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Abstract Vision is underpinned by phototransduction, a signaling cascade that converts light energy into an electrical signal. Among insects, phototransduction is best understood in Drosophila melanogaster. Comparison of D. melanogaster against three insect species found several phototransduction gene gains and losses, however, lepidopterans were not examined. Diurnal butterflies and nocturnal moths occupy different light environments and have distinct eye morphologies, which might impact the expression of their phototransduction genes. Here we investigated: 1) how phototransduction genes vary in gene gain or loss between D. melanogaster and Lepidoptera, and 2) variations in phototransduction genes between moths and butterflies. To test our prediction of phototransduction differences due to distinct visual ecologies, we used insect reference genomes, phylogenetics, and moth and butterfly head RNA-Seq and transcriptome data. As expected, most phototransduction genes were conserved between D. melanogaster and Lepidoptera, with some exceptions. Notably, we found two lepidopteran opsins lacking a D. melanogaster ortholog. Using antibodies we found that one of these opsins, a candidate retinochrome, which we refer to as unclassified opsin (UnRh), is expressed in the crystalline cone cells and the pigment cells of the butterfly, Heliconius melpomene. Our results also show that butterflies express similar amounts of trp and trpl channel mRNAs, whereas moths express ∼50× less trp, a potential adaptation to darkness. Our findings suggest that while many single-copy D. melanogaster phototransduction genes are conserved in lepidopterans, phototransduction gene expression differences exist between moths and butterflies that may be linked to their visual light environment.
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Phylogenomics reveals the evolutionary timing and pattern of butterflies and moths
Butterflies and moths (Lepidoptera) are one of the major superradiations of insects, comprising nearly 160,000 described extant species. As herbivores, pollinators, and prey, Lepidoptera play a fundamental role in almost every terrestrial ecosystem. Lepidoptera are also indicators of environmental change and serve as models for research on mimicry and genetics. They have been central to the development of coevolutionary hypotheses, such as butterflies with flowering plants and moths’ evolutionary arms race with echolocating bats. However, these hypotheses have not been rigorously tested, because a robust lepidopteran phylogeny and timing of evolutionary novelties are lacking. To address these issues, we inferred a comprehensive phylogeny of Lepidoptera, using the largest dataset assembled for the order (2,098 orthologous protein-coding genes from transcriptomes of 186 species, representing nearly all superfamilies), and dated it with carefully evaluated synapomorphy-based fossils. The oldest members of the Lepidoptera crown group appeared in the Late Carboniferous (∼300 Ma) and fed on nonvascular land plants. Lepidoptera evolved the tube-like proboscis in the Middle Triassic (∼241 Ma), which allowed them to acquire nectar from flowering plants. This morphological innovation, along with other traits, likely promoted the extraordinary diversification of superfamily-level lepidopteran crown groups. The ancestor of butterflies was likely nocturnal, and our results indicate that butterflies became day-flying in the Late Cretaceous (∼98 Ma). Moth hearing organs arose multiple times before the evolutionary arms race between moths and bats, perhaps initially detecting a wide range of sound frequencies before being co-opted to specifically detect bat sonar. Our study provides an essential framework for future comparative studies on butterfly and moth evolution.
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- Award ID(s):
- 1920936
- PAR ID:
- 10189077
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 116
- Issue:
- 45
- ISSN:
- 0027-8424
- Page Range / eLocation ID:
- 22657 to 22663
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.1907847116
