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(Monorchiidae and Gymnophallidae) Infecting the Bivalve, Donax Variabilis: It’S Just a Facultative Host!

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(Monorchiidae and Gymnophallidae) Infecting the Bivalve, Donax Variabilis: It’S Just a Facultative Host! Parasite 28, 34 (2021) Ó K.M. Hill-Spanik et al., published by EDP Sciences, 2021 https://doi.org/10.1051/parasite/2021027 Available online at: www.parasite-journal.org RESEARCH ARTICLE OPEN ACCESS Molecular data reshape our understanding of the life cycles of three digeneans (Monorchiidae and Gymnophallidae) infecting the bivalve, Donax variabilis: it’s just a facultative host! Kristina M. Hill-Spanik1, Claudia Sams1, Vincent A. Connors2, Tessa Bricker1, and Isaure de Buron1,* 1 Department of Biology, 205 Fort Johnson Road, College of Charleston, Charleston, 29412 SC, USA 2 Department of Biology, Division of Natural Sciences, University of South Carolina Upstate, 1800 University Way, Spartanburg, 29303 SC, USA Received 14 December 2020, Accepted 11 March 2021, Published online 9 April 2021 Abstract – The coquina, Donax variabilis, is a known intermediate host of monorchiid and gymnophallid digeneans. Limited morphological criteria for the host and the digeneans’ larval stages have caused confusion in records. Herein, identities of coquinas from the United States (US) Atlantic coast were verified molecularly. We demonstrate that the current GenBank sequences for D. variabilis are erroneous, with the US sequence referring to D. fossor. Two cercariae and three metacercariae previously described in the Gulf of Mexico and one new cercaria were identified morpholog- ically and molecularly, with only metacercariae occurring in both hosts. On the Southeast Atlantic coast, D. variabilis’ role is limited to being a facultative second intermediate host, and D. fossor, an older species, acts as both first and second intermediate hosts. Sequencing demonstrated 100% similarities between larval stages for each of the three dige- neans. Sporocysts, single tail cercariae, and metacercariae in the incurrent siphon had sequences identical to those of monorchiid Lasiotocus trachinoti, for which we provide the complete life cycle. Adults are not known for the other two digeneans, and sequences from their larval stages were not identical to any in GenBank. Large sporocysts, cercariae (Cercaria choanura), and metacercariae in the coquinas’ foot were identified as Lasiotocus choanura (Hopkins, 1958) n. comb. Small sporocysts, furcocercous cercariae, and metacercariae in the mantle were identified as gymnophallid Parvatrema cf. donacis. We clarify records wherein authors recognized the three digenean species but confused their life stages, and probably the hosts, as D. variabilis is sympatric with cryptic D. texasianus in the Gulf of Mexico. Key words: Coquina, Trematode, Lasiotocus, Parvatrema, Complex life cycle evolution, DNA sequencing, Western Atlantic. Re´sume´ – Les données moléculaires remodèlent notre compréhension des cycles de vie de trois Digènes (Monorchiidae et Gymnophallidae) parasites du bivalve Donax variabilis :cen’est qu’un hôte facultatif !. La telline, Donax variabilis, est un hôte intermédiaire connu de digènes Monorchiidae et Gymnophallidae. Le nombre limité de critères morphologiques pour identifier les hôtes et les stades larvaires des parasites sont à la base de confusion dans la littérature. Dans cette étude nous avons identifié par séquençage les tellines collectées sur la côte Atlantique des États-Unis. Nous démontrons que les séquences pour D. variabilis dans GenBank sont incorrectes et que celle du spécimen américain est en fait celle de D. fossor. Deux cercaires et trois métacercaires décrites au préalable dans le Golfe du Mexique ainsi qu’une nouvelle cercaire ont été identifiées morphologiquement et par séquençage. Les métacercaires seules infectent les deux hôtes. Sur la côte sud-est Atlantique, D. variabilis a un rôle limité à seulement celui de second hôte intermédiaire facultatif, et D. fossor, une espèce plus ancienne, est premier et second hôte intermédiaire. Le séquençage a montré 100 % de similarité entre les stades larvaires de chacun des trois digènes. Des sporocystes avec des cercaires à queue simple et les métacercaires dans le siphon inhalant ont des séquences identiques à celles de Lasiotocus trachinoti, pour qui nous donnons le cycle complet. Les adultes des deux autres digènes ne sont pas connus et les séquences des stades larvaires ne sont identiques à aucune dans GenBank. Des sporocystes de grande taille, les cercaires (Cercaria choanura) et les métacercaires enkystées dans le pied des tellines sont identifiées comme étant Lasiotocus choanura (Hopkins, 1958) n. comb. Des petits sporocystes avec des furcocercaires et des métacercaires dans le manteau des tellines sont identifiées comme étant le gymnophallide Parvatrema cf. donacis. Nous clarifions les *Corresponding author: [email protected] This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 K.M. Hill-Spanik et al.: Parasite 2021, 28,34 rapports de la littérature dans lesquels les auteurs ont reconnu les trois espèces de digènes mais ont confondu leurs stades larvaires et probablement les hôtes étant donné que D. variabilis vit en sympatrie avec l’espèce cryptique D. texasianus dans le Golfe du Mexique. Introduction on the SC coast. Some specimens were haphazardly collected between 2010 and 2015 from the same localities, but not Coquinas, Donax spp., are small hard-shell clams that live included in prevalence calculations. Additional coquinas in large colonies in the surf zone of sandy beaches. Their life were collected from North Wildwood, New Jersey (NJ) span is short, they are fast developing, and they are ecologically (39°00000 N, 74°78070 W) on September 6, 2020. Adult dige- significant as they are filter feeders that are preyed upon by neans were collected from Florida Pompano Trachinotus numerous species of crustaceans, shore birds, and marine fishes carolinus (L.) in October 2014 at the same localities in SC [11, 33, 36, 65]. In particular, D. variabilis Say, 1822 is and were identified and sequenced (see below) in an attempt common on the southeastern US Atlantic coast (south of to match resulting sequences with those from larval stages Chesapeake Bay to mid-east Florida) and throughout the Gulf found infecting coquinas. of Mexico from southwest Florida, USA to Campeche State, Coquina specimens were maintained on a bed of sand in Mexico [2, 66]. It has been reported as host to a variety of aerated seawater in the laboratory and examined within 3 days parasites [in 4, 32] including several digenean larvae [29, 30, post-collection. After the clams were shucked, gonads, diges- 38, 62, 63]. However, because these clams live in sympatry tive gland, mantle, foot, and both inhalant and exhalant siphons with congeneric cryptic species [1, 2], such host reports are were isolated, squashed separately on individual slides, and questionable. Furthermore, while species names were often examined for infection under a compound microscope. The attributed to the cercarial stages (e.g., Cercaria choanura inner side of the shells were also examined under the dissecting Hopkins, 1958 [30]; Cercaria fragosa Holliman, 1961 [29]), microscope. Clam tissue (uninfected gonad and adductor no association between sporocysts, cercariae, and metacercariae muscle) was fixed in 95% ethanol or directly frozen at could be made accurately at the time of those descriptions due À20 °C (SC), or whole clams were fixed in 100% EtOH to limitations in morphological characters common to these (NJ) for molecular study. Parasites from SC coquinas and fish stages [9]. Similarly, no connection could be established were isolated in filtered seawater, and parasites from NJ were between these larval stages and adults, which infect shore birds isolated from the EtOH-fixed clams. There was no attempt to and/or marine fishes. Hence, none of the monorchiid and observe the natural emergence of cercariae out of the coquinas. gymnophallid species reported from coquinas in the Gulf of Some specimens were examined and photographed fresh while Mexico have known life cycles, and the suprageneric species others, including manually-excysted metacercariae, were heat- are species inquirendae until their identity is resolved [9]. killed by slowly passing a flame under the slides on which they In coastal South Carolina (SC), coquinas D. variabilis and were placed. Parasites were fixed in either 95% ethanol or 5% D. fossor are cryptic species, and preliminary opportunistic neutral buffered formalin (NBF) for molecular and morpholog- observations over the past decade revealed that infection by ical studies, respectively. digeneans was common although unreported (Fig. 1). Using morphology, we identified two monorchiids and one gymnophallid previously described from D. variabilis in the Morphological study Gulf of Mexico, and we discovered one previously unreported ’ cercaria. The advent of molecular identification via DNA Fixed parasitic stages were stained with Semichon s ’ sequencing has made the unraveling of complex parasite life acetocarmine or Mayer s hematoxylin, dehydrated according cycles much easier compared to experimental infections (e.g., to standard protocol, and mounted in Canada balsam or [10, 40, 67]). The use of molecular tools allowed us to connect Permount. Measurements were taken using an ocular microme- fi the various life cycle stages encountered, to identify cryptic ter and are reported in micrometers unless otherwise speci ed; intermediate hosts, and to elucidate the complete life cycle
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