BACKGROUND: The flatworms (Lophotrochozoa: Platyhelminthes) are one of the major phyla of invertebrates but their interrelationships are still not well understood including unravelling the most closely related taxon of the Neodermata, which includes exclusively obligate parasites of all main groups of vertebrates with some 60,000 estimated species. Recent phylogenomic studies indicate that the freshwater 'microturbellarian' Bothrioplana semperi may be the closest ancestor to the Neodermata, but this hypothesis receives little morphological support. Therefore, additional morphological and ultrastructural characters that might help understand interrelations within the Neodermata are needed. METHODS: Ultrastructure of the excretory ducts of representatives of the most basal parasitic flatworms (Neodermata), namely monocotylid (Monopisthocotylea) and chimaericolid (Polyopisthocotylea) monogeneans, aspidogastreans (Trematoda), as well as gyrocotylidean and amphilinidean tapeworms (Cestoda), were studied using transmission electron microscopy (TEM). RESULTS: The present study revealed the same pattern of the cytoarchitecture of excretory ducts in all studied species of the basal neodermatans. This pattern is characterised by the presence of septate junctions between the adjacent epithelial cells and lateral ciliary flames along different levels of the excretory ducts. Additionally, a new character was observed in the protonephridial terminal cell of Gyrocotyle urna, namely a septate junction between terminal and adjacent duct cells at the level of the distal extremity of the flame tuft. In Amphilina foliacea, a new type of protonephridial cell with multiple flame bulbs and unique character of its weir, which consists of a single row of the ribs, is described. A remarkable difference has been observed between the structure of the luminal surface of the excretory ducts of the studied basal neodermatan groups and B. semperi. CONCLUSIONS: The present study does not provide ultrastructural support for a close relationship between the Neodermata and B. semperi.

Institute for Biology of Inland Waters Russian Academy of Sciences Borok Yaroslavl Region 152742 Russia

Institute of Parasitology Biology Centre Biology Centre of the Czech Academy of Sciences České Budějovice Czech Republic

Zobrazit více v PubMed

Caira JN, Littlewood DTJ. Worms, Platyhelminthes. In: Levin SA, editor. Encyclopedia of biodiversity. Waltham: Academic Press; 2013. pp. 437–469.

Egger B, Lapraz F, Tomiczek B, Müller S, Dessimoz C, Girstmair J, et al. A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Curr Biol. 2015;25:1347–1353. PubMed PMC

Laumer CE, Hejnol A, Giribet G. Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation. eLife. 2015;4:e05503. PubMed PMC

Appeltans W, Ahyong ST, Anderson G, Angel MV, Artois T, Bailly N, et al. The magnitude of global marine species diversity. Curr Biol. 2012;22:189–202. PubMed

Laumer CE, Giribet G. Inclusive taxon sampling suggestive of single, stepwise origin of ectolecithality in Platyhelminthes. Biol J Linn Soc. 2014;111:570–588.

Kornakova EE. Ultrastructure of excretory system in Bothrioplana semperi (Platyhelminthes, Turbellaria) Zh Evol Biokh Fiziol. 2010;46:340–346. PubMed

Kornakova EE. The origin and early evolution of Neodermata (Platyhelminthes): 1. On the possible turbellarian roots of the group—morphological approach. Parazitologiya. 2018;52:233–250.

Park JK, Kim KH, Kang S, Kiw W, Eom KS, Littlewood DTJ. A common origin of complex life cycles in parasitic flatworms: evidence from the complete mitochondrial genome of Microcotyle sebastis (Monogenea: Platyhelminthes) BMC Evol Biol. 2007;7:11–24. PubMed PMC

Perkins EM, Donnellan SC, Bertozzi T, Whittington ID. Closing the mitochondrial circle on paraphyly of the Monogenea (Platyhelminthes) infers evolution in the diet of parasitic flatworms. Int J Parasitol. 2010;40:1237–1245. PubMed

Littlewood DTJ, Waeschenbach A. Evolution: a turn up for the worms. Curr Biol. 2015;25:R448–R469. PubMed

Ehlers U. Comments on a phylogenetic system of the Platyhelminthes. Hydrobiologia. 1986;132:1–12.

Rohde K. The evolution of protonephridia of the Platyhelminthes. Hydrobiologia. 1991;227:315–321.

Rohde K. Protonephridia as phylogenetic characters. In: Littlewood DTJ, Bray RA, editors. Interrelationships of the Platyhelminthes. London: Taylor & Francis; 2001. pp. 203–212.

Hertel LA. Excretion and osmoregulation in flatworms. Trans Am Microsc Soc. 1993;112:10–17.

Boeger WA, Kritsky DC. Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. Int J Parasitol. 1997;27:1495–1511. PubMed

Boeger WA, Kritsky DC. Phylogenetic relationships of the Monogenoidea. In: Littlewood DTJ, Bray RA, editors. Interrelationships of the Platyhelminthes. London: Taylor & Francis; 2001. pp. 92–102.

Joveline R, Justine JL. Phylogenetic relationships within the polyopisthocotylean monogenean (Platyhelminthes) inferred from partial 28S rDNA sequences. Int J Parasitol. 2001;31:393–401. PubMed

Olson PD, Littlewood DTJ. Phylogenetics of the Monogenea - evidence from a medley of molecules. Int J Parasitol. 2002;32:233–244. PubMed

Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda) Int J Parasitol. 2003;33:733–755. PubMed

Littlewood DTJ, Bray RA, Waeschenbach A. Phylogenetic patterns of diversity in cestodes and trematodes. In: Morand S, Krasnov BR, Littlewood DTJ, editors. Parasite diversity and diversifications: evolutionary ecology meets phylogenetics. Cambridge: Cambridge University Press; 2015. pp. 304–319.

Pérez-Ponce G, Hernández-Mena DI. Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ Tree of Life. J Helminthol. 2019;93:260–276. PubMed

Olson PD, Littlewood DTJ, Bray RA, Mariaux J. Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda) Mol Phylogen Evol. 2001;19:443–467. PubMed

Lockyer AE, Olson PD, Littlewood DTJ. Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc. 2003;78:155–171.

Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ. Added resolution among ordinal level relationship of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogen Evol. 2007;45:311–325. PubMed

Xylander WER. The Gyrocotylidea, Amphilinidea and the early evolution of the Cestoda. In: Littlewood DTJ, Bray RA, editors. Interrelationships of the Platyhelminthes. London: Taylor & Francis; 2001. pp. 103–111.

Rohde K. The Aspidogastrea, especially Multicotyle purvisi Dawes, 1941. Adv Parasitol. 1972;10:77–151.

Rohde K. Ultrastructure of the protonephridial system of Lobatostoma manteri (Trematoda, Aspidogastrea) Submicrosc Cytol Pathol. 1989;21:599–610.

Watson NA, Rohde K. Ultrastructure of the flame bulbs and protonephridial capillaries of Rugogaster hydrolagi (Platyhelminthes, Trematoda, Aspidogastrea) Ann Parasitol Hum Comp. 1992;67:67–74. PubMed

Xylander WER. Investigations on the protonephridial system of post-larval Gyrocotyle urna and Amphilina foliacea (Cestoda) Int J Parasitol. 1992;22:287–300. PubMed

Rohde K, Cannon LRG, Watson N. Ultrastructure of the protonephridia of Monocelis (Proseriata, Monocelididae) J Submicrosc Cytol Pathol. 1988;20:425–435. PubMed

Rohde K, Watson N, Sluys R. Ultrastructure of the flame bulbs and protonephridial capillaries of Romankenkuis sp. (Platyhelminthes, Tricladida, Dugesiidae) J Submicrosc Cytol Pathol. 1990;22:489–496.

Rohde K, Cannon LRG, Watson N. Ultrastructure of the flame bulbs and protonephridial capillaries of Gieysztoria sp. (Rhabdocoela Dalyelliida), Rhinolasius sp. (Rhabdocoela Kalyptorhynchia) and Actinodactylella blanchardi (Rhabdocoela Temnocephalida) J Submicrosc Cytol. 1988;30:605–612.

Ehlers U, Sopott-Ehlers B. Zum protonephridial System von Invenusta paracnida (Proseriata, Platyhelminthes) Microfauna Marina. 1987;3:377–390.

Rohde K, Watson N. Ultrastructure of the protonephridial system of larval Austramphilina elongata (Platyhelminthes, Amphilinidea) J Submicrosc Cytol. 1987;19:113–118. PubMed

Kuperman BI. Functional morphology of lower cestodes: ontogenetic and evolutionary aspects. Leningrad: Nauka; 1988.

Xylander WER. Ultrastructure of the lycophora larva of Gyrocotyle urna (Cestoda, Gyrocotylidea). III. The protonephridial system. Zoomorphology. 1987;107:88–95.

Rohde K, Watson NA, Roubal FR. Ultrastructure of the protonephridial system of Anoplodiscus cirrusspiralis (Monogenea Monopisthocotylea) Int J Parasitol. 1992;22:443–457. PubMed

Poddubnaya LG, Xylander WER, Gibson DI. Ultrastructural characteristics of the protonephridial terminal organ and associated ducts of adult specimens of the Aspidogastrea, Digenea and Monogenea, with comments on the relationships between these groups. Syst Parasitol. 2012;82:89–104. PubMed

Rohde K, Watson NA. Development of the protonephridia of Austramphilina elongata. Parasitol Res. 1988;74:255–261.

Rohde K, Garlick PR. A multiciliate ‘starcell’ in the parenchyma of the larva of Austramphilina elongata (Amphilinidea) Int J Parasitol. 1985;15:403–407.

Rohde K. The origins of parasitism in the Platyhelminthes. Int J Parasitol. 1994;24:1099–1115. PubMed

Waeschenbach A, Webster BL, Littlewood DTJ. Adding resolution to original level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol Phylogen Evol. 2012;63:834–847. PubMed