{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T02:44:07Z","timestamp":1789699447431,"version":"4.0.1"},"reference-count":115,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2010,6,9]],"date-time":"2010-06-09T00:00:00Z","timestamp":1276041600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Little attention has been given to the role that introgression and hybridization have played in the evolution of parasites. Most studies are host-centric and ask if the hybrid of a free-living species is more or less susceptible to parasite infection. Here we focus on what is known about how introgression and hybridization have influenced the evolution of protozoan and helminth parasites of animals. There are reports of genome or gene introgression from distantly related taxa into apicomplexans and filarial nematodes. Most common are genetic based reports of potential hybridization among congeneric taxa, but in several cases, more work is needed to definitively conclude current hybridization. In the medically important Trypanosoma it is clear that some clonal lineages are the product of past hybridization events. Similarly, strong evidence exists for current hybridization in human helminths such as Schistosoma and Ascaris. There remain topics that warrant further examination such as the potential hybrid origin of polyploid platyhelminths. Furthermore, little work has investigated the phenotype or fitness, and even less the epidemiological significance of hybrid parasites.<\/jats:p>","DOI":"10.3390\/genes1010102","type":"journal-article","created":{"date-parts":[[2010,6,9]],"date-time":"2010-06-09T11:22:42Z","timestamp":1276082562000},"page":"102-123","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":75,"title":["An Infectious Topic in Reticulate Evolution: Introgression and Hybridization in Animal Parasites"],"prefix":"10.3390","volume":"1","author":[{"given":"Jillian T.","family":"Detwiler","sequence":"first","affiliation":[{"name":"Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles D.","family":"Criscione","sequence":"additional","affiliation":[{"name":"Department of Biology, Texas A&M University, 3258 TAMU, College Station, TX 77843, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2010,6,9]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1046\/j.1365-294x.2001.01216.x","article-title":"The role of hybridization in evolution","volume":"10","author":"Barton","year":"2001","journal-title":"Mol. Ecol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.tree.2003.09.010","article-title":"Ecological and evolutionary consequences of biotic homogenization","volume":"19","author":"Olden","year":"2004","journal-title":"Trends Ecol. Evol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.tree.2004.01.003","article-title":"Hybridization and adaptive radiation","volume":"19","author":"Seehausen","year":"2004","journal-title":"Trends Ecol. Evol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1146\/annurev.ecolsys.30.1.565","article-title":"Resistance of hybrid plants and animals to herbivores, pathogens, and parasites","volume":"30","author":"Fritz","year":"1999","journal-title":"Annu. Rev. Ecol. Syst."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.pt.2007.11.010","article-title":"Parasites in hybridizing communities: the Red Queen again?","volume":"24","author":"Wolinska","year":"2008","journal-title":"Trends Parasitol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1544","DOI":"10.1111\/j.1420-9101.2008.01604.x","article-title":"Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts","volume":"21","author":"Sloan","year":"2008","journal-title":"J. Evolution. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2853","DOI":"10.1046\/j.1365-294X.2003.01927.x","article-title":"Evidence for gene flow in parasitic nematodes between two host species of shrews","volume":"12","author":"Brant","year":"2003","journal-title":"Mol. Ecol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e793","DOI":"10.1371\/journal.pone.0000793","article-title":"Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis","volume":"2","author":"Slotman","year":"2007","journal-title":"PloS One"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1186\/1471-2148-8-79","article-title":"The molecular evolution of four anti-malarial immune genes in the Anopheles gambiae species complex","volume":"8","author":"Parmakelis","year":"2008","journal-title":"BMC Evolution. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.ijpara.2003.11.025","article-title":"A first glimpse into the pattern and scale of gene transfer in the Apicomplexa","volume":"34","author":"Huang","year":"2004","journal-title":"Int. J. Parasitol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1042\/BST0370792","article-title":"Prediction of horizontal gene transfers in eukaryotes: approaches and challenges","volume":"37","author":"Whitaker","year":"2009","journal-title":"Biochem. Soc. Trans."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3154","DOI":"10.1073\/pnas.0304686101","article-title":"Gene transfer in the evolution of parasite nucleotide biosynthesis","volume":"101","author":"Striepen","year":"2004","journal-title":"P. Natl. Acad. Sci U. S. A."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e538","DOI":"10.1371\/journal.pntd.0000538","article-title":"Helminth genomics: the implications for human health","volume":"3","author":"Brindley","year":"2009","journal-title":"PLoS Neglect. Trop. D."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1202","DOI":"10.1101\/gr.083386.108","article-title":"The origins of apicomplexan sequence innovation","volume":"19","author":"Wasmuth","year":"2010","journal-title":"Genome Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e94","DOI":"10.1371\/journal.ppat.0020094","article-title":"Phylogenetic relationships of the Wolbachia of nematodes and arthropods","volume":"2","author":"Fenn","year":"2006","journal-title":"PLoS Pathog."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/S0020-7519(98)00200-8","article-title":"Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia","volume":"29","author":"Bandi","year":"1999","journal-title":"Int. J. Parasitol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1172\/JCI4768","article-title":"Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility","volume":"103","author":"Hoerauf","year":"1999","journal-title":"J. Clin. Invest."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e121","DOI":"10.1371\/journal.pbio.0030121","article-title":"The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode","volume":"3","author":"Foster","year":"2005","journal-title":"PLoS Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1753","DOI":"10.1126\/science.1142490","article-title":"Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes","volume":"317","author":"Clark","year":"2007","journal-title":"Science"},{"key":"ref_20","first-page":"127","article-title":"Wolbachia sequences in the chromosomal genome of Onchocercia flexuosa indicate past Wolbachia endosymbiosis","volume":"29","author":"McNulty","year":"2008","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_21","unstructured":"McNulty, S.N., Foster, J.M., Mitreva, M., Dunning-Hotopp, J.C., Martin, J., Fischer, K., Wu, B., Davis, P.J., Kumar, S., Brattig, N.W., Slatko, B.E., Weil, G.J., and Fischer, P.U. Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One., In press."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1202","DOI":"10.1101\/gr.083386.108","article-title":"The origins of apicomplexan sequence innovation","volume":"19","author":"Wasmuth","year":"2009","journal-title":"Genome. Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1093\/oxfordjournals.molbev.a003818","article-title":"Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids","volume":"18","author":"Fast","year":"2001","journal-title":"Mol. Biol. Evol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1067","DOI":"10.1073\/pnas.0335769100","article-title":"Plant-like traits associated with metabolism of Trypanosoma parasites","volume":"100","author":"Hannaert","year":"2003","journal-title":"P. Natl. Acad. Sci. U. S. A."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"6304","DOI":"10.1073\/pnas.092525699","article-title":"Genetic complementation in apicomplexan parasites","volume":"99","author":"Striepen","year":"2002","journal-title":"P. Natl. Acad. Sci. U. S. A."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1128\/EC.1.2.181-190.2002","article-title":"Evidence for lateral transfer of genes encoding ferrdoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica","volume":"1","author":"Nixon","year":"2002","journal-title":"Eukaryot. Cell"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/S0960-9822(03)00003-4","article-title":"Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes","volume":"13","author":"Andersson","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"940","DOI":"10.1038\/35082058","article-title":"Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates","volume":"411","author":"Stanhope","year":"2001","journal-title":"Nature"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1093\/nar\/29.2.545","article-title":"A phylogenomic approach to microbial evolution","volume":"29","author":"Andersson","year":"2001","journal-title":"Nucleic Acids Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1111\/j.1365-294X.2004.02145.x","article-title":"Natural hybridization and the evolution of domesticated, pest and disease organisms","volume":"13","author":"Arnold","year":"2004","journal-title":"Mol. Ecol."},{"key":"ref_31","first-page":"724","article-title":"Morphological comparisons and hypotheses on the origin of polyploids in parthenogenetic Fasciola sp","volume":"86","author":"Terasaki","year":"2000","journal-title":"J. Parasitol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/j.exppara.2009.09.001","article-title":"Genotypic characterization and species identification of Fasciola spp. with implications regarding the isolates infecting goats in Vietnam","volume":"123","author":"Thanh","year":"2009","journal-title":"Exp. Parasitol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/0001-706X(90)90072-8","article-title":"Observations on natural and experimental interactions between Schistosoma bovis and S. curassoni from West Africa","volume":"47","author":"Rollinson","year":"1990","journal-title":"Acta Trop."},{"key":"ref_34","unstructured":"Stenmark, A., and Malmberg, G. (1986). Parasites and diseases in natural waters and aquaculture in Nordic countries, Proc. Aoo-Tax-Symp."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF00009706","article-title":"Variation of opisthaptoral hard parts of Gyrodactylus salaris Malmberg, 1957 (Monogenea: Gyrodactylidae) on rainbow trout Oncorhynchus mykiss (Walbaum, 1792) in a fish farm, with comments on the spreading of the parasite in south-eastern Norway","volume":"20","author":"Mo","year":"1991","journal-title":"Syst. Parasitol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"326","DOI":"10.1016\/0035-9203(80)90091-7","article-title":"Hybrids between Schistosoma haematobium and Smattheei and their identification by isoelectric focusing of enzymes","volume":"74","author":"Wright","year":"1980","journal-title":"T. Roy. Soc. Trop. Med. H."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.parint.2009.10.007","article-title":"Evidence of hybridization between Taenia saginata and Taenia asiatica","volume":"59","author":"Okamoto","year":"2010","journal-title":"Parasitol. Int."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5062","DOI":"10.1111\/j.1365-294X.2008.03957.x","article-title":"Introgressive hybridization of human and rodent schistosome parasites in western Kenya","volume":"17","author":"Steinauer","year":"2008","journal-title":"Mol. Ecol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2669","DOI":"10.1098\/rspb.2007.0877","article-title":"Disentangling hybridization and host colonization in parasitic roundworms of humans and pigs","volume":"274","author":"Criscione","year":"2007","journal-title":"Proc. R. Soc. B."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1093\/genetics\/160.3.1217","article-title":"A model-based method for identifying species hybrids using multilocus genetic data","volume":"160","author":"Anderson","year":"2002","journal-title":"Genetics"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.1093\/genetics\/164.4.1567","article-title":"Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies","volume":"164","author":"Falush","year":"2003","journal-title":"Genetics"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2833","DOI":"10.1111\/j.1365-294X.2006.02994.x","article-title":"Bayesian identification of admixture events using multilocus molecular markers","volume":"15","author":"Corander","year":"2006","journal-title":"Mol. Ecol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1016\/S0020-7519(98)00021-6","article-title":"Recent studies on the reproductive biology of the schistosomes and their relevance to speciation in the Digenea","volume":"28","author":"Southgate","year":"1998","journal-title":"Int. J. Parasitol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1016\/j.meegid.2010.02.007","article-title":"Applying evolutionary genetics to schistosome epidemiology","volume":"10","author":"Steinauer","year":"2010","journal-title":"Infect. Genet. Evol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1645\/0022-3395(2003)089[0416:FROANH]2.0.CO;2","article-title":"First report of a natural hybrid between Schistosoma mansoni and S. rodhaini","volume":"89","author":"Morgan","year":"2003","journal-title":"J. Parasitol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1017\/S0031182000050873","article-title":"Parthenogenesis and asexual multiplication among parasitic platyhelminths","volume":"86","author":"Whitfield","year":"1983","journal-title":"Parasitology"},{"key":"ref_47","first-page":"223","article-title":"The geographical distribution of common liver fluke (the genus Fasciola) with normal and abnormal spermatogenesis","volume":"44","author":"Terasaki","year":"1982","journal-title":"J. Vet. Med. Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.parint.2008.11.003","article-title":"Occurrence of spermic diploid and aspermic triploid forms of Fasciola in Vietnam and their molecular characterization based on nuclear and mitochondrial DNA","volume":"58","author":"Itagaki","year":"2009","journal-title":"Parasitol. Int."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3347\/kjp.2003.41.1.47","article-title":"Phylogenetic relationships of ribosomal ITS2 and mitochondrial CO1 among diploid and triploid Paragonimus westermani isolates","volume":"41","author":"Park","year":"2003","journal-title":"Korean J. Parasitol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0065-308X(08)60149-9","article-title":"Paragonimus and the genus Paragonimus","volume":"42","author":"Blair","year":"1999","journal-title":"Adv. Parasit."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1098\/rspb.2004.2675","article-title":"Occasional sex in an \u2018asexual\u2019 polyploidy hermaphrodite","volume":"271","author":"Storhas","year":"2004","journal-title":"Proc. R. Soc. B."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/S1471-4922(02)02357-7","article-title":"The clonal theory of parasitic protozoa: 12 years on","volume":"18","author":"Tibayrenc","year":"2002","journal-title":"Trends Parasitol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1016\/S0035-9203(03)90031-9","article-title":"Direct identification of Leishmania species in biopsies from patients with American tegumentary leishmaniasis","volume":"97","author":"Victoir","year":"2003","journal-title":"T. Roy. Soc. Trop. Med. Hyg."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1016\/j.ijpara.2006.06.019","article-title":"First report of genetic hybrids between two very divergent Leishmania species: Leishmania infantum and Leishmania major","volume":"36","author":"Ravel","year":"2006","journal-title":"Int. J. Parasitol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"573","DOI":"10.4269\/ajtmh.2007.76.573","article-title":"Multiple hybrid genotypes of Leishmania (Viannia) in a focus of mucocutaneous leishmaniasis","volume":"76","author":"Nolder","year":"2007","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1017\/S0031182009990977","article-title":"The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future","volume":"136","author":"Miles","year":"2009","journal-title":"Parasitology"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"7396","DOI":"10.1073\/pnas.121187198","article-title":"Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi","volume":"98","author":"Machado","year":"2001","journal-title":"P. Natl. Acad. Sci. U. S. A."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/S0020-7519(02)00264-3","article-title":"Evidence for multiple hybrid groups in Trypanosoma cruzi","volume":"33","author":"Sturm","year":"2003","journal-title":"Int. J. Parasitol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1534\/genetics.104.038745","article-title":"Two hybridization events define the population structure of Trypanosoma cruzi","volume":"171","author":"Westenberger","year":"2005","journal-title":"Genetics"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"936","DOI":"10.1038\/nature01438","article-title":"Mechanism of genetic exchange in American trypanosomes","volume":"421","author":"Gaunt","year":"2003","journal-title":"Nature"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1016\/S0020-7519(01)00138-2","article-title":"Sex and evolution in trypanosomes","volume":"31","author":"Gibson","year":"2001","journal-title":"Int. J. Parasitol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/0166-6851(93)90024-R","article-title":"Genetic exchange in Trypanosoma brucei: selection of hybrid trypanosomes by introduction of genes conferring drug resistance","volume":"60","author":"Gibson","year":"1993","journal-title":"Mol. Biochem. Parasit."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/1756-3305-1-4","article-title":"The use of yellow fluorescent hybrids to indicate mating in Trypanosoma brucei","volume":"1","author":"Gibson","year":"2008","journal-title":"Parasite. Vector."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1111\/j.1550-7408.2009.00443.x","article-title":"Genetic exchange within and between assemblages of Giardia duodenalis","volume":"56","author":"Welch","year":"2009","journal-title":"J. Eukaryot. Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/S0169-4758(99)01624-5","article-title":"Nomenclature and genetic groupings of Giardia infecting mammals","volume":"16","author":"Thompson","year":"2000","journal-title":"Parasitol. Today"},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Arnold, M.L. (2006). Evolution through genetic exchange, Oxford University Press Inc.","DOI":"10.1093\/acprof:oso\/9780199229031.001.0001"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/S0001-706X(98)00076-X","article-title":"In vitro promastigote fitness of putative Leishmania (Viannia) braziliensis\/Leishmania (Viannia) peruviana hybrids","volume":"72","author":"Torrico","year":"1999","journal-title":"Acta Trop."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/j.ijpara.2007.02.002","article-title":"Increased transmission potential of Leishmania major\/Leishmania infantum hybrids","volume":"37","author":"Volf","year":"2007","journal-title":"Int. J. Parasitol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1016\/j.pt.2006.06.012","article-title":"Phlebotominae sand flies and Leishmania parasites: friends or foes?","volume":"22","author":"Kamhawi","year":"2006","journal-title":"Trends Parasitol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1086\/592866","article-title":"Hybrid fitness in a locally adapted parasite","volume":"172","author":"Dybdahl","year":"2008","journal-title":"Am. Nat."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1017\/S0031182000058674","article-title":"Hybrids between Schistosoma mansoni and S. rodhaini: characterization by cercarial emergence rhythms","volume":"99","year":"1989","journal-title":"Parasitology"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1017\/S0031182098002947","article-title":"Experimental evidence of hybrid breakdown between genetically distinct populations of Echinostoma caproni","volume":"117","author":"Renaud","year":"1998","journal-title":"Parasitology"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1079\/JOH2005306","article-title":"The interaction of Schistosoma haematobium and S. guineensis in Cameroon","volume":"79","author":"Webster","year":"2005","journal-title":"J. Helminthol."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1080\/00222938200770391","article-title":"Mating behavior in mixed infections of Schistosoma haematobium and S","volume":"16","author":"Southgate","year":"1982","journal-title":"intercalatum. J. Nat. His."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1017\/S0031182002002883","article-title":"Mating interactions of Schistosoma haematobium and S. intercalatum with their hybrid offspring","volume":"123","author":"Webster","year":"2003","journal-title":"Parasitology"},{"key":"ref_76","first-page":"2445","article-title":"Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea: Gyrodactylidae)","volume":"56","author":"Lumme","year":"2002","journal-title":"Evolution"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"5234","DOI":"10.1111\/j.1365-294X.2007.03562.x","article-title":"Hybrid origin of Baltic salmon-specific parasite Gyrodactylus salaris: a model for speciation by host switch for hemiclonal organisms","volume":"16","author":"Kuusela","year":"2007","journal-title":"Mol. Ecol."},{"key":"ref_78","first-page":"5","article-title":"Comparison of molecular phylogeny and morphological systematic in fish parasite genus Gyrodactylus Nordmann, 1832 (Monogenea, Gyrodactylidae)","volume":"49","author":"Lumme","year":"2004","journal-title":"Zoologica Poloniae"},{"key":"ref_79","doi-asserted-by":"crossref","unstructured":"Poulin, R. (2007). Evolutionary Ecology of Parasites, Princeton University Press. [2nd ed.].","DOI":"10.1515\/9781400840809"},{"key":"ref_80","first-page":"198","article-title":"Life cycles shape parasite evolution: comparative population genetics of salmon trematodes","volume":"58","author":"Criscione","year":"2004","journal-title":"Evolution"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1016\/j.ympev.2010.01.004","article-title":"Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America","volume":"55","author":"Detwiler","year":"2010","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.ijpara.2009.08.012","article-title":"Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences","volume":"40","author":"Locke","year":"2010","journal-title":"Int. J. Parasitol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"352","DOI":"10.1038\/nature08160","article-title":"The genome of the blood fluke Schistosoma mansoni","volume":"460","author":"Berriman","year":"2009","journal-title":"Nature"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"R71","DOI":"10.1186\/gb-2009-10-6-r71","article-title":"Genomic linkage map of the human blood fluke Schistosoma mansoni","volume":"10","author":"Criscione","year":"2009","journal-title":"Genome Biol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1126\/science.1112642","article-title":"The genome of the African trypanosome Trypanosoma brucei","volume":"309","author":"Berriman","year":"2005","journal-title":"Science"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"6688","DOI":"10.1093\/nar\/gki980","article-title":"The genetic map and comparative analysis with the physical map of Trypanosoma brucei","volume":"33","author":"MacLeod","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"R103","DOI":"10.1186\/gb-2008-9-6-r103","article-title":"Genetic analysis of the human infective trypanosome, Trypanosoma brucei gambiense: chromosomal segregation, crossing over and the construction of a genetic map","volume":"9","author":"Cooper","year":"2008","journal-title":"Genome Biol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"2308","DOI":"10.1002\/elps.200305455","article-title":"Molecular epidemiological investigation of Ascaris genotypes in China based on single-strand conformation polymorphism analysis of ribosomal DNA","volume":"24","author":"Peng","year":"2003","journal-title":"Electrophoresis"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/S1471-4922(00)01944-9","article-title":"The dangers of using single locus markers in parasite epidemiology: Ascaris as a case study","volume":"17","author":"Anderson","year":"2001","journal-title":"Trends Parasitol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"790","DOI":"10.2307\/3279502","article-title":"Genetic differentiation among larval nematodes infecting fishes","volume":"64","author":"Vrijenhoek","year":"1978","journal-title":"J. Parasitol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1016\/S0020-7519(97)00024-6","article-title":"Evidence for hybridization between Paramacropostrongylus iugalis and P. typicus (Nematoda: Strongyloidea) in grey kangaroos, Macropus fuliginosus and M. giganteus, in a zone of sympatry in eastern Australia","volume":"27","author":"Chilton","year":"1997","journal-title":"Int. J. Parasitol."},{"key":"ref_92","first-page":"151","article-title":"Ricerche cariologiche ed su Parascaris univalens e Parascaris equorum","volume":"65","author":"Bullini","year":"1978","journal-title":"Accademia Nazionale dei Lincei, Rendiconti Classe Scienze Fisiche Matamatiche e Naturali, serie VIII"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/0020-7519(91)90010-5","article-title":"Genetic evidence for three species within Pseudoterranova decipiens (Nematoda, Ascaridida, Ascaridoidea) in the North Atlantic and Norwegian and Barents Sea","volume":"21","author":"Paggi","year":"1991","journal-title":"Int. J. Parasitol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1111\/j.2006.0018-0661.01956.x","article-title":"Escape from an evolutionary dead end: a triploid clone of Gyrodactylus salaris is able to revert to sex and switch host (Platyhelminthes, Monogenea, Gyrodactylidae)","volume":"143","author":"Kuusela","year":"2006","journal-title":"Hereditas"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1016\/S0020-7519(98)00037-X","article-title":"Triploid form of Fasciola in Japan: genetic relationships between Fasciola hepatica and Fasciola gigantica determined by ITS-2 sequence of nuclear rDNA","volume":"28","author":"Itagaki","year":"1998","journal-title":"Int. J. Parasitol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1007\/s00436-007-0512-0","article-title":"Sequence analysis of the first internal transcribed spacer of rDNA supports the existence of the intermediate Fasciola between Fhepatica and F. gigantica in mainland China","volume":"101","author":"Lin","year":"2007","journal-title":"Parasitol. Res."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/S1383-5769(00)00051-9","article-title":"Molecular evidence of natural hybridization between Fasciola hepatica and F. gigantica","volume":"49","author":"Agatsuma","year":"2000","journal-title":"Parasitol. Int."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"725","DOI":"10.1016\/j.ijpara.2007.10.003","article-title":"Human fascioliasis and the presence of hybrid\/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam","volume":"38","author":"Le","year":"2008","journal-title":"Int. J. Parasitol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1007\/s00436-009-1459-0","article-title":"Molecular characterization of Fasciola hepatica, Fasciola gigantica, and aspermic Fasciola sp. in China based on nuclear and mitochondrial DNA","volume":"105","author":"Peng","year":"2009","journal-title":"Parasitol. Res."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1016\/S0020-7519(99)00072-7","article-title":"Genetic diversity in parthenogenetic triploid Paragonimus westermani","volume":"29","author":"Blair","year":"1999","journal-title":"Int. J. Parasitol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1186\/1471-2164-9-482","article-title":"PwRn1, a novel Ty3\/gypsy-like retrotransposon of Paragonimus westermani: molecular characters and its differentially preserved mobile potential according to host chromosomal polyploidy","volume":"9","author":"Bae","year":"2008","journal-title":"BMC Genomics"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1079\/JOH2003185","article-title":"The origin of the triploid in Paragonimus westermani on the basis of variable regions in the mitochondrial DNA","volume":"77","author":"Agatsuma","year":"2003","journal-title":"J. Helminthol."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1017\/S0022149X00012384","article-title":"Do all human urinary infections with Schistosoma mattheei represent hybridization between Schistosoma haematobium and Schistosoma mattheei?","volume":"64","author":"Kruger","year":"1990","journal-title":"J. Helminthol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1017\/S0022149X00021969","article-title":"Hybridization experiments on five species of African schistosomes","volume":"44","author":"Taylor","year":"1970","journal-title":"J. Helminthol."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"e1000571","DOI":"10.1371\/journal.ppat.1000571","article-title":"Bidirectional introgressive hybridization between a cattle and human schistosome species","volume":"5","author":"Huyse","year":"2009","journal-title":"PLoS Pathog."},{"key":"ref_106","first-page":"3","article-title":"Hybridization of Schistosoma mansoni and S. rodhaini","volume":"48","author":"LeRoux","year":"1954","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.exppara.2008.02.004","article-title":"Using mitochondrial and nuclear markers to evaluate the degree of genetic cohesion among Echinococcus populations","volume":"119","author":"Badaraco","year":"2008","journal-title":"Exp. Parasitol."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1017\/S0031182000080689","article-title":"A putative Leishmania panamensis\/Leishmania braziliensis hybrid is a causative agent of human cutaneous leishmaniasis in Nicaragua","volume":"109","author":"Belli","year":"1994","journal-title":"Parasitology"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1111\/j.1365-3156.2006.01695.x","article-title":"Species diversity causing human cutaneous leishmaniasis in Rio Branco, state of Acre, Brazil","volume":"11","author":"Cupolillo","year":"2006","journal-title":"Trop. Med. Int. Health"},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"e261","DOI":"10.1371\/journal.pntd.0000261","article-title":"Differentiation and gene flow among European populations of Leishmania infantum MON-1","volume":"2,","author":"Kuhls","year":"2008","journal-title":"PLoS Neglect. Trop. D."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"1309","DOI":"10.1016\/j.micinf.2008.07.031","article-title":"Genetic polymorphism of Algerian Leishmania infantum strains revealed by multilocus microsatellite analysis","volume":"10","author":"Seridi","year":"2008","journal-title":"Microbes Infect."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"757","DOI":"10.1016\/j.ijpara.2006.03.006","article-title":"Towards multilocus sequence typing of the Leishmania donovani complex: resolving genotypes and haplotypes for five polymorphic metabolic enzymes (ASAT, GPI, NH1, NH2, PGD)","volume":"36","author":"Mauricio","year":"2006","journal-title":"Int. J. Parasitol."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1017\/S0031182008004794","article-title":"Evolutionary history of Trypanosoma cruzi according to antigen genes","volume":"135","author":"Rozas","year":"2008","journal-title":"Parasitology"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/S1567-1348(02)00097-7","article-title":"Infect","volume":"2","author":"Brisse","year":"2003","journal-title":"Genet. Evol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1590\/S0074-02762009000900016","article-title":"Trypansoma cruzi: ancestral genomes and population structure.","volume":"104","author":"Pena","year":"2009","journal-title":"Mem. I. 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