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The Evolutionary Diversity of Barnacles, with an Updated Classification of Fossil and Living Forms

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The Evolutionary Diversity of Barnacles, with an Updated Classification of Fossil and Living Forms applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2021, XX, 1–58. With 11 figures. The evolutionary diversity of barnacles, with an updated classification of fossil and living forms Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlaa160/6149353 by guest on 20 April 2021 BENNY K. K. CHAN1, NIKLAS DREYER1,2,3,4,*, , ANDY S. GALE5,6, HENRIK GLENNER7,8, CHRISTINE EWERS-SAUCEDO9, MARCOS PÉREZ-LOSADA10,11, GREGORY A. KOLBASOV12, KEITH A. CRANDALL10,13, and JENS T. HØEG14, 1Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan 2Department of Life Science, National Taiwan Normal University, Taipei, Taiwan 3Biodiversity Program, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan 4Natural History Museum of Denmark, Invertebrate Zoology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark 5School of Earth and Environmental Sciences, University of Portsmouth, Burnaby Building, Burnaby Road, Portsmouth PO1 3QL, UK 6Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW75BD, UK 7Marine Biodiversity Group, Department of Biology, University of Bergen, Bergen, Norway 8Center for Macroecology, Evolution and Climate, GLOBE Institute, University of Copenhagen, DK-2100, Copenhagen, Denmark 9Zoologisches Museum, Christian-Albrechts Universität zu Kiel, Kiel, Germany 10Computational Biology Institute, Department of Biostatistics and Bioinformatics, George Washington University, Washington, DC 20052, USA 11CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Universidade do Porto, Campus Agrário de Vairão, Vairão 4485-661, Portugal 12White Sea Biological Station, Biological Faculty of Moscow State University, Moscow 119899, Russia 13Department of Invertebrate Zoology, US National Museum of Natural History, Smithsonian Institution, Washington, DC 20013, USA 14Marine Biology Section, Department of Biology, University of Copenhagen, Universitetsparken 4, DK- 2100, Copenhagen, Denmark Received 27 April 2020; revised 9 October 2020; accepted for publication 29 October 2020 We present a comprehensive revision and synthesis of the higher-level classification of the barnacles (Crustacea: Thecostraca) to the genus level and including both extant and fossils forms. We provide estimates of the number of species in each group. Our classification scheme has been updated based on insights from recent phylogenetic studies and attempts to adjust the higher-level classifications to represent evolutionary lineages better, while documenting the evolutionary diversity of the barnacles. Except where specifically noted, recognized taxa down to family are argued to be monophyletic from molecular analysis and/or morphological data. Our resulting classification divides the Thecostraca into the subclasses Facetotecta, Ascothoracida and Cirripedia. The whole class now contains 14 orders, 65 families and 367 genera. We estimate that barnacles consist of 2116 species. The taxonomy is accompanied by a discussion of major morphological events in barnacle evolution and justifications for the various rearrangements we propose. ADDITIONAL KEYWORDS: classification – Crustacea – phylogeny – taxonomy – Thecostraca. I hate a barnacle as no man ever did before, not *Corresponding author. E-mail: [email protected] [Version of record, published online 25 February 2021; even a Sailor in a slow-moving ship. http://zoobank.org/ urn:lsid:zoobank.org:pub:A77C1793- Charles Darwin, in a letter to W. D. Fox, 24 B652-41CE-BB27-CD2E29DEB201] October 1852. © 2021 The Linnean Society of London, Zoological Journal of the Linnean Society, 2021, XX, 1–58 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons. org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 2 B. K. K. CHAN ET AL. INTRODUCTION to the study of fossil and extant barnacles (Darwin, 1851, 1852, 1854, 1855). Krüger (1940a, b) provided Barnacles are traditionally known as Cirripedia, a comprehensive treatment of both Ascothoracida which comprise an extremely diverse array of sessile and Cirripedia, including physiological and ecological crustaceans that are either acorn, stalked or parasitic issues, and there is still much information to be (Figs 1–5). From the classical taxonomy summarized by gleaned from this rarely cited work. Newman et al. Martin & Davis (2001), Cirripedia forms an important Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlaa160/6149353 by guest on 20 April 2021 (1969) provided a basic reference for the taxonomy and subgroup with Facetoteca (Fig. 1) and Ascothoracida morphology of both extinct and extant forms. Chapters (Fig. 2) under Thecostraca. From molecular in the books edited by Southward (1987) and Schram phylogenetic analyses (Pérez-Losada et al., 2008, & Høeg (1995) survey almost all biological issues in 2012a, b, 2014), Thecostraca forms a monophyletic the taxon, and the superb book by Anderson (1994) group, with Facetoteca being the sister group to a clade provides the most recent general account. comprising Ascothoracida and Cirripedia (Figs 3–6). In Cirripede barnacles, with mineralized shell plates, the present study, we consider the evolutionary history have left an impressive palaeontological record and classification of Thecostraca and treat the group (Withers, 1928, 1935, 1953; Newman et al., 1969; as comprising all barnacles in the widest sense. Buckeridge, 1983; Foster & Buckeridge, 1987; Gale, Barnacles (Thecostraca) rank among the most 2019) (Fig. 6), starting with Praelepas Chernyshev, biologically diverse, commonly encountered and 1930 in the middle Carboniferous (320–330 Mya) ecologically important marine crustaceans in the (Buckeridge & Newman, 2006). As explained below, world. However, they deviate from almost all other we choose here not to accept the even earlier fossils, Crustacea in that only the larval stages (naupliar Priscansermarinus Collins & Rudkin, 1981 from and cypridoid) are free-living, whereas the adults are the Cambrian and Cyprilepas Wills, 1962 from the permanently sessile as either suspension feeders or Silurian, as cirripedes. More than 400 fossil species parasites (Figs 1–5). Suspension-feeding barnacles have been described so far, and their study has been normally settle on rocky bottoms (Anderson, 1994), linked directly to the study of barnacle evolution, but several epibiotic taxa prefer to grow on mangrove systematics, taxonomy and morphological adaptations roots (or other marine plants), invertebrates (molluscs, and even ancient cetacean migratory pathways from crustaceans, marine sponges or corals) or vertebrates fossils of cetacean-associated barnacles (Buckeridge (turtles, sea snakes or whales) (Yamato et al., 1996; et al., 2018, 2019; Taylor et al., 2019; Fig. 6). Zardus & Hadfield, 2004; Seilacher, 2005; Brickner & The class Thecostraca comprises ~65 families, 367 Høeg, 2010; Hayashi et al., 2013; Dreyer et al., 2020; genera and 2116 species distributed in three subclasses: Zweifleret al., 2020), and other fouling barnacle species Facetotecta (12 species; Fig. 1), Ascothoracida (114 can also attach to man-made objects (Knight-Jones species; Fig. 2) and Cirripedia (1990 species; Figs 3–6; & Crisp, 1953). The numerous species of parasitic Supporting Information, Table S1). The Cirripedia barnacles also have a diverse array of hosts, including includes the Thoracica, the Acrothoracica and the soft corals, crustaceans, echinoderms and even sharks Rhizocephala (Fig. 7). The Thoracica are a highly (Høeg et al., 2015; Ommundsen et al., 2016; Figs 1–5). specialized group of suspension feeders. Their external Thecostracans display a highly diverse morphology body armor includes a system of mineralized plates. and biology (Ruppert et al., 2003; Høeg & Møller, 2006; These shell plates are mineralized parts of the cuticle Chan & Høeg, 2015), which has made them prime and are not shed at moults, but increase gradually in models for studies on intertidal ecology (Dayton, 1971; both thickness and area. In the variably-sized zones Carroll, 1996; Miron et al., 1999; Chan & Williams, between these plates, the cuticle is moulted regularly. 2003; Hawkins et al., 2008; Fraser & Chan, 2019; But this occurs in a highly modified fashion that produces Jung et al., 2019), larval settlement (Høeg, 1985; a system of parallel growth lines, also called ‘cuticular Clare, 1995; Walker, 1995; Maruzzo et al., 2012), slips’ (Anderson, 1994; Blomsterberg et al., 2004). The development (Walley, 1969; Turquier, 1972; Glenner, Acrothoracica, although also suspension feeders, lack 2001; Glenner et al., 2008; Høeg et al., 2012; Dreyer mineralized plates (Kolbasov & Høeg, 2000). Instead, et al., 2018a), antifouling technology (Aldred & Clare, they are symbiotic and inhabit self-excavated borings 2008) and the evolution of morphology, life cycles and in a wide array of calcareous substrata, including reproductive systems (Charnov, 1987; Høeg, 1995a, corals, coralline red algae, gastropod shells occupied by b; Buhl-Mortensen & Høeg, 2006; Ozaki et al., 2008; hermit crabs, live gastropods, bivalves, limestone and Yamaguchi et al., 2008, 2013; Pérez-Losada et al., foraminiferal chalk, thoracican barnacles and bryozoans 2009; Yusa et al., 2012; Lin et al., 2016; Dreyer et al., (Kolbasov, 2009; Botha
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