Increased competition as a cost of specialization during the evolution of resource polymorphism

bs_bs_banner Biological Journal of the Linnean Society, 2012, 107, 845–853. With 3 figures Increased competition as a cost of specialization during the evolution of resource polymorphism JEFFREY S. PAULL, RYAN A. MARTIN† and DAVID W. PFENNIG* Received 22 May 2012; revised 15 June 2012; accepted for publication 15 June 2012 Identifying the factors that promote or preclude the evolution of resource polymorphism is essential for understanding the origins of diversity. Although such polymorphisms have long been viewed as an adaptive response to intraspecific competition, they are by no means ubiquitous, even in populations experiencing strong competition. In the present study, we examined a potentially important cost of resource polymorphism. Specifically, resource polymorphism typically entails the evolution of one or more resource-use specialists, and these specialists may suffer more from competition with other specialists than generalists would with other generalists. Using spadefoot toad tadpoles as a model system, we combined stable isotope analyses with an experiment aiming to characterize dietary differences between alternative carnivore and omnivore morphs and to assess the potential ecological consequences of any such differences. We found that carnivores and omnivores represent alternative trophic specialists and generalists, respectively. We also established that the specialist morph (carnivores) experienced greater intramorph competition than the generalist morph (omnivores). We hypothesize that the greater intramorph competition faced by specialists stems ultimately from functional limitations associated with trophic specialization, which prevent specialists from switching to alternative resources when their resource is depleted. These costs may even preclude the evolution of distinct resource-use specialists, and hence resource polymorphism, in certain populations. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 845–853. ADDITIONAL KEYWORDS: functional constraints – intraspecific variation – stable isotopes – trade-offs – trophic morphology. INTRODUCTION Resource polymorphisms (i.e. the occurrence within a population of alternative morphs showing differential resource use) are striking examples of intraspecific diversity (Smith & Skúlason, 1996). Indeed, the phenotypic differences between such alternatives often resemble (in kind, if not in degree) the phenotypic differences between distinct species, suggesting that these phenotypic alternatives may represent incipient species (Liem & Kaufman, 1984; Meyer, 1987; WestEberhard, 1989; Wimberger, 1994; Skúlason, Snorrason & Jónsson, 1999; Adams & Huntingford, 2004; Calsbeek, Smith & Bardeleben, 2007; Wund et al., 2012). Moreover, alternative resource-use morphs may *Corresponding author. E-mail: †Current address: Department of Biology, North Carolina State University, Raleigh, NC, USA. function ecologically as separate species (Harmon et al., 2009), and their presence might even increase the likelihood that interacting species will coexist (Clark, 2010). Thus, identifying the factors that promote or preclude the evolution of resource polymorphism is crucial for explaining the origin and maintenance of biodiversity. Resource polymorphism is assumed to evolve as an adaptive response to intraspecific competition (Smith & Skúlason, 1996; Svanbäck et al., 2008; Pfennig & Pfennig, 2012). Longstanding theory predicts that, in a population facing intense intraspecific competition, frequency-dependent disruptive selection should favour alternative resource-use morphs (Doebeli, 2011). Empirical data largely support this prediction (Smith, 1993; Robinson, Wilson & Shea, 1996; Bolnick, 2004; Svanbäck et al., 2008; Calsbeek, 2009; Hendry et al., 2009; Martin & Pfennig, 2009; Cucherousset et al., 2011). Yet, although intraspecific © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 845–853 845 Department of Biology, CB #3280, Coker Hall, University of North Carolina, Chapel Hill, NC 27599-3280 USA 846 J. S. PAULL ET AL. expression (Ledón-Rettig & Pfennig, 2011). Moreover, previous research has revealed that competitivelymediated disruptive selection has likely acted on this variation to favour carnivore–omnivore polymorphism (Pfennig, Rice & Martin, 2007; Martin & Pfennig, 2009). We combined stable isotope analyses of tadpoles from natural populations with a controlled experiment aiming to characterize dietary differences between these alternative carnivore and omnivore morphs and to assess the potential ecological consequences of any such differences. Our data suggest that resource-use specialists may indeed experience greater competition than resource-use generalists. MATERIAL AND METHODS STABLE ISOTOPE ANALYSIS Although Pomeroy (1981) compared the gut contents of omnivores and carnivores, gut contents only reveal what individuals ate recently and therefore do not measure potential lifetime dietary differences between individuals. Additionally, and perhaps more importantly, gut contents only reveal what individuals consume and not what they actually assimilate. To characterize dietary differences between morphs, we therefore performed stable isotope analyses. We began by collecting tadpoles from four ponds near Portal, AZ, approximately 16 days after each pond filled and approximately 14 days posthatching (in all ponds, all eggs were laid on the same day; tadpoles began to metamorphose at around 16 days posthatching). In all ponds, S. multiplicata was the only species of Spea present. We collected tadpoles from randomly selected sites throughout each pond using a handheld dip net. Immediately after collection, we euthanized the tadpoles by immersion in a 0.1% aqueous solution of tricane methanesulfonate (MS 222). Tadpoles were then frozen on dry ice and shipped to the University of North Carolina, where they were prepared for morphological and stable isotope analyses. To categorize each field-caught tadpole by morphotype, we followed the methods of Pfennig et al.(2007). Briefly, we first measured each tadpole’s mass and snout–vent length (SVL). We then measured the width of the orbitohyoideus (OH) muscle and characterized the shape of each tadpole’s keratinized mouthparts (MP). In addition, we counted the number of rows of labial teeth (LT; Martin & Pfennig, 2009) and approximated the length of each tadpole’s intestines by counting the number of gut coils (GC). We standardized OH for body size (SVL) by regressing ln (i.e. natural log) OH on ln SVL and used the resulting residuals for the subsequent analyses. We then © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107, 845–853 competition is widespread and frequently strong (Gurevitch et al., 1992), resource polymorphism is far from ubiquitous (Smith & Skúlason, 1996). Thus, there may be fitness costs of resource polymorphism that (...truncated)