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Multiple Evolutionary Origins and Losses of Tooth Complexity

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Multiple Evolutionary Origins and Losses of Tooth Complexity bioRxiv preprint doi: https://doi.org/10.1101/2020.04.15.042796; this version posted April 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Multiple evolutionary origins and losses of tooth 2 complexity in squamates 3 4 Fabien Lafuma*a, Ian J. Corfe*a, Julien Clavelb,c, Nicolas Di-Poï*a 5 6 aDevelopmental Biology Program, Institute of Biotechnology, University of Helsinki, FIN- 7 00014 Helsinki, Finland 8 bDepartment of Life Sciences, The Natural History Museum, London SW7 5DB, United 9 Kingdom 10 cLaboratoire d’Écologie des Hydrosystèmes Naturels et Anthropisés (LEHNA), Université 11 Claude Bernard Lyon 1 – UMR CNRS 5023, ENTPE, F-69622 Villeurbanne, France 12 13 *Mail: [email protected]; [email protected]; [email protected] bioRxiv preprint doi: https://doi.org/10.1101/2020.04.15.042796; this version posted April 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 14 Teeth act as tools for acquiring and processing food and so hold a prominent role in 15 vertebrate evolution1,2. In mammals, dental-dietary adaptations rely on tooth shape and 16 complexity variations controlled by cusp number and pattern – the main features of the 17 tooth surface3,4. Complexity increase through cusp addition has dominated the 18 diversification of many mammal groups3,5-9. However, studies of Mammalia alone don’t 19 allow identification of patterns of tooth complexity conserved throughout vertebrate 20 evolution. Here, we use morphometric and phylogenetic comparative methods across 21 fossil and extant squamates (“lizards” and snakes) to show they also repeatedly evolved 22 increasingly complex teeth, but with more flexibility than mammals. Since the Late 23 Jurassic, six major squamate groups independently evolved multiple-cusped teeth from a 24 single-cusped common ancestor. Unlike mammals10,11, reversals to lower cusp numbers 25 were frequent in squamates, with varied multiple-cusped morphologies in several groups 26 resulting in heterogenous evolutionary rates. Squamate tooth complexity evolved in 27 correlation with dietary change – increased plant consumption typically followed tooth 28 complexity increases, and the major increases in speciation rate in squamate evolutionary 29 history are associated with such changes. The evolution of complex teeth played a critical 30 role in vertebrate evolution outside Mammalia, with squamates exemplifying a more 31 labile system of dental- dietary evolution. 32 As organs directly interacting with the environment, teeth are central to the acquisition and 33 processing of food, determine the achievable dietary range of vertebrates1, and their shapes are 34 subject to intense natural selective pressures8,12. Simple conical to bladed teeth generally 35 identify faunivorous vertebrates, while higher dental complexity – typically a result of more 36 numerous cusps – enables the reduction of fibrous plant tissue and is crucial to the feeding 37 apparatus in many herbivores4,8,13. Evidence of such dental-dietary adaptations dates back to the 38 first herbivorous tetrapods in the Palaeozoic, about 300 million years ago (Ma)13. Plant bioRxiv preprint doi: https://doi.org/10.1101/2020.04.15.042796; this version posted April 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 39 consumers with highly complex teeth have subsequently emerged repeatedly within early 40 synapsids13, crocodyliforms14, dinosaurs15, and stem- and crown-mammals6,7,9,16. Since the 41 earliest tetrapods had simple, single-cusped teeth8, such examples highlight repeated, 42 independent increases of phenotypic complexity throughout evolution17. Many such linked 43 increases in tooth complexity and plant consumption have been hypothesised to be key to 44 adaptive radiations6,9, though such links have rarely been formally tested. It is also unclear 45 whether the known differences in tooth development between tetrapod clades might result in 46 differences in the evolutionary patterns of convergent functional adaptations18,19. 47 To understand the repeated origin of dental-dietary adaptations and their role in vertebrate 48 evolution, we investigated tooth complexity evolution in squamates, the largest tetrapod 49 radiation. Squamata is recognized for including species bearing complex multicuspid teeth 50 within heterodont dentitions20, and squamate ecology spans a broad range of past and present 51 niches. Squamates express dental marker genes broadly conserved across vertebrates18, with 52 varying patterns of localization and expression compared to mammals, and structures at least 53 partially homologous to mammalian enamel knots (non-proliferative signalling centres of 54 ectodermal cells) determine tooth shape in some squamate clades19,21,22. In mammals – the most 55 commonly studied dental system – novel morphologies arise from developmental changes in 56 tooth morphogenesis23. Epithelial signalling centres – the enamel knots – control tooth crown 57 morphogenesis24, including cusp number and position and ultimately tooth complexity, by 58 expressing genes of widely conserved signalling pathways18,25. Experimental data show most 59 changes in these pathways result in tooth complexity reduction, or complete loss of teeth25, yet 60 increasing tooth complexity largely dominates the evolutionary history of mammals6-9,16. To 61 determine whether similar patterns of tooth complexity underlie all tetrapod evolution or are 62 the specific results of mammalian dental development and history, we used morphometric and 63 phylogenetic comparative methods with squamate tooth and diet data. bioRxiv preprint doi: https://doi.org/10.1101/2020.04.15.042796; this version posted April 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 64 We analysed cusp number and diet data for 545 squamate species spanning all living and extinct 65 diversity and identified species with multicuspid teeth in 29 of 100 recognized squamate 66 families (Figure 1a & Extended Data Figure 1). Within extant “lizards”, we found multicuspid 67 species in almost 56% of families (24/43). While lacking entirely in mostly predatory clades 68 (dibamids, geckos, snakes), multicuspidness dominates Iguania and Lacertoidea, the two most 69 prominent groups of plant-eating squamates. A Kruskal–Wallis test and post-hoc pairwise 70 Wilcoxon–Mann–Whitney tests show squamate dietary guilds differ statistically in tooth 71 complexity, with the proportion of multicuspid species and cusp number successively 72 increasing along a plant consumption gradient, from carnivores to insectivores, omnivores, and 73 herbivores (p-value < 0.001; Fig. 1b, Extended Data Table 1). We quantified tooth outline shape 74 in a subset of taxa spanning all major multicuspid groups with two-dimensional semi- 75 landmarks, which showed the teeth of herbivores are more protruding with a wider top cusp 76 angle (Fig. 1c). A regularized phylogenetic multivariate analysis of variance (MANOVA) on 77 principal component scores confirm statistically significant differences between diets overall 78 (p-value = 0.001; Fig.1c) with negligible phylogenetic signal in the model’s residuals (Pagel’s 79 = 0.03). Herbivore teeth differ from both the insectivorous and omnivorous morphospace 80 regions (Fig.1c, Extended Data Table 2), similarly to observations from mammals and 81 saurians4,20. Furthermore, we find support for shifts in the rate of evolution of tooth shape 82 outline independent of cusp number among the 75 species examined (log Bayes Factor = 319), 83 with particularly high rates characterising Iguanidae (Extended Data Figure 2). 84 Using Maximum-Likelihood reconstructions of ancestral character states26 across our squamate 85 phylogeny (Fig. 2, Extended Data Figure 3 and 4, Supplementary Table 1 and 2), we found 86 dental-dietary adaptations to plant consumption repeatedly evolved, arising from the 87 convergent evolution of multicuspidness. Since the Late Jurassic, six major clades and 18 88 isolated lineages independently evolved multicuspid teeth from a unicuspid ancestral bioRxiv preprint doi: https://doi.org/10.1101/2020.04.15.042796; this version posted April 16, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 89 morphology, mostly through single-cusp addition events. Similar numbers – 10 clades, 13 90 isolated lineages – show independent origins of plant consumption from carnivorous or 91 insectivorous ancestors (Fig. 2, Supplementary Table 3). Across the tree, most lineages and 92 terminal taxa are unicuspid insectivores retaining the reconstructed ancestral squamate 93 condition. However, of 102 lineages
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