1 Visual System Diversity in Coral Reef Fishes 2 Fabio Cortesi1, Laurie Mitchell1,2, Valerio Tettamanti1, Lily G. Fogg1, Fanny D

1 Visual system diversity in coral reef fishes 2 Fabio Cortesi1, Laurie Mitchell1,2, Valerio Tettamanti1, Lily G. Fogg1, Fanny de Busserolles1, 3 Karen L. Cheney2, N. Justin Marshall1 4 5 1Queensland Brain Institute, The University of Queensland, St Lucia, Queensland 4072, 6 Australia. 7 2School of Biological Sciences, The University of Queensland, St Lucia, Queensland 4072, 8 Australia. 9 10 Corresponding author: [email protected] 11 12 Abstract 13 Coral reefs are one of the most species rich and colourful habitats on earth and for many coral 14 reef teleosts, vision is central to their survival and reproduction. The diversity of reef fish visual 15 systems arises from variations in ocular and retinal anatomy, neural processing and, perhaps 16 most easily revealed by, the peak spectral absorbance of visual pigments. This review examines 17 the interplay between retinal morphology and light environment across a number of reef fish 18 species, but mainly focusses on visual adaptations at the molecular level (i.e. visual pigment 19 structure). Generally, visual pigments tend to match the overall light environment or micro- 20 habitat, with fish inhabiting greener, inshore waters possessing longer wavelength-shifted 21 visual pigments than open water blue-shifted species. In marine fishes, particularly those that 22 live on the reef, most species have between two (likely dichromatic) to four (possible 23 tetrachromatic) cone spectral sensitivities and a single rod for crepuscular vision; however, 24 most are trichromatic with three spectral sensitivities. In addition to variation in spectral 25 sensitivity number, spectral placement of the absorbance maximum (λmax) also has a surprising 26 degree of variability. Variation in ocular and retinal anatomy is also observed at several levels 27 in reef fishes but is best represented by differences in arrangement, density and distribution of 28 neural cell types across the retina (i.e. retinal topography). Here, we focus on the seven reef 29 fish families most comprehensively studied to date to examine and compare how behaviour, 30 environment, activity period, ontogeny and phylogeny might interact to generate the 31 exceptional diversity in visual system design that we observe. 32 33 Keywords: vision, eyes, opsin, gene expression, visual pigment, retinal topography 34 35 1. Introduction 36 Coral reefs are home to over 8,000 species of colourful and diverse fishes [1,2], many of which 37 rely on vision to find food, avoid predation, find mates, and compete for resources. It is how 38 vision is moulded by habitat, lifestyle, food, colour, and sex that makes this environment one 39 of the most intriguing to study and although much effort has been made to understand the 40 diversity of reef fish visual systems, our knowledge is limited to a few species within a few 41 families. 42 At first glance, the visual systems of coral reef fishes show many similar 43 morphological, physiological and molecular characteristics to other vertebrates [3]. For 44 example, the basis of vision entails a set of light-sensitive receptors consisting of a visual opsin 45 protein bound to a vitamin A derived chromophore. Upon excitation the chromophore induces 46 a conformational change in the opsin, which initiates the phototransduction cascade resulting 47 in an electric signal to the brain (Dartnall, 1976). The type of opsin protein and chromophore 48(A 1 short-shifted or A2 long-shifted) is one factor that determines λmax, the wavelength at which 49 a photoreceptor is maximally sensitive. Five ancestral opsin classes can be found in extant 50 vertebrates based on spectral sensitivity, photoreceptor specificity and evolutionary history 51 [5,6]. These are four cone opsins and one rod opsin: short-wavelength-sensitive opsins, SWS1 52 (‘ultraviolet’; A1-based λmax = 347-383 nm) and SWS2 (‘violet-blue’; A1-based λmax = 397-482 53 nm), middle-wavelength-sensitive rhodopsin-like RH2 (‘blue-green’; A1-based λmax = 452-537 54 nm), long-wavelength-sensitive LWS (‘yellow-red’; A1-based λ max = 501-573 nm), and 55 rhodopsin/rod opsin RH1 (A1 and A2-based λ max = 444-541 nm). However, in teleosts in 56 particular, opsin genes have undergone a series of duplications, deletions and functional 57 mutations so that extant coral reef fishes show a greatly altered opsin gene repertoire, often 58 with more opsin gene copies than ancestrally acquired (reviewed in [7]). In fact, reef fishes so 59 far studied are known to have up to 14 opsin genes (Blackbar soldierfish, Myripristis jacobus), 60 with many having more than seven [8], which at first glance, seems an over-abundance. 61 Despite having many different opsin genes, reef fishes have been found to rely on a 62 limited set of photoreceptor types for visual tasks. In general, two to four spectrally distinct 63 cone photoreceptors are used for colour vision during bright-light conditions, with single cones 64 expressing SWS opsins and double cones (two single cones joined together) expressing RH2 65 and LWS opsins. A single rod photoreceptor expressing RH1 is used for dim-light vision 66 (reviewed in [9]). The reason for maintaining more opsins in the genome than are apparently 67 transcribed is not quite clear but like in other fishes (e.g. salmonids [10], cichlids [11], eels 68 [12] and sculpins [13]) and marine animals (e.g. stomatopod crustaceans [14]) might include 69 shifts in gene expression across ontogeny (e.g. dottybacks [15,16]), the co-expression of 70 multiple opsins within a single photoreceptor (e.g. damselfishes [17]), the use of a different 71 pigment complement in different areas of the retina (e.g. damselfishes [17]), and a change in 72 visual system with location on the reef, such as depth, microhabitat, or latitude (e.g. snappers 73 [18] and cardinalfishes [19]) and changes in gene expression between seasons (e.g. 74 damselfishes [20]). 75 The morphology of coral reef fish eyes is also highly diverse with differences in eye 76 size (e.g. large in nocturnal and smaller in diurnal fishes [21]), ocular media (e.g. pigmented 77 vs. clear lenses [22]), and retinal structure (e.g. fewer cones in nocturnal species [23]) common 78 across species. Due to a wide variety of ecological niches, behaviour and diet, reef fishes differ 79 in the topographic distribution and density of retinal cell types depending on where they live 80 on the reef or what their food source might be. For example, temporal areas of high cell 81 densities are common in fishes that live inside the reef matrix or that feed on the benthos as 82 they focus on the visual field in front of them (e.g. angelfishes and damselfishes [24]), while a 83 band of increased cell density in the form of a horizontal streak is common in species that live 84 above the reef or feed in the water column to scan the horizon for predators and food (e.g. 85 triggerfish and wrasses [25]). 86 Two recent reviews have provided a general overview of colour vision in coral reef 87 fishes [9] and have dealt with the different mechanisms that tune vision in fishes [7]. Here, we 88 focus on seven diurnal and nocturnal reef fish families for which enough information is 89 available to highlight the diversity in visual systems that can be found across families, between 90 species, and even on the individual level, spanning diel to evolutionary timescales. 91 92 2. Vision in diurnal reef fishes 93 Diurnal reef fishes have evolved visual systems that perform well in the colourful, sunlit 94 habitats surrounding them. This includes colour vision systems with two, three, four or even 95 five different spectral sensitivities [26]. In this section, we explore why coral reef fishes might 96 need such diverse, complex colour vision by focusing on the members of four out of the seven 97 families under consideration: damselfishes (Pomacentridae), wrasses (Labridae), surgeonfishes 98 (Acanthuridae) and triggerfishes (Ballistidae). 99 2.1. Damselfishes 100 Damselfishes (Pomacentridae) are a diverse family of reef fishes with 421 described 101 species [27] belonging to the Ovalentaria clade of percomorphs. They can be found in shallow 102 to deep tropical coral reefs, warm temperate waters, and one species even inhabits freshwater 103 [28]. Not only are they abundant, but damselfishes also display a variety of colours, habitat 104 preferences, and ecologies [29,30], making them particularly well-suited to study visual system 105 evolution and adaption. 106 107 2.1.1. Visual pigments and spectral sensitivities 108 Damselfishes, in addition to a single rod photoreceptor, have between three to four 109 differently tuned cone photoreceptors within their retina. The cones range in spectral sensitivity 110 from 346 – 560 nm λ max and show typical A1-chromophore-based absorbance spectra 111 [17,26,31–34] (Fig. 1; Table S1). Hence, damselfishes have the potential for tri- or even tetra- 112 chromatic colour vision with the ability to perceive colours ranging from UV to red [20,35]. 113 As we will see shortly however, not all cones are found in all retinal areas. The photoreceptor 114 pigments can be attributed to a set of five cone opsin proteins (SWS1, SWS2B, RH2B, RH2A, 115 LWS) [8,36], of which three are commonly expressed at high levels (SWS1, RH2B, RH2A) [35] 116 (Fig. 1). 117 Opsin gene expression in damselfishes may be plastic with quantitative expression 118 changes found within species occurring at different depths and between seasons [20]. A shift 119 in opsin gene expression towards the central blue/green part of the light spectrum occurs in 120 deeper living individuals of some species (Pomacentrus spp.), but not in others (Chrysiptera 121 rollandi, Dascyllus spp.) [20]. These changes are likely related to the attenuation of shorter and 122 longer wavelengths with depth.

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