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 (covariation) of traits has long fascinated biologists because of its potential to elucidate factors that have shaped morphological evolution. Studies of tetrapod crania have identified patterns of evolutionary integration that reflect functional or developmental interactions among traits, but no studies to date have sampled widely across the species‐rich lissamphibian order Anura (frogs). Frogs exhibit a vast range of cranial morphologies, life history strategies, and ecologies. Here, using high‐density morphometrics we capture cranial morphology for 172 anuran species, sampling every extant family. We quantify the pattern of evolutionary modularity in the frog skull and compare patterns in taxa with different life history modes. Evolutionary changes across the anuran cranium are highly modular, with a well‐integrated “suspensorium” involved in feeding. This pattern is strikingly similar to that identified for caecilian and salamander crania, suggesting replication of patterns of evolutionary integration across Lissamphibia. Surprisingly, possession of a feeding larval stage has no notable influence on cranial integration across frogs. However, late‐ossifying bones exhibit higher integration than early‐ossifying bones. Finally, anuran cranial modules show diverse morphological disparities, supporting the hypothesis that modular variation allows mosaic evolution of the cranium, but we find no consistent relationship between degree of within‐module integration and disparity.
Phenotypic integration and modularity are concepts that represent the pattern of connectivity of morphological structures within an organism. Integration describes the coordinated variation of traits, and analyses of these relationships among traits often reveals the presence of modules, sets of traits that are highly integrated but relatively independent of other traits. Phenotypic integration and modularity have been studied at both the evolutionary and static level across a variety of clades, although most studies thus far are focused on amniotes, and especially mammals. Using a high-dimensional geometric morphometric approach, we investigated the pattern of cranial integration and modularity of the Italian fire salamander (Salamandra salamandra giglioli). We recovered a highly modular pattern, but this pattern did not support either entirely developmental or functional hypotheses of cranial organisation, possibly reflecting complex interactions amongst multiple influencing factors. We found that size had no significant effect on cranial shape, and that morphological variance of individual modules had no significant relationship with degree of within-module integration. The pattern of cranial integration in the fire salamander is similar to that previously recovered for caecilians, with highly integrated jaw suspensorium and occipital regions, suggesting possible conservation of patterns across lissamphibians.
Habitat is one of the most important factors shaping organismal morphology, but it may vary across life history stages. Ontogenetic shifts in ecology may introduce antagonistic selection that constrains adult phenotype, particularly with ecologically distinct developmental phases such as the free-living, feeding larval stage of many frogs (Lissamphibia: Anura). We test the relative influences of developmental and ecological factors on the diversification of adult skull morphology with a detailed analysis of 15 individual cranial regions across 173 anuran species, representing every extant family. Skull size, adult microhabitat, larval feeding, and ossification timing are all significant factors shaping aspects of cranial evolution in frogs, with late-ossifying elements showing the greatest disparity and fastest evolutionary rates. Size and microhabitat show the strongest effects on cranial shape, and we identify a “large size-wide skull” pattern of anuran, and possibly amphibian, evolutionary allometry. Fossorial and aquatic microhabitats occupy distinct regions of morphospace and display fast evolution and high disparity. Taxa with and without feeding larvae do not notably differ in cranial morphology. However, loss of an actively feeding larval stage is associated with higher evolutionary rates and disparity, suggesting that functional pressures experienced earlier in ontogeny significantly impact adult morphological evolution.
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