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Spectral Data Reveal Unexpected Cryptic Colour Polymorphism in Female Sailfin Silverside fish from Ancient Lake Matano

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Spectral Data Reveal Unexpected Cryptic Colour Polymorphism in Female Sailfin Silverside fish from Ancient Lake Matano Hydrobiologia (2014) 739:155–161 DOI 10.1007/s10750-013-1557-y SPECIATION IN ANCIENT LAKES 6 Spectral data reveal unexpected cryptic colour polymorphism in female sailfin silverside fish from ancient Lake Matano Jobst Pfaender • Suzanne M. Gray • Ingolf P. Rick • Simone Chapuis • Renny K. Hadiaty • Fabian Herder Received: 18 January 2013 / Accepted: 18 May 2013 / Published online: 19 July 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Persistent colour polymorphisms can antoniae ‘small’, a sailfin silverside species endemic to result from natural and/or sexual selection, and may ancient Lake Matano, and found evidence for a colour occur in males, females, or both sexes. Contrary to polymorphism in both sexes. The three colour morphs conspicuous patterns frequently observed in courtship distinguished by spectral data correspond to those colouration, differences in cryptic colouration are not commonly reported for males, and are also present in always perceived by the human sensory system. In the visually (to a human eye) cryptic females. Females sexually dimorphic sailfin silversides fishes, males show hue value patterns similar to those present in show conspicuous colour polymorphisms whereas males, but differ from males substantially in chroma females appear monomorphic and cryptic. We mea- and brightness. This is, to the best of our knowledge, sured the spectral composition of body, fin and the first example of a cryptic colour polymorphism in peduncle colouration in male and female Telmatherina fishes; however, its significance for the mating system remains unknown. The present finding highlights the need for incorporating female spectral data into Guest editors: T. von Rintelen, R. M. Marwoto, G. D. Haffner analyses of colour patterns, and suggests that colour & F. Herder / Speciation in Ancient Lakes – Classic Concepts analyses should include cryptic sexes. and New Approaches Keywords Colour polymorphism Á Cryptic Á Malili Electronic supplementary material The online version of this article (doi:10.1007/s10750-013-1557-y) contains Lakes Á Sulawesi Á Lake Matano Á Telmatherina supplementary material, which is available to authorized users. J. Pfaender (&) Á S. Chapuis Á F. Herder R. K. Hadiaty Sektion Ichthyologie, Zoologisches Forschungsmuseum Museum Zoologicum Bogoriense, Ichthyology Alexander Koenig, Adenauerallee 160, 53113 Bonn, Laboratory, Division of Zoology, Research Center for Germany Biology, Indonesian Institute of Sciences (LIPI), e-mail: [email protected] Jl. Raya Bogor Km 46, Cibinong 16911, Indonesia S. M. Gray Department of Biology, McGill University, 1205 Dr. Penfield Ave, Montreal, QC H3A 1B1, Canada I. P. Rick Institute for Evolutionary Biology and Ecology, University of Bonn, An der Immenburg 1, 53121 Bonn, Germany 123 156 Hydrobiologia (2014) 739:155–161 Introduction restrictions to gene flow among blue, blue-yellow and yellow male colour morphs (Herder et al., 2008; Colour polymorphism, the maintenance of two or Walter et al., 2009). more genetically determined colour morphs within a Here, we compare spectrometric data taken from single interbreeding population (Huxley, 1955), is a both sexes of the roundfin species Telmatherina common phenomenon in various animals such as antoniae ‘small’ (Fig. 1). Our results clearly confirm birds, butterflies and fishes (reviewed by Gray & the distinct colour polymorphism in males, which has McKinnon, 2007). Such polymorphisms play a role in so far only been reported based only on visual visual signalling, including mate choice and territory classification, but add the unexpected occurrence of defence (Andersson, 1994), and there is evidence that a cryptic polymorphism in females, reflecting the sexual as well as ecological selection may contribute conspicuous pattern in males. to its persistence. Alternative colour morphs can likely facilitate population divergence and speciation (Chun- co et al., 2007; Seehausen et al., 2008; Nosil et al., 2009; Hurtado-Gonzales & Uy, 2010); however, the processes maintaining within-population polymor- phism remains only partially understood. Both theo- retical work and case studies suggest that the persistence of alternative genetic colour morphs can be promoted through sensory drive, frequency-depen- dent selection, male–male competition, or heteroge- neous environments (Chunco et al., 2007; Gray & McKinnon, 2007; Forsman et al., 2008; Gray et al., 2008a; Hurtado-Gonzales & Uy, 2010; Maan & Seehausen, 2010; Castillo Cajas et al., 2012; Hancox et al., 2013). Much of the work on colour polymor- phism has focused on males with distinct courtship colouration, or on species with a persistent colour polymorphism in both sexes (Gray & McKinnon, 2007); a cryptic female colour polymorphism has not been reported from fishes thus far. Conspicuous male colour polymorphisms occur in several species of the sailfin silversides (Atherinifor- mes: Telmatherinidae) species flock in Central Su- lawesi, Indonesia (Herder et al., 2006a). Radiating in the clear waters of the ancient Malili Lakes and the surrounding watershed (Herder et al., 2006b; Pfaender et al., 2010, 2011), males of these predominantly small freshwater fishes show conspicuously elongated and coloured fins, as well as colourful bodies, whereas females appear cryptic: dusky grey to silvery or bronze-coloured body and short fins lacking conspic- uous colours, depending on the species. Extraordi- narily deep and clear Lake Matano harbours the small species flock of three endemic ‘roundfin’ sailfin silversides that most likely evolved following ecolog- ical selection pressure in sympatry (Herder et al., Fig. 1 The three distinct Telmatherina antoniae ‘small’ male 2008). Clear population structure discriminates the colour morphs (a; yellow; blue-yellow; blue) and a cryptic three morphospecies, while in contrast there are no female (b) photographed in their natural environment 123 Hydrobiologia (2014) 739:155–161 157 Materials and methods of two scans, with an integration time of 100 ms. Measured spectra were directly visually inspected and Adult T. antoniae ‘small’ ($ = 83; # = 78) were directly repeated if they failed. caught with gill nets between May and August 2010 at Since visual system characteristics of the study 53 sampling locations distributed around Lake Matano’s species are not available, we applied the segment shoreline. Directly after capture, fish were euthanized classification method following Endler (1990). This with an overdose of MS222 and reflectance spectra method is independent of the specific properties of the between 400 and 700 nm were immediately recorded at observer’s visual system, and divides the spectrum the mid-body, second dorsal fin and the peduncle (with range between 400 and 700 nm into four equal segments fish placed on a black background; Fig. 2). No colour of 75 nm each (Endler, 1990). Respectively, these four change was detectable during euthanization and the segments correspond to the violet-blue (400–474 nm), standardized measurement procedure took approxi- blue-green (475–549 nm), green-orange (550–624 nm) mately 20 s in total for each individual. For measure- and orange-red (625–699 nm) wavelengths (Endler, ments, we used a JAZ-EL200-XR1 (Ocean optics) with 1990). Each reflectance measurement was transformed a tungsten halogen light source (JAZ-VIS-NIR, into variables of brightness (intensity), chroma (satura- 300–2200 nm), a standard reflectance probe (QR-400- tion), and hue (function of the shape of the spectrum), 7-VIS-NIR, 400–2500 nm) with a 400 lmcorediam- holding visual sensitivity and environmental light eter and a diffuse white-standard (WS-1-SL, Ocean constant (see Electronic Supplementary Material Table Optics). To exclude environmental light and to obtain a S1 for details; Hofmann et al., 2006). standardized distance of 2.5 mm and a fixed angle of 90° A model-based clustering approach, implemented to the specimen, a black tube with a diameter of 5 mm in the R package ‘mclust’ (Fraley et al., 2012;R was mounted on the end of the probe and placed directly Development Core Team, 2012), was used indepen- on the corresponding measurement point. The present dently for males and females to determine the number study focused on the spectral analysis of colour morphs of colour morphs in T. antoniae ‘small,’ independent previously distinguished solely by human visual classi- of visual sensitivity or ambient light (e.g., Hofmann fication, and therefore did not incorporate UV. The et al., 2006; Gumm et al., 2011); the best model and reflectance probe chosen was hence sensitive to wave- thus the number of clusters was chosen based on the lengths between 400 and 700 nm, so that the UV part of Bayesian Information Criterion (BIC). the spectrum was not included. All body parts were A one-way ANOVA and Tukey’s post hoc test in measured once. Each spectrum is based on the average case of equal or Welch test with a Dunnet T3 post hoc 50 40 60 32 40 48 24 30 16 36 20 8 Reflectance (%) Reflectance (%) Reflectance (%) 24 10 0 450 500 550 600 650 450 500 550 600 650 450 500 550 600 650 Wavelength (nm) Wavelength (nm) Wavelength (nm) Colormorph BBB BYB YYY Fig. 2 Measured body parts and their corresponding reflectance spectra (mean values with standard deviation) for each colour morph 123 158 Hydrobiologia (2014) 739:155–161 test in case of unequal variances was applied to each the human eye, show the same morph-specific pattern colour trait (hue, chroma and brightness) of each body in hue as the males (Fig. 3; Table 1). Female sailfin part measured to test for differences
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