Mathieu Denoël

Evolutionary ecology of facultative paedomorphosis in newts and salamanders.

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 genotype × environment 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.

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata).

Current theories on the evolution of paedomorphosis suppose that several ontogenetic pathways have appeared according to different selective pressures. The aim of this study was to find out whether two distinct processes can lead to paedomorphosis in the Alpine newt, Triturus alpestris. In this respect, we compared age structures of paedomorphic and metamorphic individuals in two newt populations where the two forms lived syntopically. Whereas paedomorphosis resulted in a slower rate of somatic development in one population, it resulted in an acceleration of sexual maturation in the other population. These processes correspond to neoteny and progenesis, respectively. These results suggest that phenotypic plasticity can result from contrasted ontogenetic pathways between two populations of the same species. They give support to models that consider gonadic development as the target of selection under different environmental pressures.

LANDSCAPE-LEVEL THRESHOLDS AND NEWT CONSERVATION

Ecological thresholds are defined as points or zones at which a rapid change occurs from one ecological condition to another. The existence of thresholds in species-habitat relationships has important implications for management, but the lack of concordance across studies and the wide range of methods used make generalizations difficult. We used two different statistical methods to test for the existence of thresholds for both individual species and the whole community, using three newt species as models. Based on a sample of 371 ponds, we found significant thresholds for both landscape configuration and composition. These were for the relationships between distance to forest and occurrence of Triturus alpestris and T. helveticus, and forest and crop cover and T. helveticus. Variability in the location of thresholds observed for the different species in this study caution against their use at the community level. Future studies should be based on the identification and assessment of thresholds for targeted species. Thresholds can be a useful concept from which tools may be developed to focus conservation effort for threatened species and their habitats.

Consumptive and nonconsumptive effects of cannibalism in fluctuating age‐structured populations

Theory and empirical studies suggest that cannibalism in age-structured populations can regulate recruitment depending on the intensity of intraspecific competition between cannibals and victims and the nature of the cannibalism window, i.e., which size classes interact as cannibals and victims. Here we report on a series of experiments that quantify that window for age-structured populations of salamander larvae and paedomorphic adults. We determined body size limits on cannibalism in microcosms and then the consumptive and nonconsumptive (injuries, foraging and activity, diet, growth) effects on victims in mesocosms with seminatural levels of habitat complexity and alternative prey. We found that cannibalism by the largest size classes (paedomorphs and > or = age 3+ yr larvae) occurs mainly on young-of-the-year (YOY) victims. Surviving YOY and other small larvae had increased injuries, reduced activity levels, and reduced growth rates in the presence of cannibals. Data on YOY survival in an experiment in which we manipulated the density of paedomorphs combined with historical data on the number of cannibals in natural populations indicate that dominant cohorts of paedomorphs can cause observed recruitment failures. Dietary data indicate that ontogenetic shifts in diet should preclude strong intraspecific competition between YOY and cannibals in this species. Thus our results are consistent with previous empirical and theoretical work that suggests that recruitment regulation by cannibalism is most likely when YOY are vulnerable to cannibalism but have low dietary overlap with cannibals. Understanding the role of cannibalism in regulating recruitment in salamander populations is timely, given the widespread occurrences of amphibian decline. Previous studies have focused on extrinsic (including anthropogenic) factors that affect amphibian population dynamics, whereas the data presented here combined with long-term field observations suggest the potential for intrinsically driven population cycles.

Effects of a sublethal pesticide exposure on locomotor behavior: A video-tracking analysis in larval amphibians

Organochlorine pesticides such as endosulfan have been shown to have both lethal and sublethal effects on amphibians. In this context, behavioral endpoints have proved their usefulness in evidencing impacts of such chemicals at environmental concentrations that do not necessarily cause mortality. The recent development of video-tracking technologies now offers the possibility of accurately quantifying locomotor behaviors. However, these techniques have not yet been applied to evaluating the toxicity of pesticides in amphibians. We therefore aimed at determining the potential toxicity of endosulfan on endpoints associated with locomotion after short-term environmental endosulfan exposure in Rana temporaria tadpoles and at using these data as warning systems for survival alterations after a longer exposure. To this end, we analyzed video-tracks of 64 tadpoles (two pesticide treatments: 5 and 50 μg L(-1), one control and one solvent-control) with Ethovision XT 7 software. The highest endosulfan concentration had a significant effect on all four behavioral endpoints. Contaminated tadpoles traveled shorter distances, swam less often, at a lower mean speed, and occupied a less peripherical position than control tadpoles. The lowest endosulfan concentration had similar but lower effects, and did not affect mean speed during swimming. Survival was reduced only after a long-term exposure to endosulfan and was associated with short-term behavioral dysfunctions. These results show that endosulfan strongly affects the behavioral repertory of amphibian tadpoles, but in different ways depending on concentration, thus suggesting that the pesticide has complex modes of action. Given the importance of locomotion and space use in tadpole success in their aquatic environment, these results confirm the toxic action of endosulfan. By highlighting effects before mortality markers, video-tracking systems also show their potential as sentinels of sublethal effects of pesticides.

Sexual compatibility between two heterochronic morphs in the Alpine newt, Triturus alpestris

Paedomorphosis, in which individuals retain ancestral characteristics in the adult stage, is widespread in newts and salamanders and is suspected to play an important role in evolution. In some species, paedomorphosis is facultative with some individuals forgoing metamorphosis. Optimality models have been proposed to explain the maintenance of this polymorphism, but require the integration of reproductive patterns into the models. We investigated the frequencies of inbreeding and outbreeding in two syntopic heterochronic morphs of the Alpine newt. The two morphs are sexually compatible: encounters between and within morphs were equally successful in terms of spermatophore transfer. Behavioural observations were in agreement with the sexual compatibility observed. Nevertheless, paedomorphic males displayed to females less frequently than metamorphic males. The two morphs differ largely on the basis of sexual secondary characteristics, but the majority of these traits did not affect mating success. Because of the large flow of genes between the two heterochronic morphs and because of the absence of spatial and temporal isolation, these results do not support sympatric speciation models, but are in favour of the maintenance of polymorphism in natural populations.

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

Polyphenisms are excellent models for studying phenotypic variation, yet few studies have focused on natural populations. Facultative paedomorphosis is a polyphenism in which salamanders either metamorphose or retain their larval morphology and eventually become paedomorphic. Paedomorphosis can result from selection for capitalizing on favorable aquatic habitats (paedomorph advantage), but could also be a default strategy under poor aquatic conditions (best of a bad lot). We tested these alternatives by quantifying how the developmental environment influences the ontogeny of wild Arizona tiger salamanders (Ambystoma tigrinum nebulosum). Most paedomorphs in our study population arose from slow-growing larvae that developed under high density and size-structured conditions (best of a bad lot), although a few faster-growing larvae also became paedomorphic (paedomorph advantage). Males were more likely to become paedomorphs than females and did so under a greater range of body sizes than females, signifying a critical role for gender in this polyphenism. Our results emphasize that the same phenotype can be adaptive under different environmental and genetic contexts and that studies of phenotypic variation should consider multiple mechanisms of morph production.

Trophic specialisations in alternative heterochronic morphs

Polymorphisms are suspected of reducing competition among conspecifics in heterogeneous environments by allowing differential resource use. However the adaptive significance of alternative morphs has been poorly documented. The aim of this study is to determine food partitioning of two heterochronic morphs of the Alpine newt, Triturus alpestris, in mountain lakes. The morphs differ in the functional morphology of their feeding apparatus. Only paedomorphs are able to expel water during prey suction behind the mouth through gill slits. We observed a substantial trophic differentiation between morphs in all lakes. Paedomorphs preyed mainly on plankton, whereas metamorphs foraged on terrestrial invertebrates that fell upon the water surface. This resource partitioning may facilitate the coexistence of the alternative morphs in lakes devoid of vertebrate competitors. Food diversity may thus favour the evolutionary maintenance of facultative polymorphism in natural populations.

Resource partitioning in two heterochronic populations of Greek Alpine newts, Triturus alpestris veluchiensis

Current ecological models suggest that the maintenance of trophic polymorphisms is favoured by a different resource use in alternative morphs. Facultative paedomorphosis in newts is an example of phenotypic variation as paedomorphs retain morphological larval traits, such as gills and gill slits. The aim of this study was to find out whether heterochronic morphs occupy particular micro-habitats and focus on specific prey items. Resource partitioning was found between morphs. It concerns mainly food selection with paedomorphs preying more on plankton and less on terrestrial invertebrates than metamorphs. Some habitat specializations were also found with metamorphs being more abundant at the water surface than paedomorphs. Diel variation in habitat use of the two different morphs was minimal. Polymorphism allows Alpine newts to exploit the different resources in the lakes in order to minimize intraspecific competition, but the extent of resource partitioning depends on habitat characteristics.

Similar local and landscape processes affect both a common and a rare newt species

Although rare species are often the focus of conservation measures, more common species may experience similar decline and suffer from the same threatening processes. We tested this hypothesis by examining, through an information-theoretic approach, the importance of ecological processes at multiple scales in the great crested newt Triturus cristatus, regionally endangered and protected in Europe, and the more common smooth newt, Lissotriton vulgaris. Both species were similarly affected by the same processes, i.e. suitability of aquatic and terrestrial components of their habitat at different scales, connectivity among breeding sites, and the presence of introduced fish. T. cristatus depended more on water depth and aquatic vegetation than L. vulgaris. The results show that environmental pressures threaten both common and rare species, and therefore the more widespread species should not be neglected in conservation programs. Because environmental trends are leading to a deterioration of aquatic and terrestrial habitat features required by newt populations, populations of the common species may follow the fate of the rarest species. This could have substantial conservation implications because of the numerical importance of common species in ecosystems and because commonness could be a transient state moving towards rarity. On the other hand, in agreement with the umbrella species concept, targeting conservation efforts on the most demanding species would also protect part of the populations of the most common species.