The epicontinental fauna of the Iberian Peninsula is strongly influenced by its geographical history. As the possibilities for dispersion of organisms into and from this region were (and still are) limited, the local fauna consists almost exclusively of endemic species. Almost all Iberian freshwater fishes of the families Leuciscidae and Cyprinidae are endemic and on-going research on these taxa continually uncovers new species. Nevertheless, information on their host-specific parasites remains scarce. In this study, we investigate the diversity and phylogenetic relationships in monogeneans of the genus Dactylogyrus (gill ectoparasites specific to cyprinoid fish) in the Iberian Peninsula. Twenty-two species were collected and identified from 19 host species belonging to Cyprinidae and Leuciscidae. A high degree of endemism was observed, with 21 Dactylogyrus species reported from Iberia only and a single species, D. borealis, also reported from other European regions. Phylogenetic analysis split the endemic Iberian Dactylogyrus into two well-supported clades, the first encompassing Dactylogyrus parasitizing endemic Luciobarbus spp. only, and the second including all Dactylogyrus species of endemic leuciscids and four species of endemic cyprinids. Species delimitation analysis suggests a remarkable diversity and existence of a multitude of cryptic Dactylogyrus species parasitizing endemic leuciscids (Squalius spp. and representatives of Chondrostoma s.l.). These results suggest a rapid adaptive radiation of Dactylogyrus in this geographically isolated region, closely associated with their cyprinoid hosts. Moreover, phylogenetic analysis supports that Dactylogyrus parasites colonized the Iberian Peninsula through multiple dispersion events.

Biodiversity and Evolutionary Group Museo Nacional de Ciencias Naturales CSIC C José Gutiérrez Abascal 2 28006 Madrid Spain

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 61137 Brno Czech Republic

Department of Ecology Faculty of Science Charles University Viničná 7 128 44 Prague Czech Republic

MARE Marine and Environmental Sciences Centre ISPA Instituto Universitário Rua Jardin do Tabaco 34 1149 041 Lisbon Portugal

National Museum Václavské Náměstí 68 115 79 Prague Czech Republic

Sorbonne Université CNRS Biologie Intégrative des Organismes Marins BIOM Observatoire Océanologique F 66650 Banyuls Mer France

Zobrazit více v PubMed

Almodóvar A, Nicola GG and Elvira B (2008) Natural hybridization of Barbus Bocagei x Barbus Comizo (Cyprinidae) in Tagus River basin, central Spain. Cybium 32, 99–102.

Alvarez-Pellitero MP, Simón-Vicente F and González-Lanza MC (1981) Nuevas aportaciones sobre Dactylogyridae (Monogenea) de la cuenca del Duero (No. de España), con descripcion de Dactylogyrus polylepidis N. sp. y D. bocageii N. sp. Revista Ibérica de Parasitologia 41, 225–249.

Appleby C and Mo TA (1997) Population dynamics of Gyrodactylus Salaris (Monogenea) infecting Atlantic salmon, Salmo Salar, Parr in the river Batnfjordselva, Norway. Journal of Parasitology 83, 23–30. PubMed

Araújo MB, Lobo JM and Moreno JC (2007) The effectiveness of Iberian protected areas in conserving terrestrial biodiversity. Conservation Biology 21, 1423–1432. PubMed

Banarescu P (1989) Zoogeography and history of the freshwater fish fauna of Europe. In Holcik J (ed.), The Freshwater Fishes of Europe. Wiesbaden, DE: AULA-Verlag, pp. 80–107.

Banarescu P (1992) Zoogeography of Fresh Waters. Volume 2. Distribution and Dispersal of Freshwater Animals in North America and Eurasia. Wiesbaden, DE: AULA-Verlag.

Benovics M, Kičinjaová ML and Šimková A (2017) 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. Parasites & Vectors 10, 547. PubMed PMC

Benovics M, Desdevises Y, Vukić J, Šanda R and Šimková A (2018) The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids. Scientific Reports 8, 13006. PubMed PMC

Bianco PG (1990) Potential role of the paleohistory of the Mediterranean and Parathethys basins on the early dispersal of Euro-Mediterranean freshwater fishes. Ichthyological Exploration of Freshwaters 1, 167–184.

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

Boeger WA and Kritsky DC (1988) Neotropical Monogenea. 12. Dactylogyridae from Serrasalmus Natteri (Cypriniformes, Serrasalmidae) and aspects of their morphologic variation and distribution in Brazilian Amazon. Proceedings of the Helminthological Society of Washington 55, 188–213.

Cardoso P (2008) Biodiversity and conservation of Iberian spiders: past, present and future. Boletín Sociedad Entomólogica Aragonesa 42, 487–492.

Carstens BC, Pelletier TA, Reid NM and Satler JD (2013) How to fail at species delimitation. Molecular Ecology 22, 4369–4383. PubMed

Casal-López M, Perea S, Sousa-Santos C, Robalo JI, Torralva M, Oliva-Paterna FJ and Doadrio I (2017) Paleobiogeography of an Iberian endemic species, Luciobarbus Sclateri (Günther, 1868) (Actinopterygii, Cyprinidae), inferred from mitochondrial and nuclear markers. Journal of Zoological Systematic and Evolutionary Research 56, 127–147.

Choudhury A and Dick TA (2001) Sturgeons (Chondrostei: Acipenseridae) and their metazoan parasites: patterns and processes in historical biogeography. Journal of Biogeography 28, 1411–1439.

Corral-Lou A, Perea S, Aparicio E and Doadrio, I (2019) Phylogeography and species delineation of the genus Phoxinus Rafinesque, 1820 (Actinopterygii: Leuciscidae) in the Iberian Peninsula. Journal of Zoological Systematic and Evolutionary Research 57, 926–941.

Da Costa Eiras J (2016) Parasites of marine, freshwater and farmed fishes of Portugal: a review. Brazilian Journal of Veterinary Parasitology 25, 259–278. PubMed

Darriba D, Taboala GL, Doallo R and Posada D (2012) JModeltest2: more models, new heuristics and parallel computing. Nature Methods 9, 772. PubMed PMC

Doadrio I (1988) Delimitation of areas in the Iberian Peninsula on the basis of freshwater fishes. Bonner Zoologische Beiträge 39, 113–128.

Doadrio I (1990) Phylogenetic relationships and classification of western Palearctic species of the genus Barbus (Osteichthyes, Cyprinidae). Aquatic Living Resources 3, 265–282.

Doadrio I (2001) Atlas y libro rojo de los peces continentales de Espańa. Madrid: Dirección General de la Natureza – Museo Nacional de Ciencias Naturales.

Doadrio I and Carmona JA (2003) Testing freshwater Lago Mare dispersal theory on the phylogeny relationships of Iberian cyprinids genera Chondrostoma and Squalius (Cypriniformes, Cyprinidae). Graellsia 59, 457–473.

Doadrio I, Carmona JA and Machordom A (2002) Haplotype diversity and phylogenetic relationships among the Iberian barbels (Barbus, Cyprinidae) reveal two evolutionary lineages. Journal of Heredity 93, 147. PubMed

Dupont F (1989) Biogeographie historique des Dactylogyrus, monogénes parasites de poisons Cyprinidae dans la peninsula Balkanique. Biologia Gallo-Hellenica 13, 145–152.

Dupont F and Crivelli AJ (1988) Do parasites confer a disadvantage to hybrids? A case study of Alburnus Alburnus x Rutilus Rubilio, a natural hybrid of Lake Mikri Prespa, Northern Greece. Oceologia 75, 587–592. PubMed

Dupont F and Lambert A (1986) Study of the parasitic communities of Monogenea Dactylogyridae from Cyprinidae in Lake Mikri Prespa (Northern Greece) description of three new species from endemic Barbus: Barbus cyclolepis Prespensis Karaman. 1924. Annales de Parasitologie Humaine et Comparee 6, 597–616. PubMed

El Gharbi S, Renaud F and Lambert A (1992) Dactylogyrids (Platyhelminthes: Monogenea) of Barbus Spp. (Teleostei: Cyprinidae) from the Iberian Peninsula. Research and Reviews in Parasitology 52, 103–116.

Ergens R and Lom J (1970) Causative Agents of Fish Diseases. Prague, CZ: Academia.

Filipe AF, Araújo MB, Doadrio I, Angermeier PL and Collares-Pereira MJ (2009) Biogeography of Iberian freshwater fishes revisited: the roles of historical versus contemporary constrains. Journal of Biogeography 36, 2096–2110.

Galli P, Stefani F, Zaccara S and Crosa G (2002) Occurrence of Monogenea in Italian freshwater fish (Po river basin). Parassitologia 44, 189–197. PubMed

Galli P, Strona G, Benzoni F, Crosa G and Stefani F (2007) Monogenoids from freshwater fish in Italy, with comments on alien species. Comparative Parasitology 74, 264–272.

Gante HF (2011) Diversification of Circum-Mediterranean Barbels. In Grillo O and Venora G (eds.), Changing Biodiversity in Changing Environment. Rijeka, CR: Intech, pp. 283–298.

Gante HF, Micael J, Oliva-Paterna FJ, Doadrio I, Dowling TE and Alves MJ (2009) Diversification within glacial refugia: tempo and mode of evolution of the polytypic fish Barbus sclateri. Molecular Ecology 18, 3240–3255. PubMed

Gante HF, Doadrio I, Alves MJ and Dowling TE (2015) Semi-permeable species boundaries in Iberian barbels (Barbus and Luciobarbus, Cyprinidae). BMC Evolutionary Biology 15, 111. PubMed PMC

Gibson DI, Timofeeva TA and Gerasev PI (1996) A catalogue of the nominal species of the monogenean genus Dactylogyrus Diesing, 1850 and their host genera. Systematic Parasitology 35, 3–48.

González-Lanza C and Alvarez-Pellitero P (1982) Description and population dynamics of Dactylogyrus legionensis n.sp. from Barbus Barbus Bocagei Steind. Journal of Helminthology 56, 263–273.

Grummer JA, Bryson RW Jr and Reeder TW (2014) Species delimitation using Bayes factors: simulations and application to the Sceloporus scalaris species group (Squamata: Phrynosomatidae). Systematic Biology 63, 119–133. PubMed

Guindon S and Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 27, 1759–1767. PubMed

Gutiérrez-Galindo JF and Lacasa-Millán MI (1999) Monogenea parásitos de Cyprinidae en el río Llobregat (NE de España) (Barbus Haasi, Petersen 1925) Duero. Revista Ibérica de Parasitologia 35, 25–40.

Gutiérrez-Galindo JF and Lacasa-Millán MI (2001) Study of the Monogenea of Cyprinidae in the Llobregat River, Notheastern Spain. II. Species composition on Barbus Graellsii Steindachner, 1866. Revista Ibérica de Parasitologia 61, 91–96.

Hassouna N, Michot B and Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Research 12, 3563–3583. PubMed PMC

Hewitt GM (2011) Mediterranean Peninsulas: the evolution of hotspots. In Zachos FE and Havel JC (eds.), Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas. Berlin Heidelberg, DE: Springer, pp. 123–147.

Hsü KJ, Ryan WBF and Cita MB (1973) Late Miocene desiccation of the Mediterranean. Nature 242, 240–244.

Imoto JM, Saitoh K, Sasaki T, Yonezawa T, Adachi J, Kartavtsev YP, Miya M, Nishida M and Hanzawa N (2013) Phylogeny and biogeography of highly diverged freshwater fish species (Leuciscinae, Cyprinidae, Teleostei) inferred from mitochondrial genome analysis. Gene 514, 112–124. PubMed

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

Katoh K, Misawa K, Kuma K and Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on Fourier transform. Nucleic Acids Research 30, 3059–3066. PubMed PMC

Ketmaier V, Bianco PG, Cobolli M, Krivokapic M, Caniglia R and De Matthaeis E (2004) Molecular phylogeny of two lineages of Leuciscinae cyprinids (Telestes And Scardinius) from the peri-Mediterranean area based on cytochrome b Data. Molecular Phylogenetics and Evolution 32, 1061–1071. PubMed

Kumar S, Stecher G, Li M, Knyaz C and Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549. PubMed PMC

Kottelat M and Freyhof J (2007) Handbook of European Freshwater Fishes. Cornol, CH: Publications Kottelat.

Krasnovyd V, Vetešník L, Gettová L, Civáňová K and Šimková A (2017) Patterns of parasite distribution in the hybrids of non-congeneric cyprinid fish species: is asymmetry in parasite infection the result of limited coadaptation? International Journal for Parasitology 47, 471–483. PubMed

Lacasa-Millán MI and Gutiérrez-Galindo JF (1995) Study of the Monogenea of Cyprinidae in the Llobregat River (NE Spain) I. Parasites of Cyprinus carpio. Acta Parasitologica 2, 72–78.

Lambert A and El Gharbi S (1995) Monogenean host specificity as a biological and taxonomic indicator for fish. Biological Conservation 72, 227–235.

Lanave C, Preparata G, Sacone C and Serio G (1984) A new method for calculating evolutionary substitution rates. Journal of Molecular Evolution 20, 86–93. PubMed

Levy A, Doadrio I and Almada VC (2009) Historical biogeography of European leuciscins (Cyprinidae): evaluating Lago Mare dispersal hypothesis. Journal of Biogeography 36, 55–65.

López-López P, Maiorano L, Falcucci A, Barba E and Boitani L (2011) Hotspots of species richness, threat and endemism for terrestrial vertebrates in SW Europe. Acta Oecologica 37, 399–412.

Lux E (1990) Population dynamics and interrelationships of some Dactylogyrus and Gyrodactylus species on Cyprinus carpio. Angewandte Parasitologie 31, 143–149. PubMed

Machordom A and Doadrio I (2001) Evidence of a cenozoic Betic-Kabilian connection based on freshwater fish phylogeography (Luciobarbus, Cyprinidae). Molecular Phylogenetics and Evolution 18, 252–263. PubMed

Machordom A, Berrebi P and Doadrio I (1990) Spanish barbel hybridization detected using enzymatic markers: Barbus meridionalis Risso X Barbus Haasi Mertens (Osteichthyes, Cyprinidae). Aquatic Living Resources 3, 295–303.

Malmberg G (1957) Om forekomsten av Gyrodactylus pa svenska fiskar. Skrifter Utgivna av Sodra Sveriges Fiskeriforening, Arsskift 1956.

Mandeng FDM, Bilong Bilong CF, Pariselle A, Vanhove MPM, Bitja Nyom AR and Agnése J-FA (2015) Phylogeny of Cichlidogyrus Spp. (Monogenea, Dactylogyridea) clarifies a host-switch between fish families and reveals an adaptive component to attachment organ morphology of this parasite genus. Parasites & Vectors 8, 582. PubMed PMC

Martín J, García-Barros E, Gurrea P, Luciañez MJ, Munguira ML, Sanz MJ and Simón JC (2000) High endemism areas in the Iberian Peninsula. Belgian Journal of Entomology 2, 47–57.

Médail M and Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Annals of Missouri Botanical Garden 84, 112–127.

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

Mendoza-Palmero CA, Blasco-Costa I and Scholz T (2015) Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasites & Vectors 8, 164. PubMed PMC

Mesquita N, Cunha C, Carvalho GR and Coelho M (2007) Comparative phylogeography of endemic cyprinids in the south-west Iberian Peninsula: evidence for a new ichthyogeographic area. Journal of Fish Biology 71, 45–75.

Moravec F (2001) Checklist of the Metazoan Parasites of Fishes of Czech Republic and Slovak Republic (1873–2000). Prague, CZ: Academia.

Muñoz JA, Martinez A and Vergés J (1986) Thrust sequences in the eastern Spanish Pyrenees. Journal of Structural Geology 8, 399–405.

Penado A, Rebelo H and Goulson D (2016) Spatial distribution modelling reveals climatically suitable areas for bumblebees in undersampled parts of the Iberian Peninsula. Insect Conservation and Diversity 9, 391–401.

Perea S, Böhme M, Zupančic P, Freyhof J, Šanda R, Özulug M and Doadrio I (2010) Phylogenetic relationships and biogeographical patterns in circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evolutionary Biology 10, 265. PubMed PMC

Perea S, Vukić J, Šanda R and Doadrio I (2016) Ancient mitochondrial capture as factor of promoting mitonuclear discordance in freshwater fishes: a case study in the genus Squalius (Actinopterygii, Cyprinidae) in Greece. PLoS ONE 11, e0166292. PubMed PMC

Pérez-Ponce de León G and Choudhury A (2005) Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. Journal of Biogeography 32, 645–659.

Poulin R and Morand S (2004) Parasite Biodiversity. Washington, CO: Smithsonians Books.

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

Pugachev ON, Gerasev PI, Gussev AV, Ergens R and Khotenowsky I (2009) Guide to Monogenoidea of Freshwater Fish of Palearctic and Amur Regions. Milan, IT: Ledizione-Ledi.

Puigdefàbregas C, Muñoz, JA and Vergés, J (1992) Thrusting and foreland basin evolution in the Southern Pyrenees. In McClay KR (ed.). Thrust Tectonics. London, UK: Chapman and Hall, pp. 247–254.

Rahmouni I, Řehulková E, Pariselle A, Rkhami OB and Šimková A (2017) Four new species of Dactylogyrus Diesing, 1850 (Monogenea: Dactylogyridae) parasitising the gills of northern Morrocan Luciobarbus Heckel (Cyprinidae): morphological and molecular characterisation. Systematic Parasitology 94, 575–591. PubMed

Rambaut A, Drummond AJ, Xie D, Baele G and Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Systematic Biology 67, 901–604. PubMed PMC

Robalo JI, Almada VC, Levy A and Doadrio I (2007) Re-examination and phylogeny of the genus Chondrostoma Based on mitochondrial and nuclear data and the definition of 5 new genera. Molecular Phylogenetics and Evolution 42, 362–372. PubMed

Rohde K (1989) Simple ecological systems, simple solutions to complex problems? Evolutionary Theory 8, 305–350.

Rohde R and Watson N (1985) Morphology, microhabitats and geographical variation of Kuhnia Spp. (Monogenea: Polyopisthicotylea). International Journal for Parasitology 15, 569–586.

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA and Huelsenbeck JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across large model space. Systematic Biology 61, 539–542. PubMed PMC

Rosenbaum G, Lister GS and Duboz C (2001) Reconstruction of the tectonic evolution of the western Mediterranean since the Oligocene. Journal of Virtual Explorer 8, 107–130.

Rueda M, Rodríguez MÁ and Hawkins BA (2010) Towards a biogeographic regionalization of the European biota. Journal of Biogeography 37, 2067–2076.

Sanjur OI, Carmona JA and Doadrio I (2003) Evolutionary and biogeographical patterns within Iberian populations of the genus Squalius inferred from molecular data. Molecular Phylogenetics and Evolution 29, 20–30. PubMed

Schönhuth S, Vukić J, Šanda R, Yang L and Mayden RL (2018) Phylogenetic relationships and classification of the Holarctic family Leuciscidae (Cypriniformes: Cyprinoidei). Molecular Phylogenetics and Evolution 127, 781–799. PubMed

Seifertová M, Vyskočilová M, Morand S and Šimková A (2008) Metazoan parasites of freshwater cyprinid fish (Leuciscus Cephalus): testing biogeography hypotheses of species diversity. Parasitology 135, 1417–1435. PubMed

Šimková A and Morand S (2008) Co-evolutionary patterns in congeneric monogeneans: a review of Dactylogyrus species and their cyprinid hosts. Journal of Fish Biology 73, 2210–2227.

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

Šimková A, Desdevises Y, Gelnar M and Morand S (2001a) Morphometric correlates of host specificity in Dactylogyrus species (Monogenea) parasites of European cyprinid fish. Parasitology 123, 169–177. PubMed

Šimková A, Sasal P, Kadlec D and Gelnar M (2001b) Water temperature influencing Dactylogyrus species communities in roach, Rutilus rutilus, in Czech Republic. Journal of Helminthology 75, 373–383. PubMed

Šimková A, Kadlec D, Gelnar M and Morand S (2002) Abundance-prevalence relationship of gill congeneric ectoparasites: testing the core satellite hypothesis and ecological specialisation. Parasitological Research 88, 682–686. PubMed

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

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

Šimková A, Dávidová M, Papoušek I and Vetešník L (2013) Does interspecies hybridization affect host specificity of parasites and cyprinid fish? Parasites & Vectors 6, 95. PubMed PMC

Šimková A, Matějusová I and Cunningham CO (2006a) A molecular phylogeny of the Dactylogyridae sensu Kritsky Boeger (1989) (Monogenea) based on the D1-D3 domains of large subunit rDNA. Parasitology 133, 43–53. PubMed

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

Šimková A, Benovics M, Rahmouni I and Vukić J (2017) Host-specific Dactylogyrus parasites revealing new insights on the historical biogeography of Northwest African and Iberian cyprinid fish. Parasites & Vectors 10, 589. PubMed PMC

Simón-Vicente F (1981) Dactylogyrus Ballistae N. sp. (syn. Dactylogyrus sp., Simon Vicente y col., 1975), (Monogenea), de las branquias de Barbus Barbus Bocageii Steindachner. Revista Ibérica de Parasitologia 41, 101–110.

Sinaré Y, Boungou M, Ouéda A, Gnémé A and Kabré GB (2016) Diversity and seasonal distribution of parasites of Oreochromis niloticus in semi-arid reservoirs (West Africa, Burkina Faso). African Journal of Agricultural Research 11, 1164–1170.

Sousa-Santos C, Pereira AM, Branco P, Costa GJ, Santos JM, Ferreira MT, Lima S, Doadrio I and Robalo JI (2018) Mito-nuclear sequencing is paramount to correctly identify sympatric hybridizing fishes. Acta Ichthyologica et Piscatoria 48, 123–141.

Sousa-Santos C, Jesus TF, Fernandes C, Robalo JI and Coelho MM (2019) Fish diversification at the pace of geomorphological changes: evolutionary history of western Iberian Leuciscinae (Teleostei: Leuciscidae) inferred from multilocus sequence data. Molecular Phylogenetics and Evolution 133, 265–285. PubMed

Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22, 2688–2690. PubMed

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analyses and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313. PubMed PMC

Stange KM, Van Balen RT, Garcia-Castellanus D and Cloetingh S (2016) Numerical modelling of Quaternary terrace staircase formation in the Ebro foreland basin, southern Pyrenees, NE Iberia. Basin Research 28, 124–146.

Stierandová S, Vukić J, Vasil'eva ED, Zogaris S, Shumka S, Halačka K, Vetešník L, Švátora M, Nowak M, Stefanov T, Koščo J and Mendel J (2016) A multilocus assessment of nuclear and mitochondrial sequence data elucidates phylogenetic relationships among European spirlins (Alburnoides, Cyprinidae). Molecular Phylogenetics and Evolution 94, 479–491. PubMed

Talavera G and Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577. PubMed

Vignon M and Sasal P (2010) The use of geometric morphometrics in understanding shape variability of sclerotized haptoral structures of monogeneans (Platyhelminthes) with insights into biogeographic variability. Parasitology International 59, 183–191. PubMed

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

Waap S, Amaral AR, Gomes B and Coelho MM (2011) Multi-locus species tree of the chub genus Squalius (Leuciscidae: Cyprinidae) from western Iberia: new insights into its evolutionary history. Genetica 139, 1009–1018. PubMed

Williams PH, Araújo MB, Humphries C, Lampinen R, Hagemeijer W, Gasc PJ and Mitchell-Jones T (2000) Endemism and important areas for representing European biodiversity: a preliminary exploration of atlas data for plants and terrestrial vertebrates. Belgian Journal of Entomology 2, 21–46.

Yang L, Sado T, Hirt MV, Pasco-Viel E, Arunachalam M, Li J, Wang X, Freyhof J, Saitoh K, Simons AM, Miya M, He S and Mayden RL (2015) Phylogeny and polyploidy: resolving the classification of cyprinid fishes (Teleostei: Cypriniformes). Molecular Phylogenetics and Evolution 85, 97–116. PubMed

Zardoya R and Doadrio I (1998) Phylogenetic relationships of Iberian cyprinids: systematic and biogeographical implications. Proceedings of Royal Society of London B 265, 1365–1372. PubMed PMC

Zhang J, Kapli P, Pavlidis P and Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics (Oxford, England) 29, 2869–2876. PubMed PMC

Zhang G, Yan S, Wang M, Gibson DI and Yang T (2015) Population and community dynamics of four species of Pseudodactylogyrus (Monogenea, Dactylogyridae) on Japanese eel, Anguilla japonica (Temminck and Schlegel, 1846) cultured in two Chinese fish farms. Turkish Journal of Fish and Aquatic Sciences 15, 887–897.

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

Dactylogyrus spp. (Dactylogyridae, Monogenea) from tinfoil barb, Barbonymus schwanenfeldii imported into South Africa: morphometric and molecular characterisation

The parasites of a successful invader: monogeneans of the Asian topmouth gudgeon Pseudorasbora parva, with description of a new species of Gyrodactylus

Morphological description and molecular characterisation of Dactylogyrus matlopong sp. n. (Monogenea: Dactylogyridae) from the South African endemic Labeobarbus aeneus (Cyprinidae: Torinae)

Host-Specific Parasites Reveal the History and Biogeographical Contacts of Their Hosts: The Monogenea of Nearctic Cyprinoid Fishes

De novo developed microsatellite markers in gill parasites of the genus Dactylogyrus (Monogenea): Revealing the phylogeographic pattern of population structure in the generalist parasite Dactylogyrus vistulae

Molecular and morphological phylogeny of host-specific Dactylogyrus parasites (Monogenea) sheds new light on the puzzling Middle Eastern origin of European and African lineages