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Comparative Anatomy and Phylogenetic Contribution Of Comparative anatomy and phylogenetic contribution of intracranial osseous canals and cavities in armadillos and glyptodonts (Xenarthra, Cingulata) Kévin Le Verger, Laureano González Ruiz, Guillaume Billet To cite this version: Kévin Le Verger, Laureano González Ruiz, Guillaume Billet. Comparative anatomy and phylogenetic contribution of intracranial osseous canals and cavities in armadillos and glyptodonts (Xenarthra, Cingulata). Journal of Anatomy, Wiley, 2021, 10.1111/joa.13512. hal-03291344 HAL Id: hal-03291344 https://hal.sorbonne-universite.fr/hal-03291344 Submitted on 19 Jul 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Received: 25 April 2021 | Revised: 28 June 2021 | Accepted: 29 June 2021 DOI: 10.1111/joa.13512 ORIGINAL PAPER Comparative anatomy and phylogenetic contribution of intracranial osseous canals and cavities in armadillos and glyptodonts (Xenarthra, Cingulata) Kévin Le Verger1 | Laureano R. González Ruiz2 | Guillaume Billet1 1Museum national d’Histoire naturelle, Centre de Recherche en Paléontologie – Abstract Paris, UMR 7207 CR2P MNHN/CNRS/ The evolutionary history of the Cingulata, as for many groups, remains a highly de- UPMC, Sorbonne Universités, Paris, France bated topic to this day, particularly for one of their most emblematic representatives: 2Laboratorio de Investigaciones en the glyptodonts. There is no consensus among morphological and molecular phylog- Evolución y Biodiversidad (LIEB- FCNyCS sede Esquel, UNPSJB) y Centro de enies regarding their position within Cingulata. As demonstrated by recent works, Investigaciones Esquel de Montaña y the study of the internal anatomy constitutes a promising path for enriching morpho- Estepa Patagónica (CIEMEP), CONICET, Universidad Nacional de La Patagonia San logical matrices for the phylogenetic study of armadillos. However, internal cranial Juan Bosco (UNPSJB), Chubut, Argentina anatomy remains understudied in the Cingulata. Here we explored and compared Correspondence the anatomy of intracranial osseous canals and cavities in a diverse sample of ex- Kévin Le Verger, Museum national tant and extinct cingulates, including the earliest well- preserved glyptodont crania. d’Histoire naturelle, Centre de Recherche en Paléontologie – Paris, UMR 7207 The virtual 3D reconstruction (using X- ray microtomography) of selected canals, that CR2P MNHN/CNRS/UPMC, Sorbonne is, the nasolacrimal canal, the palatine canal, the sphenopalatine canal, the canal for Universités, Paris, France. Email: [email protected]. the frontal diploic vein, the transverse canal, the orbitotemporal canal, the canal for the capsuloparietal emissary vein and the posttemporal canal, and alveolar cavities related to cranial vascularization, innervation or tooth insertion allowed us to com- pare the locations, trajectories, and shape of these structures and to discuss their potential interest for cingulate systematics. We tentatively reconstructed evolution- ary scenarios for eight selected traits related to these structures in which glyptodonts often showed a close resemblance to pampatheres, to the genus Proeutatus, and/or to chlamyphorines. This latter pattern was partly congruent with recent molecular hypotheses, but more research is needed on these resemblances and on the potential effects of development and allometry on the observed variations. Overall, these com- parisons have enabled us to highlight new anatomical variation that may be of great interest to further explore the evolutionary history of cingulates and the origins of glyptodonts on a morphological basis. KEYWORDS alveolar cavities, cingulata, comparative anatomy, cranial canals, evolutionary scenarios, glyptodont, phylogeny Journal of Anatomy. 2021;00:1–30. wileyonlinelibrary.com/journal/joa © 2021 Anatomical Society | 1 2 | LE VERGER ET AL. 1 | INTRODUCTION Holocene (Messineo & Politis, 2009)— the complete mitochondrial genome of the Pleistocene glyptodont Doedicurus (Burmeister, 1874) The peculiar morphology of xenarthrans, which include armadil- was successfully assembled, which gave rise to a completely new los (Cingulata), sloths (Folivora), and anteaters (Vermilingua), has phylogenetic hypothesis (Delsuc et al., 2016; Mitchell et al., 2016). aroused the curiosity of anatomists since the end of the 18th cen- Based on analyses of their mitogenomes, glyptodonts were nested tury (Cuvier, 1798). Compared to other mammals, the sum of their within extant armadillos and represented the sister group of a clade unique characteristics has led them to be considered by some pre- formed by chlamyphorines and tolypeutines (Delsuc et al., 2016; vious workers, the most unusual mammals (Vizcaíno & Loughry, Mitchell et al., 2016). Although analyses of morphological matrices 2008; for a summary see Superina & Loughry, 2015). They repre- using a molecular backbone constraint can detect morphological sent the only known mammals with a carapace formed by a mosaic characters congruent with the molecular pattern (Mitchell et al., of osteoderms (fixed and mobile) covering the head, body, and tail 2016), the high level of disagreement between the two data par- (Vizcaíno & Loughry, 2008). Cingulates include extant and extinct titions may call into question the phylogenetic signal provided by armadillos, among them the four extant subfamilies Dasypodinae, morphological matrices on cingulates. Euphractinae, Tolypeutinae, and Chlamyphorinae, as well as the External cranial and postcranial skeletal anatomy are already extinct glyptodonts, a group of herbivorous and large- bodied mam- well known for many groups within Cingulata, but the internal cra- mals appearing in the late Eocene and disappearing at the beginning nial anatomy remains understudied. However, its study has already of the Holocene (Delsuc et al., 2016; see also Gaudin & Lyon, 2017 provided data of systematic interest for both the extant and extinct for an alternative classification). The phylogenetic position of glypt- xenarthran diversity (Billet et al., 2015; Billet et al., 2017; Boscaini odonts within Cingulata is particularly difficult to resolve based on et al., 2020; Boscaini et al., 2018; Fernicola et al., 2012; Tambusso morphological data because of their highly specialized anatomy and & Fariña, 2015a; Tambusso & Fariña, 2015b; Tambusso et al., 2021; the large morphological gap separating them from extant armadillos Zurita et al., 2011). Intracranial osseous canals provide important (Burmeister, 1874; Carlini & Zurita, 2010; Fariña et al., 2013). This pathways for innervation and vascularization of the head (Evans & difficulty was recently emphasized by ancient DNA studies showing de Lahunta, 2012). The diversity and phylogenetic signal of their in- that phylogenetic analyses of their mitogenomes support a position tracranial trajectories are poorly known, as these hidden structures for glyptodonts at odds with that proposed in prior morphological are rarely described in mammals, in general, including xenarthrans studies (Billet et al., 2011; Delsuc et al., 2016; Engelmann, 1985; (e.g., Wible & Gaudin, 2004). In contrast, their external openings on Gaudin & Wible, 2006; Herrera et al., 2017; Mitchell et al., 2016). the cranium are often described and scored in phylogenetic matrices While it has long been accepted that glyptodonts were closely (e.g., 37/131 of cranial characters— Gaudin & Wible, 2006). related to extant armadillos (Huxley, 1864), their exact relationships Here we present a comparative investigation of intracranial os- with the latter were never clearly resolved on the basis of mor- seous canals and cavities in a diverse sample of extant and extinct phological data. Flower (1882) initially proposed that glyptodonts cingulates, including the earliest well- preserved glyptodont crania, were the ancestors of extant armadillos but Ameghino (1884, 1889) using X- ray microtomography. The 3D virtual reconstruction of se- disputed this hypothesis, arguing that their great dental and post- lected canals and cavities related to cranial vascularization, innerva- cranial complexity, as described by Owen (1839), was evidence of tion, or upper tooth insertion enabled us to compare the locations, their derived nature. The nested position of glyptodonts among trajectories, and shape of each homologous structure and discuss extant armadillos has been supported by many authors since then, their potential interest for cingulate systematics. We tentatively re- including by recent phylogenetic analyses using morphological data constructed the evolutionary history of these traits using a molecu- (Billet et al., 2011; Castellanos, 1932, 1959; Fernicola, 2008; Gaudin larly constrained phylogeny, and we discuss the potential effects of & Wible, 2006; Herrera et al., 2017; Hoffstetter, 1958; Patterson development and allometry on their variation. These comparisons & Pascual, 1972). However, the consensus stops here. Engelmann allowed us to propose new potential characters that may be used (1985) proposed a close relationship of glyptodonts with the ex- to further explore the
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