Revision of the systematics of the Polystomoidinae (Platyhelminthes, Monogenea, Polystomatidae) with redefinition of Polystomoides Ward, 1917 and Uteropolystomoides Tinsley, 2017

Abstract

Polystomatids are platyhelminth parasites that infect mainly amphibians and freshwater turtles. For more than seven decades, chelonian polystomes were classified into three genera according to the number of hamuli, i.e. absent for Neopolystoma, one pair for Polystomoidella and two pairs for Polystomoides. Following re-examination of morphological characters, seven new genera were erected the past six years, namely Apaloneotrema, Aussietrema, Fornixtrema, Manotrema, Pleurodirotrema, Uropolystomoides and Uteropolystomoides. However, the polyphyly of Neopolystoma and Polystomoides on the one hand, and the nested position of Uteropolystomoides within a clade encompassing all Neopolystoma and Polystomoides spp. on the other, still raised questions about the validity of these genera. We therefore re-examined several types, paratypes and voucher specimens, and investigated the molecular phylogeny of polystomes sampled from the oral cavity of North American turtles to re-evaluate their systematic status. We show that all Polystomoides Ward, 1917, sensu Du Preez et al., 2022, Neopolystoma Price, 1939, sensu Du Preez et al., 2022 and Uteropolystomoides Tinsley, 2017 species, display vaginae that are peripheral and extend well beyond the intestine. We thus reassign all species of the clade to Polystomoides and propose nine new combinations; however, although Uteropolystomoides is nested within this clade, based on its unique morphological features, we propose to keep it as a valid taxon. Polystomoides as redefined herein groups all polystome species infecting either the oral cavity or the urinary bladder of cryptodires, with peripheral vaginae and with or without two pairs of small hamuli. Uteropolystomoides nelsoni (Du Preez & Van Rooyen 2015), originally described from Pseudemys nelsoni Carr is now regarded as Uteropolystomoides multifalx (Stunkard, 1924) n. comb. infecting three distinct Pseudemys species of North America.

Keywords: Classification; Neopolystoma; Polystomatidae; Polystomoides; Systematics; Uteropolystomoides.

Figure 1

A: Non-lethal procedure for retrieving a polystome from the pharyngeal pouches of a freshwater turtle; B: polystome collected on wooden stem cotton swab.

Figure 2

Micrograph of the reproductive system of Polystomoides multifalx (Stunkard, 1924). Abbreviations: Gb, genital bulb; Te, testis; Ut, Uterus with eggs; Va, vagina. Scale bar = 200 μm.

Figure 3

Bayesian tree inferred from the analysis of COI sequences. Numbers at nodes indicate Bayesian Posterior Probabilities (BPP). Only BPP ≫ 0.95 are indicated. Scale bar reflects expected changes per site. * designates haplotypes characterizing specimens of Polystomoides multifalx (Stunkard, 1924) that were, for some of them, collected from Pseudemys concinna (Le Conte), for the others, from P. floridana (Le Conte) (see Table 3 for more details).

Figure 4

Bayesian tree inferred from the analysis of 28S sequences. Numbers at nodes indicate Bayesian Posterior Probabilities (BPP). Only BPP ≫ 0.95 are indicated. Scale bar reflects expected changes per site. * designates Hnuc20 haplotype that also characterizes specimens of Polystomoides multifalx (Stunkard, 1924) (see Table 3 for more details).

Figure 5

Uteropolystomoides multifalx n. comb. (Stunkard, 1924). A: Full parasite; B: Genital bulb with genital spines; C: Sclerotized haptoral hooks. Abbreviations: Gb, genital bulb; Ha, haptor; Hm, hamulus; Hm1, hamulus 1; Hm2, hamulus 2; Mh1, marginal hooklet 1; Mo, mouth; Ph, pharynx; Su, sucker; Te, testis; Ut, Uterus with eggs; Va, vagina; Vi, vitellarium. Scale bars: A = 500 μm; B = 200 μm; C = 50 μm.