BACKGROUND: Parasite switches to new host species are of fundamental scientific interest and may be considered an important speciation mechanism. For numerous monogenean fish parasites, infecting different hosts is associated with morphological adaptations, in particular of the attachment organ (haptor). However, haptoral morphology in Cichlidogyrus spp. (Monogenea, Dactylogyridea), parasites of African cichlids, has been mainly linked to phylogenetic rather than to host constraints. Here we determined the position of Cichlidogyrus amieti, a parasite of species of Aphyosemion (Cyprinodontiformes, Nothobranchiidae) in the phylogeny of its congeners in order to infer its origin and assess the morphological changes associated with host-switching events. METHODS: The DNA of specimens of C. amieti isolated from Aphyosemion cameronense in Cameroon was sequenced and analyzed together with that of Cichlidogyrus spp. from cichlid hosts. In order to highlight the influence of the lateral transfer of C. amieti on the haptoral sclerotised parts we performed a Principal Component Analysis (PCA) to compare the attachment organ structure of C. amieti to that of congeners infecting cichlids. RESULTS: Cichlidogyrus amieti was found to be nested within a strongly supported clade of species described from Hemichromis spp. (i.e. C. longicirrus and C. dracolemma). This clade is located at a derived position of the tree, suggesting that C. amieti transferred from cichlids to Cyprinodontiformes and not inversely. The morphological similarity between features of their copulatory organs suggested that C. amieti shares a recent ancestor with C. dracolemma. It also indicates that in this case, these organs do not seem subjected to strong divergent selection pressure. On the other hand, there are substantial differences in haptoral morphology between C. amieti and all of its closely related congeners described from Hemichromis spp.. CONCLUSIONS: Our study provides new evidence supporting the hypothesis of the adaptive nature of haptor morphology. It demonstrates this adaptive component for the first time within Cichlidogyrus, the attachment organs of which were usually considered to be mainly phylogenetically constrained.

Biology Department Royal Museum for Central Africa Leuvensesteenweg 13 B 3080 Tervuren Belgium

Department of Biological Sciences University of Ngaoundéré BP 454 Ngaoundéré Cameroon

Department of Biology Laboratory of Biodiversity and Evolutionary Genomics University of Leuven Charles Debériotstraat 32 B 3000 Leuven Belgium

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

Institut des Sciences de l'Évolution IRD UMR 226 CNRS UMR 5554 Université de Montpellier CC 63 Place Eugène Bataillon 34095 Montpellier Cedex 05 France

Laboratory of Parasitology and Ecology Faculty of Sciences University of Yaoundé 1 BP 812 Yaoundé Cameroon

Present address Capacities for Biodiversity and Sustainable Development Operational Directorate Natural Environment Royal Belgian Institute of Natural Sciences Vautierstraat 29 B 1000 Brussels Belgium

Present address Department of Biological Sciences Higher Teacher Training College University of Yaoundé 1 P O Box 47 Yaoundé Cameroon

Present address IRD BP 1857 Yaoundé Cameroon

Zobrazit více v PubMed

Parenti LR. A phylogenetic and biogeographic analysis of cyprinodontiform fishes (Teleostei, Atherinomorpha) Bull. American Mus. Nat. Hist. 1981;168:335–557.

Amiet J-L. Faune du Cameroun. Compiègne: Sciences Nat; 1987.

Stiassny MLJ, Teugels GG, Hopkins CD. Poissons d’eaux douces et saumâtres de basse Guinée, ouest de l’Afrique centrale. Paris: IRD, MnHn, MRAC; 2007.

Basolo AL, Wagner WE., Jr Covariation between predation risk, body size and fin elaboration in the green swordtail, Xiphophorus helleri. Biol. J. Linn. Soc. 2004;83:87–100. doi: 10.1111/j.1095-8312.2004.00369.x. DOI

Reznick D, Bryant M, Holmes D. The evolution of senescence and post-reproductive lifespan in Guppies (Poecilia reticulata) PLoS Biol. 2006;4:136–43. doi: 10.1371/journal.pbio.0040136. PubMed DOI PMC

Dargent F, Scott ME, Hendry AP, Fussmann GF. Experimental elimination of parasites in nature leads to the evolution of increased resistance in hosts. Proc. Roy. Soc. B. 2013;280:20132371. doi: 10.1098/rspb.2013.2371. PubMed DOI PMC

Genade T, Benedetti M, Terzibasi E, Roncaglia P, Valenzano DR, Cattaneo A, Cellerino A, et al. Annual fishes of the genus Nothobranchius as a model system for aging research. Aging Cell. 2005;4:223–33. doi: 10.1111/j.1474-9726.2005.00165.x. PubMed DOI

Valenzano DR, Terzibasi E, Cattaneo A, Domenici L, Cellerino A. Temperature affects longevity and age-related locomotor and cognitive decay in the short-lived fish Nothobranchius furzeri. Aging Cell. 2006;5:275–8. doi: 10.1111/j.1474-9726.2006.00212.x. PubMed DOI

Terzibasi E, Lefrançois C, Domenici P, Hartmann N, Graf M, Cellerino A. Effects of dietary restriction on mortality and age-related phenotypes in the short-lived fish Nothobranchius furzeri. Aging Cell. 2009;8:88–99. doi: 10.1111/j.1474-9726.2009.00455.x. PubMed DOI

Cellerino A, Valenzano DR, Reichard M. From the bush to the bench: the annual Nothobranchius fishes as a new model system in biology. Biol. Rev. 2015;doi: 10.1111/brv.12183. PubMed

Reznick DN, Endler JA. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata) Evolution. 1982;36:125–48. PubMed

Reznick DN, Shaw FH, Rodd FH, Shaw RG. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata) Science. 1997;275:1934–7. doi: 10.1126/science.275.5308.1934. PubMed DOI

van Oosterhout C, Trigg RE, Carvalho GR, Magurran AE, Hauser L, Shaw PW. Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J. Evol. Biol. 2003;16:273–81. doi: 10.1046/j.1420-9101.2003.00511.x. PubMed DOI

van Oosterhout C, Joyce DA, Cummings SM. Evolution of MHC class IIB in the genome of wild and ornamental guppies, Poecilia reticulata. Heredity. 2006;97:111–8. doi: 10.1038/sj.hdy.6800843. PubMed DOI

Bartáková V, Reichard M, Janko K, Polačik M, Blažek R, Reichwald K, Cellerino A, Bryja J, et al. Strong population genetic structuring in an annual fish, Nothobranchius furzeri, suggests multiple savannah refugia in southern Mozambique. BMC Evol. Biol. 2013;13:196. doi: 10.1186/1471-2148-13-196. PubMed DOI PMC

Pinceel T, Vanschoenwinkel B, Deckers P, Grégoir A, Ver Eecke T, Brendonck L. Early and late developmental arrest as complementary embryonic bet‐hedging strategies in African killifish. Biol. J. Lin. Soc. 2015;doi: 10.1111/bij.12474.

Cable J, van Oosterhout C. The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biol. J. Linn. Soc. 2007;90:647–55. doi: 10.1111/j.1095-8312.2006.00755.x. DOI

King TA, van Oosterhoutj C, Cable J. Experimental infections with the tropical monogenean, Gyrodactylus bullatarudis: potential invader or experimental fluke? Parasitol. Int. 2009;58:249–54. doi: 10.1016/j.parint.2009.04.005. PubMed DOI

Pariselle A, Morand S, Deveney M, Pouyaud L. Parasite species richness of closely related hosts: historical scenario and “genetic” hypothesis. In: Combes C, Jourdane J, editors. Taxonomy, Ecology and Evolution of Metazoan Parasites. Perpignan: Presses de l’Université de Perpignan; 2003. pp. 147–66.

Vanhove MPM, Huyse T. Host-specificity and species-jumps in fish-parasite systems. In: Morand S, Krasnov B, Littlewood DTJ, editors. Parasite diversity and diversification: evolutionary ecology meets phylogenetics. Cambridge: Cambridge University Press; 2015. pp. 401–19.

Cable J, van Oosterhout C, Barson N, Harris PD. Gyrodactylus pictae n. sp. (Monogenea: Gyrodactylidae) from the Trinidadian swamp guppy Poecilia picta Regan, with a discussion on species of Gyrodactylus von Nordmann, 1832 and their poeciliid hosts. Syst Parasitol. 2005;60:159–64. doi: 10.1007/s11230-004-6348-4. PubMed DOI

Christison KW, Shinn AP, van As JG. Gyrodactylus thlapi n. sp (Monogenea) from Pseudocrenilabrus philander philander (Weber) (Cichlidae) in the Okavango Delta, Botswana. Syst. Parasitol. 2005;60:165–73. doi: 10.1007/s11230-004-6342-x. PubMed DOI

Birgi E, Euzet L. Monogènes parasites des poissons des eaux douces du Cameroun. Présence des genres Cichlidogyrus et Dactylogyrus chez Aphyosemion (Cyprinodontidae) Bull. Soc. Zool. Fr. 1983;108:101–6.

Brosset A. Le peuplement des Cyprinodontes du bassin de l'Ivindo. Gabon. Rev. Ecol. (Terre Vie) 1982;36:233–92.

Paperna I. Studies on Monogenetic Trematodes in Israel. 2 Monogenetic Trematodes of Cichlids. Bamidgeh. Bull. Fish Cult. Israel. 1960;12:20–33.

Paperna I. Monogenea of inland water fish in Africa. Ann. Mus. Roy. Afri. Centr. – Sci. Zool. 1979;226:1–131.

Bauer ON. Spread of parasites and diseases of aquatic organism by acclimatization: a short review. J. Fish Biol. 1991;39:679–86. doi: 10.1111/j.1095-8649.1991.tb04398.x. DOI

Bakke T, Harris P, Cable J. The biology of gyrodactylid monogeneans: the “Russian-doll Killers”. Adv. Parasitol. 2007;64:161–376. doi: 10.1016/S0065-308X(06)64003-7. PubMed DOI

Cooper N, Griffin R, Franz M, Omotayo M, Nunn CL. Phylogenetic host specificity and understanding parasite sharing in primates. Ecol. Let. 2012;15:1370–7. doi: 10.1111/j.1461-0248.2012.01858.x. PubMed DOI

Barson M, Přikrylová I, Vanhove MPM, Huyse T. Parasite hybridization in African Macrogyrodactylus spp. (Monogenea, Platyhelminthes) signals historical host distribution. Parasitology. 2010;137:1585–95. doi: 10.1017/S0031182010000302. PubMed DOI

Pariselle A, Boeger WA, Snoeks J, Bilong Bilong CF, Morand S, Vanhove MPM. The monogenean parasite fauna of Cichlids: a potential tool for host biogeography. Int. J. Evol. Biol. 2011;doi:10.4061/2011/471480. PubMed PMC

Brant SV, Loker ES. Can specialized pathogens colonize distantly related hosts? Schistosome evolution as a case study. PLoS Pathog. 2005;1:e38. doi: 10.1371/journal.ppat.0010038. PubMed DOI PMC

Pouyaud L, Desmarais E, Deveney M, Pariselle A. Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): Systematic and evolutionary implications. Mol. Phyl. Evol. 2006;38:241–9. doi: 10.1016/j.ympev.2005.08.013. PubMed DOI

Mendlová M, Pariselle A, Vyskočilová M, Šimková A. Molecular phylogeny of monogeneans parasitizing African, freshwater Cichlidae inferred from LSU rDNA sequences. Parasitol. Res. 2010;107:1405–13. doi: 10.1007/s00436-010-2008-6. PubMed DOI

Mendlová M, Desdevises Y, Civáňová K, Pariselle A, Šimková A. Monogeneans of West African Cichlid Fish: Evolution and Cophylogenetic Interactions. PLoS One. 2012;7:1–17. doi: 10.1371/journal.pone.0037268. PubMed DOI PMC

Mendlová M, Šimková A. Evolution of host specificity in monogeneans parasitizing African cichlid fish. Parasit. Vect. 2014;7:2–14. doi: 10.1186/1756-3305-7-69. PubMed DOI PMC

Stiassny MLJ. Phylogenetic intrarelationships of the family Cichlidae: an overview. In: Keenleyside MHA, editor. Cichlid fishes: behaviour, ecology and evolution. London: Chapman and Hall; 1991. pp. 1–35.

Murray AM. The fossil record and biogeography of the Cichlidae (Actinopterygii: Labroidei) Biol. J. Linn. Soc. 2001;78:517–32. doi: 10.1111/j.1095-8312.2001.tb01409.x. DOI

Vences M, Freyhof J, Sonnenberg R, Kosuch J, Veith M. Reconciling fossils and molecules: Cenozoic divergence of cichlid fishes and the biogeography of Madagascar. J. Biogeogra. 2001;28:1091–9. doi: 10.1046/j.1365-2699.2001.00624.x. DOI

Friedman M, Keck BP, Dornburg A, Eyta RI, Martin CH, Hulsey CD, et al. Molecular and fossil evidence place the origin of cichlid fishes long after Gondwanan rifting. Proc. Roy. Soc. B: Biol. Sci. 2013;280:20131733. doi: 10.1098/rspb.2013.1733. PubMed DOI PMC

Rakotofiringa S, Euzet L. Monogènes parasites de Cichlidae (Teleostei) endémiques de Madagascar. Bull. Soc. Zool. Fr. 1983;108:107–14.

Euzet L, Combes C. Les problèmes de l'espèce chez les animaux parasites. Mém. Soc. Zool. Fr. 1980;40:239–85.

Ziętara MS, Lumme J. Speciation by host-switching and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae) Evolution. 2002;56:2445–58. doi: 10.1111/j.0014-3820.2002.tb00170.x. PubMed DOI

Boeger WA, Kritsky DC, Pie MR. Context of diversification of the viviparous Gyrodactylidae (Platyhelminthes, Monogenoidea) Zool. Scr. 2003;32:437–48. doi: 10.1046/j.1463-6409.2003.00130.x. PubMed DOI PMC

Bueno-Silva M, Boeger WA, Pie MR. Choice matters: incipient speciation in Gyrodactylus corydori (Monogenoidea: Gyrodactylidae) Int. J. Parasitol. 2011;41:657–67. doi: 10.1016/j.ijpara.2011.01.002. PubMed DOI

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. Biol. J. Linn. Soc. 2011;102:694–706. doi: 10.1111/j.1095-8312.2010.01607.x. DOI

Sonnenberg R. Description of three new species of the genus Chromaphyosemion Radda, 1971 (Cyprinodontiformes:Nothobranchiidae) from the coastal plains of Cameroon with a preliminary review of the Chromaphyosemion splendopleure complex. Zootaxa. 2007;1591:1–38.

Malmberg G . On the occurence of Gyrodactylus on Swedish fishes. 1956. pp. 19–76.

Marchiori N, Pariselle A, Pereira J, Jr, Agnèse J-F, Durand J-D, Vanhove MPM. A comparative study of Ligophorus uruguayense and Ligophorus saladensis (Monogenea, Ancyrocephalidae) from Mugil liza (Teleostei, Mugilidae) in southern Brazil. Folia Parasit. 2015;62:024. doi: 10.14411/fp.2015.024. PubMed DOI

Wu XY, Chilton NB, Zhu XQ, Xie MQ, Li AX. Molecular and morphological evidence indicates that Pseudorhabdosynochus lantauensis (Monogenea: Diplectanidae) represents two species. Parasitol. 2005;130:669–77. doi: 10.1017/S0031182004007152. PubMed DOI

Hall TA. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 1999;41:95–8.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011;28:2731–9. doi: 10.1093/molbev/msr121. PubMed DOI PMC

Schwarz G. Estimating the dimension of a model. Ann. Stat. 1978;6:461–4. doi: 10.1214/aos/1176344136. DOI

Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91. doi: 10.2307/2408678. PubMed DOI

Ergens R, Gelnar M. Experimental verification of the effect of temperature on the size of hard parts of opisthaptor of Gyrodactylus katharineri Malmberg, 1964. Folia Parasitol. (Praha). 1985;32:377–80.

Appleby C. Variability of the opisthaptoral hard parts of Gyrodactylus callariatis Malmberg, 1957 (Monogenea: Gyrodactylidae) from Atlantic cod Gadus morhua L. in the Oslo Fjord, Norway. Syst. Parasitol. 1996;33:199–207. doi: 10.1007/BF01531201. DOI

Mizelle JD. New species of trematodes from the gills of Illinois fishes. Am Midl Nat. 1936;17:785–806. doi: 10.2307/2420687. DOI

Pariselle A, Euzet L. Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosys. 2009;31:849–98. doi: 10.5252/z2009n4a6. DOI

Markevich AP. Parasitic diseases of fish and their control. Publ. Koiz., Leningrad. 1934;3–100. in Russian.

Dossou C, Birgi E. Monogènes parasites d'Hemichromis fasciatus Peters, 1857 (Teleostei, Cichlidae) Ann Sci Nat Zool. 1984;6:101–9.

Paperna I. Monogenetic Trematodes collected from fresh water fish in southern Ghana. Bamidgeh, Bull. Fish Cult. 1965;17:107–15.

Pariselle A, Euzet L. Two new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) gill parasites on Hemichromis fasciatus Peters, 1858 in Africa, with remarks on parasite geographical distribution. Parasite. 2004;11:359–64. doi: 10.1051/parasite/2004114359. PubMed DOI

Řehulková E, Mendlov M, Šimková A. Two new species of Cichlidogyrus (Monogenea: Dactylogyridae) parasitizing the gills of African cichlid fishes (Perciformes) from Senegal: morphometric and molecular characterization. Parasitol. Res. 2013;112:1399–410. doi: 10.1007/s00436-013-3291-9. PubMed DOI

Young PC. Ten new species of Haliotrema Johnston and Tiegs, 1922 (Monogenoidea: Dactylogyridae) from Australian fishes and a revision of the genus. J. Zool. 1968;154:41–75. doi: 10.1111/j.1469-7998.1968.tb05039.x. DOI

Bychowsky BE, Nagibina LF. Ancyrocephalinae (Monogenoidea, Dactylogyridae) from the sea fishes of the family Pomadasyidae. An. Instit. Biolo. Uni. Nacio. Autón. México. Ser. Zool. 1970;41:19–28.

Euzet L, Suriano DM. Ligophorus n. g. (Monogenea, Ancyrocephalidae) parasite des Mugilidae (Téléostéens) en Méditerranée. Bull. Mus. Nat. Hist. Nat. 1977;472:799–822.

Rubtsova NY, Balbuena JA, Sarabeev VL, Blasco-Costa I, Euzet L. Description and morphological variability of a new species of Ligophorus and Ligophorus chabaudi (Monogenea: Dactylogyridae) on Mugil cephalus (Teleostei) from the Mediterranean basin. J. Parasitol. 2006;92:486–95. doi: 10.1645/GE-747R.1. PubMed DOI

Yamaguti S. Studies on the helminth fauna of Japan. Part 19. Fourteen new ectoparasitic trematodes of fishes. Kyoto, Japan: Published by the author. 1937:1-28.

Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993;10:512–26. PubMed

Pariselle A, Euzet L. Three new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) parasitic on Tylochromis jentinki (Steindachner, 1895) (Pisces, Cichlidae) in West Africa. Syst. Parasitol. 1994;29:229–34. doi: 10.1007/BF00009678. DOI

Dossou C. Parasites de Poissons d'eau douce du Bénin III. Espèces nouvelles du genre Cichlidogyrus (Monogenea) parasites de Cichlidae. Bull IFAN. 1982;44:295–322.

Pariselle A, Bilong Bilong CF, Euzet L. Four new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae), all gill parasites from African mouthbreeder tilapias of the genera Sarotherodon and Oreochromis (Pisces, Cichlidae), with a redescription of C. thurstonae Ergens, 1981. Syst Parasitol. 2003;56:201–10. doi: 10.1023/B:SYPA.0000003807.27452.bd. PubMed DOI

Ergens R. Nine species of the genus Cichlidogyrus Paperna, 1960 (Monogenea: Ancyrocephalinae) from egyptian fishes. Folia Parasitol. (Praha). 1981;28:205–14.

Pariselle A, Euzet L. Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae): gill parasites from West African Cichlidae of the subgenus Coptodon Regan, 1920 (Pisces), with descriptions of six new species. Syst. Parasitol. 1996;34:109–24. doi: 10.1007/BF00009685. DOI

Paperna I, Thurston JP. Monogenetic trematodes collected from cichlid fish in Uganda; including the description of five new species of Cichlidogyrus. Rev. Zool. Bot. Afri. 1969;LXXIX:15–33.

Paperna I. Parasitic helminths of inland-water fishes in Israel. Israel J. Zool. 1964;13:1–26.

Price CE, Kirk RG. First description of a monogenetic trematode from Malawi. Rev. Zool. Bot. Afri. 1967;76:137–44.

Pariselle A, Muterezi Bukinga F, Van Steenberge M, Vanhove MPM. Ancyrocephalidae (Monogenea) of Lake Tanganyika: IV: Cichlidogyrus parasitizing species of Bathybatini (Teleostei, Cichlidae): reduced host-specificity in the deepwater realm? In: Koblmüller S, Albertson RC, Genner MJ, Sefc KM, Takahashi T, editors. Advances in cichlid research: Behavior, ecology and evolutionary biology. Hydrobiologia. 2015;748:99–119. doi: 10.1007/s10750-014-1975-5. DOI

Bilong Bilong CF, Birgi E, Euzet L. Enterogyrus barombiensis n. sp. (Monogenea, Ancyrocephalidae) parasite stomacal de trois Cichlidae endémiques du Lac du cratère Barombi Mbo (Cameroun) Ann. Parasitol. Hum Comp. 1991;66:105–8.

Kaneko JJ, II, Yamada R, Brock JA, Nakamura RM. Infection of tilapia, Oreochromis mossambicus (Trewavas), by a marine monogenean, Neobenedenia melleni (MacCallum, 1927) Yamaguti, 1963 in Kaneohe Bay, Hawaii, USA, and its treatment. J. Fish Disea. 1988;11:295–300. doi: 10.1111/j.1365-2761.1988.tb01225.x. DOI

Cable J, Scott ECG, Tinsley RC, Harris PD. Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. J. Parasitol. 2002;88:183–4. doi: 10.1645/0022-3395(2002)088[0183:BFTITV]2.0.CO;2. PubMed DOI

Huyse T, Audenaert V, Volckaert FAM. Speciation and host-parasite relationships in the parasite genus Gyrodactylus (Monogenea, Platyhelminthes) infecting gobies of the genus Pomatoschistus (Gobiidae, Teleostei) Int. J. Parasitol. 2003;33:1679–89. doi: 10.1016/S0020-7519(03)00253-4. PubMed DOI

Pariselle A, Bitja Nyom AR, Bilong Bilong CF. Checklist of the ancyrocephalids (Monogenea) parasitizing Tilapia species in Cameroon, with the description of three new species. Zootaxa. 2013;3599:78–86. doi: 10.11646/zootaxa.3599.1.7. PubMed DOI

Pérez-Ponce de Léon G, Choudhury A. Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. J. Biogeogra. 2005;32:645–59. doi: 10.1111/j.1365-2699.2005.01218.x. DOI

Bilong Bilong CF. Les Monogènes parasites des poissons d’eau douce du Cameroun : biodiversité et spécificité; biologie des populations inféodées à Hemichromis fasciatus. Thèse de Doctorat d’État, Université de Yaoundé I, Yaoundé, Cameroun. 1995.

Diesing KM. Systema helminthum. Vol. 1. Vindobonae: Braumfiller W; 1850.

Mizelle JD, Price CE. Studies on monogenetic Trematodes. XXVIII. Gill parasites of the Piranha with proposal of Anacanthorus gen. n. J Parasitol. 1965;51:30–6. PubMed

Guégan J-F, Lambert A. Twelve new species of dactylogyrids (Platyhelminthes, Monogenea) from West African barbels (Teleostei, Cyprinidae), with some biogeographical implications. Syst. Parasitol. 1990;17:153–81. doi: 10.1007/BF00009552. DOI

van Every LR, Kritsky DC. Neotropical Monogenoidea. 18. Anacanthorus Mizelle and Price, 1965 (Dactylogyridae, Anacanthorinae) of Piranha (Characoidea, Serrasalmidae) from the Central Amazon, their phylogeny, and aspects of host–parasite coevolution. J Helminthol. Soc. Washin. 1992;59:52–75.

El Gharbi S, Lambert A, Berrebi P. Le genre Barbus (sous-genre Barbus et Labeobarbus) au Maroc. Génétique et Parasitologie. Cah. Ethol. 1993;13:223–6.

Šimková A, Ondračková M, Gelnar M, Morand S. Morphology and coexistence of congeneric ectoparasite species: reinforcement of reproductive isolation? Biol. J. Linn. Soc. 2002;76:125–35.

Huyse T, Malmberg G. Molecular and morphological comparisons between Gyrodactylus ostendicus n. sp. (Monogenea: Gyrodactylidae) on Pomatoschistus microps (Krøyer) and G. harengi Malmberg, 1957 on Clupea harengus membras L. Syst Parasitol. 2004;58:105–13. doi: 10.1023/B:SYPA.0000029423.68703.43. PubMed DOI

Rohde K, Rohde PP. The ecological niches of parasites. In: Rohde K, editor. Marine parasitology. Wallingford: CABI Publishing; 2005. pp. 286–93.

Šimková A, Morand S. Co-evolutionary patterns in congeneric monogeneans: a review of Dactylogyrus species and their cyprinid hosts. J. Fish Biol. 2008;73:2210–27. doi: 10.1111/j.1095-8649.2008.02064.x. DOI

Mancheva K, Karaivanova E, Atanasov G, Stojanovski S, Nedeva I. Analysis of the influence of the host body size on morphometrical characteristics of Ancylodiscoides siluri and Ancylodiscoides vistulensis. Biotec. Biotechnol. Equip. 2009;23:735–41. doi: 10.1080/13102818.2009.10818529. DOI

Poisot T, Desdevises Y. Putative speciation events in Lamellodiscus (Monogenea: Diplectanidae) assessed by a morphometric approach. Biol. J. Linn. Soc. 2010;99:559–69. doi: 10.1111/j.1095-8312.2009.01381.x. DOI

Morand S, Hafner MS, Page RDM, Reed DL. Comparative body size relationships in pocket gophers and their chewing lice. Biol. J. Linn. Soc. 2000;70:239–49. doi: 10.1111/j.1095-8312.2000.tb00209.x. DOI

Morand S, Šimková A, Matejusová I, Plaisance L, Verneau O, Desdevises Y. Investigating patterns may reveal processes: evolutionary ecology of ectoparasitic monogeneans. Int. J. Parasitol. 2002;32:111–9. doi: 10.1016/S0020-7519(01)00347-2. PubMed DOI

Huyse T, Volckaert FAM. Identification of a host-associated species complex using molecular and morphometric analyses, with the description of Gyrodactylus rugiensoides n. sp. (Gyrodactylidae, Monogenea) Int. J Parasitol. 2002;32:907–19. doi: 10.1016/S0020-7519(02)00026-7. PubMed DOI

Bush S, Sohn E, Clayton DH. Ecomorphology of parasite attachment: experiments with feather lice. J. Parasitol. 2006;92:25–31. doi: 10.1645/GE-612R.1. PubMed DOI

Rohde K, Hobbs R. Species segregation: Competition of reinforcement of reproductive barriers? In: Cremin M, editor. Parasite lives. Papers on parasites, their hosts and their associations to honour JFA Sprent. St. Lucia: University of Queensland Press; 1986. pp. 189–99.

Butlin RK. Reinforcement of premating isolation. In: Otte D, Endler JA, editors. Speciation and its consequences. Sunderland: Sinauer Associates; 1989. pp. 158–79.

Butlin RK. Reinforcement: an idea evolving. TREE. 1995;10:432–4. PubMed

Jiggins CD, Mallet J. Bimodal hybrid zones and speciation. TREE. 2000;15:250–5. PubMed

All quiet on the western front? The evolutionary history of monogeneans (Dactylogyridae: Cichlidogyrus, Onchobdella) infecting a West and Central African tribe of cichlid fishes (Chromidotilapiini)

From the Atlantic Coast to Lake Tanganyika: Gill-Infecting Flatworms of Freshwater Pellonuline Clupeid Fishes in West and Central Africa, with Description of Eleven New Species and Key to Kapentagyrus (Monogenea, Dactylogyridae)

Temporally consistent species differences in parasite infection but no evidence for rapid parasite-mediated speciation in Lake Victoria cichlid fish

Six new species of Cichlidogyrus Paperna, 1960 (Platyhelminthes: Monogenea) from the gills of cichlids (Teleostei: Cichliformes) from the Lomami River Basin (DRC: Middle Congo)

High diversity of fish ectoparasitic monogeneans (Dactylogyrus) in the Iberian Peninsula: a case of adaptive radiation?

Six new dactylogyrid species (Platyhelminthes, Monogenea) from the gills of cichlids (Teleostei, Cichliformes) from the Lower Congo Basin

Seven new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) parasitizing the gills of Congolese cichlids from northern Lake Tanganyika

The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids

Underexplored diversity of gill monogeneans in cichlids from Lake Tanganyika: eight new species of Cichlidogyrus Paperna, 1960 (Monogenea: Dactylogyridae) from the northern basin of the lake, with remarks on the vagina and the heel of the male copulatory organ

The phylogenetic position of the enigmatic Balkan Aulopyge huegelii (Teleostei: Cyprinidae) from the perspective of host-specific Dactylogyrus parasites (Monogenea), with a description of Dactylogyrus omenti n. sp

Quadriacanthus species (Monogenea: Dactylogyridae) from catfishes (Teleostei: Siluriformes) in eastern Africa: new species, new records and first insights into interspecific genetic relationships

Redescription of Cichlidogyrus tiberianus Paperna, 1960 and C. dossoui Douëllou, 1993 (Monogenea: Ancyrocephalidae), with special reference to the male copulatory organ

Reduced host-specificity in a parasite infecting non-littoral Lake Tanganyika cichlids evidenced by intraspecific morphological and genetic diversity

First insights into the diversity of gill monogeneans of 'Gnathochromis' and Limnochromis (Teleostei, Cichlidae) in Burundi: do the parasites mirror host ecology and phylogenetic history?