Macroevolutionary Dynamics of Dentition in Mesozoic Birds Reveal No Long-Term Selection Towards Tooth Loss
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Journal Pre-proof Macroevolutionary dynamics of dentition in Mesozoic birds reveal no long-term selection towards tooth loss Neil Brocklehurst, Daniel J. Field PII: S2589-0042(21)00211-X DOI: https://doi.org/10.1016/j.isci.2021.102243 Reference: ISCI 102243 To appear in: ISCIENCE Received Date: 15 June 2020 Revised Date: 16 December 2020 Accepted Date: 25 February 2021 Please cite this article as: Brocklehurst, N., Field, D.J., Macroevolutionary dynamics of dentition in Mesozoic birds reveal no long-term selection towards tooth loss, ISCIENCE (2021), doi: https:// doi.org/10.1016/j.isci.2021.102243. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2021 Journal Pre-proof 1 Macroevolutionary dynamics of dentition in Mesozoic birds reveal no long-term 2 selection towards tooth loss 3 4 Neil Brocklehurst 1* , Daniel J. Field 2 5 1 Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, UK 6 2 Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge, UK 7 8 *Lead Contact – Neil Brocklehurst, neil.brocklehurst@earth.ox.ac.uk 9 10 11 12 13 14 15 16 17 18 Journal Pre-proof 19 20 21 22 23 24 25 2 26 Summary 27 Several potential drivers of avian tooth loss have been proposed, although consensus remains 28 elusive as fully toothless jaws arose independently numerous times among Mesozoic avialans 29 and dinosaurs more broadly. The origin of crown bird edentulism has been discussed in terms 30 of a broad-scale selective pressure or trend toward toothlessness, although this has never been 31 quantitatively tested. Here, we find no evidence for models whereby iterative acquisitions of 32 toothlessness among Mesozoic Avialae were driven by an overarching selective trend. 33 Instead, our results support modularity among jaw regions underlying heterogeneous tooth 34 loss patterns, and indicate a substantially later transition to complete crown bird edentulism 35 than previously hypothesized (~ 90 MYA). We show that patterns of avialan tooth loss 36 adhere to Dollo’s law and suggest that the exclusive survival of toothless birds to the present 37 represents lineage-specific selective pressures, irreversibility of tooth loss, and the filter of 38 the K–Pg mass extinction. 39 40 Key Words 41 Birds; Teeth; Edentulism; Dollo’s Law; Phylogenetic Comparative Methods 42 43 Introduction Journal Pre-proof 44 The toothless beak is among the most characteristic features of the crown bird 45 bauplan, and toothlessness has been hypothesised to increase the evolvability of crown bird 46 jaws, partially underlying their sensational morphological disparity (Louchart & Viriot, 47 2011). Numerous potential drivers of avialan tooth loss have been proposed, including 48 selection for flight-related weight reduction (Diliger, 1957; Feduccia, 1998; Proctor & Lynch, 49 1998) (though see [Zhou et al., 2019; Lautenschlager et al., 2013]), selection for rapid 50 developmental rates precluding tooth formation (Yang & Sander, 2018), dietary shifts 2 51 favouring alternative modes of food processing (Louchart & Viriot, 2011; Lautenschalger et 52 al. 2013; Wang et al., 2017; Ksepka, et al. 2019), and selection for preening efficacy (Naish 53 2014; Mayr 2016). However, consensus remains elusive, as fully toothless jaws arose 54 independently numerous times among Mesozoic avialans and dinosaurs more broadly 55 (Louchart, A. & Viriot, L. 2011; Dilger, 1957). 56 The origin of crown bird edentulism has been discussed in terms of a trend or 57 selection toward toothlessness (Dilger, 1957; Zhou et al. 2019; Lautenschlager et al., 2013; 58 Yang & Sander, 2018), implying an overarching selective pressure favouring edentulism 59 throughout avialan evolutionary history as opposed to localised selection acting on subsidiary 60 lineages as interpreted in other studies (O’Connor, 2019; 2020). For example, Zhou et al. 61 (2019) justified their assumption of overarching selection favouring tooth loss in Avialae on 62 the basis that it evolved numerous times independently: “Tooth loss occurred independently 63 in several early avian lineages (Zhou and Zhang, 2006; Zhou et al., 2009; Davit-Béal et al., 64 2009), suggesting that reduction and eventual disappearance of the dentition might have 65 conferred some broadly applicable selective advantage” (Zhou et al., 2019, pg 39). However, 66 no studies had previously tested whether avialan edentulism was associated with increased 67 rates of diversification (i.e. higher speciation rates and/or lower extinction rates), as would be 68 predicted by overarchingJournal directional selection forPre-proof a toothless bill through the Mesozoic, nor 69 had they evaluated whether patterns of tooth loss across Avialae actually follow trend-like 70 patterns. Such an interpretation does not align with other clades in which edentulism has 71 arisen numerous times independently, such as crown mammals (Davit-Béal et al. 2019), 72 which have never been suggested to exhibit a generalised trend toward edentulism. 73 The hypothesis of long-term selection or a trend toward edentulism in Avialae can be 74 tested in two ways: identifying a shift in diversification rates associated with tooth loss could 75 indicate selection for toothlessness on a broad phylogenetic scale [Jablonski, 2008; Rabosky 2 76 & McCune, 2010), while demonstrating that regional losses of teeth within the jaws are more 77 likely to lead to further losses of teeth would support the progression of edentulism 78 throughout the jaws in a trend-like manner. We apply state-dependent diversification methods 79 and evolutionary modelling to show that tooth loss had a negligible impact on avialan 80 diversification, providing no evidence for a link between toothlessness and accelerated 81 cladogenesis. We also found no evidence for models whereby iterative acquisitions of 82 toothlessness among Mesozoic Avialae were driven by an overarching selective trend. 83 84 Results and Discussion 85 No Long-Term Selection Toward Toothlessness in Avialae 86 State-dependent diversification (SDD) methods (FiSSE [Rabosky & Goldberg, 2017)] 87 and HiSSE [Beaulieu & O’Meara, 2016]) reject the hypothesis that edentulism provided a 88 selective advantage throughout the evolutionary history of Avialae (operationally defined 89 here as the clade uniting Archaeopteryx and crown birds). Speciation rates inferred by FiSSE 90 were higher in toothed avialans than in toothless avialans (Fig.1a). However, these 91 differences were never significant (p<0.05), implying that diversification rates were not 92 substantially affected by the presence or absence of teeth (Supplementary Table 2). HiSSE 93 analyses fit a null model Journalbetter than a state-depen Pre-proofdent model, suggesting that avialan patterns 94 of speciation and extinction were unrelated to tooth loss (Fig 1b). These results are consistent 95 when considering transitions to complete toothlessness, as well as transitions to regional 96 edentulism in the premaxilla, maxilla, and dentary (Supplementary figs 1-6). We confirmed 97 that these results are not an artefact of incomplete sampling with a taxonomic jackknifing 98 approach (Close et al., 2015). Although the range of rate values and Akaike weight scores are 99 greater in jackknifed datasets, we still obtained overwhelming support for a null model over a 2 100 trait-dependant model of diversification (Supplementary Fig. 7) and found no significant 101 difference between speciation rates of toothed vs toothless taxa (Supplementary Fig 8). 102 We also found no evidence for a general trend toward edentulism throughout avialan 103 evolutionary history. Loss of teeth in one region of the upper jaw (e.g., premaxilla) did not 104 increase the likelihood of tooth loss in another region of the jaw (e.g., maxilla), and vice 105 versa. Instead, model fits supported the premaxilla and maxilla as discrete modules with 106 largely independent trajectories with respect to tooth loss and tooth retention (Fig. 2a), which 107 is understandable in light of the differing populations of primordia, tissues, and cells from 108 which these elements arise (Helm & Schneider 2003, Schneider & Helms 2003; Wang et al. 109 2020a). The independent patterns of tooth loss in the premaxilla and maxilla provide 110 evidence against strong directional selection driving transitions to toothlessness across 111 avialans. While there are several instances of tooth-loss in the premaxilla coinciding with that 112 in the maxilla (e.g., Confucuisornithidae, Gobipteryx , Schizooura ), there are also numerous 113 instances where the evolution of toothlessness in one region occurred independently of the 114 other (e.g., Jeholornis , Longipterygidae), or where the evolution of toothlessness in one 115 region preceded that in the other by more than 30 million years (Ornithurae). These 116 idiosyncratic patterns, combined with the results of our model-fitting analyses, indicate that 117 transitions toward regionalJournal or complete tooth loss Pre-proof in Avialae reflect lineage-specific patterns,