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Evidence from the Polypipapiliotrematinae N Accepted Manuscript Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf. (Opecoelidae), par- asites transmitted to butterflyfishes via predation of coral polyps Storm B. Martin, Pierre Sasal, Scott C. Cutmore, Selina Ward, Greta S. Aeby, Thomas H. Cribb PII: S0020-7519(18)30242-X DOI: https://doi.org/10.1016/j.ijpara.2018.09.003 Reference: PARA 4108 To appear in: International Journal for Parasitology Received Date: 14 May 2018 Revised Date: 5 September 2018 Accepted Date: 6 September 2018 Please cite this article as: Martin, S.B., Sasal, P., Cutmore, S.C., Ward, S., Aeby, G.S., Cribb, T.H., Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf. (Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps, International Journal for Parasitology (2018), doi: https://doi.org/10.1016/j.ijpara.2018.09.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf. (Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps Storm B. Martina,*, Pierre Sasalb,c, Scott C. Cutmorea, Selina Warda, Greta S. Aebyd, Thomas H. Cribba aSchool of Biological Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia bPSL Research University, USR 3278 EPHE-UPVD-CNRS, Centre de Recherche Insulaire et Observatoire de l’Environnement (CRIOBE) Université de Perpignan Via Domitia, 58 avenue P. Alduy, 66860 Perpignan. France cLaboratoire d’excellence Corail, EPHE, Moorea, French Polynesia dHawai‘i Institute of Marine Biology, Kāne‘ohe, Hawai‘i, United States of America *Corresponding author. E-mail address: [email protected] 1 Abstract Podocotyloides stenometra Pritchard, 1966 (Digenea: Opecoelidae) is the only trematode known to infect anthozoan corals. It causes disease in coral polyps of the genus Porites Link (Scleractinia: Poritidae) and its life-cycle depends on ingestion of these polyps by butterflyfishes (Perciformes: Chaetodontidae). This species has been reported throughout the Indo-Pacific, from the Seychelles to the Galápagos, but no study has investigated whether multiple species are involved. Here, we recollect P. stenometra from its type-host and type-locality, in Hawaiian waters, and describe four new species from examination of 768 butterflyfishes from French Polynesia. On the basis of morphology, phylogeny and life-history, we propose Polypipapiliotrema Martin, Cutmore & Cribb n. gen. and the Polypipapiliotrematinae Martin, Cutmore & Cribb n. subf., for P. stenometra (Pritchard) n. comb., P. citerovarium Martin, Cutmore & Cribb n. sp., P. hadrometra Martin, Cutmore & Cribb n. sp., P. heniochi Martin, Cutmore & Cribb n. sp., and P. ovatheculum Martin, Cutmore & Cribb n. sp. Given the diversity uncovered here and the ubiquity, abundance and diversity of butterflyfishes on coral reefs, we predict that Polypipapiliotrema will prove to comprise a rich complex of species causing disease in corals across the Indo-Pacific. The unique life-cycle of these taxa is consistent with phylogenetic distinction of the group and provides evidence for a broader basis of diversification among the family. We argue that life-cycle specialisation, in terms of adoption of disparate second intermediate host groups, has been a key driver of the diversification and richness of the Opecoelidae, the largest of all trematode families and the group most frequently encountered in coral reef fishes. Keywords: Chaetodontidae, Corallivory, Host specificity, New species, Opecoelidae, Trematodiasis, Taxonomy, Phylogeny 2 1. Introduction Among the Trematoda, Podocotyloides stenometra Pritchard, 1966 (Opecoelidae Ozaki, 1925) is noteworthy as the only species demonstrated to cause disease in anthozoan corals (Aeby, 1998). Opecoelids have complex life-cycles involving three hosts and reach the definitive host, fishes, through trophic transmission. Other opecoelids are known to exploit bivalves, crustaceans, echinoids, gastropods, insects, annelids, or small fishes as second intermediate hosts (Cribb, 2005). Cercariae of P. stenometra penetrate and encyst within coral polyp tissues, apparently only in species of Porites Link (Scleractinia: Poritidae), causing abnormal pink pigmentation and swelling such that the polyp may be unable to retract into its calyx (Cheng and Wong, 1974; Aeby, 1998). This pathology renders polyps both more conspicuous and vulnerable to predators and thus corallivorous butterflyfishes (Chaetodontidae), the definitive hosts of P. stenometra, preferentially eat infected polyps (Aeby, 2002), perpetuating the life-cycle. Considering its potential significance as a pathogen of reef-building corals, P. stenometra is surprisingly poorly known. It has been reported from butterflyfishes in Hawaiian (Pritchard, 1966), French Polynesian (Martin et al., 2018c), Seychelloise (Toman, 1992) and Great Barrier Reef (Bray and Cribb, 1989; Lucas et al., 2005) waters. Additionally, cases of suspected Porites trematodiasis have been reported from Hawai‘i (Aeby, 2006, 2007), French Polynesia (M. Rigby in Aeby, 2007), the Great Barrier Reef (Willis et al., 2001), Guam and Papua New Guinea (Aeby, 2007), the Ryuku Islands (Yamashiro, 2004), the Galapágos Archipelago (Vera and Banks, 2009) and the New Caledonian lagoon (Aeby et al., 2015). Presently, these reports are all attributed to a single species. Work et al. (2014) and Aeby et al. (2015) did note differences between infections in Hawaiian versus New Caledonian corals, but the possibility that multiple species are involved remains unexplored. The taxonomic position of P. stenometra itself also requires re-evaluation. Pritchard (1966) placed P. stenometra in Podocotyloides Yamaguti, 1934 based on general morphological similarity to the type-species, P. petalophallus Yamaguti, 1934; both are elongate with a pedunculate ventral 3 sucker, an entire ovary and vitelline follicles restricted to the hindbody. However, its inclusion in the genus is unsatisfactory. The type species and other convincing congeners are known mainly from haemulids (Perciformes), generalist benthic carnivores which do not feed on coral polyps. In contrast to those species, P. stenometra lacks a uterine sphincter, a petalloid cirrus and a canalicular seminal receptacle, the latter a defining characteristic of not just Podocotyloides but also its nominal subfamily, the Plagioporinae Manter, 1947. Recent analyses of rDNA sequence data demonstrated that P. stenometra is distantly related to species of Podocotyloides (sensu stricto) and indeed is phylogenetically distinctive among all sequenced representatives of the Opecoelidae (Martin et al., 2018c). Those analyses suggested P. stenometra requires a new genus, but were based on sequence data generated from infections in Heniochus chrysostomus Cuvier (Perciformes: Chaetodonidae) collected off Moorea, French Polynesia (Martin et al., 2018c), whereas the type combination for P. stenometra is Chaetodon quadrimaculatus Gray (Chaetodontidae) from Hawaiian waters (Pritchard, 1966). In this study we recollect and provide sequence data for P. stenometra from its type combination and prospect for unrecognised diversity among butterflyfishes from French Polynesian waters. Specifically, we assess the evidence for the occurrence of P. stenometra (sensu stricto) outside of Hawaiian waters and discuss the significance of the adoption of coral hosts apparent in the life-cycle of this trematode from an evolutionary context. 2. Materials and methods 2.1. Specimen collection Butterflyfishes were collected from Hawaiian and French Polynesian waters. In Hawai‘i, fishes were purchased from a professional collector operating from off Hale‘iwa, Waialua, O‘ahu in June, 2016. Fishes from French Polynesian waters were collected mostly by microspear on snorkel or rotenone, across several expeditions to multiple localities (Fig. 1): from off Moorea, Society 4 Islands in November-December, 1999, November, 2009, November, 2012 and April, 2017; from off the Mangareva island group in the Gambier Islands in October, 2010; from off Eiao, Fatu Hiva, Fatu Huku, Hiva Oa, Motu One, Nuku Hiva, Tahuata and Ua Pao, Marquesas Islands in October- November, 2011; from off Maria, Raivavae, Rimatara, Rurutu and Tubuai, Austral Islands in April, 2013; and from off Fakarava and Toau in November-December, 2012 and off Rangiroa in April, 2017, Tuamotu Archipelago. Fishes were dissected fresh and intestinal parasites were collected as per Cribb and Bray (2010). Trematodes were fixed, without pressure, in near-boiling saline and preserved in 80% ethanol. 2.2. Morphological study Specimens were stained and mounted as per Martin et al. (2017). Measurement data were taken from lateral mounts, using the software package cellSens Standard v1.13 via live feed from an Olympus SC50 camera mounted onto an Olympus BX53 compound microscope. Measurements are in micrometres, expressed as length
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