The phylogeny of monogeneans of the genus Thaparocleidus that parasitize the gills of Pangasiidae in Borneo and Sumatra was inferred from molecular data to investigate parasite speciation. The phylogeny of the Pangasiidae was also reconstructed in order to investigate host-parasite coevolutionary history. The monophyly of Thaparocleidus parasitizing Pangasiidae was confirmed. Low intraspecies molecular variability was observed in three Thaparocleidus species collected from geographically distant localities. However, a high intraspecies molecular variability was observed in two Thaparocleidus species suggesting that these species represent a complex of species highly similar in morphology. Distance-based and tree-based methods revealed a significant global fit between parasite and host phylogenies. Parasite duplication (i.e., intrahost speciation) was recognized as the most common event in Thaparocleidus, while the numbers of cospeciation and host switches were lower and similar to each other. When collapsing nodes correspond to duplication cases, our results suggest host switches in the Thaparocleidus-Pangasiidae system precluding congruence between host and parasite trees. We found that the morphometric variability of the parasite attachment organ is not linked to phylogeny, suggesting that the attachment organ is under adaptive constraint. We showed that haptor morphometry is linked to host specificity, whereby nonspecific parasites display higher morphometric variability than specialists.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic ; Laboratory of Biodiversity and Evolutionary Genomics University of Leuven Charles Deberiotstraat 32 3000 Leuven Belgium

Institut de Recherche sur la Biologie de l'Insecte Faculté des Sciences et Techniques UMR CNRS 6035 37200 Tours France

Institut des Sciences de l'Evolution IRD CNRS UM2 Université Montpellier 2 CC065 34095 Montpellier Cedex 05 France

Zobrazit více v PubMed

Coyne JA, Orr HA. The evolutionary genetics of speciation. Philosophical Transactions of the Royal Society B. 1998;353(1366):287–305. PubMed PMC

Via S. Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology and Evolution. 2001;16(7):381–390. PubMed

Coyne JA. Sympatric speciation. Current Biology. 2007;17(18):R787–R788. PubMed

Brooks DR, McLennan DA. Phylogeny, Ecology and Behavior: A Research Program in Comparative Biology. London, UK: The University of Chicago Press; 1991.

McCoy KD. Sympatric speciation in parasites—what is sympatry? Trends in Parasitology. 2003;19(9):400–404. PubMed PMC

Kunz W. When is a parasite species a species? Trends in Parasitology. 2002;18(3):121–124. PubMed

Šimková A, Morand S, Jobet E, Gelnar M, Verneau O. Molecular phylogeny of congeneric monogenean parasites (Dactylogyrus): a case of intrahost speciation. Evolution. 2004;58(5):1001–1018. PubMed

Page RDM. Tangled Trees: Phylogeny, Cospeciation and Coevolution. Chicago, Ill, USA: University of Chicago Press; 2003.

de Vienne DM, Giraud T, Shykoff JA. When can host shifts produce congruent host and parasite phylogenies? A simulation approach. Journal of Evolutionary Biology. 2007;20(4):1428–1438. PubMed

Light JE, Hafner MS. Codivergence in heteromyid rodents (Rodentia: Heteromyidae) and their sucking lice of the genus Fahrenholzia (Phthiraptera: Anoplura) Systematic Biology. 2008;57(3):449–465. PubMed

Humphery-Smith I. The evolution of phylogenetic specificity among parasitic organisms. Parasitology Today. 1989;5(12):385–387. PubMed

Hafner MS, Nadler SA. Phylogenetic trees support the coevolution of parasites and their hosts. Nature. 1988;332(6161):258–259. PubMed

Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science. 1994;265(5175):1087–1090. PubMed

Roberts LS, Javony JJ. Foundations of Parasitology. Dubuque, Iowa, USA: William C. Brown; 1996.

Poulin R. Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology. 1992;22(6):753–758. PubMed

Šimková A, Desdevises Y, Gelnar M, Morand S. Co-existence of nine gill ectoparasites (Dactylogyrus: Monogenea) parasitising the roach (Rutilus rutilus L.): history and present ecology. International Journal for Parasitology. 2000;30(10):1077–1088. PubMed

Desdevises Y, Morand S, Jousson O, Legendre P. Coevolution between Lamellodiscus (Monogenea: Diplectanidae) and Sparidae (Teleostei): the study of a complex host-parasite system. Evolution. 2002;56(12):2459–2471. PubMed

Zietara MS, Lumme J. Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae) Evolution. 2002;56(12):2445–2458. PubMed

Huyse T, Volckaert FAM. Comparing host and parasite phylogenies: Gyrodactylus flatworms jumping from goby to goby. Systematic Biology. 2005;54(5):710–718. PubMed

Plaisance L, Littlewood DTJ, Olson PD, Morand S. Molecular phylogeny of gill monogeneans (Platyhelminthes, Monogenea, Dactylogyridae) and colonization of Indo-West Pacific butterflyfish hosts (Perciformes, Chaetodontidae) Zoologica Scripta. 2005;34(4):425–436.

Mendlová M, Desdevises Y, Civáňová K, Pariselle A, Šimková A. Monogeneans of West African cichlid fish: evolution and cophylogenetic interactions. PloS ONE. 2012;7(5)e37268 PubMed PMC

Rohde K. Critical evaluation of intrinsic and extrinsic factors responsible for niche restriction in parasites. The American Naturalist. 1979;114(5):648–671.

Morand S, Šimková A, Matějusová I, Plaisance L, Verneau O, Desdevises Y. Investigating patterns may reveal processes: evolutionary ecology of ectoparasitic monogeneans. International Journal for Parasitology. 2002;32(2):111–119. PubMed

Šimková A, Pečínková M, Řehulková E, Vyskočilová M, Ondračková M. Dactylogyrus species parasitizing European Barbus species: morphometric and molecular variability. Parasitology. 2007;134(12):1751–1765. PubMed

Kaci-Chaouch T, Verneau O, Desdevises Y. Host specificity is linked to intraspecific variability in the genus Lamellodiscus (Monogenea) Parasitology. 2008;135(5):607–616. PubMed

Lim LHS, Timofeeva TA, Gibson DI. Dactylogyridean monogeneans of the siluriform fishes of the Old World. Systematic Parasitology. 2001;50(3):159–197. PubMed

Wu X-Y, Zhu X-Q, Xie M-Q, Wang JQ, Li A-X. The radiation of Thaparocleidus (Monogenoidea: Dactylogyridae: Ancylodiscoidinae): phylogenetic analyses and taxonomic implications inferred from ribosomal DNA sequences. Parasitology Research. 2008;102(2):283–288. PubMed

Pariselle A, Lim LHS, Lambert A. Monogeneans from Pangasiidae (Siluriformes) in Southeast Asia: X. Six new species of Thaparocleidus Jain, 1952 (Ancylodiscoididae) from Pangasius micronema . Parasite. 2006;13(4):283–290. PubMed

Roberts TR, Vidthayanon C. Systematic revision of the Asian catfish family Pangasiidae, with biological observations and descriptions of three new species. Proceedings of the Academy of Natural Sciences of Philadelphia. 1991;143:97–144.

Pouyaud L, Teugels GG, Gustiano R, Legendre M. Contribution to the phylogeny of pangasiid catfishes based on allozymes and mitochondrial DNA. Journal of Fish Biology. 2000;56(6):1509–1538.

Voris HK. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography. 2000;27(5):1153–1167.

Lim LHS. Silurodiscoides Gussev, 1961 (Monogenea: Ancyrocephalidae) from Pangasius sutchi Fowler, 1931 (Pangasiidae) cultured in Penninsular Malaysia. Raffles Bulletin of Zoology. 1990;38(1):55–53.

Pariselle A, Lim LHS, Lambert A. Monogeneans from Pangasiidae (Siluriformes) in Southeast Asia: III. Five new species of Thaparocleidus Jain, 1952 (Ancylodiscoididae) from Pangasius bocourti, P. djambal and P. hypophthalmus . Parasite. 2002;9(3):207–217. PubMed

Pariselle A, Lim LHS, Lambert A. Monogeneans from Pangasiidae (Siluriformes) in Southeast Asia: V. Five new species of Thaparocleidus Jain, 1952 (Ancylodiscoididae) from Pangasius nasutus . Parasite. 2003;10(4):317–323. PubMed

Pariselle A, Lim LHS, Lambert A. Monogeneans from pangasiidae (Siluriformes) in Southeast Asia: VII. Six new host-specific species of Thaparocleidus Jain, 1952 (Ancylodiscoididae) from Pangasius polyuranodon . Parasite. 2004;11(4):365–372. PubMed

Pariselle A, Lim LHS, Lambert A. Monogeneans from Pangasiidae (Siluriformes) in Southeast Asia: VIII. Four new non-specific species of Thaparocleidus Jain, 1952 (Ancylodiscoididae) from Pangasius polyuranodon and P. elongatus . Parasite. 2005;12(1):23–29. PubMed

Pariselle A, Lim LHS, Lambert A. Monogeneans from Pangasiidae (Siluriformes) in Southeast Asia: IX. Two new species of Thaparocleidus Jain, 1952 (Ancylodiscoididae) from Pangasius mahakamensis . Parasite. 2005;12(4):325–329. PubMed

Euzet L, Combes C. Les problèmes de l’espèce chez les animaux parasites. In: Boquet C, Genermont J, Lamotte M, editors. Les Problèmes de l’espèce dans le Règne Animal. Vol. 40. 1980. pp. 239–285. (Memoires de la Societé zoologique de France).

Sinnappah ND, Lim LHS, Rohde K, Tinsley R, Combes C, Verneau O. A paedomorphic parasite associated with a neotenic amphibian host: phylogenetic evidence suggests a revised systematic position for Sphyranuridae within anuran and turtle Polystomatoineans. Molecular Phylogenetics and Evolution. 2001;18(2):189–201. PubMed

Šimková A, Plaisance L, Matějusová I, Morand S, Verneau O. Phylogenetic relationships of the Dactylogyridae Bychowsky, 1933 (Monogenea: Dactylogyridea): the need for the systematic revision of the Ancyrocephalinae Bychowsky, 1937. Systematic Parasitology. 2003;54(1):1–11. PubMed

Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research. 1994;22(22):4673–4680. PubMed PMC

Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Research. 1999;41(41):95–98.

Swofford DL. PAUP*: Phylogenetic Analysis Using Parsimony and Other Methods. Sunderland, Mass, USA: Sinauer Associates; 2002. (Version 4.0b10).

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12):1572–1574. PubMed

Posada D, Crandall KA. Modeltest: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. PubMed

Rzhetsky A, Nei M. A simple method for estimating and testing minimum-evolution trees. Molecular Biology and Evolution. 1992;9(5):945–967.

Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39(4):783–791. PubMed

Wahlberg N, Weingartner E, Nylin S. Towards a better understanding of the higher systematics of Nymphalidae (Lepidoptera: Papilionoidea) Molecular Phylogenetics and Evolution. 2003;28(3):473–484. PubMed

Yang J, He S, Freyhof J, Witte K, Liu H. The phylogenetic relationships of the Gobioninae (Teleostei: Cyprinidae) inferred from mitochondrial cytochrome b gene sequences. Hydrobiologia. 2006;553(1):255–266.

Kumar S, Tamura K, Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics. 2004;5(2):150–163. PubMed

Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics. 2005;21(9):2104–2105. PubMed

Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology. 2003;52(5):696–704. PubMed

Legendre P, Desdevises Y, Bazin E. A statistical test for host-parasite coevolution. Systematic Biology. 2002;51(2):217–234. PubMed

Meier-Kolthoff JP, Auch AF, Huson DH, Göker M. CopyCat: cophylogenetic analysis tool. Bioinformatics. 2007;23(7):898–900. PubMed

Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms for Molecular Biology. 2010;5, article 16 PubMed PMC

Page RDM. Parallel phylogenies: reconstructing the history of host-parasite assemblages. Cladistics. 1994;10(2):155–173.

Ronquist F. TreeFitter, program and documentation. 2001, http://www.softpedia.com/progMoreBy/Publisher-Fredrik-Ronquist-Maxim-Teslenko 83341.html.

Douady CJ, Delsuc F, Boucher Y, Doolittle WF, Douzery EJP. Comparison of bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Molecular Biology and Evolution. 2003;20(2):248–254. PubMed

Pol D, Siddall ME. Biases in maximum likelihood and parsimony: a simulation approach to a 10-taxon case. Cladistics. 2001;17(3):266–281. PubMed

Gusev AV. Identification of Freshwater Fish Parasites. Leningrad, Russia: Nauka; 1985.

Pouyaud L, Desmarais E, Deveney M, Pariselle A. Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications. Molecular Phylogenetics and Evolution. 2006;38(1):241–249. PubMed

Wu X-Y, Zhu X-Q, Xie M-Q, Li A-X. The evaluation for generic-level monophyly of Ancyrocephalinae (Monogenea, Dactylogyridae) using ribosomal DNA sequence data. Molecular Phylogenetics and Evolution. 2007;44(2):530–544. PubMed

Blasco-Costa I, Míguez-Lozano R, Sarabeev V, Balbuena JA. Molecular phylogeny of species of Ligophorus (Monogenea: Dactylogyridae) and their affinities within the Dactylogyridae. Parasitology International. 2012;61:619–627. PubMed

Vignon M, Pariselle A, Vanhove MPM. Modularity in attachment organs of African Cichlidogyrus (Platyhelminthes: Monogenea: Ancyrocephalidae) reflects phylogeny rather than host specificity or geographic distribution. Biological Journal of the Linnean Society. 2011;102(3):694–706.

Šimková A, Verneau O, Gelnar M, Morand S. Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution. 2006;60(5):1023–1037. PubMed

Jarkovský J, Morand S, Šimková A, Gelnar M. Reproductive barriers between congeneric monogenean parasites (Dactylogyrus: Monogenea): attachment apparatus morphology or copulatory organ incompatibility? Parasitology Research. 2004;92(2):95–105. PubMed

Morand S, Šimková A, Gourbière S. Beyond the paradigms of cospeciation and host-switch: is sympatric speciation an important mode of speciation for parasites? Life and Environment. 2008;58(2):125–132.

Šimková A, Ondračková M, Gelnar M, Morand S. Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation? Biological Journal of the Linnean Society. 2002;76(1):125–135.

Giraud T, Gladieux P, Gavrilets S. Linking the emergence of fungal plant diseases with ecological speciation. Trends in Ecology and Evolution. 2010;25(7):387–395. PubMed PMC

Bentz S, Leroy S, Du Preez L, Mariaux J, Vaucher C, Verneau O. Origin and evolution of African Polystoma (Monogenea: Polystomatidae) assessed by molecular methods. International Journal for Parasitology. 2001;31(7):697–705. PubMed

de Vienne DM, Refrégier G, López-Villavicencio M, Tellier A, Hood ME, Giraud T. Cospeciation versus host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytologist. 2013;198(2):347–385. PubMed

Beyond morphology: cryptic diversity in 9 new Gyrodactylus species (Monogenea: Gyrodactylidae) associated with northwest African barbels (Cyprinidae) and remarks on Gyrodactylus nyingiae Shigoley, Rahmouni, Louizi, Pariselle and Vanhove, 2023

Host-specific monogeneans parasitizing freshwater fish: The ecology and evolution of host-parasite associations

Uncovering the monogenean species diversity of cyprinoid fish in Iraq using an integrative approach

Hidden biodiversity in an ancient lake: phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites