A large 28S rDNA-based phylogeny confirms the limitations of established morphological characters for classification of proteocephalidean tapeworms (Platyhelminthes, Cestoda)

Abstract

Proteocephalidean tapeworms form a diverse group of parasites currently known from 315 valid species. Most of the diversity of adult proteocephalideans can be found in freshwater fishes (predominantly catfishes), a large proportion infects reptiles, but only a few infect amphibians, and a single species has been found to parasitize possums. Although they have a cosmopolitan distribution, a large proportion of taxa are exclusively found in South America. We analyzed the largest proteocephalidean cestode molecular dataset to date comprising more than 100 species (30 new), including representatives from 54 genera (80%) and all subfamilies, thus significantly improving upon previous works to develop a molecular phylogeny for the group. The Old World origin of proteocephalideans is confirmed, with their more recent expansion in South America. The earliest diverging lineages are composed of Acanthotaeniinae and Gangesiinae but most of the presently recognized subfamilies (and genera) appear not to be monophyletic; a deep systematic reorganization of the order is thus needed and the present subfamilial system should be abandoned. The main characters on which the classical systematics of the group has been built, such as scolex morphology or relative position of genital organs in relation to the longitudinal musculature, are of limited value, as demonstrated by the very weak support for morphologically-defined subfamilies. However, new characters, such as the pattern of uterus development, relative ovary size, and egg structure have been identified, which may be useful in defining phylogenetically well-supported subgroups. A strongly supported lineage infecting various snakes from a wide geographical distribution was found. Although several improvements over previous works regarding phylogenetic resolution and taxon coverage were achieved in this study, the major polytomy in our tree, composed largely of siluriform parasites from the Neotropics, remained unresolved and possibly reflects a rapid radiation. The genus Spasskyellina Freze, 1965 is resurrected for three species of Monticellia bearing spinitriches on the margins of their suckers.

Keywords: Eucestoda; Proteocephalidae; Spasskyellina; host-parasite associations; molecular phylogeny; systematics.

Figure 1.

Bayesian inference of partial (domains 1–3) 28S rDNA sequences of a reduced taxon set of proteocephalideans (unstable taxa Sciadocephalus megalodiscus, Vermaia pseudotropii and Manaosia bracodemoca have been removed) performed using MrBayes version 3.2 using the GTR + I + G model of sequence evolution. Two parallel runs were performed for 10,000,000 generations; 4,000,000 generations were discarded as burnin. Branches with posterior probability (pp) support below 95% are collapsed; pp are indicated below branches. Asterisks mark new sequences. Red letters A to P refer to specific nodes discussed in the text. Red circles refer to the acquisition of “Type 2” uterus development; purple circles: acquisition of “intermediate type” uterus development; yellow circle: uterus development unknown (see Discussion). A mute phylogram of the same tree is inserted and the long branch leading to Sandonella sandoni is marked with an asterisk.

Figure 1.

Bayesian inference of partial (domains 1–3) 28S rDNA sequences of a reduced taxon set of proteocephalideans (unstable taxa Sciadocephalus megalodiscus, Vermaia pseudotropii and Manaosia bracodemoca have been removed) performed using MrBayes version 3.2 using the GTR + I + G model of sequence evolution. Two parallel runs were performed for 10,000,000 generations; 4,000,000 generations were discarded as burnin. Branches with posterior probability (pp) support below 95% are collapsed; pp are indicated below branches. Asterisks mark new sequences. Red letters A to P refer to specific nodes discussed in the text. Red circles refer to the acquisition of “Type 2” uterus development; purple circles: acquisition of “intermediate type” uterus development; yellow circle: uterus development unknown (see Discussion). A mute phylogram of the same tree is inserted and the long branch leading to Sandonella sandoni is marked with an asterisk.

Figure 2.

Schematic representation of proteocephalidean uterus development (a–c). The uterus observed in early immature, premature, mature, pregravid and gravid proglottids is represented from left to right. The major differences are observed in premature and mature proglottids (dotted line): a and c Development of Type 1 and 2, respectively (de Chambrier et al. 2004c) b Development of an “intermediate type” as observed in Pangasiocestus and Australotaenia (this paper) d Typical “intermediate type” uterus in a mature proglottid of Australotaenia bunthangi de Chambrier & Scholz, 2012 (holotype, MHNG-PLAT-75447). Scale in micrometers.

Figure 3.

A–C Scoleces with rostellum-like organs and retractor muscles. A Without hooks. Ritacestus ritaii (Verma, 1926) (modified from de Chambrier et al. 2011) B With hooks. Gangesia bengalensis (Southwell, 1913) (modified from Ash et al. 2012) C Partly-invaginated. Sagittal section, ho: hooks; rm: retractor muscles; lm; longitudinal muscles. Vermaia pseudotropii (Verma, 1928) (modified from Ash et al. 2010) D–F Egg modifications D Egg cluster in a capsule. Vandiermenia beveridgei (de Chambrier & de Chambrier, 2010) (modified from de Chambrier and de Chambrier 2010) E Egg with two polar projections. Brooksiella praeputialis (Rego, Santos & Silva, 1974) (modified from de Chambrier et al. 2004a) F Eggs with two polar projections. Rudolphiella spp. from Calophysus macropterus (two eggs above) and Megalonema platanum, respectively (modified from Gil de Pertierra and de Chambrier 2000) G–H Ovary size G Relatively large ovary (16.4% proglottid surface) in Gangesia agraensis Verma, 1928 (modified from Ash et al. 2012) H Relatively small ovary in Ophiotaenia lapata Rambeloson, Ranaivoson & de Chambrier (2012) (2.8% of proglottid surface) (modified from Rambeloson et al. 2012). Scale-bars: A, B, C = 100 µm; D, E = 20 µm; F = 50 µm; G = 200 µm; H = 500 µm.