Evolutionary ecology of facultative paedomorphosis in newts and salamanders

Abstract

Facultative paedomorphosis is an environmentally induced polymorphism that results in the coexistence of mature, gilled, and fully aquatic paedomorphic adults and transformed, terrestrial, metamorphic adults in the same population. This polymorphism has been of interest to scientists for decades because it occurs in a large number of caudate amphibian taxa as well as in a large diversity of habitats. Numerous experimental and observational studies have been conducted to explain the proximate and ultimate factors affecting these heterochronic variants in natural populations. The production of each alternative phenotype is based on a genotyperenvironment interaction and research suggests that differences in the environment can produce paedomorphs through several ontogenetic pathways. No single advantage accounts for the maintenance of this polymorphism. Rather, the interplay of different costs and benefits explains the success of the polyphenism across variable environments. Facultative paedomorphosis allows individuals to cope with habitat variation, to take advantage of environmental heterogeneity in the presence of open niches, and to increase their fitness. This process is expected to constitute a first step towards speciation events, and is also an example of biodiversity at the intraspecific level. The facultative paedomorphosis system is thus ripe for future studies encompassing ecology, evolution, behaviour, endocrinology, physiology, and conservation biology. Few other systems have been broad enough to provide varied research opportunities on topics as diverse as phenotypic plasticity, speciation, mating behaviour, and hormonal regulation of morphology. Further research on facultative paedomorphosis will provide needed insight into these and other important questions facing biologists.

Larval growth in polyphenic salamanders: making the best of a bad lot

“…Polyphenisms provide model systems for the study of phenotypic variation because: (1) the trait of interest has a direct environmental component; (2) alternative phenotypes are often distinct and easily distinguished; and (3) they are likely to be a direct result of selection (Caswell 1983;Smith-Gill 1983). Documenting the ecological and evolutionary contexts that produce and maintain polyphenisms is critical for understanding their role in speciation, life history evolution, the maintenance of biodiversity, and the evolution of plasticity (West-Eberhard 1986, 2003Hazel et al 1990;Via 2001;Denoël et al 2005;Emlen et al 2007;Pfennig et al 2007Tomkins and Hazel 2007;Pfennig and McGee 2010).…”

“…1;Whiteman 1994;Denoël et al 2005). The expression of each morph is considered to be a response to the individual's expected success in the aquatic versus terrestrial environment (Wilbur and Collins 1973).…”

“…The expression of each morph is considered to be a response to the individual's expected success in the aquatic versus terrestrial environment (Wilbur and Collins 1973). Facultative paedomorphosis is characterized as an environmental threshold trait, i.e., there is genetic variation with an environmental trigger (Harris 1987;Harris et al 1990;Roff 1996), and there is considerable support for the hypothesis that the origin and maintenance of facultative paedomorphosis is a result of selection (reviewed in Whiteman 1994;Denoël et al 2005).…”

“…The paedomorph advantage hypothesis predicts that paedomorphosis will be negatively related to population size structure, as estimated by size variation; as size variation increases, a greater proportion of larvae should metamorphose to escape competition with larger individuals. Numerous field and experimental studies support the idea that the development of paedomorphs is an adaptive response to good growth/survival conditions in the aquatic environment (Whiteman 1994;Denoël et al 2005). Alternatively, the "best of a bad lot" mechanism asserts that paedomorphosis arises as a default strategy when the growing conditions are so poor that larvae cannot reach the minimum critical size for metamorphosis (Wilbur and Collins 1973;Wilbur 1980).…”

“…Best of a bad lot paedomorphosis is predicted to be positively density-dependent, with the frequency of paedomorphosis increasing as salamander density increases, and positively related to population size structure, as more larvae are forced into paedomorphosis because of competition with larger individuals. Fewer empirical data are consistent with this mechanism as compared to the paedomorphic advantage (Whiteman 1994;Denoël et al 2005Denoël et al , 2007Doyle and Whiteman 2008).…”