The Anatomical Record Exceptional disparity in Australian agamid lizards is a possible result of arrival into vacant niche Journal: Anatomical Record Manuscript ID AR-18-0262.R1 Wiley - Manuscript type:ForFull LengthPeer Article Review Date Submitted by the n/a Author: Complete List of Authors: Gray, Jaimi; University of Adelaide Faculty of Sciences, School of Biological Sciences Hutchinson, Mark; South Australian Museum, Herpetology Jones, Marc; The Natural History Museum Keywords: Agamidae, Iguania, ternary diagram, morphological disparity, cranium John Wiley & Sons, Inc. Page 1 of 79 The Anatomical Record 1 2 3 4 Exceptional disparity in Australian agamid lizards is a possible 5 6 7 8 result of arrival into vacant niche 9 10 11 Jaimi A. Gray1, Mark N. Hutchinson 1,2, Marc E. H. Jones1,2,3 12 13 14 1 Department of Ecology and Evolution, School of Biological Sciences, The University of Adelaide, 15 16 17 North Terrace, Adelaide, South Australia 5005, Australia 18 19 For Peer Review 20 2 South Australian Museum, North Terrace, Adelaide, South Australia 5001, Australia 21 22 23 3Department of Earth Sciences, The Natural History Museum, London, UK 24 25 26 Corresponding author: Jaimi A. Gray 27 28 Department of Ecology and Evolution 29 30 School of Biological Sciences 31 Room 205E, Darling Building, North Terrace, University of Adelaide 32 South Australia 5005, Australia 33 Email: [email protected] 34 35 Ph: +61 418 601 992 36 37 38 Running title: “High disparity in Australian agamid lizards” 39 40 Grant sponsors: University of Adelaide (JAG), Royal Society of South Australia (JAG), Jackson 41 School of Geosciences (JAG), Australian Research Council (MEHJ); Grant numbers: Australian 42 43 Postgraduate Award, Student Small Grants Scheme, Student Travel Grant, DE130101567. 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 Page 1 of 21 59 60 John Wiley & Sons, Inc. The Anatomical Record Page 2 of 79 1 2 3 4 5 6 Abstract 7 Australia provides abundant examples of continental-scale evolutionary radiations. The collision 8 9 10 of two continental shelves around 30 Ma facilitated an influx of squamates and the subsequent 11 12 squamate radiations resulted in high taxonomic diversity. The morphological disparity seen in 13 14 15 these major squamate groups, however, remains underexplored. Here, we examine the major 16 17 cranial proportions of over 1000 specimens using 2D linear measurements to explicitly quantify 18 19 For Peer Review 20 the morphological disparity of Australian agamid lizards (Amphibolurinae) and compare it to 21 22 that of agamid, acrodont, and iguanian clades from other parts of the world. Our results 23 24 indicate the Australian Amphibolurinae have exceptionally high cranial disparity, and we 25 26 27 suggest that this is linked to the relaxed selective environment that greeted the founders of 28 29 Amphibolurinae when they first arrived in Australia. 30 31 32 Key words: Agamidae, Iguania, ternary diagram, morphological disparity, cranium 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 Page 2 of 21 59 60 John Wiley & Sons, Inc. Page 3 of 79 The Anatomical Record 1 2 3 4 Introduction 5 Evolutionary radiations (Losos and Mahler, 2010) are often linked to particular events, 6 7 8 such as a clade invading a new geographic area (Nilsson et al., 2004), new environment (e.g. 9 10 cetaceans, Slater et al., 2010) or following a major extinction event (e.g. passerine birds, Jarvis 11 12 et al., 2014). In such cases factors such as new resources, freedom from competition and an 13 14 15 absence of predators and pathogens can lead to rapid speciation (diversity) which is often, but 16 17 not always (Rundell and Price, 2009), accompanied by expansion into new ecological niches 18 19 For Peer Review 20 that drive a shift or expansion of morphospace (disparity). This phenomenon is particularly 21 22 associated with island faunas, where examples of adaptive radiations are well known, e.g. 23 24 25 Tahitian snails, (Murray et al., 1993), Hawaiian honeycreepers (Lovette et al., 2002), and 26 27 Caribbean Anolis lizards (Yoder et al., 2010; Losos, 2011). The taxonomic diversity exhibited by 28 29 30 such island radiations has been well documented, however phenotypic disparity has only 31 32 recently come under more detailed scrutiny (Harmon et al., 2003). Moreover, continental-scale 33 34 radiations remain poorly studied in general. 35 36 37 38 Australia is rich with examples of successful continental-scale evolutionary radiations. 39 40 Around 30 Ma, the northward-drifting margin of the Australian plate (Sahul shelf) collided with 41 42 continental crust of Southeast Asia (Sunda shelf) in the New Guinea-Timor region, narrowing 43 44 45 the ocean gap between the two landmasses and filling the intervening ocean with island arcs 46 47 and terrain fragments that provided an archipelagic sweepstakes route for faunal exchange 48 49 50 between tropical Asia and Australia (Hall, 2001). In this exchange, Australia (previously 51 52 temperate-polar and apparently with poor taxonomic squamate diversity) appears to have 53 54 55 received most of its current squamate taxonomic diversity, including agamids (Hugall et al., 56 57 58 Page 3 of 21 59 60 John Wiley & Sons, Inc. The Anatomical Record Page 4 of 79 1 2 3 2008; Chen et al., 2013), scincids (Skinner et al., 2011), varanids (Ast, 2001; Vidal et al., 2012), 4 5 6 elapids (Keogh, 1998; Sanders et al., 2008), typhlopids (Vidal et al., 2010) and boids (Scanlon 7 8 and Lee, 2011) from a small number of tropical Asian invaders (Oliver and Hugall, 2017). Most 9 10 11 Australian clades appear to be monophyletic, implying single origins, and all of these Australian 12 13 clades show the characteristics of adaptive radiations, with numerous species (over 1000 14 15 16 Australian squamate species) and highly varied body forms. 17 18 19 The taxonomic diversityFor associated Peer with ReviewAustralian squamates is immense (see Cogger, 20 21 2014), but their morphological disparity remains underexplored. One of the colonising groups, 22 23 24 the agamid lizards, is represented today by the amphibolurine radiation (Hugall et al., 2008; 25 26 Melville et al., 2011) which is taxonomically diverse (around 90 species) and varied in body size 27 28 (adult mass from 2-3 g to 1000 g) and ecological niche (Pianka et al., 2017). They occupy almost 29 30 31 every habitat on the Australian continent (Powney et al., 2010) and the adjacent islands of 32 33 Melanesia (Manthey and Denzer, 2006). Amphibolurinae provides a model group to investigate 34 35 36 morphological disparity of an evolutionary successful group. To date, discussions of the 37 38 morphological disparity in this group has tended to be qualitative, highlighting extreme 39 40 41 examples such as Moloch (Bell et al., 2009) or Chlamydosaurus (Shine, 1990), or if quantitative, 42 43 limited to a few factors such as limb proportions (Melville et al., 2006) and locomotor 44 45 46 performance (Thompson and Withers, 2005; Clemente et al., 2008). Broad patterns in the skull 47 48 morphology in these lizards may be associated with functional or developmental constraints, 49 50 and therefore represent an important element of the anatomy to examine in an adaptive 51 52 53 context. 54 55 56 57 58 Page 4 of 21 59 60 John Wiley & Sons, Inc. Page 5 of 79 The Anatomical Record 1 2 3 Here, we use two-dimensional linear measurements of cranial proportions to provide an 4 5 6 explicit quantitative measure of cranial disparity for Australian agamids and their relatives. We 7 8 provide insights into macroevolutionary patterns in Australian agamids and include 9 10 11 comparisons with other agamid, acrodont and iguanian clades. 12 13 14 15 Materials and methods 16 We sampled 1046 iguanians from multiple collections (see Tables 1 and S1) representing 17 18 between 33% and 100% of the genera in each sampled family. As far as available material 19 For Peer Review 20 21 allowed, we assembled a comprehensive representation of the taxonomic diversity across the 22 23 amphibolurines (see Fig. 1) and several outgroup clades, and also endeavoured to include 24 25 26 specimens that would represent the broadest range of cranial geometries. We included 27 28 iguanian families from the Acrodonta clade (Chamaeleonidae and Agamidae), and from the 29 30 31 Pleurodonta clade (all other iguanian families). The complete data set included skeletal 32 33 specimens as well as images taken of surface reconstructions of X-ray computed tomography 34 35 (CT) scans. We also included measurements from the reconstructed images of five fossils that 36 37 38 are generally regarded as early members of Iguania, the priscagamids (Alifanov, 1996), 39 40 Ctenomastax parva (Keqin and Norell, 2000) and Saichangurvel davidsoni (Conrad and Norell, 41 42 43 2007). 44 45 46 Head shape was assessed via 2D linear measurements (cf. Marugán-Lobón & Buscalioni, 47 48 2003). This approach was used to allow a large and encompassing sample size including both 49 50 51 images of specimens and images of reconstructed fossils. Use of 2D measurements enables this 52 53 study to be more readily compared to previous studies, as well as any future additions to this 54 55 56 data set. Crania were imaged in lateral view and aligned using the long axis of the maxillary 57 58 Page 5 of 21 59 60 John Wiley & Sons, Inc. The Anatomical Record Page 6 of 79 1 2 3 tooth row (defined by the anterior end of the anteriormost tooth and posterior end of the 4 5 6 posteriormost tooth, for agamids the acrodont tooth row was used due to curvature in the 7 8 anterior pleurodont teeth in many species).