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Research Article

Global selective sweep of a highly inbred genome of the cattle parasite Neospora caninum

Asis Khan, Ayako Wendy Fujita, Nadine Randle, Javier Regidor-Cerrillo, Jahangheer S. Shaik, Kui Shen, Andrew J. Oler, Mariam Quinones, Sophia M. Latham, Bartholomew D. Akanmori, Sarah Cleaveland, Elisabeth A. Innes, Una Ryan, View ORCID ProfileJan Šlapeta, Gereon Schares, Luis M. Ortega-Mora, Jitender P. Dubey, Jonathan M. Wastling, and Michael E. Grigg
PNAS November 5, 2019 116 (45) 22764-22773; first published October 21, 2019; https://doi.org/10.1073/pnas.1913531116
Asis Khan
aMolecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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Ayako Wendy Fujita
aMolecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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Nadine Randle
bInstitute of Infection and Global Health and School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, L69 3BX Liverpool, United Kingdom;
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Javier Regidor-Cerrillo
cSALUVET (Salud Verinaria y Zoonosis), Animal Health Department, Complutense University of Madrid, 28040 Madrid, Spain;
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Jahangheer S. Shaik
aMolecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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Kui Shen
dBioinformatics and Computational Biosciences Branch, Office of Cyber Infrastructure and Computational Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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Andrew J. Oler
dBioinformatics and Computational Biosciences Branch, Office of Cyber Infrastructure and Computational Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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Mariam Quinones
dBioinformatics and Computational Biosciences Branch, Office of Cyber Infrastructure and Computational Biology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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Sophia M. Latham
eDepartment of Epidemiology & Population Health, Institute of Infection and Global Health, University of Liverpool Veterinary School, L69 3GH Liverpool, United Kingdom;
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Bartholomew D. Akanmori
fImmunization and Vaccines Development Programme, Family & Reproductive Health Cluster, World Health Organization (WHO) African Region, BP 2465 Brazzaville, Congo;
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Sarah Cleaveland
gInstitute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, G12 8QQ Glasgow, Scotland;
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Elisabeth A. Innes
hMoredun Research Institute, Pentlands Science Park, EH26 0PZ Midlothian, Scotland;
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Una Ryan
iCollege of Science, Health, Education and Engineering, Murdoch University, Murdoch, WA 6150, Australia;
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Jan Šlapeta
jSydney School of Veterinary Science, Faculty of Science, The University of Sydney, Sydney, NSW 2006, Australia;
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  • ORCID record for Jan Šlapeta
Gereon Schares
kInstitute of Epidemiology, Friedrich-Loeffler-Institut/Federal Research Institute for Animal Health, D-17498 Greifswald–Insel Riems, Germany;
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Luis M. Ortega-Mora
cSALUVET (Salud Verinaria y Zoonosis), Animal Health Department, Complutense University of Madrid, 28040 Madrid, Spain;
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Jitender P. Dubey
lAnimal Parasitic Disease Laboratory, Animal and National Resources Institute, Agricultural Research Service, US Department of Agriculture, Beltsville, MD 20705;
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  • For correspondence: jitender.dubey@usda.gov griggm@niaid.nih.gov
Jonathan M. Wastling
bInstitute of Infection and Global Health and School of Veterinary Science, Faculty of Health and Life Sciences, University of Liverpool, L69 3BX Liverpool, United Kingdom;
mFaculty of Natural Sciences, University of Keele, ST5 5BG Keele, Staffordshire, United Kingdom
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Michael E. Grigg
aMolecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892;
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  • For correspondence: jitender.dubey@usda.gov griggm@niaid.nih.gov
  1. Contributed by Jitender P. Dubey, September 19, 2019 (sent for review August 6, 2019; reviewed by Damer P. Blake and Joseph Heitman)

This article has a Correction. Please see:

  • Correction for Khan et al., Global selective sweep of a highly inbred genome of the cattle parasite Neospora caninum - December 09, 2019
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Significance

The parasite Neospora caninum has a worldwide distribution and causes fetal loss in livestock. It is transmitted in cows vertically (from mother to fetus), and in some herds nearly all cattle are infected. We genotyped Neospora strains isolated from an array of infected hosts (dogs, cattle, deer, horse, rhinoceros) and observed a single, highly inbred genome that has swept globally. At first glance, data support vertical transmission as a primary mode for the expansion of the parasite genome; however, genome-level analyses identified large introgression blocks of a distinct ancestry that has recombined into the genome, consistent with a unisexual expansion model. The successful genome appears to have piggy-backed on the expansion of European cattle breeds that have been exported globally.

Abstract

Neospora caninum, a cyst-forming apicomplexan parasite, is a leading cause of neuromuscular diseases in dogs as well as fetal abortion in cattle worldwide. The importance of the domestic and sylvatic life cycles of Neospora, and the role of vertical transmission in the expansion and transmission of infection in cattle, is not sufficiently understood. To elucidate the population genomics of Neospora, we genotyped 50 isolates collected worldwide from a wide range of hosts using 19 linked and unlinked genetic markers. Phylogenetic analysis and genetic distance indices resolved a single genotype of N. caninum. Whole-genome sequencing of 7 isolates from 2 different continents identified high linkage disequilibrium, significant structural variation, but only limited polymorphism genome-wide, with only 5,766 biallelic single nucleotide polymorphisms (SNPs) total. Greater than half of these SNPs (∼3,000) clustered into 6 distinct haploblocks and each block possessed limited allelic diversity (with only 4 to 6 haplotypes resolved at each cluster). Importantly, the alleles at each haploblock had independently segregated across the strains sequenced, supporting a unisexual expansion model that is mosaic at 6 genomic blocks. Integrating seroprevalence data from African cattle, our data support a global selective sweep of a highly inbred livestock pathogen that originated within European dairy stock and expanded transcontinentally via unisexual mating and vertical transmission very recently, likely the result of human activities, including recurrent migration, domestication, and breed development of bovid and canid hosts within similar proximities.

  • Neospora caninum
  • protozoan
  • population genetics
  • genome
  • unisexual

Footnotes

  • ↵1A.W.F. and N.R. contributed equally to this work.

  • ↵2Present address: Department of Medicine, University of Pittsburgh Medical Center, Pittsburgh, PA 15213.

  • ↵3To whom correspondence may be addressed. Email: jitender.dubey{at}usda.gov or griggm{at}niaid.nih.gov.
  • Author contributions: A.W.F., S.M.L., J.P.D., J.M.W., and M.E.G. designed research; A.K., A.W.F., N.R., and S.M.L. performed research; A.K., J.R.-C., J.S.S., K.S., A.J.O., M.Q., S.M.L., B.D.A., S.C., E.A.I., U.R., J.Š., G.S., L.M.O.-M., J.P.D., J.M.W., and M.E.G. contributed new reagents/analytic tools; A.K., A.W.F., N.R., and M.E.G. analyzed data; and A.K., J.P.D., J.M.W., and M.E.G. wrote the paper.

  • Reviewers: D.P.B., Royal Veterinary College; and J.H., Duke University.

  • The authors declare no competing interest.

  • Data deposition: Sequence reads from the Illumina sequences were deposited in the NCBI Sequence Read Archive, https://www.ncbi.nlm.nih.gov, under BioProject number PRJNA534109 (accession nos. SRX5723126 [NC1], SRX5723132 [NC2], SRX5723128 [NC3], SRX5723130 [NC9], SRX5723131 [NcSP1], SRX5723129 [NcSP7], and SRX5723127 [NhOregon]).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1913531116/-/DCSupplemental.

Published under the PNAS license.

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Global selective sweep of a highly inbred genome of the cattle parasite Neospora caninum
Asis Khan, Ayako Wendy Fujita, Nadine Randle, Javier Regidor-Cerrillo, Jahangheer S. Shaik, Kui Shen, Andrew J. Oler, Mariam Quinones, Sophia M. Latham, Bartholomew D. Akanmori, Sarah Cleaveland, Elisabeth A. Innes, Una Ryan, Jan Šlapeta, Gereon Schares, Luis M. Ortega-Mora, Jitender P. Dubey, Jonathan M. Wastling, Michael E. Grigg
Proceedings of the National Academy of Sciences Nov 2019, 116 (45) 22764-22773; DOI: 10.1073/pnas.1913531116

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Global selective sweep of a highly inbred genome of the cattle parasite Neospora caninum
Asis Khan, Ayako Wendy Fujita, Nadine Randle, Javier Regidor-Cerrillo, Jahangheer S. Shaik, Kui Shen, Andrew J. Oler, Mariam Quinones, Sophia M. Latham, Bartholomew D. Akanmori, Sarah Cleaveland, Elisabeth A. Innes, Una Ryan, Jan Šlapeta, Gereon Schares, Luis M. Ortega-Mora, Jitender P. Dubey, Jonathan M. Wastling, Michael E. Grigg
Proceedings of the National Academy of Sciences Nov 2019, 116 (45) 22764-22773; DOI: 10.1073/pnas.1913531116
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