Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-25T17:27:53.641Z Has data issue: false hasContentIssue false
  • English
  • Français

Heterogeneity in helminth infections: factors influencing aggregation in a simple host–parasite system

Published online by Cambridge University Press:  30 September 2019

Richard C. Tinsley Open the ORCID record for Richard C. Tinsley [Opens in a new window] ,
Hanna Rose Vineer ,
Rebecca Grainger-Wood  and
Eric R. Morgan
Richard C. Tinsley*
Affiliation:
School of Biological Sciences, Life Sciences Building, University of Bristol, BristolBS8 1TQ, UK
Hanna Rose Vineer
Affiliation:
School of Veterinary Sciences, University of Bristol, BristolBS40 5DU, UK
Rebecca Grainger-Wood
Affiliation:
School of Biological Sciences, Life Sciences Building, University of Bristol, BristolBS8 1TQ, UK
Eric R. Morgan
Affiliation:
School of Biological Sciences, Life Sciences Building, University of Bristol, BristolBS8 1TQ, UK
*
Author for correspondence: Richard C. Tinsley, E-mail: r.c.tinsley@bristol.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

The almost universally-occurring aggregated distributions of helminth burdens in host populations have major significance for parasite population ecology and evolutionary biology, but the mechanisms generating heterogeneity remain poorly understood. For the direct life cycle monogenean Discocotyle sagittata infecting rainbow trout, Oncorhynchus mykiss, variables potentially influencing aggregation can be analysed individually. This study was based at a fish farm where every host individual becomes infected by D. sagittata during each annual transmission period. Worm burdens were examined in one trout population maintained in isolation for 9 years, exposed to self-contained transmission. After this year-on-year recruitment, prevalence was 100% with intensities 10–2628, mean 576, worms per host. Parasite distribution, amongst hosts with the same age and environmental experience, was highly aggregated with variance to mean ratio 834 and negative binomial parameter, k, 0.64. The most heavily infected 20% of fish carried around 80% of the total adult parasite population. Aggregation develops within the first weeks post-infection; hosts typically carried intensities of successive age-specific cohorts that were consistent for that individual, such that heavily-infected individuals carried high numbers of all parasite age classes. Results suggest that host factors alone, operating post-infection, are sufficient to generate strongly overdispersed parasite distributions, rather than heterogeneity in exposure and initial invasion.

Keywords

Discocotyle sagittataimmune controlMonogeneaoverdispersed distributionsparasite transmission
Type
Research Article
Information
Parasitology , Volume 147 , Issue 1 , January 2020 , pp. 65 - 77
Check for updates
Copyright
Copyright © Cambridge University Press 2019

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.)

Footnotes

*

Present address: Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool L69 3BX, UK

†

Present address: CSA Environmental, Pershore WR10 3DN, UK

‡

Present address: School of Biological Sciences, Institute for Global Food Security, Queen's University, Belfast BT9 7BL, UK

References

Anderson, RM and May, RM (1978) Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Bandilla, RM, Hakalahti, T, Hudson, P and Valtonen, E (2005) Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): a consequence of host susceptibility or exposure? Parasitology 130, 169–176.CrossRefGoogle ScholarPubMed
Bishop, SC and Morris, CA (2007) Genetics of disease resistance in sheep and goats. Small Ruminant Research 70, 48–59.CrossRefGoogle Scholar
Cable, J and van Oosterhout, C (2007) The role of innate and acquired resistance in two natural populations of guppies (Poecilia reticulata) infected with the ectoparasite Gyrodactylus turnbulli. Biological Journal of the Linnean Society 90, 647–655.CrossRefGoogle Scholar
Cable, J, Barber, I, Boag, B, Ellison, AR, Morgan, ER, Murray, K, Pascoe, EL, Sait, SM, Wilson, AJ and Booth, M (2017) Global change, parasite transmission and disease control: lessons from ecology. Philosophical Transactions of the Royal Society B: Biological Sciences 372, 20160088.CrossRefGoogle ScholarPubMed
Charlier, J, Morgan, ER, Rinaldi, L, Van Dijk, J, Demeler, J, Hoglund, J, Hetrzberg, H, Van Ranst, B, Hendrickx, G, Vercruysse, J and Kenyon, F (2014) Practices to optimise gastrointestinal nematode control on sheep, goat and cattle farms in Europe using targeted (selective) treatments. Veterinary Record 175, 250–255.CrossRefGoogle ScholarPubMed
Civitello, DJ and Rohr, JR (2014) Disentangling the effects of exposure and susceptibility on transmission of the zoonotic parasite Schistosoma mansoni. Journal of Animal Ecology 83, 1379–1386.CrossRefGoogle ScholarPubMed
Crofton, HD (1971) A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
Gamer, M, Lemon, J, Fellows, I and Singh, P (2012). irr: Various coefficients of interrater reliability and agreement. R package version 0.84. https://CRAN.R-project.org/package=irr.Google Scholar
Gannicott, AM (1997) The Biology of Discocotyle sagittata (Monogenea) Infecting Trout (PhD thesis). Bristol University, Bristol, UK.Google Scholar
Gannicott, AM and Tinsley, RC (1997) Egg hatching in the monogenean gill parasite Discocotyle sagittata from the rainbow trout (Oncorhynchus mykiss). Parasitology 114, 569–579.Google Scholar
Gannicott, AM and Tinsley, RC (1998 a) Larval survival characteristics and behaviour of the gill monogenean Discocotyle sagittata. Parasitology 117, 491–498.CrossRefGoogle ScholarPubMed
Gannicott, AM and Tinsley, RC (1998 b) Environmental effects on transmission of Discocotyle sagittata (Monogenea): egg production and development. Parasitology 117, 499–504.CrossRefGoogle ScholarPubMed
Holmstad, PR and Skorping, A (1998) Covariation of parasite intensities in willow ptarmigan, Lagopus lagopus L. Canadian Journal of Zoology 76, 1581–1588.CrossRefGoogle Scholar
Jackson, JA and Tinsley, RC (2001) Protopolystoma xenopodis (Polystomatidae: Monogenea) primary and secondary infections in Xenopus laevis. Parasitology 123, 455–463.CrossRefGoogle Scholar
Kemper, KE, Palmer, DG, Liu, SM, Greeff, JC, Bishop, SC and Karlsson, LJE (2010) Reduction of faecal worm egg count, worm numbers and worm fecundity in sheep selected for worm resistance following artificial infection with Teladorsagia circumcincta and Trichostrongylus colubriformis. Veterinary Parasitology 171, 238–246.CrossRefGoogle ScholarPubMed
Lloyd-Smith, JO, Schreiber, SJ, Kopp, PE and Getz, WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359.CrossRefGoogle ScholarPubMed
Luong, LT, Vigliotti, BA and Hudson, PJ (2011) Strong density-dependent competition and acquired immunity constrain parasite establishment: implications for parasite aggregation. International Journal for Parasitology 41, 505–511.CrossRefGoogle ScholarPubMed
Lysne, DA and Skorping, A (2002) The parasite Lernaeocera branchialis on caged cod: infection pattern is caused by differences in host susceptibility. Parasitology 124, 69–76.CrossRefGoogle ScholarPubMed
Marques, JF, Santos, MJ and Cabral, HN (2010) Aggregation patterns of macroendoparasites in phylogenetically related fish hosts. Parasitology 137, 1671–1680.CrossRefGoogle ScholarPubMed
Morgan, ER, Aziz, NAA, Blanchard, A, Charlier, J, Charvet, C, Claerebout, E, Geldhof, P, Greer, AW, Hertzberg, H, Hodgkinson, J, Höglund, J, Hoste, H, Kaplan, RM, Martínez-Valladares, M, Mitchell, S, Ploeger, HW, Rinaldi, L, Von Samson-Himmelstjerna, G, Sotiraki, S, Schnyder, M, Skuce, P, Bartley, D, Kenyon, F, Thamsborg, SM, Rose Vineer, H, De Waal, T, Williams, AR, Van Wyk, JA and Vercruysse, J (2019) 100 questions in livestock helminthology. Trends in Parasitology 35, 52–71.CrossRefGoogle ScholarPubMed
Pacala, SW and Dobson, AP (1988) The relation between the number of parasites per host a host age: population dynamic causes and maximum-likelihood estimation. Parasitology 96, 197–210.CrossRefGoogle Scholar
R Development Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rose Vineer, H, White, T, Baber, P and Morgan, ER (2019) Reduced egg shedding in nematode-resistant ewes and projected epidemiological benefits under climate change. International Journal for Parasitology (in press).CrossRefGoogle ScholarPubMed
Rubio-Godoy, M (2008) Microhabitat selection of Discocotyle sagittata (Monogenea: Polyopisthocotylea) in farmed rainbow trout. Folia Parasitologica 55, 270–276.CrossRefGoogle Scholar
Rubio-Godoy, M and Tinsley, RC (2002) Single and trickle infection with Discocotyle sagittata (Monogenea: Polyopisthocotylea): effect of exposure mode on parasite abundance and development. Folia Parasitologica 49, 269–278.CrossRefGoogle ScholarPubMed
Rubio-Godoy, M and Tinsley, RC (2004) Immunity in rainbow trout, Oncorhynchus mykiss, against the monogenean Discocotyle sagittata following primary infection. Parasitology Research 92, 367–374.CrossRefGoogle ScholarPubMed
Rubio-Godoy, M and Tinsley, RC (2008 a) Recruitment and effects of Discocotyle sagittata (Monogenea) infection on farmed trout. Aquaculture 274, 15–23.CrossRefGoogle Scholar
Rubio-Godoy, M and Tinsley, RC (2008 b) Transmission dynamics of Discocotyle sagittata (Monogenea) in farmed rainbow trout interpreted from parasite population age structure. Aquaculture 275, 34–41.CrossRefGoogle Scholar
Rubio-Godoy, M, Sigh, J, Buchmann, K and Tinsley, RC (2003 a) Immunization of rainbow trout Oncorhynchus mykiss against Discocotyle sagittata (Monogenea). Diseases of Aquatic Organisms 55, 23–30.CrossRefGoogle Scholar
Rubio-Godoy, M, Sigh, J, Buchmann, K and Tinsley, RC (2003 b) Antibodies against Discocotyle sagittata (Monogenea) in farmed trout. Diseases of Aquatic Organisms 56, 181–184.CrossRefGoogle Scholar
Rubio-Godoy, M, Porter, R and Tinsley, RC (2004) Evidence of complement-mediated killing of Discocotyle sagittata (Platyhelminthes, Monogenea) oncomiracidia. Fish and Shellfish Immunology 17, 95–103.CrossRefGoogle ScholarPubMed
Sarabeev, V, Balbuena, JA and Morand, S (2019) Aggregation patterns of helminth populations in the introduced fish, Liza haematocheilus (Teleostei: Mugilidae): disentangling host–parasite relationships. International Journal for Parasitology 49, 83–91.CrossRefGoogle ScholarPubMed
Shaw, DJ and Dobson, AP (1995) Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111(Suppl.), S111–S133.CrossRefGoogle ScholarPubMed
Shaw, DJ, Grenfell, BT and Dobson, AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle ScholarPubMed
Shvydka, S, Sarabeev, V, Estruch, VD and Cadarso-Suarez, C (2018) Optimum sample size to estimate mean parasite abundance in fish parasite surveys. Helminthologia 55, 52–59.CrossRefGoogle ScholarPubMed
Smith, JA, Wilson, K, Pilkington, JG and Pemberton, JM (1999) Heritable variation in resistance to gastro-intestinal nematodes in an unmanaged mammal population. Proceedings of the Royal Society B 266, 1283–1290.CrossRefGoogle Scholar
Tinsley, RC (1973) Ultrastructural studies on the form and function of the gastrodermis of Protopolystoma xenopi (Monogenoidea Polyopisthocotylea). Biological Bulletin 144, 541–555.CrossRefGoogle Scholar
Tinsley, RC (1999) Parasite adaptations to extreme conditions in a desert environment. Parasitology 119(Suppl.), S31–S56.CrossRefGoogle Scholar
Tinsley, RC (2004) Platyhelminth parasite reproduction: some general principles derived from monogeneans. Canadian Journal of Zoology 82, 270–291.CrossRefGoogle Scholar
Tinsley, R, Stott, L, York, J, Everard, A, Chapple, S, Jackson, J, Viney, M and Tinsley, MC (2012) Acquired immunity protects against helminth infection in a natural host population: long-term field and laboratory evidence. International Journal for Parasitology 42, 931–938.CrossRefGoogle Scholar
Turner, AK, Begon, M, Jackson, JA, Bradley, JE and Paterson, S (2011) Genetic diversity in cytokines associated with immune variation and resistance to multiple pathogens in a natural rodent population. PLoS Genetics 7, e1002343.CrossRefGoogle Scholar
Warburton, EM and Vonhof, MJ (2018) From individual heterogeneity to population-level overdispersion: quantifying the relative roles of host exposure and parasite establishment in driving aggregated helminth distributions. International Journal for Parasitology 48, 309–318.CrossRefGoogle ScholarPubMed
Wilber, MQ, Johnson, CJ and Briggs, CJ (2016) When can we infer mechanism from parasite aggregation? A constraint-based approach to disease ecology. Ecology 98, 688–702.CrossRefGoogle Scholar
Wilson, K, Bjornstad, ON, Dobson, AP, Merler, S, Poglayen, G, Randolph, SE, Read, AF and Skorping, A (2002) Heterogeneities in macroparasite infections: patterns and processes. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Hesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Disease. Oxford, UK: Oxford University Press, pp. 6–44.Google Scholar
Woolhouse, MEJ, Dye, C, Etard, J-F, Smith, T, Charlwood, JD, Garnett, GP, Hagan, P, Hii, JLK, Ndhlovu, PD, Quinnell, RJ, Watts, CH, Chandiwana, SK and Anderson, RM (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the USA 94, 338–342.CrossRefGoogle ScholarPubMed
Zhou, S, Li, WX, Zou, H, Zhang, J, Wu, SG and Wang, GT (2018) Expression analysis of immune genes in goldfish (Carassius auratus) infected with the monogenean parasite Gyrodactylus kobayashii. Fish and Shellfish Immunology 77, 40–45.CrossRefGoogle ScholarPubMed