title: Ecological host fitting of Trypanosoma cruzi TcI in Bolivia: mosaic population structure, hybridization and a role for humans in Andean parasite dispersal.
abstract: An improved understanding of how a parasite species exploits its genetic repertoire to colonize novel hosts and environmental niches is crucial to establish the epidemiological risk associated with emergent pathogenic genotypes. Trypanosoma cruzi, a genetically heterogeneous, multi-host zoonosis, provides an ideal system to examine the sylvatic diversification of parasitic protozoa. In Bolivia, T. cruzi I, the oldest and most widespread genetic lineage, is pervasive across a range of ecological clines. High-resolution nuclear (26 loci) and mitochondrial (10 loci) genotyping of 199 contemporaneous sylvatic TcI clones was undertaken to provide insights into the biogeographical basis of T. cruzi evolution. Three distinct sylvatic parasite transmission cycles were identified: one highland population among terrestrial rodent and triatomine species, composed of genetically homogenous strains (Ar = 2.95; PA/L = 0.61; DAS = 0.151), and two highly diverse, parasite assemblages circulating among predominantly arboreal mammals and vectors in the lowlands (Ar = 3.40 and 3.93; PA/L = 1.12 and 0.60; DAS = 0.425 and 0.311, respectively). Very limited gene flow between neighbouring terrestrial highland and arboreal lowland areas (distance ~220 km; FST = 0.42 and 0.35) but strong connectivity between ecologically similar but geographically disparate terrestrial highland ecotopes (distance >465 km; FST = 0.016-0.084) strongly supports ecological host fitting as the predominant mechanism of parasite diversification. Dissimilar heterozygosity estimates (excess in highlands, deficit in lowlands) and mitochondrial introgression among lowland strains may indicate fundamental differences in mating strategies between populations. Finally, accelerated parasite dissemination between densely populated, highland areas, compared to uninhabited lowland foci, likely reflects passive, long-range anthroponotic dispersal. The impact of humans on the risk of epizootic Chagas disease transmission in Bolivia is discussed.
authors.affiliation: Department of Pathogen Molecular Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK.
authors.forename: Louisa A
authors.initials: LA
authors.lastname: Messenger
authors.forename: Lineth
authors.initials: L
authors.lastname: Garcia
authors.forename: Mathieu
authors.initials: M
authors.lastname: Vanhove
authors.forename: Carlos
authors.initials: C
authors.lastname: Huaranca
authors.forename: Marinely
authors.initials: M
authors.lastname: Bustamante
authors.forename: Marycruz
authors.initials: M
authors.lastname: Torrico
authors.forename: Faustino
authors.initials: F
authors.lastname: Torrico
authors.forename: Michael A
authors.initials: MA
authors.lastname: Miles
authors.forename: Martin S
authors.initials: MS
authors.lastname: Llewellyn
mesh_terms: D000818:Animals; D001838:Bolivia; D014355:Chagas Disease / Q000469:parasitology; D004272:DNA, Mitochondrial / Q000235:genetics; D016054:DNA, Protozoan / Q000235:genetics; D051456:Gene Flow; D014644:Genetic Variation; D005828:Genetics, Population; D005838:Genotype; D005843:Geography; D006801:Humans; D006824:Hybridization, Genetic; D018895:Microsatellite Repeats; D017422:Sequence Analysis, DNA; D014349:Trypanosoma cruzi / Q000235:genetics*
chemical_list: D004272:DNA, Mitochondrial; D016054:DNA, Protozoan
keywords: Trypanosoma cruzi; ecological fitting; microsatellites; mitochondria; population genetics; sylvatic transmission
references.citation: PLoS Pathog. 2009 May;5(5):e1000410
references.pmid: 19412340
references.citation: Exp Parasitol. 2001 Mar;97(3):129-40
references.pmid: 11312575
references.citation: Exp Parasitol. 1996 Aug;83(3):275-82
references.pmid: 8823244
references.citation: BMC Genet. 2010 Oct 15;11:94
references.pmid: 20950446
references.citation: Trop Med Int Health. 2007 Jun;12(6):759-64
references.pmid: 17550473
references.citation: Parasitol Res. 2008 Aug;103(3):619-24
references.pmid: 18493795
references.citation: Acta Trop. 2007 Apr;102(1):47-54
references.pmid: 17397789
references.citation: Bioinformatics. 2012 Oct 1;28(19):2537-9
references.pmid: 22820204
references.citation: Am J Trop Med Hyg. 2008 Feb;78(2):294-7
references.pmid: 18256432
references.citation: Infect Genet Evol. 2006 Jan;6(1):46-62
references.pmid: 16376840
references.citation: Mem Inst Oswaldo Cruz. 2009 Jul;104 Suppl 1:31-40
references.pmid: 19753455
references.citation: Vet Res. 2009 Mar-Apr;40(2):26
references.pmid: 19250627
references.citation: Acta Trop. 2007 Feb;101(2):169-77
references.pmid: 17306204
references.citation: PLoS Negl Trop Dis. 2009 Sep 01;3(9):e510
references.pmid: 19721699
references.citation: J Cell Biol. 1997 Jun 16;137(6):1369-79
references.pmid: 9182668
references.citation: Parasit Vectors. 2012 Oct 10;5:226
references.pmid: 23050833
references.citation: Ecology. 2006 Jul;87(7 Suppl):S76-85
references.pmid: 16922304
references.citation: Bioinformatics. 2009 Jun 1;25(11):1451-2
references.pmid: 19346325
references.citation: Nat Methods. 2012 Jul 30;9(8):772
references.pmid: 22847109
references.citation: Heredity (Edinb). 2010 Feb;104(2):135-40
references.pmid: 19812614
references.citation: Mol Phylogenet Evol. 2007 Jul;44(1):15-25
references.pmid: 17513135
references.citation: Trop Med Int Health. 2010 Sep;15(9):1037-48
references.pmid: 20545921
references.citation: PLoS Negl Trop Dis. 2012;6(4):e1584
references.pmid: 22506081
references.citation: Am J Trop Med Hyg. 2012 Mar;86(3):455-8
references.pmid: 22403316
references.citation: Mem Inst Oswaldo Cruz. 2002 Jan;97(1):61-3
references.pmid: 11992149
references.citation: PLoS Negl Trop Dis. 2013 Nov 07;7(11):e2505
references.pmid: 24244766
references.citation: Trends Parasitol. 2013 Jun;29(6):264-9
references.pmid: 23602631
references.citation: Proc Natl Acad Sci U S A. 2012 Nov 27;109(48):E3305-13
references.pmid: 22949662
references.citation: J Med Entomol. 2010 Nov;47(6):1077-81
references.pmid: 21175056
references.citation: Trans R Soc Trop Med Hyg. 2008 Nov;102(11):1133-9
references.pmid: 18541281
references.citation: J Mol Evol. 1989 Aug;29(2):170-9
references.pmid: 2509717
references.citation: Infect Genet Evol. 2009 Dec;9(6):1265-74
references.pmid: 19632356
references.citation: Trop Med Int Health. 2003 Mar;8(3):264-8
references.pmid: 12631318
references.citation: Clin Infect Dis. 2012 Mar;54(6):845-52
references.pmid: 22238161
references.citation: Mem Inst Oswaldo Cruz. 2009 Nov;104(7):1051-4
references.pmid: 20027478
references.citation: Mem Inst Oswaldo Cruz. 2000 Jul-Aug;95(4):557-65
references.pmid: 10904415
references.citation: Parasitology. 1999 Jan;118 ( Pt 1):107-16
references.pmid: 10070668
references.citation: PLoS Negl Trop Dis. 2012;6(11):e1888
references.pmid: 23133690
references.citation: Parasit Vectors. 2014 Apr 01;7:154
references.pmid: 24690302
references.citation: Int J Parasitol. 2010 Dec;40(14):1599-607
references.pmid: 20670628
references.citation: Mol Biol Evol. 2007 Aug;24(8):1586-91
references.pmid: 17483113
references.citation: PLoS Negl Trop Dis. 2011 Jun;5(6):e1049
references.pmid: 21713026
references.citation: PLoS Negl Trop Dis. 2014 Apr 03;8(4):e2782
references.pmid: 24699407
references.citation: Parasitology. 2010 May;137(6):959-66
references.pmid: 20128943
references.citation: Proc Biol Sci. 2009 Apr 7;276(1660):1201-9
references.pmid: 19203921
references.citation: Trends Parasitol. 2005 Jan;21(1):7-10
references.pmid: 15639733
references.citation: PLoS Negl Trop Dis. 2012;6(6):e1707
references.pmid: 22745843
references.citation: Mol Ecol. 2014 Sep;23(17):4195-202
references.pmid: 25060834
references.citation: PLoS Negl Trop Dis. 2010 Nov 30;4(11):e899
references.pmid: 21152056
references.citation: Int J Parasitol. 2007 Jan;37(1):111-20
references.pmid: 17052720
references.citation: Evol Bioinform Online. 2007 Feb 23;1:47-50
references.pmid: 19325852
references.citation: Mol Biol Evol. 2011 Oct;28(10):2731-9
references.pmid: 21546353
references.citation: Lancet. 2010 Apr 17;375(9723):1388-402
references.pmid: 20399979
references.citation: Exp Parasitol. 2006 Dec;114(4):305-13
references.pmid: 16797540
references.citation: Evolution. 2006 Mar;60(3):553-62
references.pmid: 16637500
references.citation: Evolution. 1989 Jan;43(1):223-225
references.pmid: 28568501
references.citation: Mem Inst Oswaldo Cruz. 2009 Jul;104 Suppl 1:52-9
references.pmid: 19753458
references.citation: Mol Ecol. 2012 Sep;21(17):4216-26
references.pmid: 22774844
references.citation: PLoS Negl Trop Dis. 2011 Oct;5(10):e1365
references.pmid: 22039559
references.citation: Am J Trop Med Hyg. 2009 Dec;81(6):1041-9
references.pmid: 19996435
references.citation: PLoS Pathog. 2010 Jul 29;6(7):e1001023
references.pmid: 20686656
references.citation: Int J Parasitol. 2005 Feb;35(2):225-33
references.pmid: 15710443
references.citation: Emerg Infect Dis. 2004 Mar;10(3):438-46
references.pmid: 15109410
references.citation: Bioinformatics. 2009 Jan 1;25(1):126-7
references.pmid: 18984599
references.citation: Methods Mol Biol. 1993;21:15-28
references.pmid: 8220712
references.citation: PLoS One. 2013 Jul 04;8(7):e67463
references.pmid: 23861767
references.citation: Infect Genet Evol. 2011 Oct;11(7):1752-60
references.pmid: 21801854
references.citation: Parasitology. 2004 Dec;129(Pt 6):703-11
references.pmid: 15648693
references.citation: Parasitology. 2009 Oct;136(12):1509-28
references.pmid: 19691868
references.citation: Acta Trop. 2009 Apr;110(1):15-21
references.pmid: 19135020
references.citation: Am J Trop Med Hyg. 2010 Apr;82(4):574-9
references.pmid: 20348501
references.citation: BMC Genomics. 2009 Jun 01;10:255
references.pmid: 19486522
references.citation: PLoS Negl Trop Dis. 2012;6(5):e1650
references.pmid: 22685616
references.citation: Am J Trop Med Hyg. 1996 Apr;54(4):418-24
references.pmid: 8615458
references.citation: PLoS Negl Trop Dis. 2008 Apr 02;2(4):e210
references.pmid: 18382605
references.citation: Bioinformatics. 2008 Jun 1;24(11):1403-5
references.pmid: 18397895
references.citation: PLoS Negl Trop Dis. 2011 Oct;5(10):e1363
references.pmid: 22022633
references.citation: Mol Biochem Parasitol. 2014 Jul;195(2):115-22
references.pmid: 24893339
references.citation: J Med Entomol. 2009 Jul;46(4):796-809
references.pmid: 19645282
references.citation: Int J Parasitol. 2011 May;41(6):609-14
references.pmid: 21232539
references.citation: Infect Genet Evol. 2010 Mar;10(2):350-3
references.pmid: 20060504
references.citation: Rev Soc Bras Med Trop. 2003 Mar-Apr;36(2):241-8
references.pmid: 12806461
references.citation: Mem Inst Oswaldo Cruz. 2009 Jul;104 Suppl 1:60-4
references.pmid: 19753459
references.citation: PLoS One. 2013;8(2):e56198
references.pmid: 23457528
references.citation: J Parasitol Res. 2009;2009:
references.pmid: 20798881
references.citation: Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7396-401
references.pmid: 11416213
references.citation: PLoS Negl Trop Dis. 2010 Dec 14;4(12):e915
references.pmid: 21179502
references.citation: Nature. 2003 Feb 27;421(6926):936-9
references.pmid: 12606999
references.citation: Infect Genet Evol. 2007 Sep;7(5):587-93
references.pmid: 17553755
references.citation: J Med Entomol. 1981 Jul;18(4):266-78
references.pmid: 6790704
references.citation: PLoS Negl Trop Dis. 2013 Aug 01;7(8):e2358
references.pmid: 23936581
references.citation: Mem Inst Oswaldo Cruz. 2008 Aug;103(5):423-30
references.pmid: 18797753
references.citation: Trans R Soc Trop Med Hyg. 2005 May;99(5):379-88
references.pmid: 15780345
references.citation: Infect Genet Evol. 2014 Mar;22:183-91
references.pmid: 24296011
references.citation: Trop Med Int Health. 2010 Jun;15(6):727-32
references.pmid: 20374565
references.citation: Parasit Vectors. 2014 Jun 05;7:263
references.pmid: 24903849
references.citation: Ecol Lett. 2008 Nov;11(11):1123-1134
references.pmid: 18778274
references.citation: Infect Genet Evol. 2007 Jul;7(4):535-9
references.pmid: 17287152