Temporally Dissociated, Trait-Specific Modifications Underlie Phenotypic Polyphenism in Spea multiplicata Tadpoles, Which Suggests Modularity

Research Article TheScientificWorldJOURNAL (2007) 7, 715–726 TSW Development & Embryology ISSN 1537-744X; DOI 10.1100/tsw.2007.159 Temporally Dissociated, Trait-Specific Modifications Underlie Phenotypic Polyphenism in Spea multiplicata Tadpoles, Which Suggests Modularity Brian L. Storz* and Joseph Travis Department of Biological Science, Florida State University, Tallahassee, Florida E-mail: , Received November 28, 2006; Revised April 3, 2007; Accepted April 5, 2007; Published May 29, 2007 Many organisms that develop in a variable environment show correlated patterns of phenotypic plasticity in several traits. Any individual trait modification can be beneficial, neutral, or deleterious in any particular environment; the organism's total fitness, which determines if the plasticity is adaptive, is the sum of these changes. Although much is known about how plastic traits contribute to fitness, less is known about the extent to which the various trait changes involved in the plastic responses share their developmental control. Shared control suggests that the various responses evolved in unison, but independent control suggests independent evolution of many components. Spadefoot toads have evolved adaptive polyphenism to cope with developing in rapidly drying ephemeral ponds. Larvae hatch as omnivores, but on exposure to an environmental cue, may develop into carnivores. We compared trait development in the two morphs and found that differences in jaw musculature, head dimensions, and intestines emerged early in development, whereas differences in shape of the tail emerged later. In omnivores, all traits except intestine length and hind-limb length were negatively allometric with body length; in carnivores, two of three jaw muscles displayed positive allometry and, among those that were negatively allometric, all except head width showed larger allometric coefficients in carnivores. Hind-limb length was positively allometric in both forms, but the allometric coefficients did not differ significantly. Intestine length was positively allometric to body length in both forms, but in this case, omnivores exhibited the higher coefficient. These results suggest that spadefoot plasticity is trait specific and the responses are suggestive of the existence of at least two modules: a suite of trophic traits that responds early in development and a suite of tail traits that responds later. The developmental control of these suites is the subject of further investigation. KEYWORDS: Spea, spadefoot toad, modularity, development, heterochrony, allometry INTRODUCTION *Corresponding author. ©2007 with author. Published by TheScientificWorld; www.thescientificworld.com 715 Storz and Travis: Spadefoot Polyphenism Development TheScientificWorldJOURNAL (2007) 7, 715–726 Developmental plasticity, the ability to produce multiple phenotypes from one genotype, has long been of interest to biologists[1,2]. Its adaptive importance lies in the organism’s ability to perceive characteristics of the environment and, in response, to switch to a developmental pathway that will yield a phenotype better suited to that environment[3]. Developmental plasticity should be favored in fluctuating environments in which a reliable cue signals approaching change[3,4,5]. Some of the best-known examples include plant shade avoidance in response to high density[6]; alternate caterpillar morphology induced by seasonal diet differences[7]; and tadpole plasticity for larval period, morphology, and behavior in response to pond duration, temperature, food level, and predation risk[8,9,10,11,12,13,14, 15,16,17,18,19]. Studies of plasticity have shown that several traits are usually modified in a correlative manner in response to an environmental cue. For example, male sailfin mollies (Poeciliidae: Poecilia latipinna) that experience higher temperatures have a lower visceral mass for their size, but a higher testis mass[20], individual Daphnia pulex respond to predation risk by altering several aspects of their morphology and life history[21], and changes in tadpole tail morphology in response to predators usually involve changes in several individual traits[17,19,22]. When several traits change in response to an environmental cue, each individual trait modification may be beneficial, neutral, or deleterious in any particular environment, and the organism’s total fitness is the sum of these effects[23,24]. Plasticity, therefore, must be understood as alteration of entire developmental trajectories and not just as putatively adaptive shifts in a few traits[25]. If this is so, then it is important to understand how many developmental trajectories are involved, i.e., to understand if all of the traits have been molded to respond independently by selection for plasticity, whether there are interconnected units that change relatively independently of other interconnected units[26,27] or whether the individual traits are so tightly constrained by shared control into suites that they exhibit very few possible discrete plastic responses. New World spadefoot toads are an especially suitable system for studying developmental integration of plasticity and its consequences. Larvae of at least two species (Spea multiplicata and S. bombifrons) show a striking polyphenism between “typical” filter-feeding omnivores and carnivores (Fig. 1) that actively prey on microcrustaceans and conspecifics. The phenotypes are so dissimilar that they were originally classified as different subspecies[28]. This polyphenism is thought to have evolved as an adaptation for survival in temporary pond environments[14,29]. In these environments, survival depends on the ability to develop and metamorphose rapidly. Carnivorous individuals have been shown to have a competitive advantage in rapidly drying ponds because they metamorphose sooner than omnivores[30], thereby avoiding desiccation. Conversely, in long-lived ponds, omnivores have higher survival at metamorphosis because of their greater fat reserves[14,29]. Spea multiplicata tadpoles hatch as omnivores, but on exposure to an environmental cue[14], individuals may shift their ontogenies to become carnivores. Carnivores are known to have enlarged heads, enlarged jaw musculature, shortened intestines, and increased keratinization of the mouth to form a beak, relative to omnivores (Figs. 1A–C)[14,29,30,31]. However, it is not known whether these traits change independently or as developmental modules, whether the change from omnivore to carnivore represents a shift in total somatic growth or only in specific traits, or whether developmental trait modification has additional, as yet unknown, consequences. In this study, we address these questions as a first step toward investigating the developmental trajectories that produce these strikingly different morphs. We ask whether the change from omnivore to carnivore represents a shift in total somatic growth or only in specific traits, whether these tra (...truncated)