Size, microhabitat, and loss of larval feeding drive cranial diversification in frogs

Abstract

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.

Competition among small individuals hinders adaptive radiation despite ecological opportunity

“…There is also some evidence of a high rate of lineage accumulation after the re-evolution of metamorphosis in plethodontid salamanders [51]. Contrarily, the loss of an actively feeding larval stage in frogs is associated with higher evolutionary rates in traits associated with feeding specialization [52]. Further work could address the interaction between adaptive radiations and life cycle evolution.…”

Ontogenetic allometry underlies trophic diversity in sea turtles (Chelonioidea)

“…Both Nick (1912) and Pritchard and Trebbau (1984) found that the postcranial skeleton of D. coriacea also shows evidence of extensive paedomorphosis, suggesting that the paedomorphic skull may be part of a general skeletal pattern rather than the result of selection directly related to diet and the skull itself. Species develop paedomorphic morphologies in multiple evolutionary contexts, including retention of a juvenile life habit (Kordikova 2002), miniaturisation (Rieppel and Crumly 1997;Bright et al 2016;Esquerré et al 2017), diet (Denoël et al 2004;Esquerré et al 2017;Sherratt et al 2019), and other complex factors which may be unclear (Bright et al 2016;Morris et al 2019;Bardua et al 2021). Unfortunately, the selective pressures for D. coriacea to develop this phenotype are still unkonwn.…”

Complex macroevolutionary dynamics underly the evolution of the crocodyliform skull

“…Substantial variation in observed in every cranial element (figures 2 and 4 ) and the high disparity is distributed across the crocodyliform skull, particularly in the pterygoid, orbit and quadratojugal, in addition to the snout ( figure 4 ). This pattern is unusual among extant tetrapods, with the other extant archosaur lineage, birds, showing an overwhelming concentration of cranial variation in the anterior rostrum [ 26 , 28 ], while squamates and amphibians show concentrations of high disparity in the elements forming the suspensorium [ 27 , 33 , 40 ]. A more diffuse pattern of cranial disparity and evolutionary rates also characterizes non-avian dinosaurs [ 25 ], which may reflect a greater diversity of trophic niches and food acquisition strategies.…”

“…It may also result in antagonistic selection between more terrestrial and more aquatic specializations, limiting the ability to evolve in either direction. That requirement to maintain functionality in both niches may thus constrain and slow their evolution, as has been observed in other semi-aquatic vertebrates such as frogs [ 40 ].…”