we found population differentiation in repeat landscape that increases with overall intraspecific genetic differentiation among four Erebia species. At a macro-evolutionary scale, we found indications for an association between repetitive elements and karyotype changes along both Erebia and Carex phylogenies. Altogether, our results suggest that repetitive elements are associated with the level of population differentiation and chromosomal rearrangements in holocentric clades and therefore likely play a role in adaptation and potentially species diversification.

The genome sequence of the scotch argus butterfly, Erebia aethiops (Esper, 1777).

We present a genome assembly from an individual female Erebia aethiops (the scotch argus; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 473 megabases in span. The complete assembly is scaffolded into 20 chromosomal pseudomolecules, with the W and Z sex chromosomes assembled. The complete mitochondrial genome was also assembled and is 15.2 kilobases in length.

Secondary contact rather than coexistence-Erebia butterflies in the Alps.

Secondary contact zones are ideal systems to study the processes that govern the evolution of reproductive barriers, especially at advanced stages of the speciation process. An increase in reproductive isolation resulting from selection against maladaptive hybrids is thought to contribute to reproductive barrier buildup in secondary contact zones. Although such processes have been invoked for many systems, it remains unclear to which extent they influence contact zone dynamics in nature. Here, we study a very narrow contact zone between the butterfly species Erebia cassioides and Erebia tyndarus in the Swiss Alps. We quantified phenotypic traits related to wing shape and reproduction as well as ecology to compare the degree of intra- and interspecific differentiation. Even though only very few first-generation hybrids occur, we find no strong indications for current reinforcing selection, suggesting that if reinforcement occurred in our system, it likely operated in the past. Additionally, we show that both species differ less in their ecological niche at the contact zone than elsewhere, which could explain why coexistence between these butterflies may currently not be possible.

A holocentric twist to chromosomal speciation?

Chromosomal rearrangements trigger speciation by acting as barriers to gene flow. However, the underlying theory was developed with monocentric chromosomes in mind. Holocentric chromosomes, lacking a centromeric region, have repeatedly evolved and account for a significant fraction of extant biodiversity. Because chromosomal rearrangements may be more likely retained in holocentric species, holocentricity could provide a twist to chromosomal speciation. Here, we discuss how the abundance of chromosome-scale genomes, combined with novel analytical tools, offer the opportunity to assess the impacts of chromosomal rearrangements on rates of speciation by outlining a phylogenetic framework that aligns with the two major lines of chromosomal speciation theory. We further highlight how holocentric species could help to test for causal roles of chromosomal rearrangements in speciation.

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'.