Title Evolutionary Fine-Tuning of Background-Matching Camouflage

Evolutionary fine-tuning of background-matching camouflage Title among geographical populations in the sandy beach tiger beetle Author(s) Yamamoto, Nayuta; Sota, Teiji Proceedings of the Royal Society B: Biological Sciences Citation (2020), 287(1941) Issue Date 2020-12-23 URL http://hdl.handle.net/2433/259830 This is the accepted manuscript of the article, which has been published in final form at http://doi.org/10.1098/rspb.2020.2315; この論文は出版社版 Right でありません。引用の際には出版社版をご確認ご利用ください。; This is not the published version. Please cite only the published version. Type Journal Article Textversion author Kyoto University 1 Evolutionary fine-tuning of background-matching camouflage among geographic 2 populations in the sandy beach tiger beetle 3 4 5 Nayuta Yamamoto and Teiji Sota 6 7 Department of Zoology, Graduate School of Science, Kyoto University, Kyoto, Japan 8 9 10 Authors for correspondence: Nayuta Yamamoto and Teiji Sota, Department of Zoology, 11 Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan. 12 e-mail: [email protected]; [email protected]. 13 1 14 Abstract 15 Background-matching camouflage is a widespread adaptation in animals; however, few 16 studies have thoroughly examined its evolutionary process and consequences. The tiger 17 beetle Chaetodera laetescripta exhibits pronounced variation in elytral colour pattern 18 among sandy habitats of different colour in the Japanese Archipelago. In this study, we 19 performed digital image analysis with avian vision modelling to demonstrate that elytral 20 luminance, which is attributed to proportions of elytral colour components, is fine-tuned 21 to match local backgrounds. Field predation experiments with model beetles showed that 22 better luminance matching resulted in a lower attack rate and corresponding lower 23 mortality. Using restriction site-associated DNA (RAD) sequence data, we analysed the 24 dispersal and evolution of colour pattern across geographic locations. We found that sand 25 colour matching occurred irrespective of genetic and geographic distances between 26 populations, suggesting that locally adapted colour patterns evolved after the colonisation 27 of these habitats. Given that beetle elytral colour patterns presumably have a quantitative 28 genetic basis, our findings demonstrate that fine-tuning of background-matching 29 camouflage to local habitat conditions can be attained through selection by visual 30 predators, as predicted by the earliest proponent of natural selection. 31 32 Keywords: camouflage, character evolution, colouration, local adaptation 33 2 34 1. Introduction 35 Organismal appearance traits such as body colour pattern are strikingly diverse and have 36 been widely studied as evidence for evolution by natural selection and biodiversity [1–3]. 37 Anti-predator adaptation is among the most important evolutionary processes, and is 38 responsible for a myriad of putative camouflage patterns to avoid detection by visually 39 oriented predators [2–6]. A typical form of camouflage comprises cryptic colouration, 40 often referred to as background matching, which conceals individuals through similarities 41 in colouration with their natural background [4,5,7]. A fundamental prediction for this 42 type of camouflage is the evolution of a single optimal body colour that is fine-tuned to 43 match the background colouration, with respect to predator vision, thereby maximising 44 the efficacy of concealment [7–10]. 45 Previous studies have provided empirical and comparative evidence to support the 46 hypothesis that selection via predation can lead to background matching in animal 47 colouration (e.g., [11,12]). However, few studies have quantitatively examined how 48 closely prey colour matches the background from the perspectives of predator vision and 49 the efficacy of predation risk reduction in natural conditions [13,14]. A fundamental 50 criterion of camouflage theory is that closer matching of an object to its background will 51 reduce the likelihood that it is found and attacked by predators [5]. Wild animals such as 52 avian predators have visual systems that differ from the human system in terms of the 53 number of receptor types, receptor sensitivity, and ability to perceive ultraviolet (UV) 54 light [15]. Therefore, for effective camouflage, prey animals must closely resemble their 55 background in appearance with respect to predator vision; the resemblance must directly 56 relate to survival against predators in the wild. Recent advances in optical analysis 57 techniques and knowledge of colour perception have allowed modelling of predator 58 vision and consideration of how colouration might be perceived by natural predators 59 [12,16]. Some studies have used vision models to test concealment [17–21]; however, 60 tests for optimal camouflage using actual predators remain rare [13,14]. Therefore, the 61 evolutionary fine-tuning of cryptic colouration to match local backgrounds has not yet 3 62 been fully demonstrated, although it is a fundamental prediction of anti-predator 63 adaptations. 64 Traits with multiple functions (e.g., body colouration) can be affected by both biotic 65 and abiotic selection factors, as well as by phylogenetic constraints [1]. Therefore, it is 66 crucial to examine how different types of selection and phylogenetic constraints have 67 affected the evolution of body colouration, in conjunction with natural selection for 68 camouflage [22,23]. Geographic colour variation provides a good system to study colour 69 matching with spatial replication and to resolve the relative importance of different 70 processes in phenotypic evolution [24]. The study of geographic variation can also 71 provide insight into the population genetics of phenotypic evolution [25]. Background 72 matching can occur by two processes: evolutionary fine-tuning of body colour to match 73 background patterns after the colonisation of a new habitat, and colonisation of a habitat 74 with background patterns that match body colour. The relative importance of these 75 processes can be evaluated by examining the relationships of genetic, geographic, and 76 phenotypic distances among populations. 77 Tiger beetles (Coleoptera: Cicindelidae) are a species-rich group with extreme 78 colour pattern diversity, which provide an intriguing means for investigation of colour 79 pattern evolution [26,27]. Associations between body colouration and environment are 80 observed even among subspecies of tiger beetles, and have long been recognised as 81 predator-avoidance camouflage [3,28]. Previous studies have shown differences in white 82 elytral markings and activity between cool and warm periods among subspecies of tiger 83 beetles, suggesting that thermoregulation may be another important determinant of colour 84 pattern [29,30]. Furthermore, the body colouration of tiger beetles is determined 85 genetically and indicates relatedness among species, suggesting that phylogenetic 86 constraints can affect colouration [27,31,32]. The tiger beetle Chaetodera laetescripta 87 shows pronounced geographic variation in the black and ivory colour patterns of its elytra 88 in the Japanese archipelago (figure 1a), but not in continental Asia [33,34]. In Japan, C. 89 laetescripta elytral colouration resembles the local habitat colouration (figure 1b), which 4 90 varies from off-white to black due to the complicated local geology [34] (figure 1a). From 91 north to south, the Japanese Archipelago is characterised by a climatic gradient that plays 92 an important role in colour divergence among insects [35,36]. Therefore, climatic factors 93 such as temperature and solar radiation may have played a role in the colour pattern 94 divergence of C. laetescripta [37]. The tiger beetle depends on sparsely vegetated sandy 95 habitats; adults emerge during the daytime in summer (June to September) [38] and are 96 therefore likely to be exposed to visually guided predators (e.g., birds and robber flies) 97 on the bare ground, as well as to heat stress associated with their colouration [31]. 98 The objectives of this study were to demonstrate the occurrence of fine-tuned 99 background matching, examine the role of selection in camouflage optimisation in terms 100 of geographic colour variation, and explore the evolutionary process of geographic colour 101 variation in the tiger beetle C. laetescripta. First, we assessed how closely the elytral 102 colouration of the tiger beetle resembles its background from the perspective of avian 103 predator vision. Next, we tested the selective advantage of colour matching in artificial 104 models by exposing them to natural avian predators in the wild. Third, we analysed the 105 genetic structures of tiger beetle populations using high-throughput sequencing 106 (restriction site-associated DNA sequencing) [39] to investigate the evolutionary pattern 107 of background matching. Finally, we performed a phylogenetic comparative analysis to 108 test whether variations in colour patterns were primarily determined by background 109 colouration, climatic factors, or phylogenetic effects. 110 111 112 2. Materials and Methods 113 (a) Field sampling 114 C. laetescripta tiger beetles were collected from 12 sites, representing nearly the entire 115 range of their visual appearance and distribution in Japan (figure 1a; electronic 116 supplementary material, table S1). Internal tissues of the beetles were preserved in 99% 117 ethanol at –30°C until DNA extraction; the remaining exoskeletons were stored at

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