Host-parasite incongruences in rodent Eimeria suggest significant role of adaptation rather than cophylogeny in maintenance of host specificity

. 2013 ; 8 (7) : e63601. [epub] 20130704

Jazyk angličtina Země Spojené státy americké Médium electronic-print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid23861732

The degree of host specificity, its phylogenetic conservativeness and origin are virtually unknown in Eimeria. This situation is largely due to the inadequate sample of eimerian molecular data available for reliable phylogenetic analyses. In this study, we extend the data set by adding 71 new sequences of coccidia infecting 16 small-mammal genera, mostly rodents. According to the respective feasibility of PCR gene amplification, the new samples are represented by one or more of the following genes: nuclear 18S rRNA, plastid ORF 470, and mitochondrial COI. Phylogenetic analyses of these sequences confirm the previous hypothesis that Eimeria, in its current morphology-based delimitation, is not a monophyletic group. Several samples of coccidia corresponding morphologically to other genera are scattered among the Eimeria lineages. More importantly, the distribution of eimerians from different hosts indicates that the clustering of eimerian species is influenced by their host specificity, but does not arise from a cophylogenetic/cospeciation process; while several clusters are specific to a particular host group, inner topologies within these clusters do not reflect host phylogeny. This observation suggests that the host specificity of Eimeria is caused by adaptive rather than cophylogenetic processes.

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Brooks DR, McLennan DA (1993) Parascript: Parasites and the Language of Evolution. Washington, DC: Smithsonian Institute Press.

Page RDM (1996a) Temporal congruence revisited: comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Syst Biol 45: 151–167.

Huelsenbeck JP, Rannala B, Yang Z (1997) Statistical tests of host-parasite cospeciation. Evolution 51: 410–419. PubMed

Paterson AM, Gray RD (1997) Host-parasite co-speciation, host switching and missing the boat. In: Clayton DH, Moore J, editors. Host-Parasite Evolution: General Principles and Avian Models. Oxford: Oxford University Press. pp.236–250.

Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R (2010) Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol Biol 5: 16. PubMed PMC

Merkle D, Middendorf M, Wieseke N (2010) A Parameter-Adaptive Dynamic Programming Approach for Inferring Cophylogenies. BMC Bioinformatics 11: 60. PubMed PMC

Hafner MS, Nadler SA (1990) Cospeciation in host-parasite assemblages: comparative analysis of rates of evolution and timing of cospeciation events. Syst Zool 39: 192–204.

Ricklefs RE, Fallon SM, Bermingham E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst Biol 53: 111–119. PubMed

Charleston MA (1998) Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Math Biosci 149: 191–223. PubMed

Page RDM, Lee PLM, Becher SA, Griffiths R, Clayton DH (1998) A different tempo of mitochondrial DNA evolution in birds and their parasitic lice. Mol Phylogenet Evol 9: 276–293. PubMed

Huelsenbeck JP, Rannala B, Larget B (2000) A Bayesian framework for the analysis of cospeciation. Evolution 54: 352–364. PubMed

Jousson O, Bartoli P, Pawlowski J (2000) Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). J Evol Biol 13: 778–785.

Ricklefs RE, Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B Biol Sci 269: 885–892. PubMed PMC

Relman DA, Schmidt TM, Gajadhar A, Sogin M, Cross J, et al. (1996) Molecular phylogenetic analysis of Cyclospora, the human intestinal pathogen, suggests that it is closely related to Eimeria species. J Infect Dis 173: 440–445. PubMed

Pieniazek NJ, Herwaldt BL (1997) Reevaluating the molecular taxonomy: is human-associated Cyclospora a mammalian Eimeria species? Emerg Infect Dis 3: 381–383. PubMed PMC

Carreno RA, Schnitzler BE, Jeffries AC, Tenter AM, Johnson AM, et al. (1998) Phylogenetic analysis of coccidia based on 18S rDNA sequence comparison indicates that Isospora is most closely related to Toxoplasma and Neospora . J Eukaryot Microbiol 45: 184–188. PubMed

Brabec J, Kuchta R, Scholz T (2006) Paraphyly of the Pseudophyllidea (Platyhelminthes: Cestoda): circumscription of monophyletic clades based on phylogenetic analysis of ribosomal RNA. Int J Parasitol 36: 1535–1541. PubMed

Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36: 1521–1534. PubMed

Štefka J, Hypša V (2008) Host specificity and genealogy of the louse Polyplax serrata on field mice, Apodemus species: a case of parasite duplication or colonisation? Int J Parasitol 38: 731–741. PubMed

Paterson AM, Banks J (2001) Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. Int J Parasitol 31: 1012–1022. PubMed

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

Brant SV, Gardner SL (2000) Phylogeny of species of the genus Litomosoides (Nematoda: Onchocercidae): evidence of rampant host switching. J Parasitol 86: 545–554. PubMed

Perlman SJ, Spicer GS, Shoemaker DD, Jaenike J (2003) Associations between mycophagous Drosophila and their Howardula nematode parasites: a worldwide phylogenetic shuffle. Mol Ecol 12: 237–249. PubMed

Weckstein JD (2004) Biogeography explains cophylogenetic patterns in toucan chewing lice. Syst Biol 53: 154–164. PubMed

Whiteman NK, Santiago-Alarcon D, Johnson KP, Parker PG (2004) Differences in straggling rates between two genera of dove lice (Insecta: Phthiraptera) reinforce population genetic and cophylogenetic patterns. Int J Parasitol 34: 1113–1119. PubMed

Pellérdy LP (1974) Coccidia and Coccidiosis. Budapest: Akademiai Kiadó.

Lewis DC, Ball SJ (1983) Species of Eimeria of small wild rodents from the British Isles, with descriptions of two new species. Syst Parasitol 5: 259–270.

Levine ND, Ivens V (1990) The Coccidian Parasites of Rodents. Florida, Boca Raton: CRC Press.

Higgs S, Nowell F (1991) A review of the species of Eimeria infecting hosts in the genus Apodemus . Syst Parasitol 20: 203–209.

Hůrková L, Baker MA, Jirků M, Modrý D (2005) Two new species of Eimeria Schneider 1875 (Apicomplexa: Eimeriidae) from the broad-toothed field mouse, Apodemus mystacinus Danford and Alston 1877 (Rodentia: Muridae) from Jordan. Parasitol Res 97: 33–40. PubMed

Seville RS, Oliver CE, Lynch AJ, Bryant MC, Duszynski DW (2005) Eimeria species (Apicomplexa: Eimeriidae) from arctic ground squirrels (Spermophilus parryii) and red squirrels (Tamiasciurus hudsonicus) in Alaska and in Siberia, Russia. J Parasitol 91: 857–862. PubMed

Golemansky VG, Koshev YS (2007) Coccidian Parasites (Eucoccidia: Eimeriidae) in European Ground Squirrel (Spermophilus citellus L., 1766) (Rodentia: Sciuridae) from Bulgaria. Acta Zool Bulgar 59: 81–85.

Lynch AJ, Duszynski DW, Cook JA (2007) Species of Coccidia (Apicomplexa: Eimeriidae) Infecting Pikas From Alaska, U.S.A. and Northeastern Siberia, Russia. J Parasitol 93: 1230–1234. PubMed

de Vos AJ (1970) Studies on the host range of Eimeria chinchillae de Vos & van der Westhuizen, 1968. Onderstepoort J Vet Res 37: 29–36. PubMed

Upton SJ, McAllister CT, Brillhart DB, Duszynski DW, Wash CD (1992) Cross-transmission studies with Eimeria arizonensis-like oocysts (Apicomplexa) in New World rodents of the genera Baiomys, Neotoma, Onychomys, Peromyscus, and Reithrodontomys (Muridae). J Parasitol 78: 406–413. PubMed

Koudela B, Vítovec J (1994) Life cycle and pathogenicity of Eimeria strakonicensis n.sp. (Apicomplexa: Eimeriidae) in experimentally infected common voles (Microtus arvalis). Can J Zool 72: 239–246.

Jirků M, Jirků M, Oborník M, Lukeš J, Modrý D (2009) A Model for Taxonomic Work on Homoxenous Coccidia: Redescription, Host Specificity, and Molecular Phylogeny of Eimeria ranae Dobell, 1909, with a Review of Anuran-Host Eimeria (Apicomplexa: Eimeriorina). J Eukaryot Microbiol 56: 39–51. PubMed

Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, et al. (1997) Phylogenetic Relationships among Eight Eimeria Species Infecting Domestic Fowl Inferred Using Complete Small Subunit Ribosomal DNA Sequences. J Parasitol 82: 262–271. PubMed

Morrison DA, Bornstein S, Thebo P, Wernery U, Kinne J, et al. (2004) The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). Int J Parasitol 34: 501–514. PubMed

Matsubayashi M, Takami K, Niichiro A, Kimata I, Tani H, et al. (2005) Molecular characterization of crane coccidia, Eimeria gruis and E. reichenowi, found in feces of migratory cranes. Parasitol Res 97: 80–83. PubMed

Kvičerová J, Pakandl M, Hypša V (2008) Phylogenetic relationships among Eimeria spp. (Apicomplexa, Eimeriidae) infecting rabbits: evolutionary significance of biological and morphological features. Parasitology 135: 443–452. PubMed

Long PL, Joyner LP (1984) Problems in the Identification of Species of Eimeria . J Protozool 31: 535–541. PubMed

Parker BP, Duszynski DW (1986) Polymorphism of Eimerian Oocysts: A Dilemma Posed by Working with Some Naturally Infected Hosts. J Parasitol 72: 602–604. PubMed

Gardner SL, Duszynski DW (1990) Polymorphism of eimerian oocysts can be a problem in naturally infected hosts: an example from subterranean rodents in Bolivia. J Parasitol 76: 805–811. PubMed

Franzen C, Müller A, Bialek R, Diehl V, Salzberger B, et al. (2000) Taxonomic position of the human intestinal protozoan parasite Isospora belli as based on ribosomal RNA sequences. Parasitol Res 86: 669–676. PubMed

Jirků M, Modrý D, Šlapeta JR, Koudela B, Lukeš J (2002) The phylogeny of Goussia and Choleoeimeria (Apicomplexa: Eimeriorina) and the evolution of excystation structures in coccidia. Protist 153: 380–389. PubMed

Jirků M, Jirků M, Oborník M, Lukeš J, Modrý D (2009) Goussia Labbé, 1896 (Apicomplexa, Eimeriorina) in Amphibia: diversity, biology, molecular phylogeny and comments on the status of the genus. Protist 160: 123–136. PubMed

Samarasinghe B, Johnson J, Ryan U (2008) Phylogenetic analysis of Cystoisospora species at the rRNA ITS1 locus and development of a PCR-RFLP assay. Exp Parasitol 118: 592–595. PubMed

Dolnik OV, Palinauskas V, Bensch S (2009) Individual oocysts of Isospora (Apicomplexa: Coccidia) parasites from avian feces: from photo to sequence. J Parasitol 95: 169–174. PubMed

Zhao X, Duszynski DW (2001a) Molecular phylogenies suggest the oocyst residuum can be used to distinguish two independent lineages of Eimeria spp in rodents. Parasitol Res 87: 638–643. PubMed

Zhao X, Duszynski DW (2001b) Phylogenetic relationships among rodent Eimeria species determined by plastid ORF470 and nuclear 18S rDNA sequences. Int J Parasitol 31: 715–719. PubMed

Power ML, Richter C, Emery S, Hufschmid J, Gillings MR (2009) Eimeria trichosuri: phylogenetic position of a marsupial coccidium, based on 18S rDNA sequences. Exp Parasitol 122: 165–168. PubMed

Kvičerová J, Mikeš V, Hypša V (2011) Third lineage of rodent eimerians: morphology, phylogeny and re-description of Eimeria myoxi (Apicomplexa: Eimeriidae) from Eliomys quercinus (Rodentia: Gliridae). Parasitology 138: 1217–1223. PubMed

Duszynski DW, Wilber PG (1997) A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol 83: 333–336. PubMed

Schwarz RS, Jenkins MC, Klopp S, Miska KB (2009) Genomic analysis of Eimeria spp. populations in relation to performance levels of broiler chicken farms in Arkansas and North Carolina. J Parasitol 95: 871–880. PubMed

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

Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511–518. PubMed PMC

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

Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25: 1253–1256. PubMed

Posada D (2009) Selection of models of DNA evolution with jModelTest. Methods Mol Biol 537: 93–112. PubMed

Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenesis by maximum likelihood. Syst Biol 52: 696–704. PubMed

Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755. PubMed

Tracer website. Available: http://beast.bio.ed.ac.uk/Tracer. Accessed 2013 Jun 12.

Page RDM (1996b) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12: 357–358. PubMed

Yabsley MJ, Gibbs SEJ (2006) Description and phylogeny of a new species of Eimeria from double-crested cormorants (Phalacrocorax auritus) near Fort Gaines, Georgia. J Parasitol 92: 385–388. PubMed

Duszynski DW, Upton SJ (2000) Coccidia (Apicomplexa: Eimeriidae) of the Mammalian Order Insectivora. Special Publication of the Museum of Southwestern Biology. Albuquerque, New Mexico: The University of New Mexico Printing Services. No. 4, pp.1–67.

Barta JR, Schrenzel MD, Carreno R, Rideout BA (2005) The Genus Atoxoplasma (Garnham 1950) as a Junior Objective Synonym of the Genus Isospora (Schneider 1881) Species Infecting Birds and resurrection of Cystoisospora (Frenkel 1977) as the Correct Genus for Isospora Species Infecting Mammals. J Parasitol 91: 726–727. PubMed

Duszynski DW, Upton SJ (2001) The common coccidia of wild mammals. Cyclospora, Eimeria (Eimeriidae) and Cryptosporidium (Cryptosporidiidae) spp. In: Samuel WM, Pybus MJ, Kocan AA, editors. Parasitic Diseases of Wild Mammals. Iowa, Ames: Iowa State University Press. 423 p.

Zhao X, Duszynski DW, Loker ES (2001) Phylogenetic position of Eimeria antrozoi, a bat coccidium (Apicomplexa: Eimeriidae) and its relationship to morphologically similar Eimeria spp. from bats and rodents based on nuclear 18S and plastid 23S rDNA sequences. J Parasitol 87: 1120–1123. PubMed

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