Storm Martin

A substantial component of the metazoan biodiversity not yet discovered or characterised is to be found among lineages of endoparasites. The Trematoda, obligate endoparasitic flatworms, is one such lineage which is particularly diverse and successful, exploiting virtually all lineages of vertebrates and many invertebrate groups. The Opecoelidae is the richest of all trematode families, comprising over 1,000 recognised species and about 100 genera. Adult opecoelids are benign endoparasites of the intestinal tract of phylogenetically and ecologically diverse teleost fishes worldwide. They exploit both marine and freshwater fishes and are richest in tropical waters, but are also among the best represented trematode lineages known from polar and deep-sea fishes. Opecoelid life-cycles are complex and almost always involve exploitation of three hosts. The first intermediate host is apparently always a gastropod, but a broad range of invertebrates, including annelids, arthropods, cnidarians, echinoderms and molluscs, as well as fishes, may serve as second intermediate hosts.

Although opecoelids are a huge and evolutionarily derived group, they are neither diverse nor specialised in adult morphology and are mostly distinguished from other trematode lineages by some general characters together with the absence of certain specialised characters. The combination of high richness but low morphological diversity has resulted in a history of confused taxonomy. This confusion has been exacerbated by a general historical failure to sufficiently consider the plausibility of the host with respect to phylogeny and ecology when assigning species to genera or providing new reports of established species. Thus, especially generalised opecoelid species are often reported from an implausibly broad range of hosts and geographic areas or else are lumped together into loosely defined ‘wastebasket’ genera. Many genera are assumed or suspected to be polyphyletic, clouding understanding of phylogenetic relationships between genera.

The subfamilial classification of the Opecoelidae is currently inadequate. Some 13 opecoelid subfamilies have variously been proposed, although, since the early 1980’s, most authors have accepted a four subfamily hypothesis based entirely on two useful but ultimately arbitrary features of adult worms, without any consideration for other life-stages or the phylogeny or ecology of the hosts exploited. Specifically, this four subfamily system divides taxa based on the presence vs absence of a well-developed cirrus-sac enclosing the male terminal genitalia and a canalicular seminal receptacle, a specialised sperm storage structure originating from the Laurer’s canal and associated with the ovarian complex. Recent phylogenetic analyses based on molecular data have challenged this classification hypothesis. The findings suggest that, in particular, opecoelids which have both a well-defined cirrus-sac and a canalicular seminal receptacle and thus belonging to the largest subfamily, the Plagioporinae, do not form a monophyletic assemblage. Although these morphological characters continue to provide utility for segregating opecoelid taxa, consideration of greater breadth of evidence is clearly required to sufficiently organise the family.

In this thesis, a new subfamilial classification for the Opecoelidae, which both reflects phylogeny and divides taxa usefully, is sought. Novel sequence data have been generated from as many opecoelid taxa as possible. These data have revealed much about the family, especially when considered together with morphology, life-cycle, biogeography and hosts exploited. Thus, following thorough investigation of several problematic genera and study of much material, 20 new opecoelid species and 9 new genera are proposed, a further 13 species are redescribed from new host-locality combinations and some 80 new combinations and synonymies are proposed. Many more new species have been detected, including some which form complexes and require further investigation. The new analyses support monophyly of the current concepts of the Helicometrinae and Opecoelinae, but prompt dramatic revision of the concepts of the Plagioporinae and Opistholebetinae, the former is reduced and the latter expanded. The first molecular data for representatives of the Stenakrinae are also introduced, four new subfamilies are proposed, the Bathycreadiinae, Hamacreadiinae, Polypipapiliotrematinae and Pseudoplagioporinae, and it is argued that three previous concepts, the Decemtestinae, Hysterogoniinae and Podocotylinae, warrant resurrection.

Ultimately, it is proposed that the most appropriate classification for the Opecoelidae should comprise at least 15 subfamilies, distinguished on the basis of phylogenetic distinction, adult morphology, but also life-cycle ecology. It is argued that diversification of the Opecoelidae has been driven significantly by second intermediate host-switch events, with subsequent radiation driven by the colonisation of phylogenetically and/or ecologically similar definitive hosts.