The molecular phylogeny of the digenean family Opecoelidae Ozaki, 1925 and the value of morphological characters, with the erection of a new subfamily

Abstract

Large and small rDNA sequences of 41 species of the family Opecoelidae are utilised to produce phylogenetic inference trees, using brachycladioids and lepocreadioids as outgroups. Sequences were newly generated for 13 species. The resulting Bayesian trees show a monophyletic Opecoelidae. The earliest divergent group is the Stenakrinae, based on two species which are not of the type-genus. The next well-supported clade to diverge is constituted of three species of Helicometra Odhner, 1902. Based on this tree and the characters of the egg and uterus, a new subfamily, the Helicometrinae, is erected and defined to include the genera Helicometra, Helicometrina Linton, 1910 and Neohelicometra Siddiqi et Cable, 1960. The subfamily Opecoelinae is found to be monophyletic, but the Plagioporinae is paraphyletic. The single representative of the Opecoelininae (not of the type genus) is nested within a group of deep-sea 'plagioporines'. The two representatives of the Opistholebetidae are embedded within a group of shallow-water 'plagioporine' species. The Opistholebetidae is reduced to subfamily status pro tem as its morphological and biological characteristics are distinctive. This implies that as opecoelid systematics develops with more molecular evidence, several further subfamilies will be recognised. Many of the morphological characters were found to be homoplasious, but the characters defining the Helicometrinae and Opecoelinae, such as filamented eggs, reduced cirrus-sac and uterine seminal receptacle, are closely correlated with the inferred phylogeny.

The Pseudoplagioporinae, a new subfamily in the Opecoelidae Ozaki, 1925 (Trematoda) for a small clade parasitizing mainly lethrinid fishes, with three new species

“…This group includes the Opistholebetinae, the Polypipapiliotrematinae, and also two similarly distinctive clades, referred to as clade B and clade C after Bray et al. () and Martin, Cutmore, et al. (), which are expected to eventually be recognized at the subfamily level.…”

“…The four subfamily arrangement of the Opecoelidae, comprising the Opecoelinae, Plagioporinae, Stenakrinae, and Opecoelininae, dominated understanding of the group until recently. Some early phylogenetic efforts (Andres, Pulis & Overstreet, ; Curran, Overstreet, & Tkach, ; Shedko, Sokolov, & Atopkin, ) flagged potential problems with this classification hypothesis, but it was not until Bray, Cribb, Littlewood, and Waeschenbach () significantly increased the breadth of opecoelid taxa represented by phylogenetically informative sequence data that it became clear that opecoelids with both a well‐developed cirrus‐sac and a canalicular seminal receptacle did not form a monophyletic assemblage and, therefore, that the Plagioporinae would need to be divided into several subfamilies. Genuine species of the type genus, Plagioporus , are probably restricted to freshwater fishes (Cribb, ; Gibson & Bray, ) and sequence data generated by Fayton and Andres (), Fayton, Choudhury, McAllister, and Robison (), Fayton, McAllister, Robison, and Connior () and Sokolov, Shchenkov, and Gordeev () for representatives of these, and other Holarctic freshwater genera, provide evidence for a restricted concept of the Plagioporinae (see Martin, Huston, Cutmore, & Cribb, ).…”

“…However, most taxa which have been considered to belong to the Plagioporinae are marine. Already, many have been accommodated into new subfamily concepts, the Bathycreadiinae Martin, Huston, Cutmore, & Cribb, , Helicometrinae Bray, Cribb, Littlewood, & Waeschenbach, Opistholebetinae Fukui, 1929, Podocotylinae Dollfus, 1959, and Polypipapiliotrematinae Martin, Cutmore, & Cribb, , based on a combination of adult morphology, host usage, and phylogenetic distinctions (Bray et al., ; Martin, Crouch, Cutmore, & Cribb, ; Martin, Sasal, Cutmore, Ward, Aeby, & Cribb, ; Martin et al., ). Thus, the Opecoelidae is currently divided into nine subfamilies, although two sizeable clades of marine taxa (see Martin et al., ) remain without suitable subfamilial designation and the placement of multiple genera not yet represented by sequence data remains uncertain.…”

A fine‐scale phylogenetic assessment of digenean trematodes in central Alberta reveals we have yet to uncover their total diversity

“…Both of these problems are common among helminths (Jensen & Bullard, ; Roeber, Jex, & Gasser, ; Schell, ). Additionally, the revelation of cryptic species is becoming more common, as molecular methods expose diversity not identifiable by traditional, morphological methods (Detwiler, Bos, & Minchella, ; Detwiler, Zajac, Minchella, & Belden, ; Georgieva, Selbach et al, ; Herrmann, Poulin, Keeney, & Blasco‐Costa, ; Locke, McLaughlin, Dayanandan, & Marcogliese, ; Miura, Kuris, & Torchin, ; Nadler & León, ; Pérez‐Ponce de León & Poulin, ). Finally, there is a lack of general survey data on parasites, causing gaps in our understanding of diversity and richness for defined geographical locations (Adlard, Miller, & Smit, ; Adlard & O'Donoghue, ; Mollaret et al, ).…”

“…Traditionally, taxonomic descriptions of trematodes are from morphological traits of adult worm stages derived from vertebrate hosts, as their most prominent features are fully developed and measurable, contrasting the less developed features of the larval stages (Schell, ). With the onset of molecular barcoding, not only have we realized the problems of cryptic morphology and the need for multiple lines of evidence for species delineation, but that for trematodes, we can now use larval stages to delineate species (Detwiler et al, ; Georgieva, Selbach et al, ; Gordy, Locke, Rawlings, Lapierre, & Hanington, ; Locke, Mclaughlin et al, ; Schwelm, Soldánová, Vyhlídalová, Sures, & Selbach, ; Soldánová et al, ). This is advantageous in that it is considerably easier to collect larvae from snail, first‐intermediate hosts.…”