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Functional or Vestigial? The Genomics of the Pineal Gland in Xenarthra

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Abstract

Vestigial organs are historical echoes of past phenotypes. Determining whether a specific organ constitutes a functional or vestigial structure can be a challenging task, given that distinct levels of atrophy may arise between and within lineages. The mammalian pineal gland, an endocrine organ involved in melatonin biorhythmicity, represents a classic example, often yielding contradicting anatomical observations. In Xenarthra (sloths, anteaters, and armadillos), a peculiar mammalian order, the presence of a distinct pineal organ was clearly observed in some species (i.e., Linnaeus’s two-toed sloth), but undetected in other closely related species (i.e., brown-throated sloth). In the nine-banded armadillo, contradicting evidence supports either functional or vestigial scenarios. Thus, to untangle the physiological status of the pineal gland in Xenarthra, we used a genomic approach to investigate the evolution of the gene hub responsible for melatonin synthesis and signaling. We show that both synthesis and signaling compartments are eroded and were probably lost independently among Xenarthra orders. Additionally, by expanding our analysis to 157 mammal genomes, we offer a comprehensive view showing that species with very distinctive habitats and lifestyles have convergently evolved a similar phenotype: Cetacea, Pholidota, Dermoptera, Sirenia, and Xenarthra. Our findings suggest that the recurrent inactivation of melatonin genes correlates with pineal atrophy and endorses the use of genomic analyses to ascertain the physiological status of suspected vestigial structures.

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Data Availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Electronic Supplementary Materials. Specifically, all analyzed genome assemblies (ESM_1) are publicly available on NCBI. Additional data related to this paper may be requested from the authors.

Code Availability

This paper does not report original code.

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Acknowledgements

We acknowledge the various genome consortiums for sequencing and assembling the genomes.

Funding

This work is a result of the project ATLANTIDA (Grant No. NORTE-01-0145-FEDER-000040), supported by the Norte Portugal Regional Operational Programme (NORTE 2020), under the PORTUGAL 2020 Partnership Agreement and through the European Regional Development Fund (ERDF). One PhD fellowship for author RV (SFRH/BD/144786/2019) was granted by Fundação para a Ciência e Tecnologia (FCT, Portugal) under the auspices of Programa Operacional Regional Norte (PORN), supported by the European Social Fund (ESF) and Portuguese funds (MECTES). FA is supported by ARDITI (Grant No. M1420-09-5369-FSE-000002), OOM (Grant No. M1420-01-0142-FEDER-000001) and FCT through the strategic project UID/MAR/04292/2020.

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Authors and Affiliations

  1. CIMAR/CIIMAR-Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Avenida General Norton de Matos, S/N, 4450-208, Matosinhos, Portugal

    Raul Valente, Isabel Sousa-Pinto, Raquel Ruivo & L. Filipe C. Castro

  2. FCUP-Department of Biology, Faculty of Sciences, University of Porto (U. Porto), Rua Do Campo Alegre, Porto, Portugal

    Raul Valente, Isabel Sousa-Pinto & L. Filipe C. Castro

  3. MARE-Marine and Environmental Sciences Centre, ARDITI, Madeira, Portugal

    Filipe Alves

  4. OOM-Oceanic Observatory of Madeira, Funchal, Portugal

    Filipe Alves

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  1. Raul Valente
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Contributions

RV: Data curation, Formal analysis, Investigation, Methodology, Visualization and Writing—original draft. FA: Writing—review & editing. IS-P: Writing—review & editing. RR: Conceptualization, Methodology, Validation and Writing—review & editing. LFCC: Conceptualization, Methodology, Validation, Supervision, Project administration, Resources and Writing—review & editing.

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Correspondence to L. Filipe C. Castro.

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Valente, R., Alves, F., Sousa-Pinto, I. et al. Functional or Vestigial? The Genomics of the Pineal Gland in Xenarthra. J Mol Evol 89, 565–575 (2021). https://doi.org/10.1007/s00239-021-10025-1

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