Hostname: page-component-848d4c4894-nmvwc Total loading time: 0 Render date: 2024-07-01T15:55:23.019Z Has data issue: false hasContentIssue false
  • English
  • Français

Historical contingency, geography and anthropogenic patterns of exposure drive the evolution of host switching in the Blastocystis species-complex

Published online by Cambridge University Press:  29 March 2021

Justin J. S. Wilcox Open the ORCID record for Justin J. S. Wilcox [Opens in a new window] ,
John J. Lopez-Cotto  and
Hope Hollocher
Justin J. S. Wilcox*
Affiliation:
Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, Indiana 46556, USA Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates
John J. Lopez-Cotto
Affiliation:
Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, Indiana 46556, USA
Hope Hollocher
Affiliation:
Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, Indiana 46556, USA
*
Author for correspondence: Justin J. S. Wilcox, E-mail: jw5478@nyu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasites have the power to impose significant regulatory pressures on host populations, making evolutionary patterns of host switching by parasites salient to a range of contemporary ecological issues. However, relatively little is known about the colonization of new hosts by parasitic, commensal and mutualistic eukaryotes of metazoans. As ubiquitous symbionts of coelomate animals, Blastocystis spp. represent excellent candidate organisms for the study of evolutionary patterns of host switching by protists. Here, we apply a big-data phylogenetic approach using archival sequence data to assess the relative roles of several host-associated traits in shaping the evolutionary history of the Blastocystis species-complex within an ecological framework. Patterns of host usage were principally determined by geographic location and shared environments of hosts, suggesting that weight of exposure (i.e. propagule pressure) represents the primary force for colonization of new hosts within the Blastocystis species-complex. While Blastocystis lineages showed a propensity to recolonize the same host taxa, these taxa were often evolutionarily unrelated, suggesting that historical contingency and retention of previous adaptions by the parasite were more important to host switching than host phylogeny. Ultimately, our findings highlight the ability of ecological theory (i.e. ‘ecological fitting’) to explain host switching and host specificity within the Blastocystis species-complex.

Keywords

Blastocystisecological fittinghost specificityhost-switchingnichezoonosiszooanthroponosis
Type
Research Article
Information
Parasitology , Volume 148 , Issue 8 , July 2021 , pp. 985 - 993
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agosta, SJ, Janz, N and Brooks, DR (2010) How specialists can be generalists: resolving the” parasite paradox” and implications for emerging infectious disease. Zoologia (Curitiba) 27, 151–162.CrossRefGoogle Scholar
Alfellani, MA, Taner-Mulla, D, Jacob, AS, Imeede, CA, Yoshikawa, H, Stensvold, CR and Clark, CG (2013) Genetic diversity of Blastocystis in livestock and zoo animals. Protist 164, 497–509.CrossRefGoogle ScholarPubMed
Araujo, SB, Braga, MP, Brooks, DR, Agosta, SJ, Hoberg, EP, von Hartenthal, FW and Boeger, WA (2015) Understanding host-switching by ecological fitting. PLoS One 10, e0139225.CrossRefGoogle ScholarPubMed
Arisue, N, Hashimoto, T and Yoshikawa, H (2003) Sequence heterogeneity of the small subunit ribosomal RNA genes among Blastocystis isolates. Parasitology 126, 1–9.CrossRefGoogle ScholarPubMed
Auld, SK and Tinsley, MC (2015) The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms. Heredity 114, 125.CrossRefGoogle ScholarPubMed
Benson, DA, Cavanaugh, M, Clark, K, Karsch-Mizrachi, I, Lipman, DJ, Ostell, J and Sayers, EW (2012) GenBank. Nucleic Acids Research 41, D36–D42.CrossRefGoogle ScholarPubMed
Brockhurst, MA, Chapman, T, King, KC, Mank, JE, Paterson, S and Hurst, GD (2014) Running with the Red Queen: the role of biotic conflicts in evolution. Proceedings of the Royal Society of London B: Biological Sciences 281, 20141382.Google Scholar
Brucker, RM and Bordenstein, SR (2012) Speciation by symbiosis. Trends in ecology and evolution 27, 443–451.CrossRefGoogle ScholarPubMed
Cian, A, El Safadi, D, Osman, M, Moriniere, R, Gantois, N, Benamrouz-Vanneste, S, Delgado-Viscogliosi, P, Guyot, K, Li, LL, Monchy, S and Noël, C (2017) Molecular epidemiology of Blastocystis sp. in various animal groups from two French zoos and evaluation of potential zoonotic risk. PLoS One 12, e0169659.CrossRefGoogle ScholarPubMed
Clark, CG (1997) Extensive genetic diversity in Blastocystis hominis. Molecular and Biochemical Parasitology 87, 79–83.CrossRefGoogle ScholarPubMed
Clarke, A and Rothery, P (2008) Scaling of body temperature in mammals and birds. Functional Ecology 22, 58–67.Google Scholar
Combes, C and Théron, A (2000) Metazoan parasites and resource heterogeneity: constraints and benefits. International Journal for Parasitology 30, 299–304.CrossRefGoogle ScholarPubMed
Cooper, N, Griffin, R, Franz, M, Omotayo, M and Nunn, CL (2012) Phylogenetic host specificity and understanding parasite sharing in primates. Ecology Letters 15, 1370–1377.CrossRefGoogle ScholarPubMed
Crompton, DWT (1987) Host diet as a determinant of parasite growth, reproduction and survival. Mammal Review 17, 117–126.CrossRefGoogle Scholar
Dallas, T and Presley, SJ (2014) Relative importance of host environment, transmission potential and host phylogeny to the structure of parasite metacommunities. Oikos 123, 866–874.CrossRefGoogle Scholar
David, LA, Maurice, CF, Carmody, RN, Gootenberg, DB, Button, JE, Wolfe, BE, Ling, AV, Devlin, AS, Varma, Y, Fischbach, MA and Biddinger, SB (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559.CrossRefGoogle ScholarPubMed
Denoeud, F, Roussel, M, Noel, B, Wawrzyniak, I, Da Silva, C, Diogon, M, Viscogliosi, E, Brochier-Armanet, C, Couloux, A, Poulain, J and Segurens, B (2011) Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biology 12, R29.CrossRefGoogle ScholarPubMed
Desneux, N, Blahnik, R, Delebecque, CJ and Heimpel, GE (2012) Host phylogeny and specialisation in parasitoids. Ecology Letters 15, 453–460.CrossRefGoogle ScholarPubMed
Eddy, SR (1998) Profile hidden Markov models. Bioinformatics (Oxford, England) 14, 755–763.CrossRefGoogle ScholarPubMed
Edgar, RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England) 26, 2460–2461.CrossRefGoogle ScholarPubMed
Esch, KJ and Petersen, CA (2013) Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clinical Microbiology Reviews 26, 58–85.CrossRefGoogle ScholarPubMed
Escobar, LE and Craft, ME (2016) Advances and limitations of disease biogeography using ecological niche modeling. Frontiers in Microbiology 7, 1174.CrossRefGoogle ScholarPubMed
Fayer, R, Elsasser, T, Gould, R, Solano, G, Urban, J and Santin, M (2014) Blastocystis tropism in the pig intestine. Parasitology Research 113, 1465–1472.CrossRefGoogle ScholarPubMed
Fodor, E (2011) Ecological niche of plant pathogens. Annals of Forest Research 54, 3.Google Scholar
Franco, JR, Simarro, PP, Diarra, A and Jannin, JG (2014) Epidemiology of human African trypanosomiasis. Clinical Epidemiology 6, 257.Google ScholarPubMed
Gilbert, D (2003) Sequence file format conversion with command-line readseq. Current Protocols in Bioinformatics 00, A–1E.CrossRefGoogle Scholar
Goslee, SC and Urban, DL (2007) The Ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22, 1–19.CrossRefGoogle Scholar
Gürtler, RE and Cardinal, MV (2015) Reservoir host competence and the role of domestic and commensal hosts in the transmission of Trypanosoma cruzi. Acta Tropica 151, 32–50.CrossRefGoogle ScholarPubMed
Hafner, MS and Nadler, SA (1988) Phylogenetic trees support the coevolution of parasites and their hosts. Nature 332, 258.CrossRefGoogle ScholarPubMed
Harbison, CW and Clayton, DH (2011) Community interactions govern host-switching with implications for host–parasite coevolutionary history. Proceedings of the National Academy of Sciences 108, 9525–9529.CrossRefGoogle ScholarPubMed
Hedges, SB and Kumar, S (2004) Precision of molecular time estimates. TRENDS in Genetics 20, 242–247.CrossRefGoogle ScholarPubMed
Hellgren, O, Pérez-Tris, J and Bensch, S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 2840–2849.CrossRefGoogle Scholar
Hoberg, EP and Brooks, DR (2015) Evolution in action: climate change, biodiversity dynamics and emerging infectious disease. Philosophical Transactions of the Royal Society B 370, 20130553.CrossRefGoogle ScholarPubMed
Hoberg, EP, Brooks, DR and Siegel-Causey, D (1997) Host–parasite co-speciation: history, principles, and prospects. In Clayton, DH and Moore, J (eds), Host–Parasite Evolution: General Principles and Avian Models. Oxford University Press, pp. 212–235.Google Scholar
Holle, BV and Simberloff, D (2005) Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology 86, 3212–3218.CrossRefGoogle Scholar
Huang, S, Bininda-Emonds, OR, Stephens, PR, Gittleman, JL and Altizer, S (2014) Phylogenetically related and ecologically similar carnivores harbour similar parasite assemblages. Journal of Animal Ecology 83, 671–680.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Rannala, B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53, 904–913.CrossRefGoogle ScholarPubMed
Jolley, KA and Maiden, MC (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11, 595.CrossRefGoogle Scholar
Kans, J (2017) Entrez direct: E-utilities on the UNIX command line. In Entrez Programming Utilities Help [Internet]. National Center for Biotechnology Information (US).(Retrieved May 11, 2018). https://www.ncbi.nlm.nih.gov/sites/books/NBK179288.Google Scholar
Kararli, TT (1995) Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharmaceutics & Drug Disposition 16, 351–380.CrossRefGoogle ScholarPubMed
Karasov, WH and Douglas, AE (2013) Comparative digestive physiology. Comprehensive Physiology 3, 741–783.CrossRefGoogle ScholarPubMed
Karasov, WH, Martinez del Rio, C and Caviedes-Vidal, E (2011) Ecological physiology of diet and digestive systems. Annual Review of Physiology 73, 69–93.CrossRefGoogle ScholarPubMed
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Klassen, GJ (1992) Coevolution: a history of the macroevolutionary approach to studying host-parasite associations. The Journal of Parasitology 78, 573–587.CrossRefGoogle ScholarPubMed
Klegarth, AR, Sanders, SA, Gloss, AD, Lane-deGraaf, KE, Jones-Engel, L, Fuentes, A and Hollocher, H (2017) Investigating biogeographic boundaries of the Sunda shelf: a phylogenetic analysis of two island populations of Macaca fascicularis. American Journal of Physical Anthropology 163, 658–670.CrossRefGoogle ScholarPubMed
Kumar, S and Hedges, SB (1998) A molecular timescale for vertebrate evolution. Nature 392, 917.CrossRefGoogle ScholarPubMed
Kuris, AM, Blaustein, AR and Alio, JJ (1980) Hosts as islands. The American Naturalist 116, 570–586.CrossRefGoogle Scholar
Lane, KE, Holley, C, Hollocher, H and Fuentes, A (2011) The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates 52, 117–128.CrossRefGoogle Scholar
Leung, TL and Koprivnikar, J (2016) Nematode parasite diversity in birds: the role of host ecology, life history and migration. Journal of Animal Ecology 85, 1471–1480.CrossRefGoogle ScholarPubMed
Li, J, Deng, T, Li, X, Cao, G, Li, X and Yan, Y (2013) A rat model to study Blastocytis subtype 1 infections. Parasitology Research 112, 3537–3541.CrossRefGoogle ScholarPubMed
Lockwood, JL, Cassey, P and Blackburn, T (2005) The role of propagule pressure in explaining species invasions. Trends in Ecology & Evolution 20, 223–228.CrossRefGoogle ScholarPubMed
Lymbery, AJ, Morine, M, Kanani, HG, Beatty, SJ and Morgan, DL (2014) Co-invaders: the effects of alien parasites on native hosts. International Journal for Parasitology: Parasites and Wildlife 3, 171–177.Google ScholarPubMed
Moe, KT, Singh, M, Howe, J, Ho, LC, Tan, SW, Chen, XQ, Ng, GC and Yap, EH (1997) Experimental Blastocystis hominis infection in laboratory mice. Parasitology Research 83, 319–325.CrossRefGoogle ScholarPubMed
Morens, DM and Fauci, AS (2013) Emerging infectious diseases: threats to human health and global stability. PLoS Pathogens 9, e1003467.CrossRefGoogle ScholarPubMed
Morgulis, A, Coulouris, G, Raytselis, Y, Madden, TL, Agarwala, R and Schäffer, AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics (Oxford, England) 24, 1757–1764.CrossRefGoogle ScholarPubMed
Nilsson, E, Taubert, H, Hellgren, O, Huang, X, Palinauskas, V, Markovets, MY, Valkiūnas, G and Bensch, S (2016) Multiple cryptic species of sympatric generalists within the avian blood parasite Haemoproteus majoris. Journal of Evolutionary Biology 29, 1812–1826.CrossRefGoogle ScholarPubMed
Noël, C, Dufernez, F, Gerbod, D, Edgcomb, VP, Delgado-Viscogliosi, P, Ho, LC, Singh, M, Wintjens, R, Sogin, ML, Capron, M and Pierce, R (2005) Molecular phylogenies of Blastocystis isolates from different hosts: implications for genetic diversity, identification of species, and zoonosis. Journal of Clinical Microbiology 43, 348–355.CrossRefGoogle ScholarPubMed
Nylin, S, Agosta, S, Bensch, S, Boeger, WA, Braga, MP, Brooks, DR, Forister, ML, Hambäck, PA, Hoberg, EP, Nyman, T and Schäpers, A (2018) Embracing colonizations: a new paradigm for species association dynamics. Trends in Ecology & Evolution 33, 4–14.CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR and O'hara, RB (2016) vegan: Community Ecology Package. R package version 2.4-1. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Paradis, E, Claude, J and Strimmer, K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics (Oxford, England) 20, 289–290.CrossRefGoogle ScholarPubMed
Parkar, U, Traub, RJ, Vitali, S, Elliot, A, Levecke, B, Robertson, I, Geurden, T, Steele, J, Drake, B and Thompson, RA (2010) Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Veterinary Parasitology 169, 8–17.CrossRefGoogle ScholarPubMed
Pedersen, AB and Davies, TJ (2009) Cross-species pathogen transmission and disease emergence in primates. EcoHealth 6, 496–508.CrossRefGoogle ScholarPubMed
Poulin, R, Krasnov, BR and Mouillot, D (2011 a) Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Poulin, R, Krasnov, BR, Mouillot, D and Thieltges, DW (2011 b) The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society B: Biological Sciences 366, 2379–2390.CrossRefGoogle ScholarPubMed
Ramírez, JD, Sánchez, LV, Bautista, DC, Corredor, AF, Flórez, AC and Stensvold, CR (2014) Blastocystis subtypes detected in humans and animals from Colombia. Infection, Genetics and Evolution 22, 223–228.CrossRefGoogle ScholarPubMed
R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/.Google Scholar
Rollins, D, Bryant, FC and Montandon, R (1984) Fecal pH and defecation rates of eight ruminants fed known diets. The Journal of Wildlife Management 48, 807–813.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
RStudio (2016) RStudio: Integrated development environment for R (Version 0.99.903) [Computer software]. Boston, MA.Google Scholar
Santín, M, Gómez-Muñoz, MT, Solano-Aguilar, G and Fayer, R (2011) Development of a new PCR protocol to detect and subtype Blastocystis spp. from humans and animals. Parasitology Research 109, 205–212.CrossRefGoogle Scholar
Scicluna, SM, Tawari, B and Clark, CG (2006) DNA barcoding of Blastocystis. Protist 157, 77–85.CrossRefGoogle ScholarPubMed
Šidák, Z (1967) Rectangular confidence regions for the means of multivariate normal distributions. Journal of the American Statistical Association 62, 626–633.Google Scholar
Simberloff, D (2009) The role of propagule pressure in biological invasions. Annual Review of Ecology, Evolution, and Systematics 40, 81–102.CrossRefGoogle Scholar
Šlapeta, J (2013) Cryptosporidiosis and Cryptosporidium species in animals and humans: a thirty colour rainbow? International Journal for Parasitology 43, 957–970.CrossRefGoogle ScholarPubMed
Stensvold, CR and Clark, CG (2020) Pre-empting Pandora's box: Blastocystis subtypes revisited. Trends in Parasitology 36, 229–232.CrossRefGoogle ScholarPubMed
Stensvold, CR, Alfellani, MA, Nørskov-Lauritsen, S, Prip, K, Victory, EL, Maddox, C, Nielsen, HV and Clark, CG (2009) Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. International Journal for Parasitology 39, 473–479.CrossRefGoogle ScholarPubMed
Stricker, KB, Harmon, PF, Goss, EM, Clay, K and Luke Flory, S (2016) Emergence and accumulation of novel pathogens suppress an invasive species. Ecology Letters 19, 469–477.CrossRefGoogle ScholarPubMed
Svensson-Coelho, M, Loiselle, BA, Blake, JG and Ricklefs, RE (2016) Resource predictability and specialization in avian malaria parasites. Molecular Ecology 25, 4377–4391.CrossRefGoogle ScholarPubMed
Thompson, RCA, Lymbery, AJ and Smith, A (2010) Parasites, emerging disease and wildlife conservation. International Journal for Parasitology 40, 1163–1170.CrossRefGoogle ScholarPubMed
Vester, BM, Burke, SL, Dikeman, CL, Simmons, LG and Swanson, KS (2008) Nutrient digestibility and fecal characteristics are different among captive exotic felids fed a beef-based raw diet. Zoo Biology 27, 126–136.CrossRefGoogle ScholarPubMed
Vienne, DD, Refrégier, G, López-Villavicencio, M, Tellier, A, Hood, ME and Giraud, T (2013) Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytologist 198, 347–385.CrossRefGoogle ScholarPubMed
Wang, W, Owen, H, Traub, RJ, Cuttell, L, Inpankaew, T and Bielefeldt-Ohmann, H (2014a) Molecular epidemiology of Blastocystis in pigs and their in-contact humans in Southeast Queensland, Australia, and Cambodia. Veterinary Parasitology 203, 264–269.CrossRefGoogle Scholar
Wang, W, Bielefeldt-Ohmann, H, Traub, RJ, Cuttell, L and Owen, H (2014b) Location and pathogenic potential of Blastocystis in the porcine intestine. Plos One 9, e103962.CrossRefGoogle Scholar
Wilcox, JJ and Hollocher, H (2018) Unprecedented symbiont eukaryote diversity is governed by internal trophic webs in a wild non-human primate. Protist 169, 307–320.CrossRefGoogle Scholar
Wilcox, JJ, Lane-Degraaf, KE, Fuentes, A and Hollocher, H (2015) Comparative community-level associations of helminth infections and microparasite shedding in wild long-tailed macaques in Bali, Indonesia. Parasitology 142, 480–489.CrossRefGoogle ScholarPubMed
Yang, PJ, LaMarca, M, Kaminski, C, Chu, DI and Hu, DL (2017) Hydrodynamics of defecation. Soft Matter 13, 4960–4970.CrossRefGoogle ScholarPubMed
Yoshikawa, H, Koyama, Y, Tsuchiya, E and Takami, K (2016) Blastocystis phylogeny among various isolates from humans to insects. Parasitology International 65, pp.750–759.CrossRefGoogle ScholarPubMed