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

Abstract

ResearchCite this article: Mathiron AGE, Lena J-P, Baouch S, Denoël M. 2017 The 'male escape hypothesis': sex-biased metamorphosis in response to climatic drivers in a facultatively paedomorphic amphibian. 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.

Dispersal and alternative breeding site fidelity strategies in an amphibian

“…They raise interesting questions about the evolutionary pathways that contribute to the diversification of movement strategies in the wild (Cote et al 2017b): is dispersal only a by-product of the evolution of migratory movement providing temporary escape from the environmental constraints of the aquatic habitat (e.g. predation and drying up: Winandy et al 2015, Mathiron et al 2017. And, alternatively, is there a coupling of the evolutionary forces shaping migration and dispersal, implying selective pressures that act jointly on morphological, physiological, and behavioral traits affecting the movement?…”

“…before/after the reproductive period from/to overwintering and estivating terrestrial sites), and facultative habitat supplementation, resulting in breeding dispersal among ponds during the reproductive period and not considered as migratory events (Semlitsch 2008, Pittman et al 2014. Natal dispersal usually involves habitat complementation as gilled organisms leave water after metamorphosis (Mathiron et al 2017) whereas breeding dispersal can include both habitat complementation and supplementation depending whether the terrestrial phase is only used for movement across breeding patches or used for other activities such as estivation or overwintering. To date, few studies have shown that breeding pond characteristics may affect dispersal decision among ponds and result in condition-dependent dispersal (see for instance Cayuela et al 2016a).…”

Traditionally managed landscapes do not prevent amphibian decline and the extinction of paedomorphosis

“…Finally, mixed models showed that climate change affected the metamorphic phenotype in the studied populations. Although drought events can affect populations of paedomorphs in other areas (Semlitsch and Gibbons 1985, Mathiron et al 2017, it is less likely the case in Montenegro because most ponds and lakes are very deep, making them permanent aquatic habitats. In contrast, high temperatures were associated with a decrease in the occurrence of the metamorphs, the terrestrially adapted phenotypes.…”

“…, Mathiron et al. ). Yet, a genetic basis of paedomorphosis was found in some species (Voss and Shaffer ) and constraining environments can promote metamorphosis over paedomorphosis across generations (Semlitsch and Wilbur ).…”

“…This is important in the adaptation and evolution of species (Gould 1977, Deno€ el et al 2005b, Bonett and Blair 2017. Whereas it is obligate in some species that lose the ability to metamorphose, it is a polyphenism in other species (facultative paedomorphosis) and, thus, involves the coexistence of both a paedomorphic and a metamorphic phenotype as a response to environmental drivers (Oromi et al 2016, Mathiron et al 2017). Yet, a genetic basis of paedomorphosis was found in some species (Voss and Shaffer 1997) and constraining environments can promote metamorphosis over paedomorphosis across generations (Semlitsch and Wilbur 1989).…”