Evolution of hyperossification expands skull diversity in frogs

Abstract

Frogs (Anura) are one of the most diverse vertebrate orders, comprising more than 7,000 species with a worldwide distribution and extensive ecological diversity. In contrast to other tetrapods, frogs have a highly derived body plan and simplified skull. In many lineages of anurans, increased mineralization has led to hyperossified skulls, but the function of this trait and its relationship with other aspects of head morphology are largely unexplored. Using three-dimensional morphological data from 158 species representing all frog families, we assessed wide-scale patterns of shape variation across all major lineages, reconstructed the evolutionary history of cranial hyperossification across the anuran phylogeny, and tested for relationships between ecology, skull shape, and hyperossification. Although many frogs share a conserved skull shape, several extreme forms have repeatedly evolved that commonly are associated with hyperossification, which has evolved independently more than 25 times. Variation in cranial shape is not explained by phylogenetic relatedness but is correlated with shifts in body size and ecology. The species with highly divergent, hyperossified skulls often have a specialized diet or a unique predator defense mechanism. Thus, the evolution of hyperossification has repeatedly facilitated the expansion of the head into multiple new shapes and functions.Anura | cranium | dermal ornamentation | geometric morphometrics | microcomputed tomography I dentifying the factors that drive evolutionary changes in the heads of vertebrates has been a long-standing challenge because of the difficulties of sampling taxa broadly, quantifying complex morphologies, and identifying possible mechanisms responsible for generating macroevolutionary patterns. The diverse selective pressures proposed to drive extreme derivations in the skull include specializations in feeding biology (1), habitat use (2), and locomotion (3). Sexual selection also is thought to influence head morphology because the skull often is sexually dimorphic in size and shape (4, 5). The interactions among these selective pressures can result in functional trade-offs (6) that shape the head as an integrated system that must house the sensory organs, capture prey, provide protection, and partake in locomotion and reproduction (7). The nonadaptive mechanisms of architectural constraint (i.e., allometry; ref. 8) and phylogenetic conservatism (9) also have been invoked to explain morphological variation within and across lineages, particularly in cases in which extreme shifts are absent. The diversification of the skull usually results from changes in size or shape of preexisting elements or the loss of bones (10), but the origin of novel structures also may be responsible for shifts in morphology (11).Increased mineralization or hyperossification of the skull is a recurrent feature among vertebrates; it also is known as dermal ornamentation (12,13). In its most rudimentary form, additional membrane bone is deposited on the skeleton to form ridges and...

Evolution of the African slippery frogs (Anura: Conraua), including the world’s largest living frog

“…Conraua beccarii is highly unusual even among frogs in its extreme sexual dimorphism of the head (Scortecci, 1931), with the hypertrophied ‘grotesque’ head of males (Largen & Spawls, 2010) once thought to be a preservation artefact from accidental crushing (Lamotte & Perret, 1968). Recent analyses demonstrate male C. beccarii to have among the most divergent skull shapes in anurans (Paluh et al, 2020). The natural history of C. beccarii remains anecdotal and essentially unknown (Scortecci, 1931; Mertens, 1952), yet the extremely large heads of males suggest strong differences in the biology of males and females.…”

Rampant tooth loss across 200 million years of frog evolution

“…The complete loss of teeth in frogs is associated with the shortening of the lower jaw (Fig. 4), a skeletal trait that is known to occur in species that eat smaller prey (Emerson 1985, Vidal-Garcia and Keogh 2017, Paluh et al 2020). The shortening of the mandible reduces maximum gape and alters jaw biomechanics to improve the efficiency of catching many small prey items.…”

From Toad to Frog, a CT-based Reconsideration of Bufo servatus , an Eocene Anuran mummy from Quercy (France)

“…This clade is moderately supported by twelve synapomorphies on cranial and postcranial characters (see Appendix S6 in Supplement Data 1 for the detailed list). One of them, the presence of a contact between squamosals and nasals (11: 0->1) is interesting as it is considered a marker for hyperossification (Báez and Gómez, 2018;Paluh et al, 2020) and is recovered only in the Pyxicephalinae and the Ceratophryidae.…”