Selection for Social Signalling Drives the Evolution of Chameleon Colour Change

Selection for Social Signalling Drives the Evolution of Chameleon Colour Change

PLoS BIOLOGY Selection for Social Signalling Drives the Evolution of Chameleon Colour Change Devi Stuart-Fox1,2*, Adnan Moussalli3,4 1 School of Animal, Plant, and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa, 2 Department of Zoology, The University of Melbourne, Melbourne, Australia, 3 School of Biological and Conservation Sciences, University of KwaZulu Natal, Pietermaritzburg, South Africa, 4 Department of Sciences, Museum Victoria, Melbourne, Australia Rapid colour change is a remarkable natural phenomenon that has evolved in several vertebrate and invertebrate lineages. The two principal explanations for the evolution of this adaptive strategy are (1) natural selection for crypsis (camouflage) against a range of different backgrounds and (2) selection for conspicuous social signals that maximise detectability to conspecifics, yet minimise exposure to predators because they are only briefly displayed. Here we show that evolutionary shifts in capacity for colour change in southern African dwarf chameleons (Bradypodion spp.) are associated with increasingly conspicuous signals used in male contests and courtship. To the chameleon visual system, species showing the most dramatic colour change display social signals that contrast most against the environmental background and amongst adjacent body regions. We found no evidence for the crypsis hypothesis, a finding reinforced by visual models of how both chameleons and their avian predators perceive chameleon colour variation. Instead, our results suggest that selection for conspicuous social signals drives the evolution of colour change in this system, supporting the view that transitory display traits should be under strong selection for signal detectability. Citation: Stuart-Fox D, Moussalli A (2008) Selection for social signalling drives the evolution of chameleon colour change. PLoS Biol 6(1): e25. doi:10.1371/journal.pbio. 0060025 Introduction expected to be under strong selection to maximise detect- ability to conspecifics [15,16], potentially explaining the The ability to change colour in response to environmental evolution of dramatic colour change in some species. In stimuli has evolved in numerous vertebrate and invertebrate many colour-changing lineages, colour change is known to lineages including fish [1–4], amphibians [5,6], reptiles [7], facilitate both crypsis [5,10,14,17] and social communication crustaceans [8], and cephalopods [9,10]. In most lineages, [1,3,17–23]. As colour generally serves more than one purpose colour change occurs over a period of minutes or hours and is in colour-changing species, evolutionary processes under- primarily under hormonal control (e.g., [5,6,11]), whereas in lying the ability to change colour per se cannot be inferred some lineages, notably cephalopods and chameleons, chro- from functional studies of particular colour patterns. To matophores (pigment-containing cells or organs in the infer underlying evolutionary processes requires experimen- dermis) are under direct neural control, enabling the animals tal studies on closely related populations or taxa, which differ to respond extremely rapidly (within milliseconds or seconds) in their ability to change colour, or comparative tests based to changes in their natural or social environments [9,10,12]. on phylogeny. For this reason, colour change in cephalopods and chame- We used a phylogenetic comparative approach to test leons has featured in popular culture, myth and legend since whether selection for crypsis or selection for conspicuous first described in Aristotle’s Historia Animalium [13]. In most social signals (or a combination of the two) drives the lineages that have evolved colour change, however, the evolution of colour change. We measured coloration and apparent capacity for colour change varies greatly. For colour change (via reflectance spectroradiometry) in field- instance, among the more than 150 species of the family based behavioural trials conducted on 21 lineages of southern Chamaeleonidae, colour change in some is primarily limited African dwarf chameleon, Bradypodion spp. We examined to shifts in brightness (e.g., shades of brown), while others signal detectability (conspicuousness) by quantifying the show remarkable chromatic change, including striking visual contrast between display colours and the background combinations of blues, greens, oranges, yellows, and black against which they are viewed (vegetation and adjacent body [14]. Despite the animals’ marked variation in the ability to regions), based on dwarf chameleon retinal photoreceptor change colour, processes driving the evolution of this spectral sensitivities and a model of colour perception. adaptive strategy have never been examined. Two primary processes may drive the evolution of colour Academic Editor: Frans B. M. de Waal, Emory University, United States of America change: (1) natural selection for the ability to camouflage Received October 8, 2007; Accepted December 14, 2007; Published January 29, against variety of backgrounds and (2) selection for con- 2008 spicuous social signals. Like colourful hidden insect wings or Copyright: Ó 2008 Stuart-Fox and Moussalli. This is an open-access article plumage ornaments in some birds, colour change in a social distributed under the terms of the Creative Commons Attribution License, which context enables the use of signals that can be briefly exposed permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. or flashed to intended receivers (usually conspecifics) but concealed from potential predators at other times. Because Abbreviations: UVS, ultraviolet-sensitive; VS, violet-sensitive such ‘‘transitory signals’’ are only briefly exposed, they are * To whom correspondence should be addressed. E-mail: [email protected] PLoS Biology | www.plosbiology.org0022 January 2008 | Volume 6 | Issue 1 | e25 Evolution of Chameleon Colour Change Author Summary displays characteristic, species-specific submissive coloration (Figure 1). Females exhibit contrasting light and dark The ability to change colour has evolved in numerous vertebrate coloration during aggressive displays and, unlike some other and invertebrate groups, the most well-known of which are chameleons [25], do not use colour patterns to signal chameleons and cephalopods (octopuses and their relatives). There reproductive status [20,24], instead displaying a subset of is great variation among species, however, in the apparent capacity the colour variation apparent in males. Dwarf chameleons for colour change, ranging from limited changes in brightness to show greatest colour change during these interactions rather dramatic changes in hue. What drives the evolution of this than in response to model predators [26] (Figure 2), therefore remarkable strategy? We addressed this question by using a combination of field-based behavioural trials in which we quantified we measured colour change as the difference between male colour change, models of colour perception, and our knowledge of dominant and submissive coloration, which provides the best phylogenetic relationships for 21 distinct lineages of southern estimate of not only colour change within a social context but African dwarf chameleons. We show that evolutionary changes in also capacity for colour change more generally. the capacity for colour change are consistently associated with the We tested for an evolutionary correlation between the use of social signals that are highly conspicuous to the visual system degree of colour change and multiple predictor variables, of chameleons. Moreover, capacity for colour change is unrelated to which were chosen based on expectations of the crypsis and variation in the environmental backgrounds that chameleons must social signalling hypotheses. The crypsis hypothesis predicts a match in order to be camouflaged. Overall, our results suggest that positive relationship between colour change and the variance the evolution of the ability to exhibit striking changes in colour in background coloration, which chameleons need to match evolved as a strategy to facilitate social signalling and not, as popularly believed, camouflage. in order to be cryptic. Unlike cephalopods, which use a variety of camouflage strategies such as disruptive camouflage [10], dwarf chameleons rely primarily on background match- ing [26] (Figure 2). Natural selection can also act on colour Because birds are a major predator of chameleons, we also patterns through variation in habitat structure, which will applied this model using avian photoreceptor spectral influence signal transmission and thus the detectability of sensitivities to explore the role of natural selection. signals to both chameleons and their predators [15,16]. Dwarf chameleons are well suited to studying colour Accordingly, we also tested for a relationship between colour change because they vary greatly in the type and range of change and three quantitative measures of habitat structure, colours exhibited by each species. Males readily display to which varies among the 21 lineages, from grassland to dense conspecifics and exhibit species-specific conspicuous colour rainforest [24]. The social signalling hypothesis predicts a patterns (Figure 1) both to signal dominance during positive relationship between colour change and signal aggressive interactions and to court females [24]. When a conspicuousness, which we estimate as the visual contrast male loses a contest or is

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