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Unveiling the neuroanatomy of Josephoartigasia monesi and the evolution of encephalization in caviomorph rodents

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Abstract

Caviomorph rodents are an exceptional model for studying the effects of ecological factors and size relations on brain evolution. These mammals are not only speciose and ecologically diverse but also present wide body size disparity, especially when considering their fossil relatives. Here, we described the brain anatomy of the largest known rodent, Josephoartigasia monesi, uncovering distinctive features within this species regarding other taxa. Albeit resembling extant pacarana Dinomys branickii, J. monesi stands out due to its longer olfactory tract and well-developed sagittal sinus. Challenging the previous hypothesis that giant rodents possessed comparatively smaller brains, we found that J. monesi and another giant extinct rodent, Neoepiblema acreensis, are within the encephalization range of extant caviomorphs. This was unraveled while developing the a Phylogenetic Encephalization Quotient (PEQ) for Caviomorpha. With PEQ, we were able to trace brain-size predictions more accurately, accounting for species-shared ancestry while adding the extinct taxa phenotypic diversity into the prediction model. According to our results, caviomorphs encephalization patterns are not the product of ecological adaptations, and brain allometry is highly conservative within the clade. We challenge future studies to investigate caviomorphs encephalization within different taxonomic ranks while increasing the sampled taxa diversity, especially of extinct forms, in order to fully comprehend the magnitude of this evolutionary stasis.

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Data availability

The article’s supporting data and R scripts can be found in the Supporting Material and at the git-hub repository (https://github.com/jbubadue/Ferreira_et_al_Jmonesi).

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Acknowledgements

We thank Alexandra Wegmann, Gabriel Aguirre Fernández, and Jorge D. Carrillo Briceño for helping us scan the specimens, and Lawrence Witmer (Ohio University), Digimorph.org, UTCT, Timothy Rowe, and Jeri Rodgers, for providing scans of caviomorph skulls. We especially thank the reviewers Mary Silcox and Ornella Bertrand for their comments which significantly improved previous versions of this manuscript.

Funding

JDF was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)—Finance Code 001. LFG was supported by Coordenação de Amparo à Pesquisa (CAPES 88882.345599/2019-01 and PrInt 88887.583738/2020-00). JMB is supported by a postdoc fellowship funded by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro—FAPERJ (E-26/204.166/2021 and E-26/204.167/2021), and by the American Society of Mammogists (2023 Oliver Pearson Award). MTD is supported by CONICET 2020 Executing Units Project awarded to the Patagonian Institute of Geology and Paleontology (PUE-IPGP 22920200100014). LK is supported Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 422568/2018-0; 309414/2019-9; 406902/2022-4.), Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (21/2551-0002030-0), and CAPES (PrInt 8881.310240/2018-01).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Biodiversidade Animal, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, Brazil

    José Darival Ferreira

  2. Departamento de Paleontología, Museo Nacional de Historia Natural, Montevideo, Uruguay

    Andrés Rinderknecht

  3. Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, Brazil

    Jamile de Moura Bubadué

  4. Programa de Pós-Graduação em Ecologia, Departamento de Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil

    Luiza Flores Gasparetto

  5. Instituto Patagónico de Geología y Paleontología, CCT CONICET-CENPAT, Puerto Madryn, Argentina

    Maria Teresa Dozo

  6. Deparment of Paleontology, University of Zurich, Zurich, Switzerland

    Marcelo R. Sánchez-Villagra

  7. Centro de Apoio à Pesquisa Paleontológica da Quarta Colônia, Universidade Federal de Santa Maria, São João do Polêsine, Brazil

    Leonardo Kerber

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  1. José Darival Ferreira
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  3. Jamile de Moura Bubadué
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  4. Luiza Flores Gasparetto
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  5. Maria Teresa Dozo
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  6. Marcelo R. Sánchez-Villagra
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  7. Leonardo Kerber
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Contributions

AR performed the scanning of Josephoartigasia’s cranium. LK MRSV and MTD were responsible for scanning comparative specimens. JDF performed the segmentation, 3D modeling, collection of quantitative data, body mass and encephalization estimates. LFG was responsible for gathering the ecological traits. JMB conducted all the statistical analyses. All the authors contributed to the study’s design and the manuscript’s drafting, provided final approval for publication, and agree to be held accountable for the work performed herein.

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Correspondence to Leonardo Kerber.

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We confirm that this work does not violate any ethical or legal aspects of paleontological research. All specimens were analyzed with the permission of the curators of the scientific collections mentioned in the text.

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Ferreira, J.D., Rinderknecht, A., de Moura Bubadué, J. et al. Unveiling the neuroanatomy of Josephoartigasia monesi and the evolution of encephalization in caviomorph rodents. Brain Struct Funct 229, 971–985 (2024). https://doi.org/10.1007/s00429-024-02762-y

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