Base Composition, Codon Usage, and Patterns of Gene Sequence Evolution in Butterflies

Abstract

Coding sequence evolution is influenced by both natural selection and neutral evolutionary forces. In many species, the effects of mutation bias, codon usage and GC-biased gene conversion (gBGC) on gene sequence evolution have not been detailed. Quantification of how these forces shape substitution patterns is therefore necessary to understand the strength and direction of natural selection. Here, we used comparative genomics to investigate the association between base composition and codon usage bias on gene sequence evolution in butterflies and moths (Lepidoptera), including an in-depth analysis of underlying patterns and processes in one species, Leptidea sinapis. The data revealed significant G/C to A/T substitution bias at third codon position with some variation in the strength among different butterfly lineages. However, the substitution bias was lower than expected from previously estimated mutation rate ratios, partly due to the influence of gBGC. We found that A/T-ending codons were overrepresented in most species, but there was a positive association between the magnitude of codon usage bias and GC-content in third codon positions. In addition, the tRNA-gene population in L. sinapis showed higher GC-content at third codon positions compared to coding sequences in general and less overrepresentation of A/T-ending codons. There was an inverse relationship between synonymous substitutions and codon usage bias indicating selection on synonymous sites. We conclude that the evolutionary rate in Lepidoptera is affected by a complex interaction between underlying G/C -> A/T mutation bias and partly counteracting fixation biases, predominantly conferred by overall purifying selection, gBGC and selection on codon usage.

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

“…In some insects, codon usage is associated with transfer RNA (tRNA) abundance (Behura and Severson, 2011; Näsvall et al, 2023b). In Machimus atricapillus , we observed the expected result of significant positive correlation between tRNA gene count and codon frequency (Pearson’s product moment correlation coefficient; r = 0.86, P < 1.033e-07; Figure 6B; Supplementary Figure S4), implying more frequent codons in the genome utilise a greater number of tRNAs.…”

“…Superimposed on the overall low GC percentage of the honeybee genome is a bimodal pattern of GC content (Jørgensen et al, 2007; Kent and Zayed, 2013), which like the gerbil and bird examples caused genes to be missed during genome sequencing (Elsik et al, 2014). In addition, at least in one lepidopteran genus ( Leptidea ), evidence for gBGC has recently been reported (Boman et al, 2021; Näsvall et al, 2023b). The recent advent of long-read DNA sequencing, coupled with Hi-C sequencing, has enabled the rapid generation of very high quality genome assemblies.…”

The last days ofAporia crataegi(L.) in Britain: evaluating genomic erosion in an extirpated butterfly

“…Additionally, we also observed statistically significant increase in realised load but this was limited to only synonymous variants. Although synonymous variants are normally classified as neutral, they can be weakly deleterious under codon bias and Lepidoptera do exhibit an A/T codon usage bias (Näsvall et al ., 2023). In contrast, P. icarus displayed a decrease in realised load (Fig.…”