Speciation through chromosomal fusion and fission in Lepidoptera

Abstract

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’.

Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers

“…Progress will come from a combination of case studies of taxon pairs nearing complete isolation (see Stankowski et al [14], Yamasaki et al [15], Osborne et al [74] and North et al [29] in this theme issue), comparative approaches (e.g. de Vos et al [5] and Meyers et al [35] in this theme issue), theoretical studies highlighting what drives and hinders the evolution of strong RI (e.g. Blanckaert et al [16], Payne & Polechová [17] and Bisschop et al [18] in this issue), metaanalyses (as discussed in Rometsch et al [31] and Shang et al [44] in this issue), the identification of processes defining stages (see Muschick et al [23] and Tinghitella et al [32] in this issue) and combined approaches as outlined in this issue (Coughlan & Matute [30] and Satokangas et al [33]).…”

“…However, continuing divergence is not strictly part of the speciation process and in this theme issue we do not consider continuing divergence after the completion of RI. Occasionally strong RI can appear rapidly, even in a single generation, in the case of ploidy change [4], chromosomal rearrangements (as reviewed by de Vos et al [5] in this issue) and perhaps following hybridization [6,7]. However, more often the accumulation of barriers to gene flow is an extended process in which RI evolves slowly.…”

Chromosome fusion affects genetic diversity and evolutionary turnover of functional loci, but consistently depends on chromosome size

“…The consequences of chromosome fusions occur via two main effects. First, fusions can disrupt meiotic sorting of chromosomes in heterozygous individuals or result in imbalanced gametes, both of which can lead to reproductively isolated "chromosomal races" (3)(4)(5) . Second, fusion events reduce the number of unlinked DNA molecules, which results in less independence among loci.…”

Secondary contact zones of closely‐related Erebia butterflies overlap with narrow phenotypic and parasitic clines

“…Importantly, changes in chromosome numbers were more frequently anagenetic-occurring along a branch of the phylogenetic tree rather than at a speciation event. Novel chromosomes may therefore help to build up reproductive isolation over time, for example by suppressing recombination, whereas some gene flow might still be possible (de Vos et al, 2020).…”