COIS 257 1–8 Available online at www.sciencedirect.com ScienceDirect 21 3 Color vision and color formation in dragonflies Q1 Ryo Futahashi 4 53 5 Dragonflies including damselflies are colorful and large-eyed eyes (ommatidia). By contrast, dragonflies lack the tym- 54 6 insects, which show remarkable sexual dimorphism, color panal organ or ears, and their antennae are reduced and 55 7 transition, and color polymorphism. Recent comprehensive degenerated, implying their poor sense of audition and 56 8 visual transcriptomics has unveiled an extraordinary diversity of olfaction. Only a few papers have reported usage of 57 9 opsin genes within the lineage of dragonflies. These opsin chemical cues in adult dragonflies [2 ,3 ]. Unlike most 58 10 genes are differentially expressed between aquatic larvae and insects, many dragonflies change their colors during their 59 11 terrestrial adults, as well as between dorsal and ventral regions adult period. Immature males often look like females, and 60 12 of adult compound eyes. Recent topics of color formation in dramatically change their coloration in the maturation 61 13 dragonflies are also outlined. Non-iridescent blue color is process, resulting in conspicuous sexual dimorphism 62 14 caused by coherent light scattering from the quasiordered (Figure 1a). Previous ecological studies have shown that 63 15 nanostructures, whereas iridescent color is produced by their behavior is strongly dependent on visual cues [4–9]. 64 16 multilayer structures. Wrinkles or wax crystals sometimes For example, interspecific tandems have been sometimes 65 17 enhances multilayer structural colors. Sex-specific and stage- observed in the field between similarly colored species 66 18 specific color differences in red dragonflies is attributed to (Figure 1b,c) [4,10–12]. Notably, male–male tandems 67 redox states of ommochrome pigments. have been occasionally reported in species with small 68 19 69 20 Address sexual dimorphism [4,10,11,13]. One interesting example 21 70 Bioproduction Research Institute, National Institute of Advanced of male–male tandem was reported in the tiny dragonfly 22 Industrial Science and Technology (AIST), Central 6, Tsukuba, Ibaraki Nannophya pygmaea. The sexual dimorphism of N. pyg- 71 23 305-8566, Japan 72 24 maea is very distinct; mature males are reddish while mature females are blackish (Figure 1d). A spontaneous 73 25 Corresponding author: Futahashi, Ryo ([email protected]) 26 melanized male discovered in the field was observed in a 74 27 male–male tandem with a normal male, suggesting that 75 28 Current Opinion in Insect Science 2016, 17:xx–yy the melanized male was mistaken as a female (Figure 1e) 76 29 This review comes from a themed issue on Global change biology/ [13]. On the other hand, there are cases of highly diversi- 77 30 molecular physiology fied color patterns within closely-related dragonfly spe- 78 31 Edited by Takema Fukatsu and Ryo Futahashi cies [14,15 ]. In some species, interspecific differences in 79 32 wing color patterns are more prominent in sympatric 80 populations than in allopatric populations, presumably 81 33 due to character displacement to avoid interspecific mat- 82 34 doi:10.1016/j.cois.2016.05.014 ing or aggression [16–22]. Thus, body and wing colors 83 84 2214-5745/Published by Elsevier Inc. comprise essential cues for partner recognition in dragon- flies. Although many ecological and behavioral studies 85 have focused on this topic, it has been totally unknown 86 35 how dragonflies produce and perceive multiple colors 87 3637 until recently. In this article, I aim to introduce the 88 genetic basis of the color polymorphisms, and review 89 38 Introduction recent progress in molecular mechanisms underlying 90 39 About a century ago, the renowned British entomologist, the color vision and color formation in dragonflies. 40 91 Robin John Tillyard, wrote in his book entitled ‘The Biology of 41 Dragonflies’ as follows: ‘In the Dragonfly the sense of sight is Genetic basis of color polymorphisms in 92 42 extraordinary well-developed, and is probably keener than dragonflies 43 93 in any other insect’ and ‘No Order of Insects can surpass the In addition to the adult color transition during sexual 94 44 Odonata in the beauty, variety and brilliancy of its coloration, maturation, color polymorphisms are widely recognized 95 45 except it be the Lepidoptera’ [1]. A wide variety of colors in among dragonflies, especially in females, many of which 96 46 lepidopterans (butterflies and moths) are mainly recognized are controlled genetically. In most cases, one morph 97 47 in adult wings, whereas color diversity of dragonflies (in- resembles the opposite sex [4,6,15 ,23 ,24]. In male 98 48 cluding damselflies) exists in both adult wings and body. In polymorphisms, female-mimicking males are not terri- 99 49 general, color is important for visual communication as well torial in general often adopting a sneaking strategy 100 50 as thermoregulation and environmental adaptation. (Figure 2a–c). In the Japanese calopterygid damselfly 101 51 Mnais costalis, the male polymorphism can be explained 102 52 Dragonflies are diurnal insects, and their compound eyes by an autosomal, single-locus genetic model, in which 103 53 are particularly large, consisting of thousands of small female-mimicking males are recessive to territorial www.sciencedirect.com Current Opinion in Insect Science 2016, 17:1–8 Please cite this article in press as: Futahashi R: Color vision and color formation in dragonflies, Curr Opin Insect Sci (2016), http://dx.doi.org/10.1016/j.cois.2016.05.014 COIS 257 1–8 2 Global change biology/molecular physiology Figure 1 (a) immature male mature male mature female L. pachygastra C. servilia (b) (c) (d) (e) Current Opinion in Insect Science Sexual dimorphism, adult color transition, and abnormal tandem of dragonflies. (a) Sexual dimorphism and male color transition of Lyriothemis pachygastra and Crocothemis servilia. Immature adults and mature female are yellowish in both species, while coloration of mature males are very different. (b) Interspecific tandem between L. pachygastra male and C. servilia female. (c) Interspecific tandem between C. servilia male and L. pachygastra female. (d) Normal male–female tandem of Nannophya pygmaea. (e) Male–male tandem of N. pygmaea. The attached male is a spontaneous melanized mutant. Source: Figure modified from [11,13,57]. 104 123 105 males [25]. In the female polymorphisms, one morph is I. demorsa, I. senegalensis and the small red damselfly 124 106 typically male-colored, namely ‘androchrome’, and the Ceriagrion tenellum [30–33]. The female color polymor- 125 107 others are heteromorphs, namely ‘gynochrome’ [4,6,26]. phisms are shown to be maintained by negative frequen- 126 108 In the damselfly genus Ischnura, several discrete and cy-dependent selection for avoiding excessive sexual 127 109 heritable color polymorphisms have been known in harassment by males [23 ,34]. In I. elegans, experimental 128 110 females, in which there are species that have one, manipulation of morph frequencies in large outdoor cages 129 111 two, or even three female morphs with different colors demonstrated that balanced frequencies of female 130 112 on thorax and spot on the abdomen (Figure 2d–f). There morphs result in higher fecundity than biased frequencies 131 113 are also female morphs in which coloration shifts from of female morphs [35]. 132 114 androchrome to gynochrome (e.g., the form infuscans of 115 I. elegans (Figure 2e) and monomorphic female of I. Color vision and opsin gene diversity in 133 116 heterosticta) [26,27]. dragonflies 134 117 Many animals possess color vision, which increases the 135 118 The genetic bases of the female color polymorphisms ability to recognize environments and organisms. Evolu- 136 119 have been elucidated in several damselfly species. Cross- tion of animal vision is strongly correlated with the 137 120 ing experiments have shown that androchromic females diversity of opsin genes [36,37]. Different types of opsin 138 121 are dominant to gynochromic females in I. elegans and genes encode light sensor proteins sensitive to different 139 122 I. graellsii [28,29], whereas androchromic females are wavelengths. For example, the human possesses three 140 recessive in the closely-related species I. damula, opsin genes for light sensors sensitive to blue, green, or Current Opinion in Insect Science 2016, 17:1–8 www.sciencedirect.com Please cite this article in press as: Futahashi R: Color vision and color formation in dragonflies, Curr Opin Insect Sci (2016), http://dx.doi.org/10.1016/j.cois.2016.05.014 COIS 257 1–8 Dragonfly colors Futahashi 3 Figure 2 (a) (b) (c) M. costalis sneaker male territorial male female 1 cm (female mimicking) (d) (e) (f) I. elegans Current Opinion in Insect Science Male and female color polymorphisms of dragonflies. (a–c) Male wing color polymorphism of Mnais costalis. (a) Territorial male. (b) Female mimicking sneaker male. (c) Female. Arrows indicate red pterostigma. (d–f) Female body color polymorphism of the blue-tailed damselfly Ischnura elegans. (d) Mating pair of a male and an androchrome female. An androchrome female resembles a conspecific male with a blue spot on the abdomen which is brownish in gynochrome females (arrowheads). (e) Mating pair of a male and a gynochrome female (form infuscans). (f) Mating pair of a male and a gynochrome female (form infuscans-obsoleta). 141 166 142 red light, and can see light ranging from purple to red, but not species from 11 families. Dragonflies have a strikingly large 167 143 ultraviolet (UV). The honeybee possesses opsin genes for number (15–33) of opsin genes, which have evolved through 168 144 UV, blue or green light, but not for red light, which underlie dynamic gene multiplications and losses within the lineage 169 145 its perception of UV light instead of discriminating red from of dragonflies.