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Reconciling Taxonomy and Phylogeny in Hermit-Crab Symbiotic Anemones (Cnidaria: Actiniaria: Hormathiidae)

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Reconciling Taxonomy and Phylogeny in Hermit-Crab Symbiotic Anemones (Cnidaria: Actiniaria: Hormathiidae) Organisms Diversity & Evolution (2019) 19:567–583 https://doi.org/10.1007/s13127-019-00414-2 ORIGINAL ARTICLE Description of Calliactis tigris sp. nov.: reconciling taxonomy and phylogeny in hermit-crab symbiotic anemones (Cnidaria: Actiniaria: Hormathiidae) Luciana C. Gusmão1 & E. Rodríguez1 & Marymegan Daly2 Received: 22 April 2019 /Accepted: 11 August 2019 /Published online: 22 August 2019 # Gesellschaft für Biologische Systematik 2019 Abstract The symbiosis between sea anemones and hermit crabs is ubiquitous in the marine environment (except in the poles), occurring from shallow to deep waters; it involves one or more anemones living on a shell inhabited by a hermit crab. The anemone-crab partnership is a mutualism in which hermit crabs provide a hard substrate, increased access to oxygenated waters and food supply, in exchange for defense by the anemone. The vast majority of the sea anemone partners belong to three genera in family Hormathiidae: Adamsia, Calliactis, Paracalliactis. Given the remarkable nature of the symbiosis, hormathiid partners have been hypothesized to represent a monophyletic group. This has been rejected by Gusmão and Daly et al. (2010) and confirmed by our phylogenetic analysis using molecular markers (12S, 16S, 18S, 28S, COIII). We expand the results of Gusmão and Daly et al. (2010) by finding a monophyletic Paracalliactis, which was left untested in their analyses. Thus, characters of taxonomic significance associated to the symbiotic habit are interpreted as functional rather than phylogenetic. We reconcile taxonomy and the present evolutionary framework to avoid defining taxonomic groups based on characters prone to convergence. We formalize the synonymy of Adamsia and Calliactis and provide updated diagnoses for the valid genera Calliactis and Paracalliactis to bring more stability to the group. Under this new framework, we describe Calliactis tigris sp. nov. from Australia based on 21 specimens collected off the coast of New South Wales and Queensland and differentiate it from congeners and other hermit crab symbionts recorded in the Pacific Ocean. Keywords Symbiosis . Mutualism . Convergence . Adamsia . Paracalliactis . Australia Introduction hermit crab (Gusmão and Daly 2010). The anemone-crab partnership is a mutualism (Brooks and Gwaltney 1993; The symbiosis between sea anemones and hermit crabs is Mainardi and Rossi 1969) in which hermit crabs provide a ubiquitous in the marine environment (except in the poles), hard substrate that prevents the anemone’s burial and increase occurring from shallow to deep waters; it involves one or access to positive conditions, including oxygenated waters more anemones living on a gastropod shell inhabited by a and food supply (Williams and McDermott 2004). In ex- change, the anemones defend the crab from predators using their nematocysts (Ross 1971, 1974a; Ross and Boletzky Electronic supplementary material The online version of this article 1979;Christidisetal.1997). The presence of predators en- (https://doi.org/10.1007/s13127-019-00414-2) contains supplementary courages acquisition of anemones by the crab in the laboratory material, which is available to authorized users. (Balasch and Mengual 1973; Bach and Herrnkind 1980;Ross * Luciana C. Gusmão and Boletzky 1979) and reinforces the operational trigger of [email protected] this association in nature with crabs carrying one or more anemones more likely to survive encounters with predators 1 (Ross and Boletzky 1979; Brooks 1989). Some anemones Division of Invertebrate Zoology, American Museum of Natural “ ” History, Central Park West at 79th Street, New York, NY 10024, may also protect the crab by producing a living cloak (i.e., USA carcinoecium) that expands the living space of the crab 2 Museum of Biological Diversity, Ohio State University, 1315 bypassing the necessity to change to bigger shells as they Kinnear Road, Columbus, OH 43215, USA grow (Ross 1974a;Fautin1992;Dalyetal.2004). 568 Gusmão L.C. et al. Most sea anemone partners belong to three genera within examination, longitudinal and cross-sectional serial sections family Hormathiidae Carlgren 1932: Adamsia Forbes 1840, 10 μm thick were made using standard paraffin techniques Calliactis Verrill 1869, and Paracalliactis Carlgren 1928a. and stained with Heidenhain’s Azan Stain (Presnell and These genera have been hypothesized to represent a single Schreibman 1997). Undischarged cnidae capsules were iden- monophyletic group given the remarkable nature of the symbi- tified and measured in squash preparations of tissue from col- otic behavior exhibited by the partners (e.g., Ross 1974b;Ates umn, tentacles, actinopharynx, filaments, and acontia of five 1997). This idea was supported by the related morphological preserved specimens using differential interference microsco- adaptations seen in the hormathiid partners that form a morpho- py (DIC) at × 1000 magnification. Except for the rarer types, logical complex whose members are distinguished by a mosaic at least 20 capsules were measured. The presence of each type of characters (Hand 1975;Dalyetal.2004). Attributes of the of cnidae in each tissue was confirmed in histological slides. symbiosis, such as the adaptation of the pedal disc to life on a We follow a nematocyst terminology that combines the clas- shell and secretion of a carcinoecium, unite members of sification of Weill (1934) modified by Carlgren (1940), thus Adamsia and Paracalliactis and distinguish them from those differentiating “basitrichs” from “b-mastigophores” with that in Calliactis. On the other hand, both Calliactis and Adamsia of Schmidt (1969, 1972, 1974) which captures the underlying differ from Paracalliactis in having cinclides in the column. variation seen in “rhabdoids” (see Gusmão et al. 2018 for Carlgren (1928b) described the genus Paracalliactis as biolog- more details). We include photographs of each type of nema- ical intermediate between Adamsia and Calliactis. Because no tocyst for reliable comparison across terminologies and taxa support for the monophyly of hormathiid hermit-crab symbiotic (see Fautin 1988). Higher-level classification for Actiniaria anemones was recovered in the multilocus analysis of Gusmão follows Rodríguez et al. (2014). and Daly et al. (2010), similarities in morphology and behavior among these symbiotic anemones have to be interpreted as Molecular data collection and analysis related to the ways in which a symbiotic habit arises and is maintained, not to shared evolutionary history. Genomic DNA was isolated from approximately 25 mg of tis- Here, we reconcile the taxonomy of hormathiid hermit- sue of one specimen of Calliactis tigris sp. nov. and crab symbionts with the present evolutionary framework for Paracalliactis sp. using the Qiagen DNeasy kit. Whole geno- the group provided by the phylogenetic analyses of five nu- mic DNA was amplified using published primers and standard clear and mitochondrial markers (12S, 16S, 18S, 28S, COIII). protocols (e.g., Geller and Walton 2001; Daly et al. 2008; We formalize the findings of Gusmão and Daly et al. (2010) Lauretta et al. 2014) for three mitochondrial markers (12S, confirmed in our analysis, particularly the synonymy of gen- 16S, COIII) and two nuclear markers (18S, 28S). PCR products era Adamsia and Calliactis. We also expand the results of were cleaned with the Thermo Scientific Fermentas clean-up Gusmão and Daly et al. (2010) by finding a monophyletic protocol using Exonuclease I and FastAP thermosensitive alka- Paracalliactis, which was left untested in their analyses. line phosphatase per manufacturer’s specifications, but with Updated diagnoses for the valid symbiotic hormathiid genera shrimp alkaline phosphatase replaced by FastAP™. A total of Calliactis and Paracalliactis areprovidedtohelpwithtaxo- 5 μL of cleaned PCR product, at a concentration of 25 ng of nomic identification and bring more stability to this wide- product for every 200 base pairs (bp) of marker length, was spread group of sea anemones. Finally, we describe cycle-sequenced in an ABI BigDye® Terminator v3.1 Calliactis tigris sp. nov. from Australia based on 21 specimens (Applied Biosystems) reaction following the manufacturer’s collected off the coast of New South Wales and Queensland protocols. Cycle sequencing products were cleaned using and differentiate it from congeners as well as other hermit crab Centri-Sept columns (Princeton Separations; following the symbionts recorded in the Pacific Ocean. manufacturer’s protocol) containing DNA-grade Sephadex (G-50 fine; GE Healthcare) and later sequenced using PCR amplification primers on an ABI 3770x at the in-house facilities Material and methods of the American Museum of Natural History (AMNH). Forward and reverse sequences were assembled and edited in Morphological study Geneious v.10.0.9 (Kearse et al. 2012) and blasted against the nucleotide database of GenBank to confirm the successful am- The description of Calliactis tigris sp. nov. was based on 21 plification of target marker/organism. specimens collected in eastern Australia (Fig. 1) deposited in Newly generated sequences have been deposited in the Australian Museum (AM G.15586, AM G.16897, AM GenBank and combined into a dataset of sequences included G.16907, AM G.17482-17486, AM G.17489, AM in Rodríguez et al. (2014), Larson and Daly (2016), and Daly G.17491). External and internal morphology is described et al. (2017) with selected taxa within the suborder based on formalin-fixed specimens that were examined Anenthemonae Rodríguez and Daly, 2014 used
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