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Femalelimited Colour Polymorphism in the Crab Spider Synema Globosum

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Femalelimited Colour Polymorphism in the Crab Spider Synema Globosum bs_bs_banner Biological Journal of the Linnean Society, 2014, 113, 368–383. With 8 figures Female-limited colour polymorphism in the crab spider Synema globosum (Araneae: Thomisidae) HELENA AJURIA IBARRA* and TOM READER School of Life Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK Received 24 March 2014; revised 26 April 2014; accepted for publication 27 April 2014 Conspicuous colour variation, caused by the influence of the environment on phenotype or by genetic differences among individuals, is frequently observed in nature. If genetic in origin, colour variation can facilitate the study of mechanisms that contribute to the maintenance of true polymorphisms. Here we describe, for the first time, the female-limited colour polymorphism in the crab spider, Synema globosum. We looked for associations between life-history traits and female colour morph, and identified potential agents of selection that could influence the maintenance of the polymorphism. Our results showed that the polymorphism is discrete and heritable, and that differences in colour among morphs are likely to be detectable by honeybees, birds, and conspecifics. We found limited evidence of differences among morphs in morphology and ecology, and found no differences in components of reproduction. Based on the lines of evidence obtained in this study, we suggest that selection exerted by prey, predators, and/or mates is likely to influence the maintenance of the polymorphism observed in S. globosum. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 368–383. ADDITIONAL KEYWORDS: genetic variation – heritability – life-history traits – predation – reflectance spectra – sexual selection – signalling. INTRODUCTION 2008; Phifer-Rixey et al., 2008; Hampton, Hughes & Houde, 2009). Polymorphism is a widespread phenomenon in nature Variation in colour can be continuous or discrete. that occurs in a broad range of taxa. It is the presence Continuous colour variation has often been observed of multiple genetically and phenotypically distinct to be condition- or environment dependent and may forms in a population, which do not respond to changes not reflect a true (genetic) polymorphism (Hill & in the environment or body condition and can inter- Montgomerie, 1994; Fitze, Kolliker & Richner, 2003). breed to produce fertile hybrids (Roulin, 2004). Discrete variation in colour is usually genetic in Polymorphisms have been a subject of great interest in origin (Forsman et al., 2002; Vercken et al., 2007) and biological research because determining the mecha- thus requires an evolutionary explanation (Gray & nisms that generate and maintain them can shed McKinnon, 2007; Ajuria Ibarra & Reader, 2013). light on how natural selection and other evolutionary If coloration does not have a significant effect on processes shape both genotypes and phenotypes fitness, it is possible that a polymorphism is main- (Brockmann, 2001; Gray & McKinnon, 2007; tained by random genetic drift (Hoffman et al., 2006; Mitchell-Olds, Willis & Goldstein, 2007). Species that Mitchell-Olds et al., 2007). Where fitness is affected by show colour variation are good systems with which to colour, several selective mechanism(s) could play a role study the maintenance of polymorphisms because col- in maintaining colour polymorphisms (Bellido et al., oration is easy to score and is known to be involved in 2002; Oxford, 2005). For example, polymorphisms processes that influence fitness, such as thermoregu- can persist because of heterozygote advantage, where lation and inter- and intraspecific communication individuals with heterozygous genotypes have higher (Gamberale & Tullberg, 1998; Bush, Yu & Herberstein, fitness than do individuals with homozygous-dominant or -recessive genotypes (Vercken, Clobert & Sinervo, 2010). Different morphs can also persist in spa- *Corresponding author. E-mail: [email protected] tially and/or temporally heterogeneous environments, 368 © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 368–383 FEMALE COLOUR POLYMORPHISM IN SPIDERS 369 where each morph has an advantage under particular Herberstein, 2004; Tso et al., 2006; Morse, 2007; conditions (Todd et al., 2006; Forsman et al., 2011; Llandres et al., 2011; Herberstein & Gawryszewski, Parkash et al., 2011). Negative frequency-dependent 2013), sexual selection (Masta & Maddison, 2002; selection, where rare morphs have a fitness advantage Hebets & Maddison, 2005; Lim, Li & Li, 2008; Elias over common morphs, is another mechanism that can et al., 2012), and thermoregulation (Robinson & explain the maintenance of polymorphisms (Bond & Robinson, 1978), and could potentially serve a func- Kamil, 1998; Bleay, Comendant & Sinervo, 2007; tion for predator avoidance (Gunnarsson, 1987; Théry Takahashi & Watanabe, 2010). Finally, polymor- & Casas, 2002; Clark et al., 2011). To exploit this phisms can be maintained if different morphs exhibit potential fully, we need, first of all, to characterize alternative strategies that result in equal mean fitness colour variation in species of interest, to distinguish values (Roulin et al., 2003). between discrete and continuous variation, and to Colour variation is common in spiders (Holl, 1987; establish whether it reflects a true genetic polymor- Oxford & Gillespie, 1998; Gawryszewski & Motta, phism. We then need to look for fitness differences 2012; Geay et al., 2012; Kemp et al., 2013). Most among morphs and relate these to ecological factors studies of the phenomenon have concentrated on in the environment. species that are able to match their colour to that In this study, we examine conspicuous colour vari- of the background, in order to appear cryptic or ation in the crab spider Synema globosum (Fabricius to attract prey (Théry & Casas, 2002; Heiling, 1775). In this species, females can have red, yellow, Herberstein & Chittka, 2003; Heiling et al., 2005; or white coloration around the margins of the Defrize, Théry & Casas, 2010). In most cases, these opisthosoma, surrounding a characteristic black species are not truly polymorphic but rather they marking, whereas males have an almost entirely have the ability to change coloration behaviourally black opisthosoma with only two very small white (Théry & Casas, 2002; Heiling et al., 2005). Genetic areas on the lateral parts (Fig. 1). The colour varia- colour polymorphisms in spiders have been most tion in females appears to be discrete; the three extensively studied in the candy-stripe spider different colours have been found to be produced (Enoplognatha ovata) and the Hawaiian happy-face by different types of pigments in the epithelial spider (Theridion grallator) (Oxford & Gillespie, cells of the opisthosoma (Théry & Casas, 2009). 2001). Evidence implicates both genetic drift and Synema globosum is distributed in southern Europe, natural selection in the maintenance of the polymor- Asia, and northern Africa (Preston-Mafham, 1998) phism in E. ovata (Oxford & Shaw, 1986; Reillo & and is a common species in our study site (see below) Wise, 1988; Oxford, 2005), whilst selective forces are where it conspicuously occupies flowers of many thought to be most important in T. grallator (Gillespie different species and can be seen attacking flower- & Tabashnik, 1990; Gillespie & Oxford, 1998). visiting invertebrates. Adults can be found from the However, regarding the ecological factors that end of March, females with egg sacs can be found could be generating these evolutionary mechanisms, from early May, and spiderlings have been observed there is inconclusive evidence in favour of negative- from early June. The absence of adults in autumn and frequency-dependent selection in T. grallator winter months suggests an annual life cycle. We con- (Gillespie & Tabashnik, 1990; Gillespie & Oxford, ducted a survey to establish the frequencies of the 1998) and no studies in E. ovata. Other less-well- three colour morphs in the study site. We then deter- studied species of colour-polymorphic spider appear to mined if the colour variation observed in female show a correlation between colour and environmental S. globosum is discrete or continuous by quantifying factors such as substrate, temperature, and light con- the variation among female individuals using reflec- ditions (Gunnarsson, 1987; Bonte & Maelfait, 2004; tance spectra measurements. We then carried out a Kemp et al., 2013), as well as differences in prey breeding experiment to evaluate whether the poly- capture rates between morphs (Tso et al., 2002; Tso, morphism is heritable (i.e. has a genetic origin). Lin & Yang, 2004; but see also Geay et al., 2012). Finally, we investigated possible fitness differences Although, with the exceptions described above, among morphs and looked for other, more cryptic, they are not well studied, we believe that colour- traits that might correlate with colour, by examining polymorphic spiders represent excellent potential differences in morphology, behaviour on flowers, and models for investigating the maintenance of genetic reproductive output among morphs. and phenotypic diversity, and, in particular, for exam- ining the role played by ecological interactions in MATERIALS AND METHODS generating selection on colour morphs. This potential is highlighted by what is known about the ecological FREQUENCIES OF COLOUR MORPHS significance of colour in spiders: it has been observed To determine the frequencies of red, yellow, and white to be important in foraging behaviour (Heiling & female
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