Abstract

Paedomorphosis and metamorphosis are two major developmental processes that characterize the evolution of complex life cycles in many lineages. Whereas these processes were fixed in some taxa, they remained facultative in others, with alternative phenotypes expressed in the same populations. From a genetic perspective, it is still unknown whether such phenotypes form a single population or whether they show some patterns of isolation in syntopy. This has deep implications for understanding the evolution of the phenotypes, i.e. towards their persistence or their fixation and speciation. Newts and salamanders are excellent models to test this hypothesis because they exhibit both developmental processes in their populations: the aquatic paedomorphs retain gills, whereas the metamorphs are able to colonize land. Using microsatellite data of coexisting paedomorphic and metamorphic palmate newts (Lissotriton helveticus), we found that they formed a panmictic population, which evidences sexual compatibility between the two phenotypes. The high gene flow could be understood as an adaptation to unstable habitats in which phenotypic plasticity is favored over the fixation of developmental alternatives. This makes then possible the persistence of a polyphenism: only metamorphosis could be maintained in case of occasional drying whereas paedomorphosis could offer specific advantages in organisms remaining in water.

Highlights

  • Paedomorphosis and metamorphosis are two major developmental processes that characterize the evolution of complex life cycles in many lineages

  • Complex life cycles in amphibians have been highly altered during their evolution with species and even families becoming (1) obligate paedomorphs, (2) obligate metamorphs, and (3) facultative paedomorphs[16]

  • The analysis of microsatellite data from the two alternative newt phenotypes demonstrated a lack of genetic divergence between them. This is the first molecular study evidencing that coexisting paedomorphic and metamorphic newts can form a panmictic population. These results are in favor of the evolutionary scenario that predicts the persistence of facultative paedomorphosis as a polyphenism and support recent evidence found in other groups of metazoans that polymorphisms can be maintained in natural populations rather than being necessarily intermediate steps of speciation[9,31,32]

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Summary

Introduction

Paedomorphosis and metamorphosis are two major developmental processes that characterize the evolution of complex life cycles in many lineages Whereas these processes were fixed in some taxa, they remained facultative in others, with alternative phenotypes expressed in the same populations. The high gene flow could be understood as an adaptation to unstable habitats in which phenotypic plasticity is favored over the fixation of developmental alternatives This makes possible the persistence of a polyphenism: only metamorphosis could be maintained in case of occasional drying whereas paedomorphosis could offer specific advantages in organisms remaining in water. Complex life cycles in amphibians have been highly altered during their evolution with species and even families becoming (1) obligate paedomorphs (i.e., permanently aquatic larvae able of reproduction), (2) obligate metamorphs (i.e., either bi-phasic with metamorphosis or fully terrestrial, skipping the larval stage), and (3) facultative paedomorphs (i.e., with two phenotypes–the paedomorphs and the metamorphs–that can coexist in the same reproductive habitat; Fig. 1)[16]. Paedomorphs could avoid the cost of metamorphosis and gain in maturing early by progenesis, whereas metamorphs can survive catastrophes such as drying by dispersing to new habitats[28]

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