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Furcifer Pardalis</I © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb224550. doi:10.1242/jeb.224550 RESEARCH ARTICLE The colour of success: does female mate choice rely on male colour change in the chameleon Furcifer pardalis? Alexis Y. Dollion1,2,3,*, Anthony Herrel3, Olivier Marquis4, Mathieu Leroux-Coyau2 and Sandrine Meylan2 ABSTRACT However, some organisms can change colour in hours or even Colour change is involved in various functions ranging from thermo- less than a second. This is referred to as rapid colour change or and hydroregulation to camouflage and communication. The role of physiological colour change (Ligon and McCartney, 2016). colour change in communication has received increased attention Physiological colour changes can be achieved by the contraction/ over the past few decades, yet has been studied predominantly in the expansion of chromatophores (Cloney and Florey, 1968), by the context of intrasexual competition. Here, we investigate the role of mobilisation of pigments or photonic nanostructures within colour change in mate choice in an animal that can change its colour, chromatophores, or through hydraulic infiltration into photonic the panther chameleon (Furcifer pardalis). We conducted behavioural nanostructures (Liu et al., 2009). These types of colour changes are experiments and colour analysis to investigate whether colour typically mediated by hormones and/or neurotransmitters (Ligon changes, including in the UV range, are involved in mate choice. and McCartney, 2016; Umbers et al., 2014). This ability has been This study presents evidence of female mate choice for specific documented in cephalopods (Hanlon and Messenger, 2018), insects aspects of colour change in courting males, both in the visible (i.e. (Hinton and Jarman, 1973; Key and Day, 1954), arachnids human visible range: 400–700 nm) and the UV range. Females chose (Wunderlin and Kropf, 2013), crustaceans (Brown and Sandeen, males exhibiting more saturation changes regardless of the body 1948; Stevens et al., 2014), fish (Iga and Matsuno, 1986; Nilsson region and spectral range. In addition, females chose males showing Sköld et al., 2013) amphibians (Kindermann and Hero, 2016; fewer brightness changes at the level of the lateral line and males Nilsson Sköld et al., 2013), reptiles (Batabyal and Thaker, 2017; showing lower hue changes at the level of the bands and the Taylor and Hadley, 1970) and even some birds (Curio, 2004). The interbands, in the visible range. At UV wavelengths, selected males functions of physiological colour change may differ in different taxa showed more brightness changes and higher maximum brightness. and include thermoregulation (Smith et al., 2016), hydroregulation These results suggest that male colour change is important in female (Whiters, 1995), camouflage (Allen et al., 2010; Stuart-Fox et al., mate choice in the panther chameleon. 2008; Zylinski and Johnsen, 2011) and intraspecific communication (Hutton et al., 2015). KEY WORDS: Chameleon, Intersexual selection, Colour signal, In the context of animal communication, colour change has been Animal communication studied mostly during intrasexual interactions, suggesting that intraspecific communication is a prominent driver of the evolution of INTRODUCTION physiological colour change. Surprisingly, few studies have Animal colouration is not as fixed as is often assumed. Indeed, investigated the role of physiological colour change during many animals change colour during their development (Booth, intersexual interactions (Adamo et al., 2000; Batabyal and Thaker, 1990) and/or in response to environmental variation, including 2017; Boal, 1997; Kelso and Verrell, 2002; Keren-Rotem et al., season (Küderling et al., 1984), food availability (Hill et al., 2002), 2016a). Moreover, most of these studies focused on differences in circadian rhythms, breeding season (Keren-Rotem et al., 2016b; colour change between intra- and intersexual interactions, or which McGraw and Hill, 2004) or predation pressure (Hemmi et al., 2006). colours correspond to courtship, rather than evaluating the variations in This type of colour change, termed morphological colour change colour during the interaction itself. To date, no study has explored the (Leclercq et al., 2009; Umbers et al., 2014), can be achieved through role of physiological colour change in mate choice, raising questions on the anabolism or catabolism of pigments or photonic structures, whether females choose mates based on male physiological colour changes in the number of chromatophores in tissues, or the renewal change. of dead tissue (e.g. hairs, feathers, scales or cuticula) containing In some animals, like chameleons, sexual selection upon the pigments or photonic structures through moulting (Detto et al., ability to change colour is likely to occur since a strong sexual 2008). These morphological colour changes are typically achieved dimorphism both in terms of colour and the ability to change colour over time spans ranging from months to days. exists (Kelso and Verrell, 2002; Keren-Rotem et al., 2016a; Tolley and Herrel, 2013). Moreover, comparative studies have demonstrated that selection for conspicuous social signals has 1Universitéde Paris, 75006 Paris, France. 2Sorbonne Université, CNRS, IRD, INRA, Institut d’Ecologie et des Sciences de l’Environnement-Paris, iEES-Paris, 75252 likely driven the evolution of colour change in a clade of dwarf Paris, France. 3Département Adaptations du vivant, UMR 7179 C.N.R.S/M.N.H.N, chameleons (Stuart-Fox and Moussalli, 2008). Chameleons are thus 75005 Paris, France. 4Muséum national d’Histoire naturelle, Parc Zoologique de an excellent model to study whether females chose mates based on Paris, 75012 Paris, France. male physiological colour change. Chamaeleonid lizards are *Author for correspondence ([email protected]) famous for exhibiting striking and complex colour changes (Necas,̌ 1999; Teyssier et al., 2015; Tolley and Herrel, 2013) with A.Y.D., 0000-0003-1373-2588; A.H., 0000-0003-0991-4434; O.M., 0000-0001- 8215-1221; S.M., 0000-0002-0865-3335 a large repertoire (Kelso and Verrell, 2002; Ligon and McGraw, 2018). Despite previous studies describing the specific courtship Received 18 March 2020; Accepted 20 August 2020 colour patterns and female receptive colours (Karsten et al., 2009; Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb224550. doi:10.1242/jeb.224550 Kelso and Verrell, 2002; Keren-Rotem et al., 2016a), investigations combination of different light sources, allowing us to cover a into involvement of colour change in intersexual selection in spectrum close to the solar spectrum, including the UV. The overall chameleons have been neglected. set up was illuminated with a combination of nine light sources Here, we explore whether mate choice outcome relies on specific placed 56 cm above the set-up: two 60 W, 4000 K, 806 lm LED aspects of male colour change in the panther chameleon Furcifer bulbs (Lexman), two 60 W, 2700 K incandescent bulbs (OSRAM, pardalis (Cuvier 1829). The panther chameleon is an ideal study Munich, Germany), two 100 W, 2800 K, 1320 lm halogen bulbs species as it possesses a strong sexual dichromatism with males (OSRAM), one UVB fluorescent tube ReptiSun 10.0 High Output being brightly coloured and females being dull. Female colouration UVB Bulb (ZooMed Laboratoires, San Luis Obispo, CA, USA), remains constant between populations while a strong variability is one Arcadia T5 D3+ Desert 12% Reptile Fluorescent Lamp observed in males depending on their region of origin (Ferguson, (Arcadia, Croydon, UK), and one Reptile systems New Dawn T5 2004). We conducted sequential mate choice experiments and LED (Aquariums systems, Sarrebourg, France). investigated whether female mate choice relies on male colour From April to September 2018, sequential mate choice change. We predict mate choice outcome should be related to experiments were performed to assess mate choice outcomes. This brightness changes as these changes have been shown to be experimental design mimicked the reproductive behaviour of involved in intrasexual interactions in chameleons (Ligon, 2014; chameleons, as perch-dwelling lizards are likely to approach mates Ligon and McGraw, 2016, 2013, 2018). in a sequential manner during the mating season. Males were split into four different pools of four to five individuals and females in MATERIALS AND METHODS four pools of two to three individuals. To each pool of females, we Animals and husbandry assigned one specific pool of males from a different breeder with Furcifer pardalis is endemic to Madagascar and found in a wide which the sequential mate choice experiment was run. Every female range of habitats along the northern and eastern coasts. They are from each pool was exposed to all males of the paired pool (i.e. 4–5 diurnal tree-dwelling lizards living in relatively intact forests and males). The sequential mate choice experiment was repeated four forest edges, gardens, plantations and degraded habitats. This species times per female. Sequential mate choice was repeated because mate exhibits a strong sexual dimorphism and exceptionally large guarding has been observed in chameleons (Cuadrado, 2006). intraspecific variation in male colouration: females and juveniles Consequently, it is likely that females copulate several times with the are tan to brown with hints of pink or orange, while adult males are same chosen male. However, if a female
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