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The inner ear of caviomorph rodents: Phylogenetic implications and application to extinct West Indian taxa

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Abstract

With their past and current diversities, West Indian caviomorph rodents dominate the terrestrial mammalian fauna of the Caribbean archipelago. Many of these species have recently become extinct, including the emblematic giant forms known as Heptaxodontidae. The higher-level systematics and content of this family have been widely disputed over the last decades (i.e., membership in Cavioidea vs. Chinchilloidea vs. Octodontoidea). Here we analyzed the phylogenetic signal provided by several characters of the caviomorph inner ear to adress the phylogenetic affinities of the West Indian heptaxodontids. For this, we assembled an exhaustive taxonomic sampling (N = 100) of extant North and South American caviomorphs (including representatives of all families) and a wide array of West Indian forms among octodontoid echimyids (extant and extinct capromyines, as well as extinct heteropsomyines), and some heptaxodontid subfossil taxa such as Amblyrhiza, Clidomys, and Elasmodontomys. Geometric morphometrics and comparative phylogenetic methods were employed to explore shape differences of the inner ear and their potential systematic implications. Our results show that: (1) allometry is a major contributor to shape variation in the bony labyrinth; (2) shape variation bears a strong phylogenetic signal, providing diagnostic characters for Caviidae and Erethizontoidea; and (3) Amblyrhiza and Clidomys are morphologically closer to Chinchilloidea with which they have potential phylogenetic affinities. Elasmodontomys remains a problematic taxon as it exhibits inner ear features that are consistent with either Chinchilloidea or Octodontoidea, depending on how the allometric component is evaluated.

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Data availability

The landmark coordinates data and R code used for the GMM analyses are available on GitHub (https://github.com/Lea-dcnh/2023_Caviomorpha_InnerEar). The 3D surfaces models of Amblyrhiza, Clidomys, and Elasmodontomys are available on MorphoMuseuM (https://doi.org/10.18563/journal.m3.196). The remaining 3D surfaces will be used for further analyses and are available upon request to the corresponding author.

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Acknowledgments

Thanks to B. Clark, V. Fernández, and R. P. Miguez for access to the mammal collections and the computed tomography facilities at the Natural History Museum of London. We thank the curators and collection managers at AMNH, NHM, CBGP, FLMNH, MNHN, USNM, and head of the Digital Imaging Division (FLMNH) for access to specimens and sometimes scanning for us. Thanks to Anne-Claire Fabre, Sérgio Ferreira Cardoso, and Quentin Martínez for their fruitful discussions and helping with the scanning of important specimens while they were visiting the Natural History Museum of London. Thanks to Andrés Rinderknecht for sharing his medical scan of Josephoartigasia monesi to attempt the extraction of its inner ear shape morphology. Marcelo R. Sánchez-Villagra, Alexandra Wegmann, Gabriel Aguirre Fernández, and Jorge D. Carrillo Briceño for helping us scanning the specimens housed at PIMUZ. We thank the 3D data repositories morphosource, DigiMorph, and their contributors. Three-dimensional data acquisitions were performed using the micro-computed tomography (μCT) facilities of the MRI platform member of the national infrastructure France-BioImaging supported by the French Agence Nationale de la Recherche (Grant ANR-10-INBS-04, “Investissements d’Avenir”), and those of the Laboratoire d’Excellence (LabEx) Centre Méditerranéen de l’Environnement et de la Biodiversité (LabEx CeMEB, ANR10-LABX-0004). Finally, we thank the two anonymous reviewers for their insightful comments that enhanced the final version of the manuscript. This is ISEM publication n° 2023-116 SUD.

Funding

This research was supported by the Synthesis of Systematic Resources (SYNTHESYS) project, which is financed by the European Community Research Infrastructure Action (FP7: Grants GB-TAF-5737, GB-TAF-6945, and GB-TAF-1316 to the National History Museum of London), by the French Agence Nationale de la Recherche (Grants DS10, ANR-17-CE02-0005 RHINOGRAD), the LabEx CEBA (ANR-10-LABX-25-01; projects PEPS, adaptation, adaptabilité SHREWNOSE, and EMERGENCE). This work was initiated in the framework of the GAARAnti project (ANR-17-CE31-0009).

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Contributions

LDC, RL, LM and PHF conceived the study. LWVL, LK and PHF collected CT-scan data and LDC segmented and conducted morphometric analyses with assistance of LH, PHF and RL. LWVL, JVJ, POA, MB and LM collected and identified field specimens and provided paleontological information. LWVL, RDEM, LK, JVJ, POA, MB, LH and RL supplied specimens information, identifications and commentary on the manuscript. LDC, LM and PHF wrote the manuscript with inputs from all authors.

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Correspondence to Léa Da Cunha.

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The authors declare no competing interests.

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Da Cunha, L., Viñola-López, L.W., MacPhee, R.D.E. et al. The inner ear of caviomorph rodents: Phylogenetic implications and application to extinct West Indian taxa. J Mammal Evol 30, 1155–1176 (2023). https://doi.org/10.1007/s10914-023-09675-3

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