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Evolutionary Patterns of Mandible Shape Diversification of Caviomorph Rodents

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Abstract

Caviomorphs are a mainly South American rodent clade with high taxonomic and ecomorphological diversity. In this study, we combine geometric morphometric, functional, ancestral reconstruction, and macroevolutionary analyses to quantify the magnitude, direction, and rates of shape diversification of the caviomorph mandible, and to explore the morpho-functional implications and potential ecological catalysts of the observed shape changes. The mandible shape was significantly related to habits and size, and had a better fit with an evolutionary model where the main clades occupy distinct adaptive peaks. The morphological evolution of octodontoids is characterized by pulses of rate acceleration, but without reaching high disparity. Such pulses are mainly linked to the acquisition of fossorial specializations, including short and robust mandibles, and the increasement of forces at incisors. Conversely, derived cavioids show slower but continuous shape changes that allowed them to reach the most divergent, grazing morphologies in which slender mandibles with more marked antero-posterior movements for grinding action are favored. Interestingly, the major morphological changes occurred mainly during the early Oligocene and lower late Miocene, two time periods that involved global climatic events and strong changes in the vegetational structure of South America. The evolution of octodontoid and cavioid mandibles seems to be related to the occupation of subterranean and epigean niches, respectively, in the progressively expanded Cenozoic open landscapes of southern South America.

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Acknowledgements

We especially thank P. Teta, G. Cassini, S. Lucero (MACN); D. Romero, N. Martino (MMP), R. Ojeda (IADIZA), R. Bárquez, M. Díaz (CML), M. de Vivo (USP), J. Oliveira (UFRJ), W. Kliem (UFBA), Victor Pacheco (MUSM), and B. Patterson (FMNH) for granting access to osteological materials under their care. We thank S. Vizcaíno for suggestions on an early version of the manuscript. We thank S. Catalano, H. Morlon, F. Condamine, and I. Perez for help with methods. To Guest Editor G. Cassini, P. Cox, and an anonymous reviewer for their comments that greatly improved the original manuscript. The authors thank Sergio Vizcaíno, Néstor Toledo, and Guillermo Cassini for their invitation to participate in the Symposium “El paradigma de correlación forma-función en mastozoología: un tributo a Leonard Radinsky (1937–1985)” in the XXXI Jornadas Argentinas de Mastozoología during November 2018, and in this related special issue.

Funding

This study was funded by ANPCyT PICT-2016-2881 and UNLP 11/N822 grants. We thank CONICET and Fulbright Commission, and IOM, for financial support for visiting the FMNH collections.

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Authors and Affiliations

  1. Instituto de Ecorregiones Andinas (INECOA), UNJu, CONICET, IdGyM, Av. Bolivia 1661, Y4600GNE, San Salvador de Jujuy, Jujuy, Argentina

    Alicia Álvarez & Marcos D. Ercoli

  2. Sección Mastozoología, Museo de La Plata. Paseo del Bosque s/n, CONICET, B1900FWA La Plata, Buenos Aires, Argentina

    A. Itatí Olivares, Nahuel A. De Santi & Diego H. Verzi

Authors
  1. Alicia Álvarez
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  2. Marcos D. Ercoli
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  3. A. Itatí Olivares
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  4. Nahuel A. De Santi
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  5. Diego H. Verzi
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Corresponding author

Correspondence to Alicia Álvarez.

Electronic Supplementary Material

Online Resource 1

List of taxa and specimens examined. (RTF 118 kb)

Online Resource 2

Schematized representation of the methodology followed in this study, combining geometric morphometric data, ecological classifications and a time-calibrated tree (i.e., input data, orange plain arrows), and macroevolutionary and morphofunctional analyses (gray stripped arrows). White boxes indicated intermediate data, painted boxes represent results shown and discussed in main text. Functional traits values were used only for PGLS analyses and not for the assessment of evolutionary models. (PDF 547 kb)

Online Resource 3

Landmarks and semilandmarks definitions considered in this contribution (following Álvarez et al. 2020). (RTF 54.9 kb)

Online Resource 4

Phylogeny used in analyses, taken from Álvarez et al. (2017). Numerical codes (HTU) for nodes are shown. (PDF 550 kb)

Online Resource 5

Plot of the two first principal components of the PCA performed on the aligned coordinates exported from TNT, including the terminals and nodes. Phylogenetic relationships at familiar and higher levels (dark green) or between familiar and genus levels (pale green) are illustrated in a phylomorphospace-like graph. Genus and family names are labeled, see numerical codes of Online Resource 4 for other nodes and terminals. See Álvarez et al. (2020) for a detailed explanation of a PCA analysis performed in a similar dataset. (PDF 626 kb)

Online Resource 6

Data for Habitat, Habit and lnCS for each caviomorph species studied. Bibliographic sources for ecological variables are given. (XLS 73 kb)

Online Resource 7

The 95% credible set of 9 shift configurations from the BAMM shape diversification analysis of caviomorph rodents. The breaks method selected to plotting colors was the jenks method. (PDF 361 kb)

Online Resource 8

Values of functional variables analyzed (most anterior insertion of the masseteric muscle, length of coronoid process, length of ventral masseteric crest, height of condylar process). Estimations were made for tree terminals (i.e., extant species) and nodes (ancestral shapes; HTU, see Online Resource 4 for location of each node on the phylogeny). Euclidean distances were estimated taking into account all the Principal Components of a PC analysis carried out on a dataset involving the Procrustes Coordinates obtained from the optimization of mandible shape in TNT. (XLS 136 kb)

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Álvarez, A., Ercoli, M.D., Olivares, A.I. et al. Evolutionary Patterns of Mandible Shape Diversification of Caviomorph Rodents. J Mammal Evol 28, 47–58 (2021). https://doi.org/10.1007/s10914-020-09511-y

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