Selective advantages of a heterochronic phenotype. Eco-ethology of paedomorphic populations of the Alpine newt, Triturus alpestris (Amphibia, Caudata) | Avantages sélectifs d'un phénotype hétérochronique. Eco-éthologie des populations pédomorphiques du Triton alpestre, Triturus alpestris (Amphibia, Caudata)

Fonds pour la formation à la Recherche dans l'Industrie et dans l'Agriculture (Communauté française de Belgique) - FRIA

Facultative paedomorphosis is a polyphenism that has important evolutionary implications in promoting morphological differentiation and habitat use variation, and has occurred in several urodele species throughout the world. Several hypotheses based on life-history theory have been proposed to explain the wide range of habitats where facultative paedomorphosis occurs, suggesting multiple causes. In populations experiencing facultative paedomorphosis, some individuals metamorphose and mature (metamorphs), while others attain sexual maturity while still retaining traits of larval somatic morphology (paedomorphs). The paedomorphic process by which the development of somatic and reproductive organs is shifted between related individuals is assumed to significantly contribute to macro-evolutionary processes. Indeed, it implies large phenotypic variations in the absence of deep genetic changes. A way to explain the importance of these developmental heterochronies is to show their adaptive value in the micro-evolutive stage. The aim of this thesis is to determine the advantages gained by an individual that adopts a paedomorphic developmental pathway rather than a metamorphic one. To do this, we studied five factors: habitat use; resource partitioning; age and size structures; sexual compatibility; and the effect of environmental factors. The ecological and ethological characteristics of several mixed populations (composed of both paedomorphic and metamorphic individuals) of the Alpine newt Triturus alpestris (Amphibia, Salamandridae) were investigated from 1997 to 2000. These populations were located in France, Italy and Greece. The habitats occupied by dimorphic populations of the Alpine newt are highly variable. We have found the two morphs in syntopy in deep permanent lakes, and in small shallow and temporary ponds. Aquatic habitats were surrounded by various terrestrial habitats. As a result, it was not possible to correlate any particular environment type with the maintenance of the polymorphism in natural populations. The only common trait of the paedomorphic populations was that they were located at the southern margin of the range of the species (Italy, the Balkan peninsula, and southeastern France). Such a restriction of the distributional range of paedomorphosis suggests that this trait is maintained by genes which are shared only by these populations. Such a restriction may be due to Holocene colonizations from Pleistocene refugia, in which case paedomorphosis may have appeared in these refugia during the last glaciations. Nevertheless, as long as the phylogeny of the group remains uncertain, we cannot reject the possibility of an earlier origin of paedomorphosis. The two morphs primarily differed in space use and feeding habits. These differences were particularly marked in deep alpine aquatic habitats, where the paedomorphs occupy deep waters devoid of competitors, such as fish. In such waters, the paedomorphs were more abundant on the bottom and in the water column, whereas the metamorphs mainly occupied the water surface and shore. The paedomorphs primarily ingested plankton, while the metamorphs mainly foraged on terrestrial prey that had fallen on the water surface. Although these feeding habits depend on newt habitats - plankton being more abundant in the water column, and terrestrial prey at the water surface - the trophic spectrum in each habitat still differed. While the energetic values of the prey eaten by the two morphs strongly differed, by ingesting a large number of planktonic organisms, the paedomorphs attained similar or even larger caloric intake rates than metamorphs. The paedomorphs' superior body condition suggests that they may have higher long-term success than the metamorphs. Differences in body condition may also reflect the terrestrial life habit of the metamorphs, since metamorphosed individuals are able to avoid competition with reproductive adults and larvae by leaving the water. In the paedomorphic populations, several size-structured cohorts of larvae coexist, and competition among these cohorts is lowered by size-selective predation, since small larvae catch smaller prey than larger larvae and paedomorphs. Although this difference in diet was in part due to gape-size limitation, the gilled individuals also size-selected prey among a range of catchable items. Resource partitioning then favoured the coexistence of the two adult morphs, and their gilled descendants, which coexist with them. The two morphs also differed in feeding performance. Whereas the paedomorphs were better predators than metamorphs on water fleas, metamorphs were more adept at capturing large terrestrial invertebrates (flies). These differences in feeding performances were caused by the morphological particularities of the two morphs. Paedomorphs had a fish-like feeding structure with a unidirectional water flow passing through the oral cavity, and then being expelled through gill slits on the posterior side of the head. In contrast, metamorphs had a smaller oral cavity and a bidirectional water flow due to closed gill slits. Although the metamorphic structure produces less suction, it allows for catching bigger prey because of a larger gape-size (biting rather than sucking). Our measures of feeding performances confirmed the data from natural populations, with each of the morphs preferentially eating their predicted prey. The particular use of micro-habitats by the two morphs is also in agreement with optimality models predicting predation in the more profitable patches. In the Alpine newt, paedomorphosis can be produced by two main processes: neoteny and progenesis. In some populations, the two morphs reached sexual maturity at the same age (neoteny); in other populations, sexual maturity was reached earlier by paedomorphs (progenesis). Progenesis was observed in unstable water habitats. Pond drying suppressed the possibility of late maturation, which is characteristic of a neotenic developmental pathway. On the other hand, the precocious sexual maturation of paedomorphs favoured the fast colonization of new habitats, owing to a high intrinsic rate of natural increase. Neoteny was typical of permanent waters with harsh constraints on growth. By forgoing metamorphosis, larvae also avoid the cost of changing of structure (decrease in body weight in our experiments). Progenetic paedomorphosis appears then as a major trait that can be selected due to the advantages of earlier maturation. The two morphs are sexually compatible; thus, metamorphs can "exchange" genes with paedomorphs at each generation. While the two morphs markedly differ in their secondary sexual characteristics, females did not show any preference related to these characteristics. The absence of sexual isolation between the morphs shows that they are not involved in a sympatric speciation process. The maintenance of the polymorphism is more advantageous than the formation of two isolated species. Paedomorphosis occurs in aquatic habitats where total drying can occur, and where the maintenance of facultative paedomorphosis is maintained by metamorphs that have paedomorphic genes but do not (permanently) express them. In such habitats, the sexual isolation of the two morphs would lead to the extinction of paedomorphosis in the event of pond drying or similarcatastrophe. Because the environment can modify the ontogenetic pathway, paedomorphosis in the Alpine newt can be considered a polyphenism. Indeed, restricting the amount of water or food available induces paedomorphs to metamorphose. The marking of individual paedomorphs in a natural population proved that metamorphosis also occurs in the field. However, salamander density and progressive drying of aquaria did not have any apparent effect on paedomorph metamorphosis. When the possibility of a short migration across dry land was given, paedomorphs moved towards an available water basin and maintained their larval somatic characters during the migrations. By being able to migrate on land towards permanent water, paedomorphs are able to retain a feeding morphology that favors them in microhabitats where plankton is abundant.Facultative paedomorphosis in the Alpine newt allows populations to cope with environmental variability, and is adaptive in allowing precocious maturation or a larger use of resources in spatially heterogeneous environments. Thus, it is not surprising that paedomorphosis can evolve in such dissimilar environments as lowland temporary ponds and highland deep lakes. In such places, paedomorphosis appears to be the best solution as long as fish predation is relaxed. The introduction of fish throughout Europe is thus a serious problem, and has resulted in the extinction of several large paedomorphic populations. If this trend is not stopped rapidly, paedomorphosis in the Alpine newt - and in other species - will belong to the past.

Fonds de la Recherche Scientifique (Communauté française de Belgique) - F.R.S.-FNRS