Reassessment of the environmental mechanisms controlling developmental polyphenism in spadefoot toad tadpoles

Abstract

Identifying the environmental mechanism(s) controlling developmental polyphenism is the first step in gaining a mechanistic and evolutionary understanding of the factors responsible for its expression and evolution. Tadpoles of the spadefoot toad Spea multiplicata can display either a "typical" omnivorous or a carnivorous phenotype. Exogenous thyroxine and feeding on conspecific tadpoles have been accepted as triggers for development of the carnivorous phenotype on the basis of a series of studies in the early 1990s. I repeated the thyroxine and conspecific-feeding assays and demonstrated that neither exogenous thyroxine nor feeding on conspecifics induces the carnivorous phenotype. Previous researchers used simple ratio statistics to argue that field-collected carnivores and thyroxine-treated tadpoles are similar, and my results supported these claims if I used the same simple ratio methodology. However, investigation of trait developmental trajectories and allometries for field-collected carnivores and thyroxine-treated and conspecific-fed tadpoles show that these phenotypes are profoundly different.

Reassessment of the environmental model of developmental polyphenism in spadefoot toad tadpoles

“…The species' developmental physiology differences in the current study parallel those found in other studies (Storz 2004), which suggests that S. multiplicata and S. bombifrons have fundamentally different developmental physiology. Storz (2004) found that S. bombifrons could, in fact, survive to metamorphosis on a diet solely of conspecifics, while S. multiplicata could not. The more S. bombifrons is studied, the more this species appears an exception to general patterns of amphibian development.…”

“…This model for the spadefoot cue has permeated the literature, from numerous review articles (Roff 1996;Smith and Skulason 1996;Kupferberg 1997;Ketterson and Nolan 1999;Gilbert 2001;Heyland and Moroz 2005;Rose 2005;Sultan 2007) to reference texts (McDiarmid and Altig 1999;Pigliucci 2001;Hall et al 2003) to undergraduate textbooks commonly used in colleges and universities (Hall 1998;Gilbert 2006;Cain et al 2008). However, it is clear that the proximate mechanism of this model, the thyroid stimulation aspect, is not correct (Storz 2004), and recent work has shown that carnivore development involves other factors not associated with feeding, including social interactions with other tadpoles and tadpole size (Pfennig and Frankino 1997;Frankino and Pfennig 2001;current study). Additionally, although fairy shrimp density is positively associated with incidence of the carnivore phenotype, fairy shrimp density is also positively associated with pond temperature and pond-drying rate; hotter rapidly drying ponds show higher densities of fairy shrimp (Pfennig 1990), neither of which have been tested in spadefoot toads.…”

Maternal Investment Influences Expression of Resource Polymorphism in Amphibians: Implications for the Evolution of Novel Resource-Use Phenotypes

“…2) and may be able to consume them faster and earlier in development than smaller tadpoles. Larger tadpoles may thereby acquire more of the cue – shrimp ingestion – that induces the carnivore morph [24], [29], [32]. In natural ponds, larger tadpoles may be especially likely to develop into carnivores by outcompeting smaller tadpoles for shrimp [36], which is a limiting resource [40].…”

“…Tadpoles are born as omnivores, but they may develop into carnivores if they ingest anostracan fairy shrimp early in life [24], [29], [32]. However, there is considerable variation in carnivore production, and some sibships are more prone than others to produce carnivores, even when tadpoles are reared under common conditions [33], [34].…”

An inducible offense: carnivore morph tadpoles induced by tadpole carnivory

“…Although numerous extrinsic and intrinsic factors contribute to the production of this morph (Pomeroy 1981; Pfennig 1992; Pfennig and Murphy 2000; Storz 2004; Pfennig and Martin 2009; Storz et al. 2011), theory predicts the most reliable trigger should be correlated with morph functionality.…”