Genetic diversity of primate strongylid nematodes: Do sympatric nonhuman primates and humans share their strongylid worms?

. 2019 Nov ; 28 (21) : 4786-4797. [epub] 20191028

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31573713

The close phylogenetic relationship between humans and nonhuman primates (NHPs) can result in a high potential for pathogen exchange. In recent decades, NHP and human interactions have become more frequent due to increasing habitat encroachment and ecotourism. Strongylid communities, which include members of several genera, are typically found in NHPs. Using optimized high-throughput sequencing for strain-level identification of primate strongylids, we studied the structure of strongylid communities in NHPs and humans co-habiting a tropical forest ecosystem in the Central African Republic. General taxonomic assignment of 85 ITS-2 haplotypes indicated that the studied primates harbour at least nine genera of strongylid nematodes, with Oesophagostomum and Necator being the most prevalent. We detected both host-specific and shared strongylid haplotypes. Skin-penetrating Necator gorillaehaplotypes were shared between humans and gorillas but Necator americanus were much more restricted to humans. Strongylid communities of local hunter-gatherers employed as trackers were more similar to those of gorillas compared to their relatives, who spent more time in villages. This was due to lower abundance of human-origin N. americanus in both gorillas and trackers. Habituated gorillas or those under habituation did not show larger overlap of strongylids with humans compared to unhabituated. We concluded that the occurrence of the human-specific strongylids in gorillas does not increase with direct contact between gorillas and humans due to the habituation. Overall, our results indicate that the degree of habitat sharing between hosts, together with mode of parasite transmission, are important factors for parasite spillover among primates.

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Aivelo, T., & Medlar, A. (2017). Opportunities and challenges in metabarcoding approaches for helminth community identification in wild mammals. Parasitology, 145, 1-14. https://doi.org/10.1017/S0031182017000610

Anderson, R. C. (2000). Nematode parasites of vertebrates. Their development and transmission. Wallingford, UK: CABI Publishing.

Antonovics, J. (2017). Transmission dynamics: Critical questions and challenges. Philosophical Transactions of the Royal Society B, 372, 20160087. https://doi.org/10.1098/rstb.2016.0087

Avramenko, R. W., Redman, E. M., Lewis, R., Yazwinski, T. A., Wasmuth, J. D., & Gilleard, J. S. (2015). Exploring the gastrointestinal “nemabiome”: Deep amplicon sequencing to quantify the species composition of parasitic nematode communities. PLoS ONE, 10(12), e0143559. https://doi.org/10.1371/journal.pone.0143559

Bird, B. H., & Mazet, J. A. K. (2018). Detection of emerging zoonotic pathogens: An integrated one health approach. Annual Review of Animal Biosciences, 6(1), 121-139. https://doi.org/10.1146/annurev-animal-030117-014628

Blom, A., Almaši, A., Heitkönig, I. M. A., Kpanou, J. B., & Prins, H. H. T. (2001). A survey of the apes in the Dzanga-Ndoki National Park, Central African Republic: A comparison between the census and survey methods of estimating the gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes) nest group density. African Journal of Ecology, 39, 98-105. https://doi.org/10.1046/j.0141-6707.2000.00280.x

Bowden, S. E., & Drake, J. M. (2013). Ecology of multi-host pathogens of animals. Nature Education Knowledge, 4(8), 5.

Brooker, S., Bethony, J., & Hotez, P. J. (2004). Human hookworm infection in the 21st century. Advances in Parasitology, 58, 197-288. https://doi.org/10.1016/S0065-308X(04)58004-1

Callahan, B. J., Mcmurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J., & Holmes, S. P. (2015). DADA2: High resolution sample inference from amplicon data. bioRxiv, (August 2015), 0-14. https://doi.org/10.1101/024034

Calvignac-Spencer, S., Leendertz, S. A. J., Gillespie, T. R., & Leendertz, F. H. (2012). Wild great apes as sentinels and sources of infectious disease. Clinical Microbiology and Infection, 18(6), 521-527. https://doi.org/10.1111/j.1469-0691.2012.03816.x

Červená, B., Brant, S. V., Fairet, E., Shirley, M. H., Petrželková, K. J., & Modrý, D. (2016). Schistosoma mansoni in Gabon: Emerging or ignored? American Journal of Tropical Medicine and Hygiene, 95(4), 849-851. https://doi.org/10.4269/ajtmh.16-0446

Cibot, M., Guillot, J., Lafosse, S., Bon, C., Seguya, A., & Krief, S. (2015). Nodular worm infections in wild non-human primates and humans living in the Sebitoli Area (Kibale National Park, Uganda): Do high spatial proximity favor zoonotic transmission? PLOS Neglected Tropical Diseases, 9(10), e00. https://doi.org/10.1371/journal.pntd.0004133

Cleaveland, S., Laurenson, M. K., & Taylor, L. H. (2001). Diseases of humans and their domestic mammals: Pathogen characteristics, host range and the risk of emergence. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 356(1411), 991-999. https://doi.org/10.1098/rstb.2001.0889

Combes, C. (2001). Parasitism: The ecology and evolution of intimate interactions. Chicago, IL and London, UK: University of Chicago Press.

Devreese, L. (2011). Many hands make light work. Foraging strategy of agile mangabeys (Cercocebus agilis) exhibiting a permanent large grouping pattern at Bai Hokou, Central African Republic. Antwerp, Belgium: University of Antwerp.

Doležalová, J., Vallo, P., Petrželková, K. J., Foitová, I., Nurcahyo, W., Mudakikwa, A., … Modrý, D. (2015). Molecular phylogeny of anoplocephalid tapeworms (Cestoda: Anoplocephalidae) infecting humans and non-human primates. Parasitology, 142, 1278-1289. https://doi.org/10.1017/S003118201500058X

Dounias, E., & Froment, A. (2006). When forest-based hunter-gatherers become sedentary: Consequences for diet and health. Unasylva, 57(224), 26-33.

Dunay, E., Apakupakul, K., Leard, S., Palmer, J. L., & Deem, S. L. (2018). Pathogen transmission from humans to great apes is a growing threat to primate conservation. EcoHealth, 15, 148-162. https://doi.org/10.1007/s10393-017-1306-1

Gasser, R. B., de Gruijter, J. M., & Polderman, A. M. (2006). Insights into the epidemiology and genetic make-up of Oesophagostomum bifurcum from human and non-human primates using molecular tools. Parasitology, 132, 453-460.

Ghai, R. R., Chapman, C. A., Omeja, P. A., Davies, T. J., & Goldberg, T. L. (2014). Nodule worm infection in humans and wild primates in Uganda: Cryptic species in a newly identified region of human transmission. PLOS Neglected Tropical Diseases, 8(1), e264. https://doi.org/10.1371/journal.pntd.0002641

Ghai, R. R., Simons, N. D., Chapman, C. A., Omeja, P. A., Davies, T. J., Ting, N., & Goldberg, T. L. (2014). Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLOS Neglected Tropical Diseases, 8(10), e3256. https://doi.org/10.1371/journal.pntd.0003256

Hasegawa, H., Modrý, D., Kitagawa, M., Shutt, K. A., Todd, A., Kalousová, B., … Petrželková, K. J. (2014). Humans and great apes cohabiting the forest ecosystem in Central African Republic harbour the same hookworms. PLOS Neglected Tropical Diseases, 8, e2715. https://doi.org/10.1371/journal.pntd.0002715

Hasegawa, H., Shigyo, M., Yanai, Y., McLennan, M. R., Fujita, S., Makouloutou, P., … Huffman, M. A. (2017). Molecular features of hookworm larvae (Necator spp.) raised by coproculture from Ugandan chimpanzees and Gabonese gorillas and humans. Parasitology International, 66(2), 12-15. https://doi.org/10.1016/j.parint.2016.11.003

Hawdon, M. J., Li, T., Zhan, B., & Blouin, M. S. (2001). Genetic structure of populations of the human hookworm, Necator americanus, in China. Molecular Ecology, 10, 1433-1437. https://doi.org/10.1046/j.1365-294X.2001.01296.x

Hu, M., Chilton, N. B., & Gasser, R. B. (2002). The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). International Journal for Parasitology, 32(2), 145-158. https://doi.org/10.1016/S0020-7519(01)00316-2

Jiang, H., Lei, R., Ding, S.-W., & Zhu, S. (2014). Skewer: A fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinformatics, 15(1), 182. https://doi.org/10.1186/1471-2105-15-182

Kalousová, B., Hasegawa, H., Petrželková, K. J., Sakamaki, T., Kooriyma, T., & Modrý, D. (2016). Adult hookworms (Necator spp.) collected from researchers working with wild western lowland gorillas. Parasites and Vectors, 9(1), 75. https://doi.org/10.1186/s13071-016-1357-0

Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772-780. https://doi.org/10.1093/molbev/mst010

Krief, S., Jamart, A., Mahé, S., Leendertz, F. H., Mätz-Rensing, K., Crespeau, F., … Guillot, J. (2008). Clinical and pathologic manifestation of oesophagostomosis in African great apes: Does self-medication in wild apes influence disease progression? Journal of Medical Primatology, 37(4), 188-195. https://doi.org/10.1111/j.1600-0684.2008.00285.x

Lichtenfels, J. R., Kharchenko, V. A., & Dvojnos, G. M. (2008). Illustrated identification keys to strongylid parasites (strongylidae: Nematoda) of horses, zebras and asses (Equidae). Veterinary Parasitology, 156, 4-161. https://doi.org/10.1016/j.vetpar.2008.04.026

Lockwood, C. A., Kimbel, W. H., & Lynch, J. M. (2004). Morphometrics and hominoid phylogeny: Support for a chimpanzee-human clade and differentiation among great ape subspecies. PNAS, 101(13), 4356-4360. https://doi.org/10.1073/pnas.0306235101

Lott, M. J., Hose, G. C., & Power, M. L. (2015). Parasitic nematode communities of the red kangaroo, Macropus rufus: Richness and structuring in captive systems. Parasitology Research, 114(8), 2925-2932. https://doi.org/10.1007/s00436-015-4494-z

Macintosh, A. J. J., Jacobs, A., Garcia, C., Shimizu, K., Mouri, K., Huffman, M. A., & Hernandez, A. D. (2012). Monkeys in the middle: Parasite transmission through the social network of a wild primate. PLoS ONE, 7(12), e51144. https://doi.org/10.1371/journal.pone.0051144

Mapua, M. I., Qablan, M. A., Pomajbíková, K., Petrželková, K. J., Hůzová, Z., Rádrová, J., … Modrý, D. (2015). Ecology of malaria infections in western lowland gorillas inhabiting Dzanga Sangha Protected Areas, Central African Republic. Parasitology, 142, 890-900. https://doi.org/10.1017/S0031182015000086

McKenna, M. L., McAtee, S., Bryan, P. E., Jeun, R., Ward, T., Kraus, J., … Mejia, R. (2017). Human intestinal parasite burden and poor sanitation in rural Alabama. American Journal of Tropical Medicine and Hygiene, 97(5), 1623-1628. https://doi.org/10.4269/ajtmh.17-0396

McLean, E. R., Kinsella, J. M., Chiyo, P., Obanda, V., Moss, C., & Archie, E. A. (2012). Genetic identification of five strongyle nematode parasites in wild african elephants (Loxodonta africana). Journal of Wildlife Diseases, 48(3), 707-716. https://doi.org/10.7589/0090-3558-48.3.707

McMurdie, P. J., & Holmes, S. (2014). Waste not, want not: Why rarefying microbiome data is inadmissible. PLOS Computational Biology, 10(4), e1003531. https://doi.org/10.1371/journal.pcbi.1003531

Mittermeier, R. A., Rylands, A. B., Wilson, D. E., & Nash, S. D. (2012). Handbook of the Mammals of the World (Vol. 3). Primates. Barcelona:Lynx Edicions.

Morens, D. M., & Fauci, A. S. (2013). Emerging infectious diseases: Threats to human Health and global stability. PLoS Path, 9(7), 7-9. https://doi.org/10.1371/journal.ppat.1003467

Morse, S. S., Mazet, J. A. K., Woolhouse, M., Parrish, C. R., Carroll, D., Karesh, W. B., … Daszak, P. (2012). Prediction and prevention of the next pandemic zoonosis. The Lancet, 380(9857), 1956-1965. https://doi.org/10.1016/S0140-6736(12)61684-5

Nakano, T., Okamoto, M., Ikeda, Y., & Hasegawa, H. (2006). Mitochondrial cytochrome c oxidase subunit 1 gene and nuclear rDNA regions of Enterobius vermicularis parasitic in captive chimpanzees with special reference to its relationship with pinworms in humans. Parasitology Research, 100(1), 51-57. https://doi.org/10.1007/s00436-006-0238-4

Narat, V., Guillot, J., Pennec, F., Lafosse, S., Grüner, A. C., Simmen, B., … Krief, S. (2015). Intestinal helminths of wild bonobos in forest-savanna mosaic: Risk assessment of cross-species transmission with local people in the Democratic Republic of the Congo. EcoHealth, 12(4), 621-633. https://doi.org/10.1007/s10393-015-1058-8

Negrey, J. D., Reddy, R. B., Scully, E. J., Phillips-Garcia, S., Owens, L. A., Langergraber, K. E., … Goldberg, T. L. (2019). Simultaneous outbreaks of respiratory disease in wild chimpanzees caused by distinct viruses of human origin. Emerging Microbes and Infections, 8, 139-149. https://doi.org/10.1080/22221751.2018.1563456

Oksanen, A. J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., Hara, R. B. O., … Wagner, H. (2014). vegan: Community Ecology Package. R Package Version 2.2-0. http://CRAN.Rproject.org/package=veganISBN 0-387-95457-0

Ota, N., Hasegawa, H., McLennan, M. R., Kooriyama, T., Sato, H., Pebsworth, P. A., & Huffman, M. A. (2015). Molecular identification of Oesophagostomum spp. from “village” chimpanzees in Uganda and their phylogenetic relationship with those of other primates. Royal Society Open. Science, 2(11), 150471. https://doi.org/10.1098/rsos.150471

Pafčo, B., Benavides, J. A., Pšenková-Profousová, I., Modrý, D., Červená, B., Shutt, K. A., … Petrželková, K. J. (2017). Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? Parasitology Research, 116(12), https://doi.org/10.1007/s00436-017-5667-8

Pafčo, B., Čížková, D., Kreisinger, J., Hasegawa, H., Vallo, P., Shutt, K., … Modrý, D. (2018). Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Scientific Reports, 8, 5933. https://doi.org/10.1038/s41598-018-24126-3

Pedersen, A. B., Altizer, S., Poss, M., Cunningham, A. A., & Nunn, C. L. (2005). Patterns of host specificity and transmission among parasites of wild primates. International Journal for Parasitology, 35(6), 647-657. https://doi.org/10.1016/j.ijpara.2005.01.005

Poulin, R., & George-Nascimento, M. (2007). The scaling of total parasite biomass with host body mass. International Journal for Parasitology, 37, 359-364. https://doi.org/10.1016/j.ijpara.2006.11.009

Poulin, R., & Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology, 24(1), 24-28. https://doi.org/10.1016/j.pt.2007.10.002

Remis, M. J., & Robinson, C. A. J. (2017). Nonhuman primates and “others” in the Dzanga Sangha Reserve: The role of anthropology and multispecies approaches in ethnoprimatology. In K. Dore, E. Riley, & A. Fuentes (Eds.), Ethnoprimatology: A practical guide to research at the human-nonhuman primate interface (pp. 190-205). Cambridge, UK: Cambridge University Press.

Robinson, C. A. J., & Remis, M. J. (2015). Entangled realms: Hunters and hunted in the Dzanga-Sangha Dense Forest Reserve (APDS). Central African Republic. Anthropological Quarterly, 87(3), 613-633. https://doi.org/10.1353/anq.2014.0036

Roeber, F., Jex, A. R., & Gasser, R. B. (2013). Next-generation molecular-diagnosticctools for gastrointestinal nematodes of livestock, with an emphasiscon small ruminants. A turning point? Advances in parasitology, 83, 267-333. https://doi.org/10.1016/B978-0-12-407705-8.00004-5

Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahé, F. (2016). VSEARCH: A versatile open source tool for metagenomics. PeerJ, 4, e2584. https://doi.org/10.7717/peerj.2584

Rothman, J., & Bowman, D. D. (2003). A review of the endoparasites of mountain gorillas. In D. D. Bowman (Ed.), Companion and exotic animal parasitology. New York, NY: International Veterinary Information Service. Retrieved from www.ivis.org

Rwego, I. B., Isabirye-Basuta, G., Gillespie, T. R., & Goldberg, T. L. (2008). Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conservation Biology, 22(6), 1600-1607. https://doi.org/10.1111/j.1523-1739.2008.01018.x

Sak, B., Petrzelkova, K. J., Kvetonova, D., Mynarova, A., Shutt, K. A., Pomajbikova, K., … Kvac, M. (2013). Long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. PLoS ONE, 8(8), https://doi.org/10.1371/journal.pone.0071840

Schindler, R., de Gruijter, J. M., Polderman, M., & Gasser, R. B. (2005). Definition of genetic markers in nuclear ribosomal DNA for a neglected parasite of primates, Ternidens deminutus (Nematoda: Strongylida) - Diagnostic and epidemiological implications. Parasitology, 131, 539-546. https://doi.org/10.1017/S0031182005007936

Shutt, K., Heistermann, M., Kasim, A., Todd, A., Kalousova, B., Profosouva, I., … Setchell, J. M. (2014). Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: Implications for conservation management. Biological Conservation, 172, 72-79. https://doi.org/10.1016/j.biocon.2014.02.014

Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312-1313. https://doi.org/10.1093/bioinformatics/btu033

Tanaka, R., Hino, A., Tsai, I. J., Palomares-Rius, J. E., Yoshida, A., Ogura, Y., … Kikuchi, T. (2014). Assessment of helminth biodiversity in wild rats using 18S rDNA based metagenomics. PLoS ONE, 9(10), e110769. https://doi.org/10.1371/journal.pone.0110769

Taylor, L. H., Latham, S. M., & Woolhouse, M. E. (2001). Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 356(1411), 983-989. https://doi.org/10.1098/rstb.2001.0888

Van Wyk, J. A., Cabaret, J., & Michael, L. M. (2004). Morphological identification of nematode larvae of small ruminants and cattle simplified. Veterinary Parasitology, 119(4), 277-306. https://doi.org/10.1016/j.vetpar.2003.11.012

Verweij, J. J., Pit, D. S., van Lieshout, L., Baeta, S. M., Dery, G. D., Gasser, R. B., & Polderman, A. M. (2001). Determining the prevalence of Oesophagostomum bifurcum and Necator americanus infections using specific PCR amplification of DNA from faecal samples. Tropical Medicine & International Health, 6(9), 726-31.

Vlčková, K., Kreisinger, J., Pafčo, B., Čížková, D., Tagg, N., Hehl, A. B., & Modrý, D. (2018). Diversity of Entamoeba spp. in African great apes and humans: An insight from Illumina MiSeq high-throughput sequencing. International Journal for Parasitology, 48, 519-530. https://doi.org/10.1016/j.ijpara.2017.11.008

Wang, L.-F., & Crameri, G. (2014). Emerging zoonotic viral diseases. Revue Scientifique Et Technique De L'office International Des Epizooties, 33(2), 569-581. https://doi.org/10.20506/rst.33.2.2311

Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naıve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267. https://doi.org/10.1128/AEM.00062-07

Wang, Y., Naumann, U., Wright, S. T., & Warton, D. I. (2012). Mvabund- an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution, 3(3), 471-474. https://doi.org/10.1111/j.2041-210X.2012.00190.x

Webster, J. P., Borlase, A., & Rudge, J. W. (2017). Who acquires infection from whom and how? Disentangling multi-host and multi-mode transmission dynamics in the “elimination” era. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160091. https://doi.org/10.1098/rstb.2016.0091

Woolhouse, M. E. J., Taylor, L. H., & Haydon, D. T. (2001). Population biology of multihost pathogens. Science, 292(5519), 1109-1112. https://doi.org/10.1126/science.1059026

Zhang, J., Kobert, K., Flouri, T., & Stamatakis, A. (2014). PEAR: A fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics, 30(5), 614-620. https://doi.org/10.1093/bioinformatics/btt593

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