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Comparative Anatomy and Phylogenetic Contribution of Intracranial Osseous Canals And bioRxiv preprint doi: https://doi.org/10.1101/2021.04.21.440734; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 TITLE: 2 Comparative anatomy and phylogenetic contribution of intracranial osseous canals and 3 cavities in armadillos and glyptodonts (Xenarthra, Cingulata). 4 5 SHORT RUNNING TITLE: 6 Internal cranial structures in armadillos 7 8 AUTHORS: 9 KÉVIN LE VERGER1*; LAUREANO R. GONZÁLEZ RUIZ2; and GUILLAUME BILLET1 10 11 1 Museum national d’Histoire naturelle, Centre de Recherche en Paléontologie – Paris, UMR 12 7207 CR2P MNHN/CNRS/UPMC, Sorbonne Universités, 8 rue Buffon, CP 38, 75005 Paris, 13 France. 14 15 2 Laboratorio de Investigaciones en Evolución y Biodiversidad (LIEB-FCNyCS sede Esquel, 16 UNPSJB) y Centro de Investigaciones Esquel de Montaña y Estepa Patagónica (CIEMEP), 17 CONICET, Universidad Nacional de La Patagonia San Juan Bosco (UNPSJB), Roca 780, 9200, 18 Esquel, Chubut, Argentina. 19 20 * Corresponding author: Kévin Le Verger; address: 8 rue Buffon, CP 38, 75005 Paris, France; 21 telephone number: 01.40.79.53.79; fax number: 01.40.79.35.80. E-mail: kevin.le- 22 [email protected]. 23 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.21.440734; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 ABSTRACT 25 The evolutionary history of the Cingulata, as for many groups, remains a highly debated 26 topic to this day, particularly for one of their most emblematic representatives: the glyptodonts. 27 There is no consensus among morphological and molecular phylogenies relative to their position 28 within Cingulata. As demonstrated by recent works, the study of the internal anatomy constitutes 29 a promising path for enriching morphological matrices for the phylogenetic study of armadillos. 30 However, internal cranial anatomy remains under-studied in the Cingulata. Here we explored and 31 compared the anatomy of intracranial osseous canals and cavities in a diverse sample of extant and 32 extinct cingulates, including the earliest well-preserved glyptodont crania. The virtual 3D 33 reconstruction (using X-ray microtomography) of selected canals, i.e., the nasolacrimal canal, the 34 palatine canal, the sphenopalatine canal, the canal for the frontal diploic vein, the transverse canal, 35 the orbitotemporal canal, the canal for the capsuloparietal emissary vein and the posttemporal 36 canal, and alveolar cavities related to cranial vascularization, innervation or tooth insertion allowed 37 us to compare the locations, trajectories and shape of these structures and to discuss their potential 38 interest for cingulate systematics. We tentatively reconstructed evolutionary scenarios for eight 39 selected traits on these structures, in which glyptodonts often showed a greater resemblance to 40 pampatheres, to the genus Proeutatus and/or to chlamyphorines. This latter pattern was partly 41 congruent with recent molecular hypotheses, but more research is needed on these resemblances 42 and on the potential effects of development and allometry on the observed variations. Overall, 43 these comparisons have enabled us to highlight new anatomical variation that may be of great 44 interest to further explore the evolutionary history of cingulates and the origins of glyptodonts on 45 a morphological basis. 46 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.21.440734; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 47 Keywords: Glyptodont – Cingulata – Cranial canals – Alveolar cavities – Comparative anatomy – 48 Evolutionary scenarios – Phylogeny. 49 50 1. INTRODUCTION 51 52 The peculiar morphology of xenarthrans, which include armadillos (Cingulata), sloths 53 (Folivora) and anteaters (Vermilingua), has aroused the curiosity of anatomists since the end of 54 the 18th century (Cuvier, 1798). Compared to other mammals, the sum of their unique 55 characteristics has led them to be considered by some earlier workers the most unusual mammals 56 (Vizcaíno & Loughbry, 2008; for a summary see Superina & Loughry, 2015). They represent the 57 only known mammals with a carapace formed by a mosaic of osteoderms (fixed and mobile) 58 covering the head, body and tail (Vizcaíno & Loughry, 2008). Cingulates include extant and 59 extinct armadillos, among them the four extant subfamilies Dasypodinae, Euphractinae, 60 Tolypeutinae, and Chlamyphorinae, as well as the extinct glyptodonts, a group of herbivorous and 61 large bodied mammals appearing in the late Eocene and disappearing at the beginning of the 62 Holocene (Delsuc et al., 2016; see also Gaudin & Lyon, 2017 for an alternative classification). The 63 phylogenetic position of glyptodonts within Cingulata is particularly difficult to resolve based on 64 morphological data because of their highly specialized anatomy and the large morphological gap 65 separating them from extant armadillos (Burmeister, 1874; Carlini & Zurita, 2010; Fariña et al., 66 2013). This difficulty was recently emphasized by ancient DNA studies showing that phylogenetic 67 analyses of their mitogenomes support a position for glyptodonts at odds with that proposed in 68 prior morphological studies (Engelmann, 1985; Gaudin & Wible, 2006; Billet et al., 2011; Delsuc 69 et al., 2016; Mitchell et al., 2016; Herrera et al., 2017). 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.21.440734; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 70 While it has long been accepted that glyptodonts were closely related to extant armadillos 71 (Huxley, 1864), their exact relationships with the latter were never clearly resolved on the basis 72 morphological data. Flower (1882) initially proposed that glyptodonts were the ancestors of extant 73 armadillos but Ameghino (1884, 1889) disputed this hypothesis, arguing that their great dental and 74 postcranial complexity, as described by Owen (1839) was evidence of their derived nature. The 75 nested position of glyptodonts among extant armadillos has been supported by many authors since 76 then, including by recent phylogenetic analyses using morphological data (Castellanos, 1932, 77 1959; Hoffstetter, 1958; Patterson & Pascual, 1972; Fernicola, 2008; Gaudin & Wible, 2006; Billet 78 et al., 2011; Herrera et al., 2017). However, the consensus stops here. Engelmann (1985) proposed 79 a close relationship of glyptodonts with the extinct Eutatini (Proeutatus and Eutatus) and 80 pampatheres, whereas the analysis of Gaudin & Wible (2006) retrieved glyptodonts in an apical 81 position nested within a large clade gathering euphractines, chlamyphorines, the extinct 82 pampatheres and some extinct eutatines. A similar hypothesis was also supported by other studies, 83 but with much variation in the composition of this large apical clade (Fernicola, 2008; Porpino et 84 al., 2010; Billet et al., 2011; Fernicola et al., 2017; Herrera et al., 2017). Most of these studies, 85 however, unvaryingly proposed a close relationship between the extinct giant pampatheres and 86 glyptodonts, in agreement with Patterson & Pascual (1972). Thanks to the progress made in ancient 87 DNA studies and the recent extinction of glyptodonts – at the beginning of the Holocene (Messineo 88 & Politis, 2009) – the complete mitochondrial genome of the Pleistocene glyptodont Doedicurus 89 Burmeister, 1874 could be successfully assembled, which gave rise to a completely new 90 phylogenetic hypothesis (Delsuc et al., 2016; Mitchell et al., 2016). Based on analyses of their 91 mitogenomes, glyptodonts are nested within extant armadillos and represent the sister group of a 92 clade formed by chlamyphorines and tolypeutines (Delsuc et al., 2016; Mitchell et al., 2016). 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.21.440734; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 93 Although analyses of morphological matrices using a molecular backbone constraint can detect 94 morphological characters congruent with the molecular pattern (Mitchell et al., 2016), the high 95 level of disagreement between the two data partitions may call into question the phylogenetic 96 signal provided by morphological matrices on cingulates. 97 External cranial and postcranial skeletal anatomy are already well known for many groups 98 within Cingulata, but the internal cranial anatomy remains understudied. However, its study has 99 already provided data of systematic interest for both the extant and extinct xenarthran diversity 100 (Zurita et al., 2011; Fernicola et al., 2012; Billet et al., 2015; Tambusso & Fariña, 2015a; Tambusso 101 & Fariña, 2015b; Billet et al., 2017; Boscaini et al., 2018; Boscaini et al., 2020; Tambusso et al., 102 2021). Intracranial osseous canals provide important pathways for innervation and vascularization 103 of the head (Evans & de Lahunta, 2012). The diversity and phylogenetic signal of their intracranial 104 trajectories are poorly known, as these hidden
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