Hostname: page-component-78c5997874-ndw9j Total loading time: 0 Render date: 2024-11-15T11:17:49.817Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  22 January 2020

Michal Benovics Open the ORCID record for Michal Benovics [Opens in a new window] ,
Yves Desdevises ,
Radek Šanda ,
Jasna Vukić ,
Mathilde Scheifler ,
Ignacio Doadrio ,
Carla Sousa-Santos  and
Andrea Šimková
Michal Benovics*
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137 Brno, Czech Republic
Yves Desdevises
Affiliation:
Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, F-66650, Banyuls/Mer, France
Radek Šanda
Affiliation:
National Museum, Václavské Náměstí 68, 115 79 Prague, Czech Republic
Jasna Vukić
Affiliation:
Department of Ecology, Faculty of Science, Charles University, Viničná 7, 128 44 Prague, Czech Republic
Mathilde Scheifler
Affiliation:
Sorbonne Université, CNRS, Biologie Intégrative des Organismes Marins, BIOM, Observatoire Océanologique, F-66650, Banyuls/Mer, France
Ignacio Doadrio
Affiliation:
Biodiversity and Evolutionary Group, Museo Nacional de Ciencias Naturales-CSIC, C/José Gutiérrez Abascal 2, 28006, Madrid, Spain
Carla Sousa-Santos
Affiliation:
MARE – Marine and Environmental Sciences Centre, ISPA – Instituto Universitário, Rua Jardin do Tabaco 34, 1149-041, Lisbon, Portugal
Andrea Šimková
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 61137 Brno, Czech Republic
*
Author for correspondence: Michal Benovics, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

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.

Keywords

Cyprinoideahost-specificityIberian PeninsulaMonogeneaphylogenyspecies delimitation
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 418 - 430
Check for updates
Copyright
Copyright © Cambridge University Press, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
Araújo, MB, Lobo, JM and Moreno, JC (2007) The effectiveness of Iberian protected areas in conserving terrestrial biodiversity. Conservation Biology 21, 1423–1432.CrossRefGoogle ScholarPubMed
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.Google Scholar
Banarescu, P (1992) Zoogeography of Fresh Waters. Volume 2. Distribution and Dispersal of Freshwater Animals in North America and Eurasia. Wiesbaden, DE: AULA-Verlag.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Cardoso, P (2008) Biodiversity and conservation of Iberian spiders: past, present and future. Boletín Sociedad Entomólogica Aragonesa 42, 487–492.Google Scholar
Carstens, BC, Pelletier, TA, Reid, NM and Satler, JD (2013) How to fail at species delimitation. Molecular Ecology 22, 4369–4383.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Da Costa Eiras, J (2016) Parasites of marine, freshwater and farmed fishes of Portugal: a review. Brazilian Journal of Veterinary Parasitology 25, 259–278.Google Scholar
Darriba, D, Taboala, GL, Doallo, R and Posada, D (2012) JModeltest2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle Scholar
Doadrio, I (1988) Delimitation of areas in the Iberian Peninsula on the basis of freshwater fishes. Bonner Zoologische Beiträge 39, 113–128.Google Scholar
Doadrio, I (1990) Phylogenetic relationships and classification of western Palearctic species of the genus Barbus (Osteichthyes, Cyprinidae). Aquatic Living Resources 3, 265–282.CrossRefGoogle Scholar
Doadrio, I (2001) Atlas y libro rojo de los peces continentales de Espańa. Madrid: Dirección General de la Natureza – Museo Nacional de Ciencias Naturales.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Dupont, F (1989) Biogeographie historique des Dactylogyrus, monogénes parasites de poisons Cyprinidae dans la peninsula Balkanique. Biologia Gallo-Hellenica 13, 145–152.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
Ergens, R and Lom, J (1970) Causative Agents of Fish Diseases. Prague, CZ: Academia.Google Scholar
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.CrossRefGoogle Scholar
Galli, P, Stefani, F, Zaccara, S and Crosa, G (2002) Occurrence of Monogenea in Italian freshwater fish (Po river basin). Parassitologia 44, 189–197.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Guindon, S and Gascuel, O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 27, 1759–1767.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Hsü, KJ, Ryan, WBF and Cita, MB (1973) Late Miocene desiccation of the Mediterranean. Nature 242, 240–244.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Kottelat, M and Freyhof, J (2007) Handbook of European Freshwater Fishes. Cornol, CH: Publications Kottelat.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Lambert, A and El Gharbi, S (1995) Monogenean host specificity as a biological and taxonomic indicator for fish. Biological Conservation 72, 227–235.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.Google Scholar
Lux, E (1990) Population dynamics and interrelationships of some Dactylogyrus and Gyrodactylus species on Cyprinus carpio. Angewandte Parasitologie 31, 143–149.Google ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Malmberg, G (1957) Om forekomsten av Gyrodactylus pa svenska fiskar. Skrifter Utgivna av Sodra Sveriges Fiskeriforening, Arsskift 1956.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Mendoza-Palmero, CA, Blasco-Costa, I and Scholz, T (2015) Molecular phylogeny of Neotropical monogeneans (Platyhelminthes: Monogenea) from catfishes (Siluriformes). Parasites & Vectors 8, 164.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Moravec, F (2001) Checklist of the Metazoan Parasites of Fishes of Czech Republic and Slovak Republic (1873–2000). Prague, CZ: Academia.Google Scholar
Muñoz, JA, Martinez, A and Vergés, J (1986) Thrust sequences in the eastern Spanish Pyrenees. Journal of Structural Geology 8, 399–405.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Poulin, R and Morand, S (2004) Parasite Biodiversity. Washington, CO: Smithsonians Books.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Rohde, K (1989) Simple ecological systems, simple solutions to complex problems? Evolutionary Theory 8, 305–350.Google Scholar
Rohde, R and Watson, N (1985) Morphology, microhabitats and geographical variation of Kuhnia Spp. (Monogenea: Polyopisthicotylea). International Journal for Parasitology 15, 569–586.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Rueda, M, Rodríguez, MÁ and Hawkins, BA (2010) Towards a biogeographic regionalization of the European biota. Journal of Biogeography 37, 2067–2076.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Šimková, A, Verneau, O, Gelnar, M and Morand, S (2006b) Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution 60, 1023–1037.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Stamatakis, A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England) 22, 2688–2690.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analyses and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
Supplementary material: PDF

Benovics et al. supplementary material

Tables S1-S2

Download Benovics et al. supplementary material(PDF)
PDF 507.6 KB