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
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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
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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. Insect opsin proteins can be classified into two 170
146 gray (Figure 3a). Conventionally, it has been thought that types, visual and non-visual opsins, and the former are 171
147 most animals have 2–5 opsin proteins for color vision. subdivided into UV type, short-wavelength (SW) type, 172
148 and long-wavelength (LW) type [40 ,45,46 ]. The number 173
149 In dragonflies, notably, the structure and function of of visual opsin genes in dragonflies is extraordinarily large 174
150 adult compound eyes are markedly different between compared to other insects (Figure 3c,d) [40 ,46 ]. Expres- 175
151 the dorsal and ventral regions [38,39,40 ] (Figure 3b). sion patterns of visual opsin genes differ markedly between 176
152 The dorsal region of compound eye is predominantly the dorsal and ventral eyes, as well as between larval and 177
153 sensitive to short wavelength, presumably specialized adult stages (Figure 3e–g). Larvae express smaller number of 178
154 for prey detection against the bright background of the opsin genes than adults in accordance with their less visual 179
155 sky [38,39,40 ]. The ventral region of compound eye dependence. In the adult compound eyes, the dorsal region, 180
156 has been shown to contain at least three to five classes of which perceives the SW-skewed light directly from the sky, 181
157 spectral receptors covering a spectral range from UV to expresses more SW opsin genes, whereas the ventral region, 182
158 red (Figure 3a) [41–43,44 ]. It should be noted that which perceives reflected light from objects on the ground, 183
159 sensitivity of green photoreceptor cells is variable, expresses more LW opsin genes (Figure 3e–g) [40 ]. These 184
160 and the extremely broad sensitivity implies co-expres- differential opsin expression patterns highlight the versatile 185
161 sion of multiple opsin genes in a single photoreceptor behavioral and ecological adaptations of aquatic larvae and 186
162 cell (Figure 3a, dashed line). terrestrial adults of dragonflies. 187
163
164 The dorso-ventral differentiation of compound eyes in Coloration mechanism in dragonflies 188
165 dragonflies is supported at the molecular level by a Animal colors can be generally categorized into struc- 189
comprehensive transcriptome analysis of 12 dragonfly tural colors and pigment colors. Non-iridescent blue
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4 Global change biology/molecular physiology
Figure 3
(a) (c) visual blue green red human
Paleoptera UV SW LW others total (visual)
1 5104 20 (16) Sympetrum frequens (Odonata)
2 0 1 7 10 (3) Acyrthosiphon pisum (Hemiptera)
Insecta 1 0 1 1 3 (2) Pediculus humanus (Phthiraptera)
Neoptera 1 1 2 1 5 (4) Apis mellifera (Hymenoptera) honeybee 1 1 2 0 4 (4) Nasonia vitripennis (Hymenoptera) UV SW LW 1 0 1 1 3 (2) Tribolium castaneum (Coleoptera)
(blue) (green) Endopterygota
(Holometabola) 1 1 2 2 6 (4) Bombyx mori (Lepidoptera)
2 1 1 2 6 (4) Heliconius melpomene (Lepidoptera)
dragonfly (Hemicordulia tau) 1 1 1 2 5 (3) Danaus plexippus (Lepidoptera)
2 1 3 1 7 (6) Drosophila melanogaster (Diptera)
1 1 6 2 10 (8) Aedes aegypti (Diptera)
1 1 7 3 12 (9) Anopheles gambiae (Diptera)
(d) 1 2 8 4 15 (11) Indolestes peregrinus (Lestidae)
Zygoptera 300 400 500 600 700(nm0 1 1 9 4 15 (11) Mnais costalis (Calopterygidae)
UV 1 2 9 4 16 (12) Ischnura asiatica (Coenagrionidae)
Anisozygoptera
ocelli
(b) Odonata 1 7114 23 (19) Epiophlebia superstes (Epiophlebiidae) antenna
antenna 1 8 21 3 33 (30) Anax parthenope (Aeshnidae)
1 3 10 4 18 (14) Asiagomphus melaenops (Gomphidae) Anisoptera
1 3 10 4 18 (14) Tanypteryx pryeri (Petaluridae) dorsal 1 4 11 4 20 (16) Anotogaster sieboldii (Cordulegastridae)
1 6144 25 (21) Macromia amphigena (Macromiidae) 6 13 4 24 (20) Somatochlora uchidai (Corduliidae)
ventral 1
1 5 10 4 20 (16) Orthetrum albistylum (Libellulidae) 1 mm 1 5 10 4 20 (16) Sympetrum frequens (Libellulidae)
(e) UV SW LW (f) S. frequens larva (g) S. frequens adult SW opsin genes are dorsal 3 1 mainly used in dorsal 1 region of adult eyes ventral 1 5 Adult ocelli 1
Larva (head) 1 3 Adult expresses LW opsin genes are Larva expresses a small a large number mainly used in ventral number of opsin genes total 1 5 10 of opsin genes region of adult eyes
Current Opinion in Insect Science
Diversity and differential expression pattern of opsin genes in dragonflies. (a) Normalized photoreceptor spectral sensitivities of human, honeybee,
and the dragonfly Hemicordulia tau. UV, ultraviolet; SW, short wavelength; LW, long wavelength. Dashed lines indicate green photoreceptor with
broad or narrow sensitivity. (b) Frontal view of adult head of Sympetrum frequens. (c) The number of opsin genes of S. frequens in comparison
with those in the genomes of diverse insects. (d) Numbers of opsin genes mapped on the dragonfly phylogeny. (e) The number of opsin genes
that are expressed in the dorsal or ventral regions of the adult compound eye, adult head region containing ocelli, or in the larval head of S.
frequens. Each gene was expressed at a specific life stage and in a specific region. (f) Summary of opsin gene expression in S. frequens larva. (g)
Summary of opsin gene expression in S. frequens adult.
Source: Figure modified from [36,40,42].
190 193
191 integumentary coloration of dragonflies have evolved by coherent light scattering from the quasiordered 194
192 more than 10 times independently within the dragonfly nanostructures within pigment cells [47], and become 195
lineage [47]. These blue colors are structural, produced darkish under the low temperature conditions, which
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Figure 4
(a)C. japonica (b) Decarboxylated- Xanthommatin xanthommatin
HOOC (NH )HC 2 HOOC (NH2)HC Melanin (+)
Multilayer (+) CH 2 CH2 HO HO COOH immature male CO CO
N N N O O O O
HOOC (NH )HC 2 HOOC (NH2)HC
Multilayer (+) CH CH Melanin (+++) 2 2 mature male HO HO COOH CO CO Male maturation H H N N N N
OH O OH O Reduced form Oxidized form Melanin (+) mature female 1 cm Multilayer (-) Xanthommatin ratio is higher in vivid red color species
Current Opinion in Insect Science
Mechanisms of sex-specific and stage-specific color changes. (a) Sex-specific and stage-specific structural color of wings in Calopteryx
japonica. Structural color of mature male can be explained by an optical multilayer model, and only mature male has multilayer structure in veins
and high melanin concentration in wing membrane. (b) Summary of sex-specific and stage-specific redox changes of ommochrome pigments in
red dragonflies. Two ommochrome pigments are major components of red pigments in three dragonflies Crocothemis severia, Sympetrum
darwinianum, and Sympetrum frequens. Xanthommatin ratio is different in accordance with the shade of red. Reduced form ratio of ommochrome
pigments is dramatically higher in mature male compared to mature female and immature individuals.
196 226
197 can be explained by vertical migration of the ommochrome of epidermal pigments in red dragonflies of the genera 227
198 pigment granules [48]. Some dragonflies represent con- Crocothemis and Sympetrum are two ommochrome pig- 228
199 spicuous iridescent colors on their wings and/or body. ments, xanthommatin (vivid red color in reduced form) 229
200 Molecular aspects underlying sex-specific and stage-spe- and decarboxylated xanthommatin (dull red color in 230
201 cific iridescent color change have been reported in the reduced form). In the red dragonflies, both males and 231
202 jewelwing damselfly Calopteryx japonica. Wings of imma- females are yellow in the immature adult stage, and only 232
203 ture males are light brown and turn bluish with metallic males turn into red upon sexual maturation. The shade of 233
204 veins upon sexual maturation, whereas wings of mature color is primarily determined by the redox states of the 234
205 females remain light brown (Figure 4a). These color dif- ommochrome pigments. Only mature males exhibit very 235
206 ferences are attributable to the existence of multilayer high proportions of the reduced ommochrome pigments 236
207 structure in veins and high melanin concentration in wing (Figure 4b) [57]. Moreover, ratios of two ommochrome 237
208 membrane in mature males [49,50]. Multilayer structure pigments are correlated with the different shade of red 238
209 has also been reported in several dragonflies with metallic among the dragonfly species; mature males of C. servilia in 239
210 wings [51–53,54 ,55 ]. Subtle differences in the multi- crimson-red color contain more xanthommatin compared 240
211 layer structure produce a notable color difference between to mature males of S. frequens and S. darwinianum in 241
212 the bluish dorsal wing surface and the greenish ventral cinnabar-red color (Figure 4b) [57]. Considering that 242
213 wing surface of the damselfly Matronoides cyaneipennis [53]. the reduced pigments show antioxidant abilities [57], 243
214 In addition to the multilayer structure, wrinkles or wax the highly accumulated reduced pigments in mature 244
215 crystals on the wing surface are also important for enhance- males may have an additional benefit for protecting them 245
216 ment of iridescent colors [54 ,55 ]. against oxidative stresses by UV radiation upon territorial 246
217 behaviors under sunshine. 247
218 As for pigment coloration, wing pigments of Japanese
219 calopterygid damselfly M. costalis were analyzed by tracer Conclusion and perspective 248
220 experiments with radiolabeled pigment precursors. Ty- Recent progress in comprehensive visual transcriptomics 249
221 rosine was incorporated in the orange wing cells of terri- unveils an extreme diversity of opsin genes in dragonflies, 250
222 torial males (Figure 2a), whereas tryptophan was as suggested by Tillyard. Plausibly, although speculative, 251
223 incorporated in the red pterostigmas of both territorial the extraordinary variation of opsin gene repertoire may 252
224 and sneaker males (Figure 2a,b), suggesting that pig- be involved in the evolution of diverse coloration in 253
225 ments of orange wings and red pterostigmas are melanin dragonflies. Moreover, molecular mechanisms underlying 254
and ommochrome, respectively [56]. Major components structural color formation and pigment-based adult color
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255 316
12. Sa´ nchez-Guille´ n RA, Co´ rdoba-Aguilar A, Cordero-Rivera A, 317
256 transition have become clarified in recent years. Mean-
Wellenreuther M: Genetic divergence predicts reproductive 318
257 while, gene regulatory networks of color pattern forma- isolation in damselflies. J Evol Biol 2014, 27:76-87.
319
258 tion in dragonflies still remain unknown, and the
13. Futahashi R, Futahashi H: A record of a black mutant of 320
259 responsible genes underlying color polymorphisms have Nannophya pygmaea Rambur, 1842. Tombo 2007, 50:73-74.
321
260 not been identified in any dragonfly species. Genes
14. Sa´ nchez Herrera M, Kuhn WR, Lorenzo-Carballa MO, Harding KM, 322
261 involved in melanin and ommochrome synthesis pathway Ankrom N, Sherratt TN, Hoffmann J, Van Gossum H, Ware JL, 323
Cordero-Rivera A, Beatty CD: Mixed signals? Morphological 324
262 are widely conserved among insects [58–64]. Investiga-
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263 tion for dragonfly pigment synthesis genes has just some neotropical polythore damselflies. PLoS One 2015, 326
10:e0125074.
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328
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267 orthologues of known pigment synthesis genes or previ- This paper investigates the phylogenetic relationships of 17 Megalagrion
332
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270 Acknowledgements maculata and C. aequabilis (Odonata: Calopterygidae). Syst
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337
272 I would like to thank Genta Okude, Masahiko Tanahashi and Mizuko 338
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274 Q2 work was supported by JSPS KAKENHI Grant Numbers 23780058,
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www.sciencedirect.com Current Opinion in Insect Science 2016, 17:1–8
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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