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Incisor enamel microstructure of West Indian caviomorph hystricognathous rodents (Octodontoidea and Chinchilloidea)

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Abstract

Analysis of the incisor enamel microstructure of extinct and extant West Indian caviomorph rodents emphasizes a clear microstructural distinction between the Echimyidae (Capromyinae and Heteropsomyinae) among Octodontoidea and the “Heptaxodontidae”, whose phylogenetic affinities are debated. All capromyines and heteropsomyines have a pattern of enamel characterized by a rectangular crystallite arrangement, which is biomechanically strongest in limiting crack propagation most efficiently (subtype [Sbt.] 3 of multiserial Hunter-Schreger bands [HSBs]). This enamel condition is exclusive to all mainland octodontoids. In stark contrast, “heptaxodontids” sampled here exhibit much less derived enamel subtypes of multiserial HSBs, with parallel to acute angular crystallite arrangement (Sbt. 1 [Clidomys], Sbt. 1–2 [Elasmodontomys], and low acute Sbt. 2 [Amblyrhiza]), less well adapted for prevention of crack propagation. The incisor enamel microstructure of Amblyrhiza and Clidomys is consistent with a chinchilloid assignment, as reflected by the anatomy of their auditory region and their unusual dental pattern. For Elasmodontomys, the primitive condition of its incisor enamel is difficult to reconcile with its highly nested phylogenetic position within the Octodontoidea clade (among the Capromyinae), as recently inferred from aDNA analyses. The different enamel patterns among extinct and extant West Indian caviomorphs indicate distinct high-level taxonomic groups, but restricted to the Octochinchilloi (Octodontoidea and Chinchilloidea) among Caviomorpha. The great diversity of caviomorphs on the Caribbean islands resulted from intra-archipelago diversification through time, but their high-level phylogenetic diversity can only be explained by distinct sources, implying de facto multiple (potentially time-staggered) natural colonizations of the West Indies. The chinchilloid-compatible enamel and dental pattern characterizing Borikenomys from lower Oligocene deposits in Puerto Rico strongly suggest a link with some of the recently-extinct “heptaxodontids”, which would substantiate their much greater antiquity in the Caribbean islands.

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Data availability statement

Incisor specimens analyzed (polished cross sections and remaining parts of incisors) during the current study are available from the institutions that provided them (see specimen catalog numbers). The figured and extra SEM micrographs generated and analyzed during the current study are available from the corresponding author upon reasonable request.

Notes

  1. Chinchilloidea in its modern view, i.e., including Chinchillidae (Chinchillinae and Lagostominae), Dinomyidae and fossil kinds, and all the extinct close relatives, notably the giant neoepiblemids (e.g., Kramarz et al. 2013; Kerber et al. 2017, 2018, 2019; Rinderknecht et al. 2018; Boivin et al. 2019a; Rasia et al. 2021).

  2. “Ancient DNA suggests single colonization and within-archipelago diversification of Caribbean caviomorph rodents” (Woods et al. 2020).

  3. The dental pattern of Clidomys is much more reminiscent of that of neoepiblemid chinchilloids (i.e., laminar pattern but without heterogeneity of the enamel layer).

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Acknowledgements

We are indebted to Jonathan I. Bloch (Florida Museum of Natural History, Gainesville, USA) for access to the paleontological collections of his institute, as well as S. Diaz Franco (Cuba) for the donation of his collection to one of us (LWVL). Many thanks to Thomas Martin (Universität Bonn, Germany) for his useful advice regarding the enamel microstructure of rodent incisors and for sharing enamel microstructure data over the last few decades. We are very grateful to our fossil preparator, Anne-Lise Charruault (ISE-M, France), for her availability and for the preparation and handling of the epoxy resin for the embedding of the incisor specimens, as well as for the access to the polishing facilities of the lab. We warmly thank Chantal Cazevieille (Institut des Neurosciences de Montpellier [INM], France) for access to an electron microscope scanning facility, and also for her welcome and much appreciated help in obtaining detailed images of enamel microstructures. Thank you very much to Odile Maincent (Devé, Saint-Barthélemy, French West Indies) for her hospitality and help during our successive field seasons in Saint-Barth, and for her great interest in our work. We extend our gratitude to Iván Quintero and Ángel Acosta-Colón for assistance with localities in Puerto Rico. We are also grateful to our colleagues François Pujos (IANIGLA, Mendoza, Argentina), Hernán Santos-Mercado (UPRM, Mayagüez, Puerto-Rico), Eduardo J. Cruz (UPRM, Puerto Rico), our late colleague and friend Gilles Merzeraud (Géosciences Montpellier, France), Mélody Philippon and Jean-Jacques Cornée (Géosciences Montpellier & Pointe-à-Pitre [Guadeloupe, French West Indies]), who contributed to some of the fieldwork seasons in Puerto Rico and Saint-Barthélemy in the framework of the GAARAnti project. Finally, we thank Thomas Martin (Universität Bonn, Germany), Daniela Kalthoff (Associate Editor; The Swedish Museum of Natural History, Sweden) and another anonymous reviewer, who provided formal reviews of this manuscript that enhanced the final version. This is ISE-M publication 2022-188 Sud.

Funding

This research was supported by the French Agence Nationale de la Recherche (ANR) in the framework of the GAARAnti project (ANR-17-CE31-0009) and LabEx CEBA (ANR-10-LABX-25–01).

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Marivaux, L., López, L.W.V., Boivin, M. et al. Incisor enamel microstructure of West Indian caviomorph hystricognathous rodents (Octodontoidea and Chinchilloidea). J Mammal Evol 29, 969–995 (2022). https://doi.org/10.1007/s10914-022-09631-7

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