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UC Irvine UC Irvine Previously Published Works UC Irvine UC Irvine Previously Published Works Title Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies. Permalink https://escholarship.org/uc/item/0rn1k318 Journal Molecular biology and evolution, 34(9) ISSN 0737-4038 Authors McCulloch, Kyle J Yuan, Furong Zhen, Ying et al. Publication Date 2017-09-01 DOI 10.1093/molbev/msx163 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Sexual Dimorphism and Retinal Mosaic Diversification following the Evolution of a Violet Receptor in Butterflies Kyle J. McCulloch,*,1 Furong Yuan,1 Ying Zhen,2 Matthew L. Aardema,2,3 Gilbert Smith,1,4 Jorge Llorente-Bousquets,5 Peter Andolfatto,2,6 and Adriana D. Briscoe*,1 1Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 2Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 3Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY 4School of Biological Sciences, Bangor University Brambell Laboratories, Bangor Gwynedd, UK 5Museo de Zoologıa, Departamento de Biologıa Evolutiva, Facultad de Ciencias, Universidad Nacional AutonomadeMe ´xico, Me´xico, D.F., Me´xico Downloaded from https://academic.oup.com/mbe/article-abstract/34/9/2271/3827455 by guest on 24 December 2019 6The Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ *Corresponding authors: E-mails: [email protected]; [email protected]. Associate editor: Patricia Wittkopp 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 behav- iorally 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. Key words: butterflies, color vision, photoreceptor cells, short-wavelength opsin, gene duplication, pseudogenes. Article Introduction variable. Diversity in cichlid spectral classes of photoreceptors How animal eyes have evolved to handle the variety of col- is also produced by expression level differences (O’Quin et al. orful stimuli they encounter in their world is a key question in 2012; Schulte et al. 2014), coexpression of opsins (Dalton et al. visual ecology. Across the animal kingdom, the number of 2017), and by structural changes in the opsin gene (Parry et al. opsin-based photoreceptors used by different species for vi- 2005; Seehausen et al. 2008; Hofmann and Carleton 2009; sion is highly variable. Some insects like honeybees have eyes Dalton et al. 2015). Another example is dragonflies which containing only three opsin-based photoreceptors express up to 30 opsin mRNA transcripts, a number that (Wakakuwa et al. 2005;seeFriedrich et al. 2011 for an over- varies between families within the order, although it is not view). Other animals have evolved a greatly expanded pho- yet known in which photoreceptor cells these opsins are ex- toreceptor set, mediated by opsin duplication, expression pressed (Futahashi et al. 2015) differences, and filtering effects in the eye. For instance, mantis The family Papilionidae alone contains species with eight shrimp have at least 16 spectrally distinct photoreceptors, (Papilio xuthus)(Koshitaka et al. 2008), nine (Troides aecus) which they have achieved through multiple opsin gene du- (Chen et al. 2013), and 15 (Graphium sarpedon)(Chen et al. plications as well as complex patterns of filtering in the eye 2016) spectral classes of photoreceptor. Other groups of but- (Cronin and Marshall 1989; Cronin et al. 2014; Bok et al. 2015). terflies, notably those in the family Nymphalidae, get by with African cichlid fishes have seven ancestrally duplicated opsin three opsins (Briscoe et al. 2003; Macias-Munoz~ et al. 2016), genes, and across the cichlid family the subset of these opsins and some even lack the heterogeneously expressed filtering that are expressed in the photoreceptors of a given species is pigments that expand the number of long wavelength- ß The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: [email protected] Mol. Biol. Evol. 34(9):2271–2284 doi:10.1093/molbev/msx163 Advance Access publication May 15, 2017 2271 McCulloch et al. doi:10.1093/molbev/msx163 MBE sensitive photoreceptors found in other butterflies (Briscoe the H. erato eye is sexually dimorphic; each sex possesses a and Bernard 2005). Thus, butterflies rival the mantis shrimp in distinct set of ommatidial types based on short-wavelength sheer number of spectral types of photoreceptor but some opsin expression (fig. 1A–D). By contrast, other investigated butterfly species are more like bees, with only three types. nymphalid butterflies such as Danaus plexippus, Limenitis However, even among the relatively well-studied butterflies, arthemis astyanax and Vanessa cardui have sexually mono- visual system comparisons between closely related species are morphic eyes (Briscoe et al. 2003; Sauman et al. 2005; Frentiu rare (although see Frentiu et al. 2007a; Chen et al. 2016). Also, et al. 2015). Female H. erato have UV1, UV2, blue (B), and long while high levels of photoreceptor spectral diversity have wavelength (L) rhodopsin-expressing cells with peak sensitiv- been observed across animal families such as Papilionidae, ities at 355, 390, 470, and 555 nm, respectively. Males have the far less is known about diversification of eyes between closely same opsins and sensitivities except they lack a UV1- related species. Given the importance of the social use of expressing photoreceptor cell (McCulloch et al. 2016a). The color in animals, especially butterflies, it would be surprising complete absence of one class of opsin in one sex is a new Downloaded from https://academic.oup.com/mbe/article-abstract/34/9/2271/3827455 by guest on 24 December 2019 if photoreceptor spectral diversification did not play some form of sexual dimorphism. Among butterflies with known role in speciation. Yet we know little about the first steps in visual system sex differences, opsin mRNA expression levels eye evolution immediately following the fixation of duplicate are sexually dimorphic in the dry season forms of the nym- opsin genes. phalid Bicyclus anynana (Everett et al. 2012). Male and female Moreover, while numerous kinds of photoreceptors have pierids have the same opsin spatial expression patterns, been discovered in different organisms, the benefits to evolv- whereas spectral sensitivity is tuned by sexually dimorphic ing a new spectral type of photoreceptor and a visual system spatial expression of filter pigments (Arikawa et al. 2005; making use of it are less well understood. Here we begin to Ogawa et al. 2012, 2013). In some lycaenid butterflies, sex close this gap in our knowledge of visual system evolution by differences are achieved by coexpression of two opsins in conducting an extensive investigation of the retinal mosaics the photoreceptor cells of a female-specific ommatidial and opsin sequence evolution of Heliconius species in com- type (Sison-Mangus et al. 2006). parisontooutgroupspeciesinthegenusEueides. Famous for In light of the rapidly evolving wing signals within and be- their spectacular wing color pattern evolution and mimicry, tween species in the genus Heliconius (for examples of wing Heliconius butterflies are also interesting for their eyes (Reed color pattern variation in H. erato and H. melpomene see Van et al. 2011; Martin et al. 2012; Nadeau et al. 2016). Other Belleghem et al. 2017 and Heliconius Genome Consortium nymphalid butterflies like the monarch butterfly Danaus plex- 2012) and the novel pattern of UV opsin expression found ippus or the painted lady Vanessa cardui have eyes that ex- in H. erato, we thought that Heliconius would be a good can- press three opsins which together with the chromophore 11- didate for investigating how eye evolution and speciation cis-3-hydroxyretinal encode ultraviolet (UV)-, blue (B)-, and might relate to one another. Other Heliconius
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