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

Abstract

Summary1. 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 antipredator 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.

Using kernels and ecological niche modeling to delineate conservation areas in an endangered patch‐breeding phenotype

“…Unfortunately, detection probability cannot be integrated into kernel analysis. Nevertheless, previous analyses showed that detection probability with the survey methods is very high in the study area, therefore, analyses not taking into account detection probability yield results that are nearly identical to analyses integrating detection probability (Denoe¨l and Ficetola 2014). In order to depict the effect of the two kernel approaches (without/with barrier) and of the KDE values (i.e., isopleths of different percentages, from 10% to 95%) on the surface of the utilization distribution, we used linear mixed models.…”

“…The absence of paedomorphic individuals in these habitats is caused by a variety of factors (Denoe¨l and Ficetola 2014). For instance, shallow ponds could dry up and thus host metamorphic individuals only.…”

“…As variables such as barriers and land cover could influence utilization distributions (Benhamou and Corne´lis 2010), we evaluated whether integrating these elements into KDE analyses can improve the outcome of analyses. To this end, we used populations of paedomorphic palmate newts (Lissotriton helveticus) in Larzac as a model system for four main reasons: (1) the study area is inhabited by a high rate of populations with paedomorphosis, allowing quantitative analyses (68% of the known cases of paedomorphosis in the palmate newt have been identified in this area, which comprises 0.5% only of the species distribution range); (2) paedomorphosis is not uniformly distributed across space; (3) all paedomorphs are limited to distinctly individualized patches, i.e., ponds; (4) paedomorphs are locally and globally declining because of environmental modifications, thus making it essential to delineate areas where conservation efforts are explicitly targeted towards them (Denoe¨l et al 2005, Denoe¨l 2007, Denoe¨l and Ficetola 2014.…”

The importance of phenotypic diversity in conservation: Resilience of palmate newt morphotypes after fish removal in Larzac ponds (France)

“…2 for a map of the area). They were classed in three categories (hereafter pond type): ten ponds (hereafter control ponds) have never been reported to have contained fish (Gabrion et al 1977;Denoël and Ficetola 2014); ten ponds (hereafter extirpation ponds) had fish that were extirpated by conservation management (i.e., removal, n = 4) or natural disappearance (n = 6) between 2000 and 2006; and ten ponds (hereafter fish ponds) had fish present during the 2014 survey (Supplementary Table 1). Previous visits to the fish ponds showed that they also contained fish in the period .…”

“…The presence of fish in extirpation ponds was also determined by our own previous field observations for eight ponds and by local reports for two ponds (Rondeau et al 2000) (Supplementary Table 1). All of the studied ponds were selected to have adequate features (except fish presence in fish ponds) to sustain newt populations and paedomorphs, following our previous results on the ecology of palmate newts in Larzac (Denoël and Lehmann 2006;Denoël and Ficetola 2014). This means that temporary and recently built ponds were not included in this study.…”