Introduction
Teeth allow most vertebrates to acquire food –and therefore energy—from their environment (Lucas, 2004). As such, they are one of the critical interfaces between an animal and its environment and their evolution depends both on intrinsic and extrinsic constraints. Teeth play different roles, from food acquisition to food processing, and have different functions (e.g., cutting, crushing, grinding, piercing). These functions depend on both food properties and/or food processing behavior and are related to tooth shape (e.g., Crofts et al., 2020). Work by Crofts and colleagues (2020), based on pioneering studies by Lucas (2004) and Massare (1987), showed how tooth morphology is associated with prey properties and dental biomechanics (e.g., toughness, bending abilities, mode of failure). Rounded teeth, for example, allow to crush hard prey items, they are tough, can barely bend and consequently are susceptible to fragmentation (Crofts et al., 2020). Because of their tight and reliable relationship with diet and their abundance in the fossil record, teeth have been suggested to be good indicators of past climate and paleoenvironments (e.g., Evans, 2013), and are used to make inferences on the ecology of extinct species (Bellwood et al., 2014; Evans & Pineda-Munoz, 2018; Fischer et al., 2022; Frederickson et al., 2018; Massare, 1987). By extension, tooth morphology could also be used to infer the feeding habits of secretive species that are sometimes only known from museum specimens, providing the link between tooth shape and food properties has been established. While most dental morphology studies have focused on mammals, because they benefit from a large variety of diets and tooth shapes (Berkovitz & Shellis, 2018; Ungar, 2010, 2015), a significant amount of work has been done on non-mammalian vertebrates (Berkovitz & Shellis, 2017). Yet, quantitative comparisons of tooth morphology and its link to dietary ecology, in a phylogenetically and ecologically broad sample of species remain rather scarce for non-mammalian vertebrates. In this study, we investigated the relationship between dietary ecology and tooth shape in a group of non-model vertebrates: snakes.
Among vertebrates, macrostomatan snakes are peculiar as they are the only taxon able to ingest prey larger than their head without processing it. This behavior is related to an extraordinary organization of the skull that has become highly kinetic. Indeed, snakes must coordinate the movements of eight pairs of cranial bones to catch, subdue, manipulate, and swallow their prey (Cundall & Greene, 2000; Moon et al., 2019). Despite the complexity of their feeding behavior, snakes have independently adopted a wide variety of dietary preferences (gastropods, mammals, birds, crustaceans) providing an opportunity to study possible convergences in their feeding apparatus (Rhoda et al., 2020). In addition to constraints related to the physical properties of their food items, some feeding behaviors may impose high loads on snake teeth, such as eating live and vigorous prey, with or without the support of a solid substrate. These various mechanical challenges may have driven the evolution of tooth shape in snakes. Despite their richness and complexity in shape (Vaeth et al., 1985; Young & Kardong, 1996), studies on snake tooth morphology are scarce and either lack of a quantitative approach or are phylogenetically limited (Berkovitz & Shellis, 2017; Britt et al., 2009; Evans et al., 2019; Rajabizadeh et al., 2020; Ryerson & Van Valkenburgh, 2021). Fangs, and mostly front fangs, have recently attracted some scientific attention (Broeckhoven & du Plessis, 2017; Cleuren, Parker, et al., 2021; Crofts et al., 2019; du Plessis et al., 2018; Kundanati et al., 2020; Palci et al., 2021). Yet, fangs are phylogenetically and functionally limited; their only purpose is to puncture the prey to deliver venom and consequently, fangs are not representative of snake tooth diversity. Indeed, they are but two highly derived teeth out of sometimes over 200 teeth (D. Rhoda pers. obs.).
Snake teeth are usually described as pointy and curved (Berkovitz & Shellis, 2017). They would therefore be considered as “piercing” specialists in the classification scheme as described in (Crofts et al., 2020), and should be associated with a restricted diet composed of soft invertebrates and small fish. Yet, as previously mentioned, snakes show a broad variety of diets, but also a wide variety of feeding behaviors that involve their teeth such as ‘chewing’ (Tumlison & Roberts, 2018), ripping (Bringsøe et al., 2020; Jayne et al., 2002; Noonloy et al., 2018), slicing (Cundall & Greene, 2000; Kojima et al., 2020), or swallowing without piercing (e.g. Dasypeltis sp. ). Snake teeth are also involved in the whole feeding sequence, from prey capture to swallowing. Yet, the diversity of tooth morphology and function in snakes remains under-explored. Here, we quantified and compared the dentary tooth morphology of 63 species that cover the phylogenetic and ecological breadth of snakes. We tested four factors related to feeding that could be associated with morphological adaptations of the teeth:
We dissected the dentary bone of 63 species of snakes and used micro-CT scanning to obtain high resolution scans of the teeth. We then used 3D geometric morphometrics to compare both the external and internal shape of the teeth. Shape information on inner part of the teeth allowed us to compare the thickness of the hard tissues that compose the tooth. We also measured the length and maximal and average degrees of curvature. Next, we used phylogenetic comparative methods to test the importance of our predictive ecological factors as drivers of tooth shape to establish the link between tooth shape variation and dietary ecology in snakes.