Abstract
Understanding how organisms adapt to their local environment is central to evolution. With new whole-genome sequencing technologies and the explosion of data, deciphering the genomic basis of complex traits that are ecologically relevant is becoming increasingly feasible. Here, we studied the genomic basis of wing shape in two Neotropical butterflies that inhabit large geographical ranges. Heliconius butterflies at high elevations have been shown to generally have rounder wings than those in the lowlands. We reared over 1,100 butterflies from 71 broods of H. erato and H. melpomene in common-garden conditions and showed that wing aspect ratio, that is, elongatedness, is highly heritable in both species and that elevation-associated wing aspect ratio differences are maintained. Genome-wide associations with a published data set of 666 whole genomes from across a hybrid zone, uncovered a highly polygenic basis to wing aspect ratio variation in the wild. We identified several genes that have roles in wing morphogenesis or wing aspect ratio variation in Drosophila flies, making them promising candidates for future studies. There was little evidence for molecular parallelism in the two species, with only one shared candidate gene, nor for a role of the four known colour pattern loci, except for optix in H. erato. Thus, we present the first insights into the heritability and genomic basis of within-species wing aspect ratio in two Heliconius species, adding to a growing body of evidence that polygenic adaptation may underlie many ecologically relevant traits.
Highlights
Climate change is forcing organisms to “move, adapt, or die”
We combine the power of hybrid zones across steep environmental clines, common garden rearing, and whole-genome sequencing to study the genomic basis of a potentially adaptive trait in the wild
We found that wing aspect ratio is highly correlated between mothers and their offspring in two butterfly species, highly repeatable across common-garden reared offspring families, and correlated with the altitude at which the mother was collected (Figure 2)
Summary
Climate change is forcing organisms to “move, adapt, or die”. With temperatures rising and land-use changing in the lowlands, shifting to higher elevations might be the only way to flee extinction for many taxa (Chen et al, 2011). We used forward (GWAS) and reverse genetic approaches with wholegenome data of 666 of H. erato (n = 479) and H. melpomene (n = 187) individuals to identify regions associated with quantitative variation in wing aspect ratio and determined which regions diverged between extremes of the cline and had signatures of selective sweeps. This genomic data set was obtained from a study that developed a new low-cost linked-read sequencing technology, “haplotagging”, to examine colour pattern clines in an altitudinally structured hybrid zone (Figure 1c, Meier et al 2021). We present the first study to examine the heritability and genomic basis of wing aspect ratio of two butterfly species in the wild
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