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

Abstract

Genetic recombination is a key molecular mechanism that has profound implications on both micro- and macro-evolutionary processes. However, the determinants of recombination rate variation in holocentric organisms are poorly understood, in particular in Lepidoptera (moths and butterflies). The wood white butterfly (Leptidea sinapis) shows considerable intraspecific variation in chromosome numbers and is a suitable system for studying regional recombination rate variation and its potential molecular underpinnings. Here, we developed a large whole genome resequencing data set from a population of wood whites to obtain high-resolution recombination maps using linkage disequilibrium information. The analyses revealed that larger chromosomes had a bimodal recombination landscape, potentially due to interference between simultaneous chiasmata. The recombination rate was significantly lower in subtelomeric regions, with exceptions associated with segregating chromosome rearrangements, showing that fissions and fusions can have considerable effects on the recombination landscape. There was no association between the inferred recombination rate and base composition, supporting a negligible influence of GC-biased gene conversion in butterflies. We found significant but variable associations between the recombination rate and the density of different classes of transposable elements (TEs), most notably a significant enrichment of SINEs in genomic regions with higher recombination rate. Finally, the analyses unveiled significant enrichment of genes involved in farnesyltranstransferase activity in recombination cold-spots, potentially indicating that expression of transferases can inhibit formation of chiasmata during meiotic division. Our results provide novel information about recombination rate variation in holocentric organisms and has particular implications for forthcoming research in population genetics, molecular/genome evolution and speciation.

Sex-specific recombination landscape in a species with holocentric chromosomes

“…The absence of this association in bulb mites might be explained by the heterogeneous distribution of GC content across chromosomes, peaking in gene-dense central regions and similarly elevated in the highly recombining chromosome ends (Figure 3B). Yet, among holocentric organisms, the relationship between recombination rate and GC content shows variable patterns, ranging from negative association (Bernstein & Rockman, 2016; Kaur & Rockman, 2014; Torres et al, 2023) to positive ones (Stapley et al, 2017) suggesting a complex interplay between GC-biased gene conversion and opposing mutation bias toward AT nucleotides (Boman et al, 2021).…”

A macroevolutionary role for chromosomal fusion and fission inErebiabutterflies

“…The higher overall degree of anagenetic fusions observed in this study might reflect their ability to gradually reduce recombination rates, as has been found in mice [ 44 ], and other butterflies [ 45 ]. Genome-wide crossing-over rates correspondingly seem to be considerably higher when chromosomes are short, or evolve to become shorter [ 46 , but see 47 ].…”

GC content across insect genomes: phylogenetic patterns, causes and consequences

“…We suggest that the increase in GC content towards the ends of chromosomes implies that GC-biased gene conversion (gBGC) is prevalent in Lepidoptera, Hymenoptera and Coleoptera genomes. This implication is drawn because gBGC is a recombination-associated event (Duret and Galtier, 2009; Figuet et al, 2014; Pessia et al, 2012; Romiguier and Roux, 2017) and there is evidence that recombination rates increase towards the subtelomeric regions of chromosomes in insects, as in many other taxa (Coop and Przeworski, 2007; Haenel et al, 2018; Ma et al, 2015; Mouresan et al, 2019; Näsvall et al, 2023a; Rockman et al, 2010; Shipilina et al, 2022; Torres et al, 2023).…”