High-density linkage maps and chromosome level genome assemblies unveil direction and frequency of extensive structural rearrangements in wood white butterflies (Leptideaspp.)

Abstract

Karyotypes are generally conserved between closely related species and large chromosome rearrangements typically have negative fitness consequences in heterozygotes, potentially driving speciation. In the order Lepidoptera, most investigated species have the ancestral karyotype and gene synteny is often conserved across deep divergence, although examples of extensive genome reshuffling have recently been demonstrated. The genus Leptidea has an unusual level of chromosome variation and rearranged sex chromosomes, but the extent of restructuring across the rest of the genome is so far unknown. To explore the genomes of the wood white (Leptidea) species complex, we generated eight genome assemblies using a combination of 10X linked reads and HiC data, and improved them using linkage maps for two populations of the common wood white (L. sinapis) with distinct karyotypes. Synteny analysis revealed an extensive amount of rearrangements, both compared to the ancestral karyotype and between the Leptidea species, where only one of the three Z chromosomes was conserved across all comparisons. Most restructuring was explained by fissions and fusions, while translocations appear relatively rare. We further detected several examples of segregating rearrangement polymorphisms supporting a highly dynamic genome evolution in this clade. Fusion breakpoints were enriched for LINEs and LTR elements, which suggests that ectopic recombination might be an important driver in the formation of new chromosomes. Our results show that chromosome count alone may conceal the extent of genome restructuring and we propose that the amount of genome evolution in Lepidoptera might still be underestimated due to lack of taxonomic sampling.

The fine-scale recombination rate variation and associations with genomic features in a butterfly

“…As mentioned above, our results showed that the reduced recombination rate towards chromosome ends was not ubiquitous across all chromosomes; eight chromosome ends (one for each of the following chromosomes: 5, 6, 10, 11, 16, 25, 27 and 29) did not show a significant reduction in the recombination rate as compared to each respective intra-chromosomal level. Four of these exceptions (one chromosome end for each of chromosomes 5, 11, 25 and 27) coincide with recently identified fission and fusion polymorphisms segregating in the wood white population in Scandinavia (Höök et al 2022). These results show that fission/fusion events can have immediate effects on the distribution of crossover events within and between chromosomes.…”

“…A formal analysis showed that the recombination rate in the subtelomeres (last 5 100 kb windows at each end of the chromosomes) was significantly reduced (2.46 cM / Mb) compared to the 100 kb windows located in proximal positions of the chromosomes i.e., outside of the subtelomeric regions (Wilcoxon’s test, W = 1,310,856, p-value = 3.18 * 10 −66 ). It should be noted that this does not necessarily reflect a low recombination rate in the telomeres, but rather in the subtelomeric regions, since telomeric repeats were not covered in the wood white genome assembly (Höök et al 2022). We also analyzed each chromosome separately and found a reduction in recombination rate in subtelomeric regions in 50 out of the 58 chromosome ends (29 chromosome pairs, 2n = 58; Supplementary Table 1).…”

“…Potential associations between recombination and TE densities have mainly been investigated in organisms with defined centromeres (Kent et al 2017), while investigations in holocentric species are scarce (but see Lavoie et al 2013, Baril Hayward 2022, Smolander et al 2022). To investigate the potential asso- ciations between the recombination rate and genomic features in the wood white, we used density information for TEs previously identified in the species (Höök et al 2022). The analysis revealed that associations between the recombination rate and the abundance of TEs varied considerably depending on the TE class.…”

“…The wood white genome assembly used as reference was developed for another study (Höök et al 2022). In brief, one mated adult female wood white was caught in Sweden and kept in the lab for egg laying.…”

“…Hence, some wood white populations differ significantly from the ancestral Lepidoptera chromosome number of n = 31 (Robinson 1971, Ahola et al 2014). Previous studies suggest that recurrent chromosome fissions and fusions underlie this variation (Dincă et al 2011, Talla et al 2017) and that at least a handful of fission/fusion polymorphisms segregate in the Swedish population (Höök et al 2022). The rapid karyotype evolution in wood whites provides a unique system for characterizing the regional variation in recombination rate in a natural population of a holocentric species, and combining it with investigating the effects of segregating chromosome rearrangements on the recombination landscape.…”