Multiple evolutionary origins and losses of tooth complexity in squamates

Abstract

Teeth act as tools for acquiring and processing food, thus holding a prominent role in vertebrate evolution. In mammals, dental-dietary adaptations rely on tooth complexity variations controlled by cusp number and pattern. Complexity increase through cusp addition has dominated the diversification of mammals. However, studies of Mammalia alone cannot reveal patterns of tooth complexity conserved throughout vertebrate evolution. Here, we use morphometric and phylogenetic comparative methods across fossil and extant squamates to show they also repeatedly evolved increasingly complex teeth, but with more flexibility than mammals. Since the Late Jurassic, multiple-cusped teeth evolved over 20 times independently from a single-cusped common ancestor. Squamates frequently lost cusps and evolved varied multiple-cusped morphologies at heterogeneous rates. Tooth complexity evolved in correlation with changes in plant consumption, resulting in several major increases in speciation. Complex teeth played a critical role in vertebrate evolution outside Mammalia, with squamates exemplifying a more labile system of dental-dietary evolution.

Fig. 1. The diversity of squamate dental morphologies correlates with a gradient of plant consumption.

a Relative proportions (%) of tooth complexity levels in all known squamate suborders/super-families (left) and 76 families (right) based on cusp number data for 545 living and extinct species (including the most ancient known squamate Megachirella wachtleri), two rhynchocephalians, and the stem lepidosaurian Sophineta cracoviensis, with example teeth for each complexity level redrawn from microCT-scan data (not to scale). b Relative proportions (%) of tooth complexity levels in 545 squamates sorted by diet. c Discrete cosine transform analysis of multicuspid tooth labial view profiles from 75 extant and fossil squamate species, with 95% confidence ellipses for insectivorous, omnivorous, and herbivorous morphologies. Theoretical tooth profiles at the extreme positive and negative values of each axis reconstructed from the first 21 harmonic coefficients. Scalebar = 50 million years (My). Dagger = extinct taxon. Silhouettes: Phylopic (http://phylopic.org) courtesy of T. Michael Keesey (used without modification, CC0 1.0 and CC-BY 3.0 https://creativecommons.org/licenses/by/3.0/), David Orr (CC0 1.0), Iain Reid (used without modification, CC-BY 3.0 https://creativecommons.org/licenses/by/3.0/), Alex Slavenko (CC0 1.0), and Steven Traver (CC0 1.0), and F.L. after Darren Naish (used with permission) and Ted M. Townsend (silhouette drawn from photograph, CC-BY 2.5 https://creativecommons.org/licenses/by/2.5/deed.en); see Methods for full license information. Source data are provided as a Source Data file.

Fig. 2. Multiple independent acquisitions of multicuspid teeth and plant consumption are found across squamate phylogeny.

Known and maximum likelihood ancestral state reconstructions of the number of cusps (branch colours) and diet (node pie charts and branch tip small circles) in squamates. Pie charts indicate the most ancient nodes with >50% combined relative likelihood for omnivorous and herbivorous diets; also shown are the first nodes with >50% relative likelihood for herbivory within already omnivorous clades. Branch tip circles indicate omnivorous/herbivorous species. Six major clades show independent originations of multicuspid teeth: 1: Gerrhosauridae (node 616; see Supplementary Fig. 1). 2: Teiioidea + Polyglyphanodontia (informally Teiioidea sensu lato; node 686). 3: total group Lacertidae (informally Lacertidae sensu lato; node 740). 4: Chamaeleonidae (node 930). 5: non-Uromastycinae agamids (informally Agamidae sensu stricto; node 949). 6: total group Pleurodonta (node 971). Independent originations of plant consumption (isolated terminal branches not included): 1’: unnamed clade including the most recent common ancestor (MRCA) to Correlophus ciliatus and Rhacodactylus auriculatus and all its descendants (node 563). 2’: Cordyloidea (node 609). 3’: unnamed clade including the MRCA to Eumeces schneideri and Scincus scincus and all its descendants (node 652). 4’: Chalcides (node 657). 5’: Egerniinae (node 674). 6’: unnamed clade including the MRCA to Polyglyphanodon sternbergi and Teius teyou and all its descendants (node 688). 7’: Gallotia (node 750). 8’: Podarcis (node 765). 9’: crown Acrodonta (node 929). 10’: total group Pleurodonta (node 971). P: Permian. Tr: Triassic. J: Jurassic. K: Cretaceous. Pg: Paleogene. Ng: Neogene. Scalebar = 10 million years. Silhouettes: Phylopic (http://phylopic.org) courtesy of T. Michael Keesey (from a photograph by Frank Glaw, Jörn Köhler, Ted M. Townsend & Miguel Vences, used without modification, CC-BY 3.0 https://creativecommons.org/licenses/by/3.0/), Michael Scroggie (CC0 1.0), Alex Slavenko (CC0 1.0), and Jack Meyer Wood (CC0 1.0), and F.L. after Dick Culbert (silhouette drawn from photograph, CC-BY 2.0 https://creativecommons.org/licenses/by/2.0/deed.en), Scott Robert Ladd (silhouette drawn from photograph, CC-BY 3.0 https://creativecommons.org/licenses/by/3.0/), and Darren Naish (used with permission); see Methods for full license information.

Fig. 3. Dynamics of squamate tooth complexity and plant consumption evolution.

Squamate lineages sorted by cusp number (a, single-cusped: n = 651, two-cusped: n = 145, three-cusped: n = 238, more than three cusps: n = 33) and diet (c, carnivore: n = 246, insectivore: n = 556, omnivore: n = 203, herbivore: n = 62) per 10 million year-time bins based on maximum likelihood ancestral state reconstructions. Lineages showing increasing (n = 61) or decreasing (n = 31) tooth complexity (b) and increasing (n = 51) or decreasing (n = 64) plant consumption (d) per 10 million year-time bins. KTR: Cretaceous Terrestrial Revolution (~125–80 Ma). Q: Quaternary. Decreases in both cusp number and plant consumption proportion first outnumber increases during the Cretaceous Terrestrial Revolution (KTR), while the Cretaceous–Paleogene boundary (in red) shows the change towards the Cenozoic pattern of approximately twice as many cusp increases as decreases, and similar numbers of plant consumption increase and decrease from the Paleogene on. Source data are provided as a Source Data file.

Fig. 4. Dental-dietary rates of phenotypic evolution and squamate diversification patterns.

Log-transformed averaged rate scalars of the character transition rates of tooth complexity (a) and diet (b) across squamates. Positive values (i.e., rate scalar > 1) indicate increased relative transition rates. c Rates of squamate speciation for one maximum shift credibility configuration (MSC) out of ten similar independent replicates. Thirteen rate shifts (A–M) present in at least five MSC replicates are indicated proportionally to their magnitude compared to the background rate. d Mean rates of squamate speciation and extinction (in My⁻¹), and turnover (extinction/speciation) through time; see also Supplementary Fig. 10. Shaded areas: 95% confidence interval. 1: Gerrhosauridae (node 616; see Supplementary Fig. 1). 2: Teiioidea + Polyglyphanodontia (informally Teiioidea sensu lato, node 686). 3: total group Lacertidae (informally Lacertidae sensu lato, node 740). 4: Chamaeleonidae (node 930). 5: non-Uromastycinae agamids (informally Agamidae sensu stricto, node 949). 6: total group Pleurodonta (node 971). 1’: unnamed clade including the most recent common ancestor (MRCA) to Correlophus ciliatus and Rhacodactylus auriculatus and all its descendants (node 563). 2’: Cordyloidea (node 609). 3’: unnamed clade including the MRCA to Eumeces schneideri and Scincus scincus and all its descendants (node 652). 4’: Chalcides (node 657). 5’: Egerniinae (node 674). 6’: unnamed clade including the MRCA to Polyglyphanodon sternbergi and Teius teyou and all its descendants (node 688). 7’: Gallotia (node 750). 8’: Podarcis (node 765). 9’: crown Acrodonta (node 929). 10’: total group Pleurodonta (node 971). A: crown Squamata. B: Egerniinae. C: Polyglyphanodontia. D: Podarcis. E: Mosasauria. F: crown Alethinophidia. G: Chilabothrus. H: Varanus. I: total group Pleurodonta. J: crown Pleurodonta. K: Phrynosoma. L: unnamed clade including the most recent common ancestor (MRCA) of Liolaemus darwinii and L. scapularis and all its descendants. M: unnamed clade including the MRCA of Ctenosaura quinquecarinata and Cyclura cornuta and all its descendants. Direct correspondences between increased speciation and increased (green) or decreased (magenta) tooth complexity/plant consumption are indicated. P: Permian. Tr: Triassic. J: Jurassic. K: Cretaceous. Pg: Paleogene. Ng: Neogene. Q: Quaternary. KTR: Cretaceous Terrestrial Revolution (~125–80 Ma). K–Pg: Cretaceous–Paleogene extinction event (66 Ma). Scalebars = 50 million years.