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Untangling the diversity and evolution of tentacles in scallops, oysters, and their relatives (Bivalvia: Pteriomorphia)

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Abstract

Tentacles are fascinating, multifunctional organs found in many aquatic invertebrate groups. In bivalves, tentacles are morphologically diverse, performing protective and sensory roles in taxa from different ecological niches. Such diversity is particularly accentuated in Pteriomorphia, a clade comprising scallops, oysters, file clams, and relatives. However, little is known about the evolution of these organs and their role in bivalve radiation. To test hypotheses of convergent tentacular evolution and a possible association between tentacles and body orientation on the substrate, we first examined tentacle morphology in 108 preserved species representing 15 families across Pteriomorphia. Morphological descriptions of tentacle type (inner mantle fold tentacles, IFT; middle mantle fold tentacles, MFT) and position (marginal and submarginal) are provided, expanding the knowledge of less studied bivalve taxa. Then, we placed the morphological dataset under a molecular phylogenetic framework to estimate ancestral states. IFT had likely four independent origins, while MFT emerged twice independently. After being gained, tentacles have not been lost. In addition, evolution of MFT coincides with transitions in body position with the midsagittal plane parallel to the substrate in the clades of scallops (Pectinida) and oysters (Ostreida). Such a shift could be related to the increase of mantle exposure, favoring the emergence of serially repeated organs, such as tentacles. Altogether, our results support the convergent evolution of tentacles across different taxonomic levels, corroborating the plasticity of the molluscan body and the relevance of evolutionary convergences in the radiation of bivalves.

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Data availability

All data generated or analyzed during this study are included in this article (Table 1) and its supplementary information (Online Resources 1–3). Phylogenetic tree used in the study is publicly archived in Dryad under the DOI https://doi.org/10.5061/dryad.pk0p2ngjp.

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Acknowledgments

The authors acknowledge the grants 2015/09519-4 and 2017/01365-3, São Paulo Research Foundation (FAPESP) (to JAA and JEARM), and the National Science Foundation (DEB 1754331) (to JMS). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 (to JAA and JEARM). This study is part of the first author’s Doctorate’s thesis through the Graduate Program in Zoology of the Institute of Biosciences (University of São Paulo). The authors thank the following institutions that provided materials for the development of this study: Museum of Comparative Zoology (MCZ), Museum of Zoology “Prof. Adão José Cardoso” of the University of Campinas (ZUEC), Museum of Zoology of the University of São Paulo (MZSP), Santa Barbara Museum of Natural History (SBMNH), and Smithsonian National Museum of Natural History (USNM). The authors also acknowledge the helpful comments and suggestions provided by Dr. Reuben Shipway and an anonymous reviewer. This is a contribution of NP-BioMar (Research Center for Marine Biodiversity – USP).

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São Paulo Research Foundation (FAPESP), grant 2015/09519-4 and 2017/01365-3. Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. National Science Foundation (NSF), grant DEB 1754331.

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  1. Department of Zoology, University of São Paulo, Rua do Matão, Travessa 14, n. 101, São Paulo, São Paulo, 05508-090, Brazil

    Jorge A. Audino & José Eduardo A. R. Marian

  2. Department of Ecology, Evolution and Organismal Biology, Iowa State University, 2200 Osborn Dr., Ames, IA, 50011, USA

    Jeanne M. Serb

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Jorge A. Audino. The first draft of the manuscript was written by Jorge A. Audino, and all authors commented on and edited previous versions of the manuscript. All authors read and approved the final manuscript.

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Supplementary information

Online Resource 1

Character codes and states used for ancestral state estimations for sequenced species in the pteriomorphian phylogeny. (PDF 124 kb)

Online Resource 2

Table with the likelihood ratio test (LRT) between the symmetrical model (Symm; equal transition rates) and the asymmetrical model (Asymm; different transition rates) applied to our dataset. (PDF 72.5 kb)

Online Resource 3

Evolution of lateral branches on inner fold tentacles in pearl oysters and relatives. The clade Pterioidea is indicated by the gray box. Lateral branches on the inner fold tentacles (in blue) were acquired twice in the family Margaritidae, represented by the genus Pinctada, and in Pteriidae, represented by Pteria. Likelihood proportions for ancestral states are indicated in pie charts. (TIF 11720 kb)

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Audino, J.A., Serb, J.M. & Marian, J.E.A.R. Untangling the diversity and evolution of tentacles in scallops, oysters, and their relatives (Bivalvia: Pteriomorphia). Org Divers Evol 21, 145–160 (2021). https://doi.org/10.1007/s13127-021-00482-3

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