Metamorphosis shapes cranial diversity and rate of evolution in salamanders

Abstract

Metamorphosis is widespread across the animal kingdom and induces fundamental changes in the morphology, habitat, and resources used by an organism during its lifetime. Metamorphic species are likely to experience more dynamic selective pressures through ontogeny compared to those with single-phase life cycles, which may drive divergent evolutionary dynamics. Here, we reconstruct the cranial evolution of the salamander using geometric morphometric data from 148 species spanning their full phylogenetic, developmental, and ecological diversity. We demonstrate that life cycle influences cranial shape diversity and rate of evolution. Shifts in rate of cranial evolution are consistently associated with transitions from biphasic to either direct-developing or paedomorphic life cycle strategies. Direct-developers exhibit the slowest rates of evolution and lowest disparity, and paedomorphic species the highest. Species undergoing complete metamorphosis (biphasic and direct-developing) exhibit greater cranial modularity (evolutionary independence among regions) than do paedomorphic species, which undergo differential metamorphosis. Biphasic and direct-developing species also display elevated disparity relative to evolutionary rate for bones associated with feeding, whereas this is not the case for paedomorphic species. Metamorphosis has profoundly influenced salamander cranial evolution, requiring greater autonomy of cranial elements and facilitating the rapid evolution of regions that are remodelled through ontogeny. Rather than compounding functional constraints on variation, metamorphosis appears to have promoted salamander morphological evolution over 180 million years, which may explain the ubiquity of this complex life cycle strategy across disparate organisms. MainDevelopmental processes play a fundamental role in structuring the morphological diversity of organisms 1-3 , being both a driver of, and a constraint on, phenotypic change 1,4,5 . As such, shifts in development and life history can have profound impacts on the evolutionary trajectories of lineages. Early attempts to delineate these effects resulted in the recapitulationist doctrine, stating that ontogeny replicates phylogeny 6 . However, studies of groups such as amphibians have shown that shifts in developmental strategies (e.g., biphasic, direct-development, paedomorphy, and viviparity) have occurred many times. In some cases, metamorphic species can even eliminate later ontogenetic stages and mature with larval

Evolutionary integration of the frog cranium

“…2020; Fabre et al. 2020), suggesting that the genetic, developmental, and functional interactions of traits that shape phenotypic integration are replicated in patterns of trait evolution. As discussed above, many studies have suggested that evolutionary modularity promotes diversification of form.…”

“…2019b; Fabre et al. 2020). As such, we used the estimated within‐ and between‐module correlations ( ρ ) for the best‐supported model and grouped highly integrated regions into larger modules as previously described (Felice and Goswami 2018; Marshall et al.…”

“…Frogs with a free‐living, feeding larval stage may therefore experience fewer developmental or genetic constraints, which may lead to a decrease in strength of phenotypic integration and a greater partitioning of traits into modules, or to greater variation in patterns of phenotypic integration across taxa, both of which would be reflected in greater evolutionary modularity. Some support for this hypothesis is offered by recent analysis of evolutionary modularity in salamanders, with species undergoing complete metamorphosis exhibiting elevated cranial modularity compared with pedomorphic taxa (Fabre et al., 2020). Life history may therefore have a significant and persistent influence on the strength and pattern of cranial integration, and this effect is expected to be particularly strong in lineages with disparate free‐living developmental stages, such as frogs.…”

“…2020; Fabre et al. 2020) crania, in analyses exploring much wider ranges of models. However, the most diverse lissamphibians, frogs, have not yet been incorporated into these studies.…”

Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts

“…Most salamanders switch from a 'free-feeding' larval-to a post-metamorphic stage during ontogeny via metamorphosis [1][2][3]. A recent study suggests that in species undergoing metamorphosis, parts of the skull associated with feeding develop faster and more independently from the rest [4]. This in turn suggests that the form and function of skeletal elements associated with feeding may be more exible.…”