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Biological Journal of the Linnean Society, 2019, 127, 245–259. With 7 figures.

The repeated evolution of dental apicobasal ridges in aquatic-feeding mammals and

MATTHEW R. MCCURRY1,2*, ALISTAIR R. EVANS3,4, ERICH M. G. FITZGERALD4, 5,6,7 8 9,10 COLIN R. MCHENRY , JOSEPH BEVITT and NICHOLAS D. PYENSON Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021

1Australian Museum Research Institute, Sydney, NSW 2010, Australia 2PANGEA Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia 3School of Biological Sciences, Monash University, Melbourne, VIC 3800, Australia 4Geosciences, Museums Victoria, Melbourne, VIC 3001, Australia 5School of Engineering, University of Newcastle, Newcastle, NSW 2308, Australia 6School of Environmental and Life Sciences, University of Newcastle, Newcastle, NSW 2308, Australia 7Department of and Developmental Biology, Monash University, Melbourne, VIC 3800, Australia 8Australian Centre for Neutron Scattering, Australian Nuclear Science and Technology Organisation, Sydney, NSW 2234, Australia 9Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA 10Mammalogy and , Burke Museum of Natural History and Culture, University of Washington, Seattle, WA 98195, USA

Received 17 November 2018; revised 12 February 2019; accepted for publication 13 February 2019

Since the , Earth’s aquatic ecosystems have been ecologically dominated by numerous lineages of predatory . Many of these groups evolved elevated ridges of enamel that run down the apical–basal axis of their teeth, referred to here as apicobasal ridges. This trait is commonly used as a taxonomic tool to identify fossil species and higher groupings, but the function of the ridges and their associated ecological significance are poorly understood. Here, we aim to clarify the phylogenetic distribution of apicobasal ridges among amniotes and to examine how the morphology of apicobasal ridges varies across species. We show that these ridges have evolved independently numerous times and are almost exclusively found in aquatic-feeding species. Ridge morphology varies, including tall, pronounced ridges, low, undulating ridges and interweaving ridges. Their internal structure also varies from tooth crowns with locally thickened enamel to undulating enamel–dentine interface. We assess the relative merits of different hypothetical functions of the ridges and propose that although apicobasal ridges might provide some strengthening of the tooth, their morphology and pattern of evolution do not indicate that this is their primary function. Instead, we suggest that apicobasal ridges serve to increase the efficiency of puncture, grip and/or removal.

ADDITIONAL KEYWORDS: aquatic – – feeding – function – morphology – palaeobiology – palaeontology – ridges – striations – teeth.

INTRODUCTION and mosasaurs in the era to and cetaceans, among others, in the Cenozoic era (Pyenson The upper trophic levels of aquatic predator guilds have et al., 2014). Repeated invasions of the aquatic been dominated by mammal and lineages in environment by independent lineages of mammals the past 250 Myr: from , sauropterygians and reptiles provide an important system to study adaptation to new and challenging environments. *Corresponding author. E-mail: [email protected] For example, the evolutionary convergence of similar

Published by Oxford University Press on behalf of The Biological Journal of the Linnean Society 2019, 2019, 127, 245–259 245 246 M. R. MCCURRY ET AL. stream-lined body forms and paddle-like limbs among that invaded the aquatic environment independently. many of these aquatic groups is a textbook All specimens were isolated teeth, which prevented example of selection generating hydrodynamic profiles exact tooth position from being recorded. If multiple in an aquatic environment (Kelley & Pyenson, 2015). tooth types (e.g. incisors and molars) were present Many other characteristics, including the structure of for mammals, both were included in the analysis. We the inner ear (Neenan et al., 2017) and bone density selected the teeth based on quality of preservation. (Wall, 1983), are also associated with living in the Teeth with excessively damaged surfaces that aquatic environment. Here, we examine another prevented complete measurement of more than one convergent feature of these groups that is widespread cross-section were excluded. Teeth with high levels of but poorly understood, namely the evolution of wear were also not incorporated into the analysis. Where apicobasal ridges on the teeth of aquatic amniotes. possible, we selected specimens to encompass a wide Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021 Apicobasal ridges are elevated ridges of enamel range of ridge and tooth morphotypes, e.g. pronounced that run down the apical–basal axis of the surface of ridges, fine ridges, robust tooth morphotypes, slender teeth. These structures have previously been variously tooth morphotypes and multicusped teeth. described as accessory dental ridges (Vaeth et al., 1985), cristae rugosae (Rothausen, 1968), enamel ridges (Ketchum & Benson, 2011), ornamentation Scanning and creation of three-dimensional (Foffa et al., 2018), longitudinal dental ridges (Ketchum models & Benson, 2011) or tooth striations (Massare, 1987). The specimens were digitized using high-resolution Apicobasal ridges differ from carinae or medial–lateral micro-computed tomography (microCT scans) or neutron dental ridges in that they occur in greater number and scanning using either Nikon Metrology’s combined over large areas of the teeth. Here, we will follow the 225/450 kV microfocus X-ray and computed tomography terminology of (Zverkov et al., 2018) and refer to these (CT) walk-in vault system at Chesapeake Testing in structures as apicobasal ridges, because this term is an Belcamp, MD, USA or the DINGO neutron beamline at accurate description and prevents confusion with wear Australia’s Nuclear Science and Technology Organisation striations, which are micron-scale features caused by (ANSTO) in Lucas Heights, NSW, Australia (Supporting attrition over the life of the tooth (Gordon, 1984). Information, Supplementary Section 1). Specimens Apicobasal ridges have been described in a wide were sourced from six museum collections: The Royal variety of extant and extinct vertebrate taxa (Tarlo, Ontario Museum, Toronto, Canada (ROM), the National 1960; Vaeth et al., 1985; Massare, 1987; Motani, 1996; Museum of Natural History, Smithsonian Institution, Fitzgerald, 2006; Albright et al., 2007; Hasegawa et al., Washington, DC, USA (USNM), Museums Victoria, 2010), but the ecological associations or functions of Melbourne, Victoria, Australia (NMV), the Australian the trait have not been anchored in their necessary Museum, Sydney, NSW, Australia (AM), phylogenetic context. It is often assumed that these Korner, Richmond, Queensland, Australia (KK) and the ridges function in strengthening the tooth, and thus Natural History Museum, London, UK (NHMUK). The that the taxa that possess them fed on hard prey teeth were digitally isolated (segmented) from the CT items (Vaeth et al., 1985; Young & Kardong, 1996) but scans using MIMICS (Materialize, 2015) and exported the function of the ridges has never been empirically as three-dimensional surface models in STL (standard established. Other hypotheses of possible functions triangular language) format. include increasing puncturing efficiency, increasing removal efficiency and improving grip (Vaeth et al., Morphometrics 1985; Zverkov et al., 2018). Here, we aim to describe apicobasal ridges operationally in aquatic mammals We collected cross-sections of the three-dimensional and reptiles to clarify the phylogenetic distribution models at one-quarter, one-half and three-quarters of of the trait, describe the variation of apicobasal ridge the distance from the base of the tooth crown to the cusp morphology among species and discuss different of the tooth in Rhino v.5 (McNeel, 2015). Crown height functional explanations of this trait. was measured as the longitudinal height between the tip of the tooth cusp and the base of the enamel crown (Fig. 1A). We measured the maximal number of ridges within any of the three cross-sections. If the MATERIAL AND METHODS cross-section containing the most ridges was missing sections of the enamel surface, we listed these taxa as Specimen selection not assessed for this measure. At each cross-section, we Thirty-four specimens (either original specimens measured the height of each ridge and the width of each or casts) were selected for use in the study. These ridge. We measured ridge width as the distance between represented > 20 species and approximately six groups the locally most central points on the undulating surface

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Figure 1. Measurement of ridge morphology in interruptus (USNM 16153). A, each tooth was sectioned orthogonal to the longitudinal axis of the tooth at one-quarter, one-half and three-quarters of tooth crown height. B, cross- section extracted at one-half crown height from one tooth. C, ridge width and ridge height were measured. D, the percentage of the surface containing enamel ridges was measured by drawing an angle between the outer two ridges and the centroid of the most apical cross-section of the tooth. of the cross-section. Ridge height was measured as the Pagel’s binary character correlation test in Phytools length of a perpendicular line between this line and (Revell, 2012) to test for an association between aquatic the most external point on the ridge (Fig. 1C). We then feeding and apicobasal ridges using a simplified amniote calculated the average ridge width and ridge height phylogeny that included both terrestrial and aquatic based on all ridges measured from the three cross- taxa. Details of this test are shown in the Supporting sections. By averaging results from three cross-sections, Information (Supplementary Section 2). we ensured that comparisons could be undertaken even when ridges were missing from some cross-sections. We measured the percentage of the surface containing RESULTS enamel ridges by drawing an angle between each of the the outer two ridges and the centroid of the most apical Phylogenetic distribution cross-section of the tooth and then converting this degree Apicobasal dental ridges have evolved independently in to a percentage by dividing by 360 and then multiplying a wide variety of taxa. Here, we show that these ridges by 100 (Fig. 1D). We measured enamel thickness in have evolved at many times across Amniota, including a cross-section at approximately halfway between within cetaceans, pinnipeds, and and the base of the tooth crown and the cusp of the tooth. in a wide variety of marine reptiles (Fig. 2 and additional Enamel thickness was measured at both the apex of a information on snakes within the text). a Pagel’s ridge and in between ridges to produce an average value test using a simplified amniote phylogeny revealed that for enamel thickness. Teeth were classed as recurved the evolution of apicobasal ridges is associated with if they had one side of the tooth (whether lingual or feeding within the aquatic environment (P = 0.0352). posterior) with a concave surface. We conducted reduced Within cetaceans, ridges are common in archaeocetes major axis (RMA) regressions between variables in [Zygorhiza kochii (Kellogg, 1936)], in early mysticetes PAST (Hammer et al., 2001). We conducted a principal [e.g. Janjucetus hunderi (Fitzgerald, 2006)] and in components analysis on the crown height, average ridge early odontocetes [e.g. on the incisors of Squalodon height and average ridge width using the ‘princomp’ calvertensis (Kellogg, 1923)]. In many of these species function in the stats package of R (R Core Team, 2013). the ridges are strongly anastomosed, with ridges Principal component (PC) plots were made using the interweaving into each other (Supporting Information, ‘autoplot’ function in ggplot2 (Wickham & Chang, 2008) Supplementary Section 1). Ridges are not present and ggfortify (Horikoshi & Tang, 2016). We also ran a in all extant cetacean species, with the exception

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Figure 2. Phylogenetic distribution and morphological similarity of apicobasal ridges. The phylogeny was adapted from Kelley & Pyenson (2015) and Müller et al. (2010). Each lineage represents both independent evolution of apicobasal dental ridges and independent transitions between feeding in the terrestrial environment and feeding in the aquatic environment. The groups represented contain species that possess apicobasal dental ridges but may also contain species without the trait. Example photographs or computed tomographic renders of apicobasal ridged teeth (top) and close-up of the tooth

Published by Oxford University Press on behalf of The Biological Journal of the Linnean Society 2019, 2019, 127, 245–259 APICOBASAL RIDGES IN AQUATIC AMNIOTES 249 of the rough-toothed dolphin (Steno bredanensis) In most taxa, the enamel–dentine junction that does possess interesting surface textures on undulates approximately parallel to the external the teeth, which have been referred to as ‘wrinkled’ surface of the enamel (Fig. 4B–D, F). One exception to or ‘ridge like’(Jefferson, 2018). The aquatic-feeding this observation is in the sauropterygians, where the snakes Acrochordus javanicus, buccata enamel–dentine junction does not fluctuate; instead, and leopardinus all possess extensive the ridges are formed by the localized thickening of ridging (Vaeth et al., 1985). Some pterosaurs also enamel (Fig. 4A). In Ichthyosauria, the thick enamel possess apicobasal dental ridges (e.g. Siroccopteryx layer forms a wavelike structure, but undulating and moroccoensis). We were unable to view extensive thick/thin in certain locations (Fig. 4E). collections of pterosaurs for this project, but it appears Regression analysis showed which characteristics of that the trait might be restricted to those species that the ridges were correlated with the size of the teeth Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021 feed in the aquatic environment. (crown height). The ridge height and ridge width Apicobasal ridges predominantly occur in taxa that were correlated with the size of the teeth (R2 = 0.382, feed within the aquatic environment, including those P = 0.0003 and R2 = 0.544, P = 0.0001, respectively) but that are fully aquatic (e.g. ichthyosaurs, plesiosaurs) the number of ridges was not correlated with tooth size and those that are terrestrial but access the aquatic (R2 = 0.1035, P = 0.1133) (Fig. 5; Table 1). Regressions environment to catch prey (Charig & Milner, 1986; between log10 tooth size and log10 ridge height and log10 Ibrahim et al., 2014). For example, the theropod ridge width indicate that ridge height is positively Baryonyx has been shown to feed on both terrestrial allometric against tooth size (slope coefficient = 1.376), species and fish and possesses apicobasal ridges but ridge width is negatively allometric against tooth on its teeth (Charig & Milner, 1986). In many of the size (slope coefficient = 0.874) (Table 1). cases reported here, the evolution of apicobasal dental We found no correlation between enamel thickness ridges has occurred in association with a transition and ridge height, width or number or ridges. We also from a terrestrial-feeding style to an aquatic-feeding found no correlation between tooth robusticity (crown niche (e.g. in sauropterygians, the trait evolves early height/crown width) and ridge height, width or number in their history, being present in ; Shang, of ridges. We did find a significant negative correlation 2007). Yet, in other cases, the taxa possessing ridged between enamel thickness and tooth robusticity (Fig. teeth are nested within groups that are missing ridges, 6; Table 1). e.g. leopard seals possess apicobasal ridges, but other In the principal component analyses, PC1 explained pinnipeds lack them despite their aquatic lifestyle. 79.82% of the variation in the data and was highly correlated with tooth size (Fig. 7; Tables 2 and 3). Morphological variation Principal component 2 explained 16.09% of the variation and mainly summarized variation in the height of the Apicobasal ridges vary in morphology throughout the ridges. Principal component 3 explained 4.1% of the phylogeny (Fig. 2). In some cases, the ridges are very total variation and summarized differences in the pronounced [e.g. in macropredatory pliosaurids, such relative width of the ridges. There was some clustering as Kronosaurus Longman, 1924]; in others they are between phylogenetic groups in the morphospace extremely fine [e.g. in Leidy, 1851]. In plot (Fig. 7; Tables 2 and 3), with sauopterygians and some specimens, the ridges are triangular in cross- cetaceans clustering as groups with thinner ridges. section (e.g. Kronosaurus), and in other cases they are rounded (e.g. Ichthyosaurus). The location of the ridges also varies among taxa. In some species, the ridges occur on only the recurved surface (e.g. in some DISCUSSION pliosaurs); in others, ridges are absent from the apex of the tooth [e.g. Deinosuchus Holland, 1909] (Fig. 3D). Phylogenetic distribution In recurved teeth, there is a tendency for ridges to Mapping the presence of apicobasal ridges onto the be present, or more numerous, only on the recurved amniote phylogeny indicates that apicobasal ridges surface of the tooth (Fig. 3B, C). have evolved independently many times and that all

surfaces (bottom). A, Deinosuchus rugosus (USNM 5351). B, Spinosaurus (ROM 64659). C, Ichthyosaurus (NMV P 202402). D, indet. (NMV P 30660). E, Globidens alabamensis (USNM540758). F, Hydrurga leptonyx (NMV C 31561). G, Mammalodontidae indet. (NMV P 221271). Apicobasal ridges are also present in aquatic-feeding snakes (Vaeth et al., 1985), Paralonectes merriami (Nicholls & Brinkman, 1993), Tanystrophus longobardicus (Nosotti, 2007) and pterosaurs (Kellner & Tomida, 2000), but photographs of these are not depicted. Silhouettes were sourced from phylopic (http://phylopic.org/; Müller et al., 2010; Kelley & Pyenson, 2015).

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Figure 3. Renders of three-dimensional models generated from computed tomography scans, showing variation in the location of ridges. A, Ichthyosauria indet. (USNM 412523), with ridges on all surfaces of the tooth. B, Kronosaurus queenslandicus (KKF 0534), with ridges occurring in higher density on the recurved surface of the tooth and extending to the tooth tip. C, the early mysticete Aetiocetus cotylalveus (USNM 25210), with ridges only on the recurved surface of the tooth. D, the crocodilian Deinosuchus rugosus (USNM 5351), with ridges missing from the apical surface of the tooth. species that possess the ridged teeth feed in the aquatic from histology, sedimentology and cranial morphology environment [Fig. 7; with the exception of ridges found (Cuff & Rayfield, 2013; Foffa et al., 2014; Ibrahim at the base of the tooth in some species, e.g. et al., 2014). Lachesis muta von Linné, 1767; Young & Kardong, 1996] Apicobasal ridges appear to be found in aquatic- and in some therapsids (Brink 1960). The evolution of feeding taxa and are uncommon (if not completely the ridges occurs in many lineages from the to absent) in terrestrial-feeding taxa. Although outside the present day. The fact that this trait has evolved so of the scope of this project, we also noted that several many times in aquatic-feeding mammals and reptiles species of fish, including Carcharias taurus and some indicates that it was selected for and imposes some extinct Tristichopterid fish, also possess apicobasal benefit to these predators in that environment. ridges (Cunningham, 2000; Clément et al., 2009). Why does this trait predominantly occur in aquatic- Interestingly, some secondarily aquatic amniotes feeding species? Ridges are absent from the teeth of lack this trait, including extant odontocetes, extant aquatic herbivorous taxa, such as sirenians, and from crocodilians and extant and extinct taxa, some secondarily aquatic predators, such as extant such as walruses (Odobenus rosmarus) and their dolphins, otters and many seals. Living species that relatives. There are at least some instances of similar possess apicobasal ridges (Acrochordus javanicus, features in terrestrial species; in particular, we note , Helicops leopardinus and that some terrestrial snakes normally possess ridges Hydrurga leptonyx) feed on very different prey items only at the base of the teeth (e.g. in Lachesis muta; from one another. Species that possess apicobasal ridges Young & Kardong, 1996), but it seems to be only an vary in diets from those consisting of invertebrates to extremely rare occurrence in terrestrial-feeding those consisting of fish and even diets consisting of species. The enantiornithine Sulcavis large prey, such as penguins and seals (Vaeth et al., geeorum possesses teeth with longitudinal grooves 1985; Hall-Aspland & Rogers, 2004). that might have a similar function to apicobasal The aquatic abilities of spinosauruids have received ridges, but unfortunately, we were unable to examine considerable attention (Charig & Milner, 1986; Holtz, this specimen to include in this analysis (O’Connor 1998; Amiot et al., 2010; Ibrahim et al., 2014; Arden et al., 2013). et al., 2018; Henderson, 2018). Recent analysis of buoyancy and balance suggest that Spinosaurus was not particularly well adapted for pursuit in Morphological variation the aquatic environment (Henderson, 2018). However, Although having arisen multiple times, the precise isotope evidence suggests that Spinosaurus was a morphology of apicobasal dental ridges varies between semiaquatic predator (Amiot et al., 2010). Our results lineages, from wide, blunt ridges to pronounced, support the idea that Spinosaurus engaged in some sharp ridges (Fig. 7). Previous studies have drawn degree of hunting aquatic prey, owing to the presence distinctions between different levels of striations, of apicobasal ridges. This finding agrees with evidence classifying them as primary, secondary or tertiary

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Figure 4. Cross-sections through the teeth of various aquatic mammals and reptiles, showing where the enamel–dentine junction undulates approximately parallel to the outer enamel surface (B–F) or the ridges are formed by localized thickening of enamel (A). A, Polyptycodon interruptus (USNM 16153). B, Globidens alabamensis (USNM 540758). C, Goniopholis crassidens (USNM 16115). D, Spinosaurus aegyptiacus (ROM 64659). E, Ichthyosaurus communis (ROM 01860). F, Zygorhiza kochii (USNM 11962). levels (Hornung & Reich, 2015). Overall tooth shape considerably (Fig. 7). It is still possible that multiple and skull shape have been found to be related to the functions are represented at each location within this diet of aquatic predators, with ecologically similar morphospace. species clustering together in morphospace (Massare, The ridges also vary in internal structure. In some 1987; Kelley & Motani, 2015; McCurry et al., 2017a, cases, the enamel is locally thickened to produce the b; Foffa et al., 2018). In contrast, the ridges do not pronounced ridges, similar to the enamel thickening cluster as separate morphotypes but instead overlap that produces crenulations in other (Zhao

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ridges, but here we treat them in a similar manner to true ridges of other taxonomic groups. Studies have shown that the internal morphology of the teeth varies among different species (Maxwell et al., 2012). The width, height and number of enamel ridges scales with the size of the tooth (Fig. 5). This could indicate that it is the relative size of the ridges that is selected for rather than their absolute size. However, the relative size of the ridges could be related to a developmental constraint. Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021

Function Four hypotheses have been proposed for the function of apicobasal ridges. First, ridges might act as cutting edges to decrease the amount of force required to puncture a prey item (Wright, et al., 1979; Vaeth et al., 1985; Foffa et al., 2018). It is possible that the ridges act as cutting blades to assist in puncture efficiency. This function would be comparable to that of armour-piercing arrowheads (Jones, 1992). Terrestrial taxa would also benefit from increased puncture efficiency in teeth; therefore, for this trait to evolve in so many aquatic species it would probably need to offer a specific advantage in puncturing aquatic prey, such as fish. Although many of the aquatic species with this characteristic do feed on fish, there are others, like the leopard seal, H. leptonyx, whose vertebrate prey are largely penguins and seals. The mechanical requirements for catching and processing penguins and seals are similar to those for the prey of many terrestrial predators (Hall-Aspland & Rogers, 2004; Hocking, et al., 2013). Vaeth et al. (1985) noted that many teeth lack the ridges at their apex, where they would presumably have the most benefit for increasing puncturing efficiency. Second, the ridges might allow the prey item to be Figure 5. Scaling relationships of tooth and ridge removed from the teeth more easily before ingestion variables. Tooth crown height vs. average ridge width (Vaeth et al., 1985). Prey items can become stuck on (N = 34; A), average ridge height (N = 34; B) and number of the teeth of predators. In the aquatic environment, ridges (N = 26; C). this represents a substantial problem because the forelimbs are often paddle like, being adapted for et al., 2006; Skinner et al., 2010), whereas in other locomotion rather than manipulation of prey. It is groups the enamel is a reasonably uniform thickness, possible that apicobasal dental ridges could prevent but the enamel–dentine junction undulates (Fig. vacuum suction being formed between the tooth and 4). These differences in internal morphology might the prey being bitten in much the same way that a indicate that at least two different developmental ‘Granton edged’ or ‘anti-stick’ knife does (Scobie, 2014). pathways might be responsible for the evolution of This function could play an important role in inertial morphologically similar ridges on the external surface feeding in aquatic ecosystems, where buoyancy (Zhao et al., 2006). prevents the predator from using gravity to assist with As has been noted previously in the literature, the swallowing prey. external morphology of the ichthyosaur teeth included Third, the ridges might have evolved to provide better in this analysis is produced by infolding of the dentine grasp of a prey item to prevent its escape (Vaeth et al., and enamel, termed plicidentine (Sander, 1999; 1985; Massare, 1987; Young et al., 2014b). Cephalopods Maxwell et al., 2012). In a strict sense these are not and fish represent a substantial component of prey

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Table 1. RMA regression analysis results x variable y variable Slope Intercept R2 P-value

Crown height Ridge width 0.016296 0.088044 0.54381 0.0001 Crown height Ridge height 0.0067153 −0.081761 0.38186 0.0003 Crown height Number of ridges −0.80783 57.425 0.10352 0.1133

Log10 crown height Log10 ridge width 0.87411 −1.5233 0.46425 0.0001

Log10 crown height Log10 ridge height 1.376 −2.973 0.28589 0.0012

Log10 crown height Log10 number of ridges −0.93347 2.7866 0.088943 0.1433

Enamel thickness Crown height 0.0077472 0.011669 0.030694 0.4879 Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021 Enamel thickness Ridge width 0.49764 −0.03368 0.0041014 0.7991 Enamel thickness Ridge height 1.732 0.050479 0.053879 0.3476 Enamel thickness Number of ridges −0.0084472 0.48463 0.11924 0.2659 Tooth robusticity Enamel thickness −0.25881 0.7646 0.22539 0.0465 Tooth robusticity Ridge width 0.63008 −0.57006 0.020236 0.4224 Tooth robusticity Ridge height 0.26279 −0.36055 0.0054123 0.6834 Tooth robusticity Number of ridges −34.004 94.77 -0.35392 0.0803

available within the aquatic environment. It is this raises the question of why taxa with apicobasal possible that these types of prey are harder to grasp dental ridges do not always have thicker enamel (Fig. than other prey items. Apicobasal dental ridges might 6). Apicobasal dental ridges have evolved on a wide represent a way to maximize grip on this slippery prey variety of different tooth morphologies, including by increasing the amount of surface area in contact extremely slender teeth, such as those of nothosaurs, with the prey item. This hypothetical function is in multicusped teeth, such as those of basilosaurids, direct opposition to helping the teeth to remove from and robust teeth, such as those of Globidens Gilmore, the prey item. 1912. Although it is clear that some species possessing We found that recurved teeth are more likely to have apicobasal ridges feed on hard prey items (for denser spacing of ridges on the recurved surface of the example, the teeth of have been found teeth, or for the ridges to occur only on these surfaces of imbedded in shells; Buffetaut, 1982), it is also the teeth. The recurved surfaces of the teeth come into clear that other species that possess apicobasal ridges contact with the prey during the puncturing phase, lack anatomical traits associated with . while on the opposite side of the tooth a dead space The occurrence of apicobasal ridges in such a wide forms, similar to the condition in recurved theropod range of tooth morphotypes, including those that are dinosaur teeth (D’Amore, 2009). This hints that the not normally associated with the application of high ridges might be of functional benefit only when they forces during feeding, does not support the idea that are in contact with the prey. However, it is also possible this trait evolved purely to strengthen the teeth. Here, that this could represent an adaptation to deal with a we also show that apicobasal ridges are not always specific type of stress, e.g. localized compressive stress associated with other durophagous traits, such as on the recurved surface during biting. tooth robusticity or thickened enamel. Fourth, the ridges might strengthen the tooth (Young & Kardong, 1996; Ciampaglio et al., 2005; Young et al., 2014a, b; Foffa et al., 2018). Aquatic amniotes Diverse functions tend to shake their prey more than terrestrial taxa The possibility of differing functions for morphologically when it needs to be processed into smaller pieces varied apicobasal ridges has been discussed a number before consumption (Taylor, 1987). It is possible that of times in previous studies. Massare (1987) classified the ridges act to strengthen the tooth, much in the the teeth of marine predators into a number of different same way that the longitudinal groove (fuller) of functional types and noted that ridges were present swords or bayonets acts to lighten the blade. Fullers in pierce, crush, smash, generalist and cut functional remove material from the spine of the blade which is groups. It was suggested that the ridges might help close to its neutral axis, creating a stiffer blade for the teeth to either cut or grasp prey. Young et al. a given weight of material (Bauchau & Craig, 2009). (2014a) suggested that a specific ridge morphotype However, most strengthen the teeth by with a combination of denticles and pseudo-denticals increasing enamel thickness (McGraw et al., 2012). formed by anastomosing ridges might be linked to a If the ridges do act to strengthen the tooth, then durophagous and generalized diet where both crushing

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Figure 6. Regression analysis between measures associated with durophagy (enamel thickness and tooth robusticity) and characteristics of the ridges (ridge width, ridge height and number of ridges). and flesh slicing are important (Young et al., 2013, ‘cut,’ ‘generalist’ or ‘crunch’ guilds vs. variable (but 2014a), where they could help to increase grip and/or never high-relief) ridges that were associated with strengthen the tooth. Foffa (2018) drew distinctions ‘pierce’ guilds. Foffa (2018) also suggests that some between high-relief ridges that were associated with ridging is associated with durophagy, whereas the

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Figure 7. Morphospace plot of principal component (PC) scores from principal components analysis of crown height, ridge height and ridge width. All groups overlap in PC1; , and Dinosauria tend to have high PC2 values, whereas and Ichthyosauria have low PC2 values; and Cetacea and Sauropterygia have higher PC3 values, whereas the other groups have lower PC3 values. heavily ornamented crowns of pliosaurs are ‘used for indication that the ridges are more pronounced in cutting’. Ciampaglio et al., (2005) suggests that folded species with more robust dentition, but other ridge or ridged enamel ‘increases the strength of the crown’, morphotypes (e.g. anastomosed ridges) might also be but then also notes its presence of fine longitudinal associated with other finer-scale characteristics of ridges in teeth used to puncture or restrain prey. diet. Nevertheless, we regard these ridge morphotypes We acknowledge that more specific classifications of as variations in a similar structure that appears to ridge morphotypes could perform different functions have evolved in response to the selective pressures of or indeed multiple functions. We did not find any feeding in the aquatic environment.

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Table 2. Principal components analysis variation 2. Ridge height, ridge width or the number of ridges is explained not correlated with characteristics associated with durophagy (thickened enamel or robust teeth). PC value Percentage variation Cumulative variation 3. Recurved teeth show a preference for denser spacing of ridges on the recurved surface or smooth PC1 79.82 79.82 surfaces on the other tooth surfaces, indicating that PC2 16.09 95.9 the ridges function only when the tooth is in contact PC3 4.1 100 with a prey item. 4. Ridges are extremely uncommon in terrestrial- Abbreviation: PC, principal component. feeding taxa, indicating that the function of these ridges is specific to some aspect of aquatic feeding. Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021 Table 3. Principal components analysis loadings Determining the exact function (or combination of PC1 PC2 PC3 functions) of the ridges will require empirical testing. Nevertheless, the surprisingly consistent evolution Crown height 0.439 0.848 0.295 of this trait in aquatic-feeding taxa represents an Average ridge width 0.470 – −0.880 example of convergent evolution related to feeding in Average ridge height 0.765 −0.526 0.371 the aquatic environment.

Abbreviation: PC, principal component.

Future research ACKNOWLEDGEMENTS Analysis of the phylogenetic distribution of the trait Neil Kelley assisted in clarifying the phylogenetic within fish could prove useful in linking the trait to occurrence of this trait in taxa. We ecological or behavioural characteristics. Studies of the would also like to thank Carlos Peredo, Alex Boersma function of the ridges using biomechanical modelling and Brian Beatty for useful discussion on this topic. approaches, such as finite element analysis or physical The project would not have been possible without the experimentation, would also be useful in determining scanning time supplied by NTS Chesapeake Testing the function of the trait. In future studies, researchers and the Australian Nuclear Science and Technology might also like to attempt to correlate the crown shape Organisation. David Zahra provided technical or position of the teeth within the tooth row with the assistance with scanning specimens at ANSTO. structure of the ridges. NTS Chesapeake Testing provided advice, technical support and resources for microCT scanning, and we thank C. Peitsch, R. Peitsch and C. Schueler for help. Conclusions We would like to acknowledge the support of a Peter Apicobasal dental ridges have evolved independently Buck Predoctoral fellowship (NMNH), the Remington numerous times. The trait appears to occur almost Kellogg Fund (National Museum of Natural History) exclusively in taxa that feed within the aquatic and the Basis Foundation (to N.D.P.) that supported environment. There is variation in the morphology of M.R.M. to undertake this work. We would like to thank the ridges, but we did not observe distinct clustering David Pickering (Museums Victoria), Kevin Seymour of any groups in morphospace. The internal structure (ROM) and Martha Richter (NHM) for their help with also varies, with some having tooth crowns with locally accessing specimens. Domenic D’Amore, Davide Foffa thickened enamel and others evolving undulating and one anonymous reviewer provided feedback that enamel and dentine surfaces. This indicates that greatly helped to improve the manuscript. different genetic mechanisms might be responsible for the trait in different . We propose that the ridges do not serve primarily to REFERENCES strengthen the tooth but instead function to improve grip, removal efficiency and/or puncture efficiency. We Albright BL, Gillette DD, Titus AL. 2007. Plesiosaurs from base this conclusion on the following four findings. the Upper Cretaceous (Cenomanian–Turonian) Tropic Shale of Southern Utah, part 2: . Journal of Vertebrate 1. Apicobasal ridges evolve on the surface of a wide Paleontology 27: 41–58. variety of tooth morphologies, including those that Amiot R, Buffetaut E, Lécuyer C, Wang X, Boudad L, are not normally associated with high loading Ding Z, Fourel F, Hutt S, Martineau F, Medeiros MA. regimes, e.g. slender or recurved teeth (Foffa et al., 2010. Oxygen isotope evidence for semi-aquatic habits 2018). among spinosaurid theropods. Geology 38: 139–142.

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SUPPORTING INFORMATION Additional Supporting Information may be found in the version of this article at the publisher's web-site: Supplementary Section 1. Table of specimens used in the study. Supplementary Section 2. Test for relationship between apicobasal ridges and aquatic habitat in amniotes. Downloaded from https://academic.oup.com/biolinnean/article/127/2/245/5427318 by guest on 27 September 2021

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