Variant antigen diversity in Trypanosoma vivax is not driven by recombination.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
12 02 2020
Historique:
received: 30 08 2019
accepted: 18 01 2020
entrez: 14 2 2020
pubmed: 14 2 2020
medline: 24 4 2020
Statut: epublish

Résumé

African trypanosomes (Trypanosoma) are vector-borne haemoparasites that survive in the vertebrate bloodstream through antigenic variation of their Variant Surface Glycoprotein (VSG). Recombination, or rather segmented gene conversion, is fundamental in Trypanosoma brucei for both VSG gene switching and for generating antigenic diversity during infections. Trypanosoma vivax is a related, livestock pathogen whose VSG lack structures that facilitate gene conversion in T. brucei and mechanisms underlying its antigenic diversity are poorly understood. Here we show that species-wide VSG repertoire is broadly conserved across diverse T. vivax clinical strains and has limited antigenic repertoire. We use variant antigen profiling, coalescent approaches and experimental infections to show that recombination plays little role in diversifying T. vivax VSG sequences. These results have immediate consequences for both the current mechanistic model of antigenic variation in African trypanosomes and species differences in virulence and transmission, requiring reconsideration of the wider epidemiology of animal African trypanosomiasis.

Identifiants

pubmed: 32051413
doi: 10.1038/s41467-020-14575-8
pii: 10.1038/s41467-020-14575-8
pmc: PMC7015903
doi:

Substances chimiques

DNA, Protozoan 0
Protozoan Proteins 0
Variant Surface Glycoproteins, Trypanosoma 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

844

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/M022811/1
Pays : International
Organisme : Wellcome Trust (Wellcome)
ID : WT206815/Z/17/Z
Pays : International
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/R021139/1
Pays : International

Références

Giordani, F., Morrison, L. J., Rowan, T. G., De Koning, H. P. & Barrett, M. P. The animal trypanosomiases and their chemotherapy: a review. Parasitology 143, 1862–1889 (2016).
pubmed: 27719692 pmcid: 5142301 doi: 10.1017/S0031182016001268
Shaw, A. P. M., Cecchi, G., Wint, G. R. W., Mattioli, R. C. & Robinson, T. P. Mapping the economic benefits to livestock keepers from intervening against bovine trypanosomosis in Eastern Africa. Prev. Vet. Med. 113, 197–210 (2014).
pubmed: 24275205 doi: 10.1016/j.prevetmed.2013.10.024
Gardiner, P. R. Recent studies of the biology of Trypanosoma vivax. Adv. Parasitol. 28, 229–317 (1989).
pubmed: 2683616 doi: 10.1016/S0065-308X(08)60334-6
Osório, A. L. A. R. et al. Trypanosoma (Duttonella) vivax: its biology, epidemiology, pathogenesis, and introduction in the New World—a review. Mem. Inst. Oswaldo Cruz 103, 1–13 (2008).
pubmed: 18368231 doi: 10.1590/S0074-02762008000100001
Morrison, L. J., Vezza, L., Rowan, T. & Hope, J. C. Animal African Trypanosomiasis: time to increase focus on clinically relevant parasite and host species. Trends Parasitol. 32, 599–607 (2016).
pubmed: 27167665 doi: 10.1016/j.pt.2016.04.012
Hoare, C. A. The Trypanosomes of Mammals. A Zoological Monograph (Blackwell, 1972).
Vickerman, K. & Evans, A. Studies on the ultrastructure and respiratory physiology of Trypanosoma vivax trypomastigote stages. Trans. R. Soc. Trop. Med. Hyg. 68, 45 (1974).
Tetley, L. & Vickerman, K. Surface ultrastructure of Trypanosoma vivax bloodstream forms. Trans. R. Soc. Trop. Med. Hyg. 73, 321 (1979).
Van der Ploeg, L. H., Cornelissen, A. W., Barry, J. D. & Borst, P. Chromosomes of kinetoplastida. EMBO J. 3, 3109–3115 (1984).
pubmed: 6526012 pmcid: 557825 doi: 10.1002/j.1460-2075.1984.tb02266.x
Jackson, A. P. et al. Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species. Proc. Natl. Acad. Sci. USA 109, 3416–3421 (2012).
pubmed: 22331916 doi: 10.1073/pnas.1117313109
Horn, D. Antigenic variation in African trypanosomes. Mol. Biochem. Parasitol. 195, 123–129 (2014).
pubmed: 24859277 pmcid: 4155160 doi: 10.1016/j.molbiopara.2014.05.001
Mugnier, M. R., Stebbins, C. E. & Papavasiliou, F. N. Masters of disguise: antigenic variation and the VSG coat in Trypanosoma brucei. PLOS Pathog. 12, e1005784 (2016).
pubmed: 27583379 pmcid: 5008768 doi: 10.1371/journal.ppat.1005784
Jackson, A. P. et al. A cell-surface phylome for African trypanosomes. PLoS Negl. Trop. Dis. 7, e2121 (2013).
pubmed: 23556014 pmcid: 3605285 doi: 10.1371/journal.pntd.0002121
Robinson, N. P., Burman, N., Melville, S. E. & Barry, J. D. Predominance of duplicative VSG gene conversion in antigenic variation in African trypanosomes. Mol. Cell. Biol. 19, 5839–5846 (1999).
pubmed: 10454531 pmcid: 84433 doi: 10.1128/MCB.19.9.5839
Hall, J. P. J., Wang, H. & Barry, J. D. Mosaic VSGs and the scale of Trypanosoma brucei antigenic variation. PLoS Pathog. 9, e1003502 (2013).
pubmed: 23853603 pmcid: 3708902 doi: 10.1371/journal.ppat.1003502
Nantulya, V. M., Musoke, A. J. & Moloo, S. K. Apparent exhaustion of the variable antigen repertoires of Trypanosoma vivax in infected cattle. Infect. Immun. 54, 444–447 (1986).
pubmed: 3770950 pmcid: 260181 doi: 10.1128/IAI.54.2.444-447.1986
Barry, J. D. Antigenic variation during Trypanosoma vivax infections of different host species. Parasitology 92, 51–65 (1986).
pubmed: 2421230 doi: 10.1017/S0031182000063447
Dar, F. K., Paris, J. & Wilson, A. J. Serological studies on trypanosomiasis in East Africa: IV: comparison of antigenic types of Trypanosoma vivax group organisms. Ann. Trop. Med. Parasitol. 67, 319–329 (1973).
pubmed: 4761941 doi: 10.1080/00034983.1973.11686893
Murray, A. K. & Clarkson, M. J. Characterization of stocks of Trypanosoma vivax. II. Immunological studies. Ann. Trop. Med. Parasitol. 76, 283–292 (1982).
pubmed: 7125758 doi: 10.1080/00034983.1982.11687543
Silva Pereira, S. et al. Variant antigen repertoires in Trypanosoma congolense populations and experimental infections can be profiled from deep sequence data with a set of universal protein motifs. Genome Res. 28, 1383–1394 (2018).
pubmed: 30006414 pmcid: 6120623 doi: 10.1101/gr.234146.118
Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).
pubmed: 27004904 pmcid: 27004904 doi: 10.1093/molbev/msw054
Hutchinson, O. C. et al. Variant surface glycoprotein gene repertoires in Trypanosoma brucei have diverged to become strain-specific. BMC Genomics 8, 234 (2007).
pubmed: 17629915 pmcid: 1934917 doi: 10.1186/1471-2164-8-234
Bruen, T. C., Philippe, H. & Bryant, D. A simple and robust statistical test for detecting the presence of recombination. Genetics 172, 2665–2681 (2006).
pubmed: 16489234 pmcid: 1456386 doi: 10.1534/genetics.105.048975
Cadioli, F. A. et al. First report of Trypanosoma vivax outbreak in dairy cattle in São Paulo state, Brazil. Rev. Bras. Parasitol. Vet., Jaboticabal 21, 118–124 (2012).
doi: 10.1590/S1984-29612012000200009
Mugnier, M. R., Cross, G. A. M. & Papavasiliou, F. N. The in vivo dynamics of antigenic variation in Trypanosoma brucei. Science 347, 1470–1473 (2015).
pubmed: 25814582 pmcid: 4514441 doi: 10.1126/science.aaa4502
Jayaraman, S. et al. Application of long read sequencing to determine expressed antigen diversity in Trypanosoma brucei infections. PLoS Negl. Trop. Dis. 13, e0007262 (2019).
pubmed: 30943202 pmcid: 6464242 doi: 10.1371/journal.pntd.0007262
Marcello, L. & Barry, J. D. Analysis of the VSG gene silent archive in Trypanosoma brucei reveals that mosaic gene expression is prominent in antigenic variation and is favored by archive substructure. Genome Res. 17, 1344–1352 (2007).
pubmed: 17652423 pmcid: 1950903 doi: 10.1101/gr.6421207
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).
pubmed: 2231712 doi: 10.1016/S0022-2836(05)80360-2
Berriman, M. et al. The genome of the African trypanosome Trypanosoma brucei. Science 309, 416–422 (2005).
pubmed: 16020726 doi: 10.1126/science.1112642
Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H. & Frost, S. D. W. GARD: a genetic algorithm for recombination detection. Bioinformatics 22, 3096–3098 (2006).
pubmed: 17110367 doi: 10.1093/bioinformatics/btl474
Dar, F. K., Paris, J. & Wilson, A. J. Serological studies on trypanosomiasis in East Africa. Ann. Trop. Med. Parasitol. 67, 319–329 (1973).
pubmed: 4761941 doi: 10.1080/00034983.1973.11686893
Liu, D., Albergante, L., Newman, T. J. & Horn, D. Faster growth with shorter antigens can explain a VSG hierarchy during African trypanosome infections: a feint attack by parasites. Sci. Rep. 8, 10922 (2018).
pubmed: 30026531 pmcid: 6053454 doi: 10.1038/s41598-018-29296-8
Berriman, M. et al. The architecture of variant surface glycoprotein gene expression sites in Trypanosoma brucei. Mol. Biochem. Parasitol. 122, 131–140 (2002).
pubmed: 12106867 doi: 10.1016/S0166-6851(02)00092-0
Becker, M. et al. Isolation of the repertoire of VSG expression site containing telomeres of Trypanosoma brucei 427 using transformation-associated recombination in yeast. Genome Res. 14, 2319–2329 (2004).
pubmed: 15520294 pmcid: 525691 doi: 10.1101/gr.2955304
Hertz-Fowler, C. et al. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE 3, e3527 (2008).
pubmed: 18953401 pmcid: 2567434 doi: 10.1371/journal.pone.0003527
Majiwa, P. A. O., Young, J. R., Englund, P. T., Shapiro, S. Z. & Williams, R. O. Two distinct forms of surface antigen gene rearrangement in Trypanosoma brucei. Nature 297, 514–516 (1982).
pubmed: 6896361 doi: 10.1038/297514a0 pmcid: 6896361
Young, J. R. et al. Analysis of genomic rearrangements associated with two variable antigen genes in Trypanosoma brucei. Nucleic Acids Res. 10, 803–819 (1982).
pubmed: 6278436 pmcid: 326204 doi: 10.1093/nar/10.3.803
Young, J. R., Miller, N., Williams, R. O. & Turner, M. J. Are there two classes of VSG gene in Trypanosoma brucei? Nature 306, 196–198 (1983).
pubmed: 6646202 doi: 10.1038/306196a0 pmcid: 6646202
Morrison, L. J., Marcello, L. & McCulloch, R. Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cell. Microbiol. 11, 1724–1734 (2009).
pubmed: 19751359 doi: 10.1111/j.1462-5822.2009.01383.x pmcid: 19751359
Boothroyd, C. E. et al. A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei. Nature 459, 278–281 (2009).
pubmed: 19369939 pmcid: 2688456 doi: 10.1038/nature07982
Glover, L., Alsford, S. & Horn, D. DNA break site at fragile subtelomeres determines probability and mechanism of antigenic variation in African trypanosomes. PLoS Pathog. 9, e1003260 (2013).
pubmed: 23555264 pmcid: 3610638 doi: 10.1371/journal.ppat.1003260
King, A. A., Shrestha, S., Harvill, E. T. & Bjørnstad, O. N. Evolution of acute infections and the invasion‐persistence trade‐off. Am. Nat. 173, 446–455 (2009).
pubmed: 19231966 pmcid: 4101379 doi: 10.1086/597217
Alizon, S., Hurford, A., Mideo, N. & van Baalen, M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245–259 (2009).
pubmed: 19196383 doi: 10.1111/j.1420-9101.2008.01658.x
Sekoni, V. O., Saror, D. I., Njoku, C. O., Kumi-Diaka, J. & Opaluwa, G. I. Comparative haematological changes following Trypanosoma vivax and T. congolense infections in Zebu bulls. Vet. Parasitol. 35, 11–19 (1990).
pubmed: 2343522 doi: 10.1016/0304-4017(90)90112-O
Mattioli, R. C., Faye, J. A. & Büscher, P. Susceptibility of N’Dama cattle to experimental challenge and cross-species superchallenges with bloodstream forms of Trypanosoma congolense and T. vivax. Vet. Parasitol. 86, 83–94 (1999).
pubmed: 10496692 doi: 10.1016/S0304-4017(99)00117-X
Gardiner, P. R., Assoku, R. K. G., Whitelaw, D. D. & Murray, M. Haemorrhagic lesions resulting from Trypanosoma vivax infection in ayrshire cattle. Vet. Parasitol. 31, 187–197 (1989).
pubmed: 2763442 doi: 10.1016/0304-4017(89)90069-1
Williams, D. J. L., Logan-Henfrey, L. L., Authié, E., Seely, C. & Mcodimba, F. Experimental infection with a haemorrhage‐causing Trypanosoma vivax in N’Dama and Boran cattle. Scand. J. Immunol. 36, 34–36 (1992).
doi: 10.1111/j.1365-3083.1992.tb01615.x
Rurangirwa, F. R., Musoke, A. J., Nantulya, V. M. & Tabel, H. Immune depression in bovine trypanosomiasis: effects of acute and chronic Trypanosoma congolense and chronic Trypanosoma vivax infections on antibody response to Brucella abortus vaccine. Parasite Immunol. 5, 267–276 (1983).
pubmed: 6408588 doi: 10.1111/j.1365-3024.1983.tb00743.x
Maikaje, D. B., Sannusi, A., Kyewalabye, E. K. & Saror, D. I. The course of experimental Trypanosoma vivax infection in Uda sheep. Vet. Parasitol. 38, 267–274 (1991).
pubmed: 1882495 doi: 10.1016/0304-4017(91)90139-M
Fidelis, O. L. Jr et al. Evaluation of clinical signs, parasitemia, hematologic and biochemical changes in cattle experimentally infected with Trypanosoma vivax. Braz. J. Vet. Parasitol. 2961, 69–81 (2016).
doi: 10.1590/S1984-29612016013
Parra-Gimenez, N. & Reyna-Bello, A. Parasitological, hematological, and immunological response of experimentally infected sheep with Venezuelan isolates of Trypanosoma evansi, Trypanosoma equiperdum, and Trypanosoma vivax. J. Parasitol. Res. 2019, 8528430 (2019).
pubmed: 30881699 pmcid: 6381555 doi: 10.1155/2019/8528430
Batista, J. S. et al. Infection by Trypanosoma vivax in goats and sheep in the Brazilian semiarid region: from acute disease outbreak to chronic cryptic infection. Vet. Parasitol. 165, 131–135 (2009).
pubmed: 19665308 doi: 10.1016/j.vetpar.2009.07.005
Barry, J. D. in African Trypanosomiasis in Vaccination Strategies of Tropical Diseases (ed. Liew, F. Y.) 217 (CRC Press, 1989).
Paiva, F. et al. Trypanosoma vivax em bovinos no Pantanal do Estado Do Mato Grosso Do Sul, Brasil: I—Acompanhamento Clínico. Rev. Bras. Parasitol. Veterinária 9, 135–141 (2000).
Silva, T. M. F. et al. Pathogenesis of reproductive failure induced by Trypanosoma vivax in experimentally infected pregnant ewes. Vet. Res. 44, 1–9 (2013).
pubmed: 23289625 pmcid: 3598889 doi: 10.1186/1297-9716-44-1
Hamilton, P. B., Adams, E. R., Malele, I. I. & Gibson, W. C. A novel, high-throughput technique for species identification reveals a new species of tsetse-transmitted trypanosome related to the Trypanosoma brucei subgenus, Trypanozoon. Infect. Genet. Evol. 8, 26–33 (2008).
pubmed: 17964224 doi: 10.1016/j.meegid.2007.09.003
Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821–829 (2008).
pubmed: 18349386 pmcid: 2336801 doi: 10.1101/gr.074492.107
Rogers, M. B. et al. Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res. 21, 2129–2142 (2011).
pubmed: 22038252 pmcid: 3227102 doi: 10.1101/gr.122945.111
Tihon, E., Imamura, H., Dujardin, J. C. & Van Den Abbeele, J. Evidence for viable and stable triploid Trypanosoma congolense parasites. Parasites Vectors 10, 1–8 (2017).
doi: 10.1186/s13071-017-2406-z
Emms, D. M. & Kelly, S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 16, 157 (2015).
pubmed: 26243257 pmcid: 4531804 doi: 10.1186/s13059-015-0721-2
Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).
pubmed: 17846036 pmcid: 17846036 doi: 10.1093/bioinformatics/btm404
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
pubmed: 22388286 pmcid: 3322381 doi: 10.1038/nmeth.1923
Ward, J. H. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236–244 (1963).
doi: 10.1080/01621459.1963.10500845
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Preprint at https://arxiv.org/abs/1303.3997 (2013).
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 2723002 pmcid: 2723002 doi: 10.1093/bioinformatics/btp352
Van der Auwera, G. A. et al. From fastQ data to high-confidence variant calls: The genome analysis toolkit best practices pipeline. Curr. Protoc. Bioinforma. 43, 1–33 (2013). 11.10.
doi: 10.1002/0471250953.bi1110s43
Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).
pubmed: 21653522 pmcid: 3137218 doi: 10.1093/bioinformatics/btr330
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
pubmed: 20525638 doi: 10.1093/sysbio/syq010
Lefort, V., Longueville, J.-E. & Gascuel, O. SMS: Smart Model Selection in PhyML. Mol. Biol. Evol. 34, 2422–2424 (2017).
pubmed: 28472384 pmcid: 5850602 doi: 10.1093/molbev/msx149
Brener, Z. Contribuição ao estudo da terapêutica experimental da doença de Chagas (Universidade Federal de Minas Gerais, Belo Horizonte, 1961).
Cuypers, B. et al. Multiplexed Spliced-Leader Sequencing: A high-throughput, selective method for RNA-seq in Trypanosomatids. Sci. Rep. 7, 1–11 (2017).
doi: 10.1038/s41598-017-03987-0
González-Andrade, P. et al. Diagnosis of trypanosomatid infections: Targeting the spliced leader RNA. J. Mol. Diagnostics 16, 400–404 (2014).
doi: 10.1016/j.jmoldx.2014.02.006
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 21572440 pmcid: 3571712 doi: 10.1038/nbt.1883
Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
pubmed: 27043002 pmcid: 27043002 doi: 10.1038/nbt.3519
Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).
pubmed: 2864565 pmcid: 2864565 doi: 10.1186/gb-2010-11-3-r25
Sistrom, M. et al. Comparative genomics reveals multiple genetic backgrounds of human pathogenicity in the Trypanosoma brucei complex. Genome Biol. Evol. 6, 2811–2819 (2014).
pubmed: 25287146 pmcid: 4224348 doi: 10.1093/gbe/evu222
Weir, W. et al. Population genomics reveals the origin and asexual evolution of human infective trypanosomes. Elife 5, e11473 (2016).
pubmed: 26809473 pmcid: 4739771 doi: 10.7554/eLife.11473
Arenas, M. & Posada, D. Coalescent simulation of intracodon recombination. Genetics 184, 429–437 (2010).
pubmed: 19933876 pmcid: 2828723 doi: 10.1534/genetics.109.109736
Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).
pubmed: 15034147 pmcid: 390337 doi: 10.1093/nar/gkh340
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278 pmcid: 2832824 doi: 10.1093/bioinformatics/btq033
O’Fallon, B. D. ACG: rapid inference of population history from recombining nucleotide sequences. BMC Bioinforma. 14, 40 (2013).
doi: 10.1186/1471-2105-14-40
Milne, I. et al. TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25, 126–127 (2009).
pubmed: 18984599 doi: 10.1093/bioinformatics/btn575

Auteurs

Sara Silva Pereira (S)

Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool, L3 5RF, UK.

Kayo J G de Almeida Castilho Neto (KJG)

Department of Veterinary Pathology, Faculty of Agrarian and Veterinary Sciences, São Paulo State University (UNESP), Jaboticabal, SP, Brazil.

Craig W Duffy (CW)

Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool, L3 5RF, UK.

Peter Richards (P)

Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool, L3 5RF, UK.

Harry Noyes (H)

Institute of Integrative Biology, University of Liverpool, Biosciences Building, Crown Street, Liverpool, L69 7ZB, UK.

Moses Ogugo (M)

Livestock Genetic Programme, International Livestock Research Institute, 30709 Naivasha Road, Nairobi, Kenya.

Marcos Rogério André (M)

Department of Veterinary Pathology, Faculty of Agrarian and Veterinary Sciences, São Paulo State University (UNESP), Jaboticabal, SP, Brazil.

Zakaria Bengaly (Z)

International Research Centre for Livestock Development in the Sub-humid Zone (CIRDES), No. 559, rue 5-31 angle, Avenue du Gouverneur Louveau, Bobo-Dioulasso, Burkina Faso.

Steve Kemp (S)

Livestock Genetic Programme, International Livestock Research Institute, 30709 Naivasha Road, Nairobi, Kenya.

Marta M G Teixeira (MMG)

Department of Parasitology, Institute of Biomedical Sciences, University of Sao Paulo, Avenue Professor Lineu Prestes, 1374 Cidade Universitaria, Sao Paulo, SP, 05508-000, Brazil.

Rosangela Z Machado (RZ)

Department of Veterinary Pathology, Faculty of Agrarian and Veterinary Sciences, São Paulo State University (UNESP), Jaboticabal, SP, Brazil.

Andrew P Jackson (AP)

Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, 146 Brownlow Hill, Liverpool, L3 5RF, UK. a.p.jackson@liv.ac.uk.

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