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Mol Biol Evol. 2017 Sep 1;34(9):2271-2284. doi: 10.1093/molbev/msx163.

Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies.

Author information

1
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA.
2
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ.
3
Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY.
4
School of Biological Sciences, Bangor University Brambell Laboratories, Bangor Gwynedd, UK.
5
Museo de Zoología, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, México, D.F., México.
6
The Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ.

Abstract

Numerous animal lineages have expanded and diversified the opsin-based photoreceptors in their eyes underlying color vision behavior. However, the selective pressures giving rise to new photoreceptors and their spectral tuning remain mostly obscure. Previously, we identified a violet receptor (UV2) that is the result of a UV opsin gene duplication specific to Heliconius butterflies. At the same time the violet receptor evolved, Heliconius evolved UV-yellow coloration on their wings, due to the pigment 3-hydroxykynurenine (3-OHK) and the nanostructure architecture of the scale cells. In order to better understand the selective pressures giving rise to the violet receptor, we characterized opsin expression patterns using immunostaining (14 species) and RNA-Seq (18 species), and reconstructed evolutionary histories of visual traits in five major lineages within Heliconius and one species from the genus Eueides. Opsin expression patterns are hyperdiverse within Heliconius. We identified six unique retinal mosaics and three distinct forms of sexual dimorphism based on ommatidial types within the genus Heliconius. Additionally, phylogenetic analysis revealed independent losses of opsin expression, pseudogenization events, and relaxation of selection on UVRh2 in one lineage. Despite this diversity, the newly evolved violet receptor is retained across most species and sexes surveyed. Discriminability modeling of behaviorally preferred 3-OHK yellow wing coloration suggests that the violet receptor may facilitate Heliconius color vision in the context of conspecific recognition. Our observations give insights into the selective pressures underlying the origins of new visual receptors.

KEYWORDS:

butterflies; color vision; gene duplication; photoreceptor cells; pseudogenes; short-wavelength opsin

PMID:
28505307
DOI:
10.1093/molbev/msx163
[Indexed for MEDLINE]

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