The 'male escape hypothesis': sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian

Abstract

Paedomorphosis is a major evolutionary process that bypasses metamorphosis and allows reproduction in larvae. In newts and salamanders, it can be facultative with paedomorphs retaining gills and metamorphs dispersing. The evolution of these developmental processes is thought to have been driven by the costs and benefits of inhabiting aquatic versus terrestrial habitats. In this context, we aimed at testing the hypothesis that climatic drivers affect phenotypic transition and the difference across sexes because sex-ratio is biased in natural populations. Through a replicated laboratory experiment, we showed that paedomorphic palmate newts (Lissotriton helveticus) metamorphosed at a higher frequency when water availability decreased and metamorphosed earlier when temperature increased in these conditions. All responses were sex-biased, and males were more prone to change phenotype than females. Our work shows how climatic variables can affect facultative paedomorphosis and support theoretical models predicting life on land instead of in water. Moreover, because males metamorphose and leave water more often and earlier than females, these results, for the first time, give an experimental explanation for the rarity of male paedomorphosis (the 'male escape hypothesis') and suggest the importance of sex in the evolution of paedomorphosis versus metamorphosis.

Keywords: climate; drying; facultative paedomorphosis; metamorphosis; newt; sex-ratio.

Figure 1.

Proportion (±s.e.) of paedomorphic palmate newts that metamorphosed in high and low water level tanks and at high and low temperatures (n = 20 paedomorphs, 10 of each sex per treatment). Dark grey boxes: males; light grey boxes: females, T: water temperature. See text for statistics.

Figure 2.

Timing of metamorphosis (survival curves) for paedomorphic palmate newts in both sexes and two temperature treatments (all at low water level). High temperature: thick red lines, low temperature: thin green lines, males: interrupted lines, females: continuous lines. See table 2 for statistical pairwise comparisons. (Online version in colour.)