Heterochrony in a complex world: disentangling environmental processes of facultative paedomorphosis in an amphibian

1. Heterochrony, the change in the rate or timing of development between ancestors and their descendants, plays a major role in evolution. When heterochrony produces polymorphisms, it offers the possibility to test hypotheses that could explain its success across environments. Amphibians are particularly suitable to exploring these questions because they express complex life cycles (i.e. metamorphosis) that have been disrupted by heterochronic processes (paedomorphosis: retention of larval traits in adults). The large phenotypic variation across populations suggests that more complex processes than expected are operating, but they remain to be investigated through multivariate analyses over a large range of natural populations across time.

2. In this study we compared the likelihood of multiple potential environmental determinants of heterochrony. We gathered data on the proportion of paedomorphic and metamorphic palmate newts (Lissotriton helveticus) across more than 150 populations during 10 years, and used an information-theoretic approach to compare the support of multiple potential processes.

3. Six environmental processes jointly explained the proportion of paedomorphs in populations: predation, water availability, dispersal limitation, aquatic breathing, terrestrial habitat suitability, and anti-predator refuges. Analyses of variation across space and time supported models based on the advantage of paedomorphosis in favourable aquatic habitats.

4. Paedomorphs were favoured in deep ponds, in conditions favourable to aquatic breathing (high oxygen content), with lack of fish, and surrounded by suitable terrestrial habitat. Metamorphs were favoured by banks allowing easy dispersal.

5. These results indicate that heterochrony relies on complex processes involving multiple ecological variables and exemplifies why heterochronic patterns occur in contrasted environments. On the other hand, the fast selection of alternative morphs shows that metamorphosis and paedomorphosis developmental modes could be easily disrupted in natural populations.