Tapeworms of the order Caryophyllidea are the earliest diverging 'true' tapeworms (Eucestoda) and parasitise cypriniform and siluriform fishes almost exclusively. They are typified by a monozoic (non-proglottised) body plan, which is a characteristic shared with early diverging 'cestodarians' Gyrocotylidea and Amphilinidea. Here we present the most comprehensive multi-gene molecular phylogeny of this group, to date. Specimens of 63 species from 32 genera (~50% and ~75% of known species and genus diversity, respectively) were gathered during an intense and targeted 15-year collecting effort. Phylogenetic reconstructions provide high nodal support for three major lineages, which only partly correspond to currently recognised families. The three well-supported clades were as follows: Clade A was in an unsupported position at the base of the tree and was almost exclusively comprised of parasites of catfishes (Siluriformes) from the Afrotropical and Indomalayan regions, including the type genus of the Lytocestidae (Lytocestus). Clade B formed the sister group to the remaining taxa (Clade C) and was composed of species that parasitise cyprinids and loaches (Cypriniformes: Cyprinoidei and Cobitoidei) from the Palaearctic Region. This clade included the type genus of the Caryophyllaeidae (Caryophyllaeus). Clade C comprised Nearctic species from suckers and minnows (Cypriniformes: Catostomidae and Cyprinoidei), which were previously accommodated in two families, i.e. Capingentidae and Caryophyllaeidae. This clade included the type genus of the Capingentidae (Capingens). In addition to Clades A-C, Balanotaenia bancrofti from the monotypic Balanotaeniidae, which parasitises plotosid catfishes in Australia, and Lytocestoides tanganyikae, which parasitises African cichlids, formed a poorly supported clade at the base of the tree. Whereas morphological characteristics traditionally used to differentiate caryophyllidean families do not characterise molecular lineages, host association and biogeographical distribution play a key role in the circumscription of the three well-supported clades revealed by molecular data. Thus, the taxonomic rearrangement proposed herein was guided by the molecular clades. The names of all four extant families were preserved and family affinity was determined by topological clustering with the type genera of the families. The family diagnoses of the Lytocestidae, Caryophyllaeidae and Capingentidae are amended. Biogeographic patterns are indicative of separate Gondwanan and Laurasian radiations having taken place. Regarding the Gondwanan radiation in the Siluriformes, the topology in Clade A indicates an Asian origin with a subsequent African colonisation. Concerning Laurasia, separate radiations appear to have taken place in the Cypriniformes in the temperate zones of North America and Eurasia. Complete absence of caryophyllideans in the Neotropical Region, where numerous catfishes occur, may be due to the Gondwanan radiation having taken place after the continental separation of Africa and South America.

Department of Life Sciences Natural History Museum Cromwell Road London SW7 5BD United Kingdom

Institute of Parasitology Biology Centre of the Czech Academy of Sciences Branišovská 31 370 05 České Budějovice Czech Republic

Institute of Parasitology Slovak Academy of Sciences Hlinkova 3 040 10 Košice Slovak Republic

References provided by Crossref.org

Fish tapeworms (Cestoda) in the molecular era: achievements, gaps and prospects

New cytogenetic data on Caryophyllaeus laticeps and Paracaryophyllaeus gotoi, parasites of evolutionary interest

Archigetes Leuckart, 1878 (Cestoda, Caryophyllidea): diversity of enigmatic fish tapeworms with monoxenic life cycles

Molecular evidence of three closely related species of Biacetabulum Hunter, 1927 (Cestoda: Caryophyllidea): a case of recent speciation in different fish hosts (Catostomidae)?

Caryophyllidean tapeworms (Cestoda), Nearctic parasites of fish in Mexico, including description of a new species of Isoglaridacris and the first report of Khawia japonensis, an invasive parasite of common carp (Cyprinus carpio)

Disentangling taxonomy of Biacetabulum (Cestoda, Caryophyllidea), parasites of catostomid fishes in North America: proposal of Megancestus gen. n. to accommodate B. carpiodi