Hostname: page-component-76dd75c94c-28gj6 Total loading time: 0 Render date: 2024-04-30T07:30:32.479Z Has data issue: false hasContentIssue false
  • English
  • Français

The incubatory chamber of marsupial carditids (Bivalvia: Carditidae: Thecaliinae) as an exaptation

Published online by Cambridge University Press:  19 March 2021

Damián Eduardo Pérez Open the ORCID record for Damián Eduardo Pérez [Opens in a new window]  and
Ignacio María Soto
Damián Eduardo Pérez*
Affiliation:
Instituto Patagónico de Geología y Paleontología (IPGP CCT CONICET-CENPAT), Boulevard Brown 2915, U9120CD, Puerto Madryn, Chubut, Argentina. E-mail: trophon@gmail.com
Ignacio María Soto
Affiliation:
Grupo de Biología Integral de Sistemas Evolutivos, Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, UBA, and CONICET-Instituto de Ecología, Genética y Evolución de Buenos Aires, CABA, Argentina. E-mail: soto@ege.fcen,uba.ar
*
*Corresponding author.
Get access Rights & Permissions [Opens in a new window]

Abstract

Marsupial carditids of the subfamily Thecaliinae are characterized by the presence of an “incubatory chamber” in female shells, where the eggs hatch and develop during their first stages. According to recent phylogenetic studies, Thecaliinae are closely related to Carditinae, a group that has a byssal gape. This structure occurs in the same area as the incubatory chamber, and both structures could be evolutionarily related. Using the newest phylogenetic context for the subfamilies, we test whether the incubatory chamber of Thecaliinae is related to characters present in Carditinae. We also provided a more precise definition of the implied structures. Two distinct morphologies for the incubatory chamber are described: one with an exteriorly opened pouch (present in the genera Powellina and Milneria) and the other with a completely internal funicular infold (present in Thecalia). The byssal gape is present in the Cardiobyssata clade (Carditamerinae + (Carditinae + Thecaliinae)), and we discuss whether the incubatory chamber could be the result of an exaptation event, and the possible evolutionary pathways implied. According to the present evidence, we propose a co-optation of the byssal gape into a new function (brooding of larvae) at some point during the transition from the Carditinae to the Thecaliinae lineages, thus determining an exaptation. Adaptative processes probably modified this structure into the incubatory chamber (an external pouch first, and a funicular infold later). We discuss alternative scenarios and implications on phylogenetic studies and the importance of considering non-adaptative evolutionary scenarios in the study of evolutionary narratives.

Type
Articles
Information
Paleobiology , Volume 47 , Issue 3 , August 2021 , pp. 503 - 516
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adams, A., and Angas, G. F.. 1864. Descriptions of new species of shells, chiefly from Australia, in the collection of Mr. Angas. Proceedings of the Zoological Society of London 1864:35–40.Google Scholar
Adams, H., and Adams, A.. 1857. The genera of recent mollusks arranged according to their organization, Vol. 2. Reeve & Benham, London.Google Scholar
Armbruster, W. S. 1997. Exaptations link evolution of plant-herbivore and plant-pollinator interactions: a phylogenetic inquiry. Ecology 78:1661–1672.Google Scholar
Arnold, E. N. 1994. Investigating the origin of performance advantage: adaptation, exaptation and lineage effects. Pp. 123–168 in Eggleton, P. and Vane-Wright, R., eds. Phylogenetics and ecology. Academic Press, London.Google Scholar
Baum, D., and Larson, A.. 1991. Adaptation reviewed: a phylogenetic methodology for studying character macroevolution. Systematic Zoology 40:1–18.CrossRefGoogle Scholar
Blackburn, D. 2002. Use of phylogenetic analysis to distinguish adaptation from exaptation. Behavioral and Brain Sciences 25:507–508.CrossRefGoogle Scholar
Bruguière, J. G. 1792. Encyclopédie méthodique ou par ordre de matières. Histoire naturelle des vers, Vol. 1. Pancoucke, Paris.Google Scholar
Carter, J., Harries, P., Malchus, N., Sartori, A., Anderson, L., Bieler, R., Bogan, A., Coan, E., Cope, J., Cragg, S., García-March, J., Hylleberg, J., Kelley, P., Kleeman, K., Kříž, J., McRoberts, C., Mikkelsen, P., Pojeta, J. Jr., Tëmkin, I., Yancey, T., and Zieritz, A.. 2012. Illustrated glossary of the Bivalvia. Part N (revised), vol. 1, chap. 31. Treatise Online 48:1–209.Google Scholar
Chavan, A. 1969. Superfamily Carditacea Fleming, 1920. Pp. N543–N561 in Moore, R. C., ed. Mollusca 6, Bivalvia, Vol. 2. Part N of R. C. Moore, ed. Treatise on invertebrate paleontology. Geological Society of America, New York, and University of Kansas, Lawrence.Google Scholar
Coan, E. V. 1974. Is there double trouble in marsupial clams? The Veliger 17:183–184.Google Scholar
Coan, E. V. 1977. Preliminary review of the northwest American Carditidae. The Veliger 19:375–386.Google Scholar
Coe, W. R. 1943. Sexual differentiation in mollusks. I. Pelecypods. Quarterly Review of Biology 18:154–164.CrossRefGoogle Scholar
Conrad, T. A. 1838. Fossils of the Tertiary Formations of the United States. E.G. Dorsey, Philadelphia.Google Scholar
Conrad, T. A. 1867. Description of a new genus of Astartidae. American Journal of Conchology 3:191.Google Scholar
Cossmann, M., and Peyrot, A.. 1912. Conchologie Néogènique de l'Aquitaine. Actes de la Société Linnéenne de Bordeaux 66:121–324.Google Scholar
Cox, L. R. 1969. General features of Bivalvia. Pp. N2–N129 in Moore, R. C., ed. Mollusca 6, Bivalvia, Vol. 1. Part N of R. C. Moore, ed. Treatise on invertebrate paleontology. Geological Society of America, New York, and University of Kansas, Lawrence.Google Scholar
Dall, W. H. 1871. Descriptions of sixty new forms of mollusks from the West Coast of North America and the North Pacific Ocean, with notes on others already described. American Journal of Conchology 7:93–159.Google Scholar
Dall, W. H. 1881. American work in the department of recent Mollusca during the year 1880. American Naturalist 15:704–718.CrossRefGoogle Scholar
Dall, W. H. 1890. Contributions to the Tertiary fauna of Florida, Part 3. Transactions of the Wagner Free Institute of Science of Philadelphia 3:475–565.Google Scholar
Dall, W. H. 1902. Synopsis of the Carditacea and of the American species. Proceedings of the Academy of Natural Sciences of Philadelphia 53:696–716.Google Scholar
Dall, W. H. 1903. Contributions to the Tertiary fauna of Florida with special reference to the Silex Beds of the Caloosahatchie River, Part IV. Transactions of the Wagner Free Institute of Science of Philadelphia 3:1219–1654.Google Scholar
Dall, W. H. 1916. Diagnoses of new species of marine bivalve mollusks from the northwest coast of America in the collection of the United States National Museum. Proceedings of the United States National Museum 52:393–417.CrossRefGoogle Scholar
Dall, W.H., Bartsch, P., and Rehder, H.. 1938. A manual of the recent and fossil marine pelecypod molluscs of the Hawaiian Islands. Bernice P. Bishop Museum Bulletin 153:1–233.Google Scholar
Darwin, C. 1872. The origin of species by means of natural selection, or the preservation of favoured races in the struggle for life, 6th ed. John Murray, London.Google Scholar
del Río, C. J. 1995. Sexual dimorphism in the Tertiary carditid Venericardia inaequalis (Philippi) (Argentina). Anales de la Sociedad Científica Argentina 226:103–114.Google Scholar
de Pinna, M. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367–394.CrossRefGoogle Scholar
Deshayes, G. P. 1854. Descriptions of twenty new species of the genus Cardita from the collection of Hugh Cuming, Esq. Proceedings of the Zoological Society of London 20:100–103.Google Scholar
Dillwyn, L. W. 1817. A descriptive catalogue of Recent shells, arranged according to the Linnean method; with particular attention to the synonymy, Vol. 1. John and Arthur Arch, London.Google Scholar
Dockery, D. III. 1997, Carditamera williamsi, a new species from the Late Eocene of Mississippi. Mississippi Geology 18:57–60.Google Scholar
Dunker, W. 1860. Neue japanische Mollusken. Malakozoologische Blätter 6:221–240.Google Scholar
Férussac, A. 1822. Tableaux systématiques des animaux mollusques classés en familles naturelles, dans lesquels on a établi la concordance de tous les systèmes; survis d'un prodrome général por tous les mollusques terrestres ou fluviátiles, vivants ou fossiles. Chez Arthus Bertrand, Paris.Google Scholar
Finlay, H. 1926. A further commentary on New Zealand molluscan systematics. Transactions and Proceedings of the Royal Society of New Zealand 57:320–485.Google Scholar
Gmelin, J. F. 1791. Vermes. Pp. 3021–3910 in Gmelin, J. F., ed. Caroli a Linnaei Systema Naturae per Regna Tria Naturae, Ed. 13, Tome 1(6). G.E. Beer, Leipzig.Google Scholar
González, V. L., and Giribet, G.. 2015. A multilocus phylogeny of archiheterodont bivalves (Mollusca, Bivalvia, Archiheterodonta). Zoologica Scripta 44:41–58.CrossRefGoogle Scholar
Gould, S. J. 2002. The structure of the evolutionary theory. Belknap Press, Cambridge.CrossRefGoogle Scholar
Gould, S. J., and Lewontin, R.. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London B 205:581–598.Google Scholar
Gould, S. J., and Vrba, E. S.. 1982. Exaptation—a missing term in the science of form. Paleobiology 8:4–15.CrossRefGoogle Scholar
Grant, T., and Kluge, A.. 2004. Transformation series as an ideographic character concept. Cladistics 20:23–31.CrossRefGoogle Scholar
Gray, J. 1828. On the nursing pouch or chamber of the Chama concamerata of Gmelin. The Philosophical Magazine, 2nd series, 3:117.CrossRefGoogle Scholar
Harvey, M. 1995. Reproduction in Carditamera floridana (Conrad) (Bivalvia: Carditidae). Ph.D. thesis. Department of Biological Science, Florida State University, Tallahassee, Fla.Google Scholar
Heaslip, W. G. 1968. Cenozoic evolution of the alticostate venericards in Gulf and East Coastal North America. Palaeontographica Americana 6:55–135.Google Scholar
Heaslip, W. G. 1969. Sexual dimorphism in bivalves. Pp. 61–75 in Westermann, G. E. G., ed. Sexual dimorphism in fossil Metazoa and taxonomic implications. Series A1. International Union of Geological Sciences, Prague.Google Scholar
Heinberg, C. 1993. Birkelundita, a new genus (Bivalvia, Carditacea) from the Upper Cretaceous white chalk of Europe. Bulletin of the Geologic Society of Denmark 40:185–195.CrossRefGoogle Scholar
Huber, M. 2010. Compendium of bivalves. A full-color guide to 3.300 of the world's marine bivalves. A status on Bivalvia after 250 years of research. ConchBooks, Hackenheim, Germany.Google Scholar
Jones, G. F. 1963. Brood protection in three southern California species of the pelecypod Cardita. Wasman Journal of Biology 21:141–148.Google Scholar
Kauffman, E., and Buddenhagen, C. H.. 1969. Protandric sexual dimorphism in Paleocene Astarte (Bivalvia) of Maryland. Pp. 76–93 in Westermann, G. E. G., ed. Sexual dimorphism in fossil Metazoa and taxonomic implications. Series A1. International Union of Geological Sciences, Prague.Google Scholar
Lamarck, J. P. B. A. de. 1819. Histoire naturelle des animaux sans vertèbres, Vol. 6, Part 1. Paris.Google Scholar
Lamy, E. 1922. Révision des Carditacea vivants du Muséum National d'Histoire Naturelle de Paris. Journal of Conchyliology 66:218–276.Google Scholar
Linnaeus, C. 1758. Systema naturae per regnatria naturae. Edition decima, reformata. Holmiae, Impensis Direct. Laurentii Salvii, Stockholm.Google Scholar
Maddison, W. P., and Maddison, D. R.. 2017. Mesquite: a modular system for evolutionary analysis, Version 3.2. http://mesquiteproject.org.Google Scholar
McLennan, D. 2008. The concept of co-option: Why evolution often looks miraculous. Evolution & Education Outreach 1:247–258.CrossRefGoogle Scholar
Megerle von Mühlfeld, J. C. 1811. Entwurf eines neuen Systems der Schaltiergeh€ause. Magazin f€ur die neuesten Entdecklungen in der gesammten Naturkunde von der Gesellschaft Naturforschaft Freunde zu Berlin 5:38–72.Google Scholar
Mivart, G. J. 1871. On the genesis of species. MacMillan and Co., London.CrossRefGoogle Scholar
Olsson, A. 1961. Mollusks of the tropical eastern Pacific particularly from the southern half of the Panamic-Pacific faunal province (Panamá to Perú). Paleontological Research Institution, Ithaca, N.Y.Google Scholar
Pérez, D. E. 2019. Phylogenetic relationships of the family Carditidae (Bivalvia: Archiheterodonta). Journal of Systematic Palaeontology 17:1139–1175.CrossRefGoogle Scholar
Pérez, D. E., and del Río, C.. 2017. Systematics of the family Carditidae (Bivalvia: Archiheterodonta) in the Cenozoic of Argentina. Zootaxa 4338:51–84CrossRefGoogle ScholarPubMed
Pérez, D. E., and Giachetti, L.. 2020. Is Cyclocardia (Conrad) a wastebasket taxon? Exploring the phylogeny of the most diverse genus of the Carditidae (Archiheterodonta, Bivalvia). Palaeontology 63:477–495.CrossRefGoogle Scholar
Pérez, D. E., Alvarez, M., and del Río, C.. 2017. Un posible caso de dimorfismo sexual en “Venericardia” patagonica (Sowerby, 1846) (Bivalvia: Carditidae). Revista Brasileira de Paleontología 20:195–202.CrossRefGoogle Scholar
Ramirez, M. 2007. Homology as a parsimony problem: a dynamic homology approach for morphological data. Cladistics 23:588–612.Google Scholar
Reeve, L. A. 1843. Conchologia Iconica. London.Google Scholar
Röding, P. F. 1798. Museum Boltenianum sve catalogus cimeliorum e tribus regn is naturae quae olim collegerat. Pars Secunda Contineus conchylis sive testacea univalvia, bivalvia et mult ivalvia. Joa. Fried. Bolten M.D. p.d., Hamburg.Google Scholar
Rudwick, M. 1964. Brood pouches in the Devonian brachiopod Uncites. Geological Magazine 101:329–333.CrossRefGoogle Scholar
Sacco, F. 1899. I Molluschi dei terreni terziarii del Piemonti e della Liguria, Parte XXVII (Unionidae, Carditidae, Astartidae, Crassatellidae, Lasaeidae, Galeommidae, Cardiidae, Limnocardiidae e Chamidae). Carlo Clausen, Turin.Google Scholar
Schneider, J. 1993. Brooding of larvae in Cardita aviculina Lamarck, 1819 (Bivalvia: Carditidae). The Veliger 36:94–95.Google Scholar
Smith, E. A. 1885. Report on the Lamellibranchiata collected by HMS Challenger during the years 1873–1876. Reports of the scientific results of the voyage of H.M.S. “Challenger.” Zoology 1335:1–341.Google Scholar
Sowerby, G.B. I 1833, Descriptions of new species of shells from the collection formed by Mr. Cuming on the western coast of South America, and among the islands of the southern Pacific Ocean. Proceedings of the Committee of Science and Correspondence of the Zoological Society of London 2:194–202.Google Scholar
Stanley, S. 1975. Adaptative themes in the evolution of the Bivalvia (Mollusca). Annual Review of Earth and Planetary Sciences 3:165–212.CrossRefGoogle Scholar
Stenzel, H. B., and Krause, E. K.. 1957. Pelecypoda from the type locality of the Stone City beds (Middle Eocene) of Texas. Texas University Publication 5704:1–237.Google Scholar
Thiele, G. 1935. Handbuch der systematischen Weichtierkunde. Teil 3:779–1022. G. Fischer, Jena.Google Scholar
Vermeij, G. 2013. Molluscan marginalia: hidden morphological diversity at the bivalve shell edge. Journal of Molluscan Studies 79:283–295.CrossRefGoogle Scholar
Yonge, C. M. 1969. Functional morphology and evolution within the Carditacea (Bivalvia). Proceedings of the Malacological Society of London 38:493–597.Google Scholar