Evolution of the bomolochiform superfamily complex (Copepoda: Cyclopoida): New insights from ssrDNA and morphology, and origin of umazuracolids from polychaete-infesting ancestors rejected

Abstract

Poecilostome cyclopoids are among the most morphologically diverse copepods, having established symbiotic relationships with teleosts, elasmobranchs and invertebrate hosts belonging to no fewer than 14 marine phyla. Many parasitic lineages display radically divergent body plans and on that basis have traditionally been placed at higher taxonomic rank than they deserve. The most recent example is the monotypic family Umazuracolidae, established for a derived fish parasite with bomolochiform affinities. Phylogenetic analysis of complete ssrDNA (18S) sequences of 44 species belonging to 21 families of cyclopoid copepods shows that there is no support for the familial distinctiveness of the Umazuracolidae. Both maximum parsimony tree reconstruction and Bayesian inference, operating under the GTR + I + Γ model of nucleotide substitution, unambiguously placed Umazuracola elongatus in the Taeniacanthidae within the predominantly fish parasitic bomolochiform complex, refuting the original suggestion of a shared most recent common ancestry with polychaete symbionts. The phylogenies also revealed that the bomolochiform families and the Clausidiidae (and allies) form a monophyletic group, the clausidiiform complex, with high nodal support under both methods. Bayesian inference suggested a diphyletic origin of the “Poecilostomatoida” with the clausidiiform family-group holding a basal position while the traditional cyclopoid families form a monophyletic group in apposition to a second poecilostomatoid clade; however, maximum parsimony results were equivocal, depending on outgroup selection. Scrutiny of the morphological characters diagnosing the monotypic families Tegobomolochidae and Tuccidae demonstrated that they merely represent derived lineages within more inclusive taxa, the former being related to a group of nostril-inhabiting genera within the Bomolochidae, the latter forming the sistergroup of Taeniacanthodes within the Taeniacanthidae. The taeniacanthid genus Makrostrotos occupies a position at the base of the bomolochiform complex and is fixed as the type of a new family, Makrostrotidae. Although both morphological and molecular evidence hint that the Bomolochidae is nested within a paraphyletic Taeniacanthidae, the status quo of maintaining both families is favoured here pending additional molecular data. The bomolochiform complex, comprising the Bomolochidae, Taeniacanthidae, Telsidae and Makrostrotidae, is attributed superfamilial rank as the Bomolochoidea. A recent controversial phylogenetic analysis of the poecilostomatoid families is shown to be flawed, being based on a dataset containing imperfect or misleading information, and characters whose states were wrongly assessed.