Abstract
Major changes in chromosome number and structure are linked to a series of evolutionary phenomena, including intrinsic barriers to gene flow or suppression of recombination due to chromosomal rearrangements. However, chromosome rearrangements can also affect the fundamental dynamics of molecular evolution within populations by changing relationships between linked loci and altering rates of recombination. Here, we build chromosome-level assembly Eueides isabella and, together with a recent chromosome-level assembly of Dryas iulia, examine the evolutionary consequences of multiple chromosome fusions in Heliconius butterflies. These assemblies pinpoint fusion points on 10 of the 20 autosomal chromosomes and reveal striking differences in the characteristics of fused and unfused chromosomes. The ten smallest autosomes in D. iulia and E. isabella, which have each fused to a longer chromosome in Heliconius, have higher repeat and GC content, and longer introns than predicted by their chromosome length. When fused, these characteristics change to become more in line with chromosome length. The fusions also led to reduced diversity, which likely reflects increased background selection and selection against introgression between diverging populations, following a reduction in per-base recombination rate. We further show that chromosome size and fusion impact turnover rates of functional loci at a macroevolutionary scale. Together these results provide further evidence that chromosome fusion in Heliconius likely had dramatic effects on population level processes shaping rates of neutral and adaptive divergence. These effects may have impacted patterns of diversification in Heliconius, a classic example of an adaptive radiation.
Highlights
Structural changes in the genome can be an important factor for speciation (Feulner and De-Kayne 2017), population divergence, and adaptation (De Storme and Mason 2014)
Chromosome-Level Assembly of the Eueides isabella Genome and Serial Chromosome Fusion at the Origin of Heliconius Using a combination of high coverage long (Pacific Biosciences reads) and short-read data, we generated a highly complete de novo assembly for E. isabella
We have shown that Nymphalidae chromosomes differ significantly by size, both in terms of nucleotide composition and gene structure
Summary
Structural changes in the genome can be an important factor for speciation (Feulner and De-Kayne 2017), population divergence, and adaptation (De Storme and Mason 2014). Studies of structural evolution often focus on small to mediumscale structural variants, such as inversions or translocations, large-scale structural changes, like chromosome fusion, can have substantial and immediate evolutionary impacts. Fusion events reduce the number of unlinked DNA molecules, which results in less independence among loci. This lower per chromosome recombination rate may be favored in certain circumstances. Fusions may aid adaptation if recombination is reduced between coadapted alleles at multiple loci (Guerrero and Kirkpatrick 2014; Veller et al 2019, 2020). A beneficial alteration of the recombination landscape might explain why chromosomal fusions could become fixed despite initial deleterious impacts on meiosis in species with monocentric chromosomes (Lunt et al 2014; Fradin et al 2017)
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