Field and experimental evidence that competition and ecological opportunity promote resource polymorphism

Biological Journal of the Linnean Society, 2010, 100, 73–88. With 4 figures Field and experimental evidence that competition and ecological opportunity promote resource polymorphism RYAN A. MARTIN* and DAVID W. PFENNIG Department of Biology, University of North Carolina, Chapel Hill, NC 27599, USA bij_1380 73..88 Resource polymorphism – the occurrence within a single population of discrete intraspecific morphs showing differential resource use – has long been viewed as an important setting for evolutionary innovation and diversification. Yet, relatively few studies have evaluated the ecological factors that favour resource polymorphism. Here, we combine observations of natural populations with a controlled experiment to assess the role of intraspecific competition (specifically, the density of conspecifics) and ecological opportunity (specifically, the range of resources available) on the expression of resource polymorphism in spadefoot toad tadpoles. We found that greater conspecific densities and a greater range of available resources together promoted the expression of resource polymorphism. We conclude that, ecological opportunity, in the form of diverse available resources, along with intraspecific competition, may be a prerequisite for resource polymorphism to evolve, because such polymorphisms require diverse resources onto which each morph can specialize as an adaptive response to minimize competition. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 73–88. ADDITIONAL KEYWORDS: character displacement – character release – Spea multiplicata. INTRODUCTION Resource polymorphism – the occurrence within a single population of discrete intraspecific morphs showing differential resource use – rivals speciation as an important source of evolutionary innovation and diversification. Such polymorphisms occur in diverse taxa and they embody some of the most dramatic examples of diversity within species (Smith & Skúlason, 1996; West-Eberhard, 2003). Moreover, resource polymorphisms may represent a critical, early stage in the speciation process (Pfennig & McGee, 2010). Despite their potential significance, relatively little is known about the conditions that favour the evolution of resource polymorphisms. Generally, such polymorphism is thought to reflect an adaptive response to intraspecific competition for resources (reviewed in Smith & Skúlason, 1996). In a population that exploits a continuously varying resource gradient, intraspecific competition should cause disruptive *Corresponding author. E-mail: selection to favour resource polymorphism, because individuals with extreme resource-use traits specialize on less common, but underutilized, resources (see recent reviews in Bolnick, 2004; Martin & Pfennig, 2009). This process is driven by negative frequencydependent selection, in which rare resource-use phenotypes have a fitness advantage. In essence, resource polymorphism may be the intraspecific analogue of ecological character displacement; i.e. it may arise through a process of ‘intraspecific character displacement’ (sensu West-Eberhard, 2003). Resource polymorphism likely requires more than intraspecific resource competition to evolve, however. Although nearly all taxa experience such competition, resource polymorphism is not present in most taxa. As with interspecific character displacement, the evolution of resource polymorphism likely also necessitates ecological opportunity: specifically, the presence of underutilized resources (Pfennig, Rice & Martin, 2006). Because resource polymorphism entails the evolution of a novel resource-use phenotype, underutilized resources must be present for this new phenotype to exploit. In their absence, niche width © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 73–88 73 Received 17 July 2009; accepted for publication 3 November 2009 74 R. A. MARTIN and D. W. PFENNIG erally not practical, however, because of the time required to observe an evolutionary response. One way around this problem is to use species in which alternative resource-use morphs arise through phenotypic plasticity. By using these species, one can investigate the conditions that favour the expression of resource polymorphism and infer that these same conditions have likely favoured the evolution of resource polymorphism. In this study, we undertook such an approach to evaluate the importance of intraspecific competition and ecological opportunity in mediating the expression of resource polymorphism in North American spadefoot toads (genus Spea). Four characteristics of Spea make them ideal for such investigations. First, Spea tadpoles express a striking resource polymorphism, the extremes of which are represented by an ‘omnivore’ ecomorph, which primarily feeds on organic detritus on the pond bottom, and a ‘carnivore’ ecomorph, which primarily feeds on anostracan fairy shrimp in the water column (Pomeroy, 1981). Second, different natural populations differ in their degree of expression of this resource polymorphism, as evidenced by variation among populations in the degree of bimodality and variance in trophic morphology (e.g. see Fig. 1). Thus, we could take advantage of this variation to ask what factors predict variation in the degree of expression of resource polymorphism. Third, previous research has revealed that disruptive selection, arising from intraspecific competition for resources, favours these extreme ecomorphs (Martin & Pfennig, 2009). Finally, an individual’s trophic phenotype depends largely on its diet, with the most extreme carnivores being induced among individuals that eat the most fairy shrimp (Pfennig, 1990). As noted above, systems in which resource polymorphism arises through such phenotypic plasticity can be used to investigate the conditions that favour the expression of resource polymorphism under the assumption that these same conditions favoured the evolution of the resource polymorphism. Such an assumption underlies many investigations into the selective basis of traits that arise through phenotypic plasticity (WestEberhard, 2003). Although this assumption may not hold in situations where inducing and selective environments become decoupled (e.g. because of a recent change in the environment), it appears to be valid in the Spea system. Specifically, previous studies suggest that the same conditions that induce the alternative morphs also selectively favour these morphs (e.g. see Pfennig & Murphy, 2002). Using spadefoot toad tadpoles as our model system, we employed observations of natural populations and a controlled experiment to evaluate the importance of intraspecific competition (specifically, the density of © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 73–88 expansion (and, thus, the evolution of resource polymorphism) is not feasible. Such niche width expansion becomes more f (...truncated)