Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape inTriturusnewts

Abstract

In vertebrates with complex, biphasic, life cycles, larvae have a distinct morphology and ecological preferences compared to metamorphosed juveniles and adults. In amphibians, abrupt and rapid metamorphic changes transform aquatic larvae to terrestrial juveniles. The main aim of this study is to test whether, relative to larval stages, metamorphosis (1) resets the pattern of variation between ontogenetic stages and species, (2) constrains intraspecific morphological variability, and (3) similar to the “hour‐glass” model reduces morphological disparity. We explore postembryonic ontogenetic trajectories of head shape (from hatching to completed metamorphosis) of two well‐defined, morphologically distinct Triturus newts species and their F1 hybrids. Variation in head shape is quantified and compared on two levels: dynamic (across ontogenetic stages) and static (at a particular stage). Our results show that the ontogenetic trajectories diverge early during development and continue to diverge throughout larval stages and metamorphosis. The high within‐group variance and the largest disparity level (between‐group variance) characterize the metamorphosed stage. Hence, our results indicate that metamorphosis does not canalize head shape variation generated during larval development and that metamorphosed phenotype is not more constrained relative to larval ones. Therefore, metamorphosis cannot be regarded as a developmental constraint, at least not for salamander head shape.

Metamorphosis shapes cranial diversity and rate of evolution in salamanders

“…However if stages are not autonomous, structures that are required for different functions at different ontogenetic stages could be constrained in terms of their morphological evolution 25 . Thus, metamorphosis may either increase developmental canalization, leading to reduced morphological diversity in metamorphic forms, or it could reset the pattern of variation between larval and adult stages and allow greater morphological diversity across species 26 .…”

“…Ledbetter and Bonett 33 showed that limbs evolve faster and are less constrained for aquatic species (mostly paedomorphic) than terrestrial species (mostly direct-developing). Vučić, et al 26 demonstrated that metamorphosis cannot be regarded as a developmental constraint on the overall external head in a newt. Finally, Blankers, et al 34 hypothesized that developmental constraints on phenotype may limit morphological evolution to different microhabitats in plethodontids based on analysis of body and appendage lengths.…”

“…Consequently, assessing every cranial element is critical for uncovering the complexity of salamander cranial evolution. We test the prediction that adult phenotypes in biphasic and direct-developing species have a lower disparity and evolutionary rate than paedomorphic species, as developmental canalization has been hypothesized to constrain developmental processes during metamorphosis 26 . In addition, we investigate whether complexity of life cycle or extent of metamorphosis influence evolutionary modularity.…”

Effects of thiourea on the skull of Triturus newts during ontogeny

“…In natural unimodal hybrid populations, hybrids cannot be distinguished based on external morphology from parental species ( Arntzen et al, 2018 ). Additionally, it has been shown in the laboratory that values of tail shape, size and colouration patterns ( Vučić et al, 2018 ), as well as general head shape during larval development and after metamorphosis ( Vučić et al, 2019 ), are intermediate between hybrids and the parental species during ontogeny ( Vučić et al, 2019 ). Taking into account the aforementioned, we decided to use hybrid larvae (obtained from experimental crosses) to explore possible differences in cranial morphology due to different TH levels during larval development, since we were not interested in interspecific divergence at this point.…”

Reproductive characteristics of two Triturus species (Amphibia: Caudata)

“…These two species have slightly different habitat preferences [22] and belong to different ecomorphotypes [23]. They show morphological differences at hatching, throughout larval development and after metamorphosis [24][25][26]. The larvae of the two species also differ in antioxidative response [27].…”