Progenesis as an intrinsic factor of ecological opportunity in a polyphenic amphibian

Abstract

Paedomorphosis, a developmental heterochrony involving the retention of larval traits at the adult stage, is considered a major evolutionary process because it can generate phenotypic variation without requiring genetic modifications. Two main processes underlie paedomorphosis: neoteny, a slowdown of somatic development, and progenesis, a precocious maturation associated with body size reduction. Being essentially a truncation of ontogeny, progenesis has often been deemed an evolutionary dead end with advantages attributed to precocious reproduction or small body size required in specific environmental contexts (e.g. parasitism, interstitial life), but there is a lack of studies on the immediate ecological consequences of progenesis. Because body size is a key factor determining trophic ecology in animals, we hypothesized that progenesis might intrinsically promote ecological opportunity via body size reduction (i.e. ‘the trophic advantage of progenesis’ hypothesis). We tested this hypothesis in facultatively progenetic palmate newts Lissotriton helveticus using stable isotope niche modelling and diet reconstruction in conjunction with traditional stomach content analyses and body condition (BC) assessment. We show that not only did progenetic individuals occupy a different trophic niche than metamorphic individuals in all populations, but the smaller they were compared to metamorphs due to progenesis, the more different they were in terms of trophic ecology, with no negative effect on their BC. Altogether, the results suggest that via body size reduction, progenesis may generally act as an intrinsic factor of ecological opportunity, allowing the use of existing but previously unavailable resources, even in habitats where seemingly little opportunity exists. We argue that beyond the classically recognized fitness advantages of progenetic development, this process may also generally bring an immediate trophic advantage via body size reduction, which would have important implications to understand the evolution and adaptiveness of this process in many different taxa, from marine meiofauna to primates. A free Plain Language Summary can be found within the Supporting Information of this article.

Repeated ecological and life cycle transitions make salamanders an ideal model for evolution and development

“…8,141,142 Progenesis allows for reproduction before drying could occur, 36,126 permitting the colonization of under-used trophic niches. 143 The smaller the progenetic individuals, the more trophically distant they can be from the metamorphosed adults. This allows for use of alternate food resources while keeping similar energy inputs.…”

First record of the amphibamiform Micropholis stowi from the lower Fremouw Formation (Lower Triassic) of Antarctica

“…The determination of an individual's developmental trajectory is linked to abiotic (e.g., water quality) and biotic (e.g., population density) factors and the specific advantages between terrestrial and aquatic environments. This phenomenon often facilitates intraspecific niche differentiation between morphs (e.g., Lejeune et al, 2018Lejeune et al, , 2020. Developmental plasticity was not well-known or characterized in many temnospondyls prior to Schoch and Rubidge (2005) but has subsequently been explored in a number of taxa.…”

Can We Share? Feeding Strategy in Three Syntopic Newts in Artificial Habitats

“…Based on volumetric data, T. carnifex displayed the same feeding behavior as already observed with numerical data, whereas L. italicus behaved as predicted for an optimal forager by decreasing the niche width in isolation (reduced interspecific competition and intra-guild predation) and increasing it in syntopic conditions. The occurrence of potential interspecific competition can explain the observed differences in L. italicus volumetric niche width values in isolated vs. syntopic conditions [21,23]. Lissotriton italicus, by taking advantage of its small body size, may reduce competition with T. carnifex widening the niche width by using resources located in fissures and cracks of well walls not previously included in the diet [23,51].…”

“…The occurrence of potential interspecific competition can explain the observed differences in L. italicus volumetric niche width values in isolated vs. syntopic conditions [21,23]. Lissotriton italicus, by taking advantage of its small body size, may reduce competition with T. carnifex widening the niche width by using resources located in fissures and cracks of well walls not previously included in the diet [23,51]. This trophic behaviour may also help the species to avoid predation by T. carnifex which seems to feed on L. italicus in the study area [8].…”

“…Indeed, heterospecific individuals may narrow or widen species' niche reducing the available resources uniformly (expansion) or in a patchy manner (contraction) [20,21]. A reduction in food diversity may further decrease species' trophic niche width [22,23].…”