Polyphenism Evolution: Phenotypic Plasticity and Locomotor Performance in Spadefoot Toads

Polyphenisms, where an individual can express one of two or more alternative, discrete phenotypes, are well suited to study the ecological conditions that favor the maintenance of phenotypic variation within a single population. In particular, polyphenisms can be used as powerful tools for studying the relationships between genotypic and phenotypic variation, performance, and fitness. They can also be used to study the proximate mechanisms that underlie phenotype development, and the role of developmental plasticity in morphological diversification.

Tadpoles of the spadefoot toads, Scaphiopus multiplicatus and S. bombifrons, exhibit a trophic polyphenism; when the desert ponds inhabited by larvae of these species begin to dry and anostracan prey are present, typical omnivorous larvae may develop an alternative, carnivore morphology. Carnivores possess rapid growth and development but have lower resistance to starvation as metamorphs.

As part of my dissertation research, David Pfennig and I studied the effects of genotype, individual condition, and the environment on morph expression in tadpoles of these species. I also investigated the consequences of morph expression for locomotor performance in metamorphs. My overall goal was to test the hypothesis that the environment and individual condition interact to affect the fitness costs or benefits of expressing either larval phenotype. We found that such condition-dependent fitness determines individual, adaptive morph expression and influences maintenance of this polyphenism.

Our early work showed differences among species and sibships in the propensity to exhibit the alternative morph in response to a standardized cue and kin environment. We later found that the propensity to express the carnivore morph is also affected by absolute and relative tadpole size; although smaller individuals have lower thresholds for carnivore-morph induction, they are effectively outcompeted for the dietary cue that triggers carnivore expression by larger tadpoles. Hence, larger tadpoles effectively have a greater likelihood of carnivore expression in nature. Finally, we found a negative correlation in the propensity to express the carnivore morph and mean development rate among sibships and species within the genus. However, this correlation breaks down when examined among individuals within sibships or when effects of temperature on development are considered.

I found that larval phenotype affects several aspects of metamorph locomotor performance. Although tadpoles of both omnivore and carnivore morphs metamorphose into indistinguishable toadlets, there are substantial differences in metamorph performance rooted in larval history. Larval morph interacts with several ecological factors to produce (morphology-independent) differences among types in maximal speed, the onset of fatigue, and endurance. These post-metamorphic effects of larval phenotype on fitness enhance the benefits of condition-dependent larval morph expression and likely play a role in polyphenism maintenance.

Relevant publications

P.M. Brakefield and W. A. Frankino. 2009. Polyphenisms in Lepidoptera: Multidisciplinary approaches to studies of evolution and development. in: Phenotypic Plasticity in Insects: Mechanisms and Consequences. Ananthakrishnan, TN and D. W. Whitman (Eds.). Oxford University Press.

Frankino, W. A., and R. A. Raff. 2004. Evolutionary importance and pattern of phenotypic plasticity: Insights gained from development. Pp. 64-81 in T. J. DeWitt and S. M. Scheiner, eds. Phenotypic Plasticity, Functional and Conceptual Approaches. Oxford Press.

Frankino, W. A., and D. W. Pfennig. 2001. Condition-dependent expression of alternative phenotypes in spadefoot toad tadpoles. Evolutionary Ecology Research 3:939-951.

Pfennig, D. W., and W. A. Frankino. 1997. Kin-mediated morphogenesis in facultatively cannibalistic tadpoles. Evolution 51:1993-1999.