Multiple evolutionary origins and losses of tooth complexity in squamates

Abstract

Teeth act as tools for acquiring and processing food and so hold a prominent role in 14 vertebrate evolution 1,2 . In mammals, dental-dietary adaptations rely on tooth shape and 15 complexity variations controlled by cusp number and pattern -the main features of the 16 tooth surface 3,4 . Complexity increase through cusp addition has dominated the 17 diversification of many mammal groups 3,5-9 . However, studies of Mammalia alone don't 18 allow identification of patterns of tooth complexity conserved throughout vertebrate 19 evolution. Here, we use morphometric and phylogenetic comparative methods across 20 fossil and extant squamates ("lizards" and snakes) to show they also repeatedly evolved 21 increasingly complex teeth, but with more flexibility than mammals. Since the Late 22Jurassic, six major squamate groups independently evolved multiple-cusped teeth from a 23 single-cusped common ancestor. Unlike mammals 10,11 , reversals to lower cusp numbers 24 were frequent in squamates, with varied multiple-cusped morphologies in several groups 25 resulting in heterogenous evolutionary rates. Squamate tooth complexity evolved in 26 correlation with dietary change -increased plant consumption typically followed tooth 27 complexity increases, and the major increases in speciation rate in squamate evolutionary 28 history are associated with such changes. The evolution of complex teeth played a critical 29 role in vertebrate evolution outside Mammalia, with squamates exemplifying a more 30 labile system of dental-dietary evolution. 31As organs directly interacting with the environment, teeth are central to the acquisition and 32 processing of food, determine the achievable dietary range of vertebrates 1 , and their shapes are 33 subject to intense natural selective pressures 8,12 . Simple conical to bladed teeth generally 34 identify faunivorous vertebrates, while higher dental complexity -typically a result of more 35 numerous cusps -enables the reduction of fibrous plant tissue and is crucial to the feeding 36 apparatus in many herbivores 4,8,13 . Evidence of such dental-dietary adaptations dates back to the 37 first herbivorous tetrapods in the Palaeozoic, about 300 million years ago (Ma) 13 . Plant tooth morphogenesis 23 . Epithelial signalling centres -the enamel knots -control tooth crown 56 morphogenesis 24 , including cusp number and position and ultimately tooth complexity, by 57 expressing genes of widely conserved signalling pathways 18,25 . Experimental data show most 58 changes in these pathways result in tooth complexity reduction, or complete loss of teeth 25 , yet 59 increasing tooth complexity largely dominates the evolutionary history of mammals [6][7][8][9]16 . To 60 determine whether similar patterns of tooth complexity underlie all tetrapod evolution or are 61 the specific results of mammalian dental development and history, we used morphometric and 62 phylogenetic comparative methods with squamate tooth and diet data. 63We analysed cusp number and diet data for 545 squamate species spanning all ...

Dental form and function in the early feeding diversification of dinosaurs

“…4A). These results are in line with studies showing that herbivorous, omnivorous, and insectivorous squamates have teeth that are similar in morphological complexity ( 23 , 24 ) and microwear patterns ( 33 ). As noted previously ( 23 ), these natural similarities hinder the discrimination of these dietary categories, especially separating omnivores from insectivores, among extinct taxa.…”

“…Tooth shape determines the ability of the feeding apparatus to break down different food items and thus obtain nutrients and energy ( 22 ), and this is subject to strong selective pressures. Consequently, the evolution of diverse dental morphologies in a clade can reflect the adaptation to a wide variety of diets and feeding strategies ( 23 , 24 ), although historical and developmental factors can impose constraints on this process ( 25 ). Modern quantitative techniques can characterize different functional aspects of the dentition, such as morphological diversity, complexity, and mechanics.…”

The developmental origins of heterodonty and acrodonty as revealed by reptile dentitions

“…Lepidosaurian reptiles, including Squamata (lizard and snakes) and Rhynchocephalia (tuatara and extinct relatives), are extremely diverse and represent ideal model systems to assess major aspects of tooth diversity found in nonmammalian lineages. In this group, species represent a multitude of ecologies and show a large array of dental phenotypes, ranging from simple conical to complex multicuspid teeth, directly reflecting dietary specialization ( 19 ). Some lepidosaurs also bear atypical heterodont dentitions, signifying that they bear teeth with different shapes or implantation modes in different parts of the skull and/or jaw, while others are homodont, having only one tooth type ( 15 , 18 , 20 , 21 ).…”

“…In contrast, EDAR localizes to the inner enamel epithelium (IEE), although its distribution is more widespread toward the cervical loops than in mouse. Since EDA is a key regulator of tooth shape evolution across vertebrates ( 3 , 4 ), this differential expression pattern could potentially contribute to some differences between mouse and lizard dental morphology ( 19 , 38 ). Additional EDA expression sites not previously described include the mesenchymal condensation and IEE at cap and bell stages, respectively.…”

A reappraisal of Jeddaherdan aleadonta (Squamata: Acrodonta), the purported oldest iguanian lizard from Africa

“…Jeddaherdan aleadonta, widely accepted as a mid-Cretaceous acrodontan since its original description (e.g. Ibrahim et al, 2020;Evans, 2022;Ijouiher, 2022), has been considered in various studies as a key taxon critical for understanding the origin and evolutionary history of iguanian lizards, with important implications for both palaeobiogeographic reconstructions (Simoes et al, 2017;Bittencourt et al, 2020;Rage and Gheerbrant, 2020) and node calibrations (Lafuma et al, 2021;Marjanović, 2021;Paparella, 2021;although Marjanović (2021) cautiously "preferred not to use Jeddaherdan to date the origin of Iguania as long as further material has not been discovered"). However, our study shows that the holotype and only known specimen of J. aleadonta is a dentary fragment of a recent (or subfossil) subadult of Uromastyx sp., which is a common lizard in the Kem Kem area today (represented by the species U. nigriventris; Wilms et al, 2009;Tamar et al, 2018).…”