Species of Characidotrema Paperna & Thurston, 1968 (Monogenea: Dactylogyridae) from fishes of the Alestidae (Characiformes) in Africa: new species, host-parasite associations and first insights into the phylogeny of the genus

Abstract

Background: African tetras (Alestidae) belonging to Brycinus Valenciennes are known to be parasitized with monogeneans attributed to two genera, Annulotrema Paperna & Thurston, 1969 and Characidotrema Paperna & Thurston, 1968 (Dactylogyridae). During a survey of monogeneans parasitizing alestids, species of Characidotrema were collected in Cameroon, D. R. Congo, Senegal, South Africa, Sudan and Zimbabwe. This paper provides new morphological data and the first molecular analysis broadening our knowledge on the diversity of these parasites.

Results: Seven species (four known and three new) of Characidotrema are reported from two species of Brycinus: C. auritum n. sp. and C. vespertilio n. sp. from B. imberi (Peters); and C. brevipenis Paperna, 1969, C. nursei Ergens, 1973, C. pollex n. sp., C. spinivaginus (Paperna, 1973) and C. zelotes Kritsky, Kulo & Boeger, 1987 from B. nurse (Rüppell). Species identification was based on morphological analysis of the sclerotized structures supported by nuclear ribosomal DNA (partial 18S rDNA, ITS1, and 28S rDNA) sequence data. Morphological analysis confirmed that the most apparent character distinguishing species in the genus is the morphology of the male copulatory organ and vagina. Observations on the haptoral sclerotized elements of these parasites by means of phase contrast microscopy revealed the presence of a sheath-like structure relating to the ventral anchor, a feature that supplements the generic diagnosis of Characidotrema. Maximum Likelihood and Bayesian analyses of the large subunit (28S) rDNA sequences recovered Characidotrema species isolated from the two Brycinus hosts as monophyletic, and indicated a closer relationship of this group to monogeneans parasitizing African cyprinids (Dactylogyrus spp.) and cichlids (species of Cichlidogyrus Paperna, 1960, Scutogyrus Pariselle & Euzet, 1995, and Onchobdella Paperna, 1968) than to those from catfishes (species of Quadriacanthus Paperna, 1961, Schilbetrema Paperna & Thurston, 1968 and Synodontella Dossou & Euzet, 1993). The overall agreement between the morphological diversification of the MCOs and the molecular tree observed in this study indicates that significant phylogenetic signals for clarifying relationships among species of Characidotrema are present in the characteristics of the MCO.

Conclusions: It seems that intra-host speciation is an important force shaping the present distribution and diversity of Characidotrema but further studies are necessary to confirm this hypothesis and assess questions related to the phylogeny of these parasites. To identify potential co-speciation events, co-phylogenetic analyses of these monogeneans and their alestid hosts are required.

Keywords: Africa; Alestidae; Brycinus; Characidotrema; DNA; Dactylogyridae; Diversity; Monogenea.

Fig. 1

Scheme of measurements for sclerotized structures of Characidotrema spp. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar. DB, dorsal bar; H, hook. VAG, vagina; MCO, male copulatory organ; il, inner length; ol, outer length; ir, inner root length; or, outer root length; p, point length; tl, total length; w, width; al, arm lenght; pl, posteromedial projection length; cl, tube curved length; bl, base length; bw, base width; bpa, basal process angle

Fig. 2

Characidotrema brevipenis Paperna, 1969. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 3

Characidotrema nursei Ergens, 1973. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 4

Characidotrema spinivaginus (Paperna, 1973) Kritsky, Kulo & Boeger, 1987. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 5

Characidotrema zelotes Kritsky, Kulo & Boeger, 1987. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 6

Characidotrema pollex Kičinjaová & Řehulková n. sp. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 7

Characidotrema auritum Kičinjaová & Řehulková n. sp. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 8

Characidotrema vespertilio Kičinjaová & Řehulková n. sp. Sclerotized structures. Abbreviations: VA, ventral anchor; DA, dorsal anchor; VB, ventral bar; DB, dorsal bar; I-VII, hooks; VAG, vagina; MCO, male copulatory organ

Fig. 9

Maximum Likelihood tree inferred from the analysis of 28S rDNA sequences including 34 selected species of African Dactylogyridae. Values along branches indicate posterior probabilities and boostrap values resulting from Bayesian Inference (BI) and Maximum Likelihood (ML) analyses. Only values > 0.95 for BI and > 70% for ML are shown. The phylogenetic tree was rooted using three species belonging to the Anoplodiscidae (Anoplodiscus cirrusspiralis Roubal, Armitage & Rohde, 1983) and the Diplectanidae (Diplectanum blaiense Gupta & Khanna, 1974 and Laticola paralatesi (Nagibina, 1976) Yang, Kritsky, Sun, Zhang, Shi & Agrawal, 2006)

Fig. 10

Haptoral sclerotized elements of Characidotrema brevipenis Paperna, 1969 showing the sheath-like structure associated with the shaft and point of the ventral anchors (Phase-contrast micrograph combined with line drawings)

Fig. 11

Maximum Likelihood tree showing the division of Characidotrema spp. in accordance with the morphology of the MCO (a) and vagina (b). Arrows indicate one of the principal characters dividing Characidotrema spp. into two morphological groups