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Hormonal Regulation of Female Nuptial Coloration in a Fish Hormones And Hormones and Behavior 54 (2008) 549–556 Contents lists available at ScienceDirect Hormones and Behavior journal homepage: www.elsevier.com/locate/yhbeh Hormonal regulation of female nuptial coloration in a fish Helen Nilsson Sköld a,⁎, Trond Amundsen b, Per Andreas Svensson c, Ian Mayer d, Jens Bjelvenmark a, Elisabet Forsgren b,e a Department of Marine Ecology, Göteborg University, 566 Kristineberg, SE-450 34 Fiskebäckskil, Sweden b Department of Biology, Norwegian University of Science and Technology, NO-7491 Trondheim, Norway c School of Biological Sciences, Monash University, VIC 3800, Australia d Department of Biology, University of Bergen, NO-5020 Bergen, Norway e Norwegian Institute for Nature Research, NO-7485 Trondheim, Norway article info abstract Article history: Physiological color change in camouflage and mating is widespread among fishes, but little is known about Received 20 November 2007 the regulation of such temporal changes in nuptial coloration and particularly concerning female coloration. Revised 11 April 2008 To better understand regulation of nuptial coloration we investigated physiological color change in female Accepted 23 May 2008 two-spotted gobies (Gobiusculus flavescens). Females of this species develop an orange belly that acts as an Available online 10 June 2008 ornament. The orange color is caused by the color of the gonads combined with the chromathophore based – Keywords: pigmentation and transparency of the skin. Often during courtship and female female competition, a rapid Sexual selection increase in orange coloration, in combination with lighter sides and back that increases skin and body Female ornament transparency, gives the belly an intense ‘glowing’ appearance. To understand how this increased orange Chromatophores coloration can be regulated we analysed chromatic and transparency effects of neurohumoral agents on Gobiusculus flavescens abdominal skin biopsies in vitro. We found prolactin and α-melanocyte stimulating hormone (MSH) to Prolactin increase orange coloration of the skin. By contrast, melatonin and noradrenaline increased skin transparency, Melanocyte stimulating hormone but had a negative effect on orange coloration. However, mixtures of melatonin and MSH, or melatonin and Melatonin prolactin, increased both orange coloration and transparency. This effect mimics the chromatic ‘glow’ effect that commonly takes place during courtship and intra sexual aggression. Notably, not only epidermal chromatophores but also internal chromatophores lining the peritoneum responded to hormone treatments. There were no chromatic effects of the sex steroids 17β-estradiol, testosterone or 11-ketotestosterone. We hypothesize that similar modulation of nuptial coloration by multiple hormones may be widespread in nature. © 2008 Elsevier Inc. All rights reserved. Splendid body coloration and patterns are widespread among chromatophores in the skin (morphological color changes: Sugimoto, animals and are often the result of sexual selection (Andersson, 1994). 2002), skin patterns can be modified within minutes by reflective The nuptial coloration is commonly influenced by sex hormones changes in iridophores and through aggregation or dispersion of the (Rhodes et al., 1997; Noriega and Hayes, 2000;Toft and Baatrup, 2001; pigment-containing organelles inside the chromatophores (physiolo- Larsson et al., 2002; Toft and Baatrup, 2003). Although nuptial body gical color change: Kodric-Brown, 1998; Burton, 2002; Sköld et al., coloration in teleost fishes, as well as in many other animals, is 2002; Mähtiger et al., 2003). Such temporal pigment dispersal generally more pronounced in the males, females in several fish increases body pigmentation while pigment aggregation results in species also develop nuptial color patterns as they become sexually less body pigmentation (Fujii and Oshima,1994, Svensson et al., 2005). receptive (McLennan, 1995; Beeching et al., 1998; Takahashi, 2000). Reduction in black body pigmentation due to melanophore pigment The body coloration and patterns are often caused by chromatophores, aggregation commonly also results in greater skin transparency (Fujii which are large star shaped pigment-containing cells located in the and Oshima, 1994). Long-term chromatophore pigment dispersal also skin. The chromatophores are grouped into subclasses based on their stimulates pigment transfer to surrounding cells and induces color: xanthophores (yellow), erythrophores (red/orange), irido- chromatophore production (Sugimoto, 2002). phores (reflective/iridescent), leucophores (white), melanophores Physiological color change is very widespread, perhaps ubiquitous, (black/brown) and cyanophores (blue). In addition to the seasonal among fishes and is under hormonal and/or neuronal regulation (Fujii color change, which is caused by changes in the number of and Oshima, 1994). Such color modulation may provide camouflage (DeLoach and Humann, 1999; Healey, 1999; Höglund et al., 2002)or ⁎ Corresponding author. act in social signalling (DeMartini, 1985; Kodric-Brown, 1998; Höglund E-mail address: [email protected] (H.N. Sköld). et al., 2002). Fish species showing temporal modulation of coloration 0018-506X/$ – see front matter © 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.yhbeh.2008.05.018 550 H.N. Sköld et al. / Hormones and Behavior 54 (2008) 549–556 include many of the splendidly colored fishes inhabiting coral reefs, understanding male ornamentation (Cotton et al., 2006) while female which undergo major or minor changes in coloration depending on ornamentation has traditionally received less attention (but see social or ecological context (e.g. Thresher, 1984; Michael, 2001; Amundsen, 2000; Amundsen and Pärn, 2006; Kraaijeveld et al., DeLoach and Humann 1999). Examples include several angelfishes 2007; Haselton et al., 2007). (Pomacanthidae) and damselfishes (Pomacentridae) in which both To better understand physiological mechanisms of color regulation sexes attain temporary colors or patterns during courtship, and in a species for which the social and sexual context of physiological cardinalfishes (Apogonidae) in which females of several species sport color change is known, we have investigated the two-spotted goby, temporal color changes (Thresher, 1984). Physiological color change Gobiusculus flavescens. The two-spotted goby is a small, semi-pelagic may allow fishes to be normally inconspicuous but to attain bright and sexually dimorphic marine fish with paternal care and dynamic colors during brief spells of courtship, as in the bluelip parrotfish sex roles (Gordon, 1983; Skolbekken and Utne-Palm, 2001; Bjelven- (Cryptotomus roseus) that sports bright gold, pink, blue and green mark and Forsgren, 2003; Forsgren et al., 2004). The females develop colors only when swooping down to court females in the seagrass colorful orange bellies as the gonads mature (Svensson, 2006). The (DeLoach and Humann, 1999). Nuptial color patterns can in many degree of belly coloration varies among fully mature females, and fishes therefore potentially become more conspicuous during court- males show a preference for females with the most colorful bellies ship by physiological color change using chromatophores (Rowland (Amundsen and Forsgren, 2001). The orange color is carotenoid-based et al., 1991; Kodric-Brown, 1998; Berglund, 2000; Berglund and and caused by the additive effect of the pigmented abdominal skin Rosenqvist, 2001; Svensson et al., 2005). and the pigmented gonads being visible through the semi-transparent Despite that physiological color change apparently plays a major skin (Svensson et al., 2005; Svensson, 2006). Thus, in breeding G. role in the mating and thus reproductive behaviour of many fishes flavescens females, the distinctive orange belly coloration is the (and other poikilothermic animals), there are remarkably few studies consequence of three components: skin transparency, skin coloration on function and physiological mechanisms behind temporary changes and gonad coloration (Svensson et al. 2005). Both during courtship in nuptial body coloration in an ecological or evolutionary context. and in agonistic interactions between females, two-spotted goby Few studies have analysed physiological mechanisms of color females actively display their strikingly orange bellies by conspicu- regulation in species for which the social and sexual context of ously bending their body towards the courted male or the female physiological color change is known. The phenomenon has further competitor (Amundsen and Forsgren, 2001; Berger, 2002; Fig. 1). rarely been studied in the wild beyond verbal descriptions. Despite The dorsal side of a mature two-spotted goby female (down to the well-described regulation of chromatophores at the cellular and around the lateral line) is rich in melanophores, in contrast to the belly molecular levels that has revealed a number of potential regulatory (ventral side, below the lateral line) which has sparse melanophore mechanisms (Fujii and Oshima, 1994; Fujii, 2000; Sköld et al., 2002), pigmentation but instead a high density of erythrophores and there is little information about the processes that modulate xanthophores (Svensson et al., 2005; Figs. 1 and 2). Observations coloration and patterns, including hormonal regulation, in larger both in the wild and in the laboratory have revealed that a striking areas of the skin or at the level of the whole fish. In addition, ecological physiological color change takes place within minutes when female research on sexual selection and
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