Genomics of altitude-associated wing shape in two tropical butterflies

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 study 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 1100 butterflies from 71 broods of H. erato and H. melpomene in common-garden conditions and show that wing aspect ratio, i.e. elongatedness, is highly heritable in both species and elevation-associated wing shape differences are maintained. Genome-wide associations with a published dataset of 666 whole genomes from across a hybrid zone, uncovered a highly polygenic basis to wing shape variation in the wild. We identify several genes that have roles in wing morphogenesis or wing shape 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 shape in two Heliconius species, adding to a growing body of evidence that polygenic adaptation may underlie many ecologically relevant traits.

Repeated genetic adaptation to high altitude in two tropical butterflies

“…With so many potential targets of selection within SHDRs, we do not attempt to infer biological function or adaptive significance from the whole gene set. Instead, we checked for overlaps with regions recently associated with wing shape variation across an altitudinal cline of Southern Ecuador in H. erato and H. melpomene 34 . Rounder wings are generally associated with high altitude across 13 species of Heliconius 33 and subtle altitudeassociated wing shape variation is highly heritable in H. erato and H. melpomene 34 .…”

“…Instead, we checked for overlaps with regions recently associated with wing shape variation across an altitudinal cline of Southern Ecuador in H. erato and H. melpomene 34 . Rounder wings are generally associated with high altitude across 13 species of Heliconius 33 and subtle altitudeassociated wing shape variation is highly heritable in H. erato and H. melpomene 34 . We found that five out of 12 previously identified candidate wing shape loci 34 , overlapped with SHDRs in H. erato, three of which corresponded to SHDRs detected in all transects.…”

“…Rounder wings are generally associated with high altitude across 13 species of Heliconius 33 and subtle altitudeassociated wing shape variation is highly heritable in H. erato and H. melpomene 34 . We found that five out of 12 previously identified candidate wing shape loci 34 , overlapped with SHDRs in H. erato, three of which corresponded to SHDRs detected in all transects. In contrast, only two wing shape loci (out of 16) overlapped with H. melpomene SHDRs, one of which was an allopatric SHDR.…”

“…One gene on chromosome 13 stood out, rugose, as it was associated with wing shape in both H. erato and H. melpomene 34 and overlapped with SHDRs shared in all transects in both species. In Drosophila mutants, rugose has been shown to affect social interactions, locomotion, and hyperactivity 68 .…”

“…In contrast, most other species in this genus have specialised to highland Andean or lowland Amazonian habitats, with topography and climate shown to correlate with speciation rates across the clade 32 . Phenotypic differences between highland and lowland populations of H. erato and H. melpomene have recently been identified, such as in wig shape 33,34 or heat tolerance 35 . We search for signatures of local adaptation to high altitude with extensive sampling that harnesses the power of natural spatial replication within and across sides of the Andes, in order to assess the extent of molecular parallelism in adaptation to high altitude.…”