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

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.

Experimental evidence that host choice by parasites is age-dependent in a fish-monogenean system

“…fish older than one), and they attributed this pattern to an ontogenetic decline of susceptibility in older fish. Another study using a fish-monogenean system also found that adult individuals were more resistant than subadult (Konijnendijk et al 2013), demonstrating the importance of fish immunity in controlling monogenean infections (Buchmann and Bresciani 2006;Tinsley et al 2020). Thus, our results indicate a trade-off between the host resistance and parasite preference, resulting in high parasite burdens on subadult hosts.…”

“…Although some fish parasite studies have shown that larger hosts are able to accommodate more parasite than small ones (Cantatore and Timi, 2015;Braicovich et al 2016), a decline of susceptibility in older fish also have been suggested to affect the fish infection outcomes (Tinsley et al 2020;Bailey et al 2021). In a recent experiment, Bailey et al (2021) found that the disease severity was greater in young than juvenile (i.e.…”

“…In addition, the subadult hosts also might offer the most favourable space-time-energy budget for parasite development and reproduction, as well as constitute the best compromise for parasite fitness due to their underdeveloped immune systems (Théron et al 1998;Woolhouse 1998;Kołodziej-Sobocińska et al 2018). The complexities involving the relationship between fish age and immunity (Izhar and Ben-Ami, 2015;Ashby and Bruns 2018;Ben-Ami 2019;Izhar et al 2020;Tinsley et al 2020) suggest that a more direct manipulation of resource quality and resistance to infection would be a development for future research on parasite transmission dynamics.…”

Helminth communities in amphibians from Latvia, with an emphasis on their connection to host ecology

“…A number of local or intrinsic factors affect helminth aggregations in amphibians, such as spatial heterogeneity, host body size, parasite dimensions and virulence, and parasite and intermediatehost productivities (Campião et al, 2015;Johnson & Wilber, 2017;Toledo et al, 2017;Mihaljevic et al, 2018). In addition, fish studies suggest a high importance of individual host susceptibility (Tinsley et al, 2020) and show more complicated mechanisms determining helminth infection rates, such as ontogenic dietary shifts that change parasite intake pathways (Saad-Fares & Combes, 1992), or the presence of certain parasite infection levels that are optimal for the host body condition (Maceda-Veiga et al, 2016). Common invasion pathways or biological interactions (such as mutual facilitation or competition) may cause parasite species associations in hosts (Dallas et al, 2019) that, so far, have been noted in very few amphibian helminth community studies (Hamann et al, 2006a(Hamann et al, , 2010(Hamann et al, , 2013a(Hamann et al, , 2014.…”

Laboratory infection rates and associated mortality of juvenile Chinook Salmon (Oncorhynchus tshawytscha) from parasitic copepod (Salmincola californiensis)

“…A hurdle model is a two‐part model that fits two linear models: the first a logistic linear model that estimates infection prevalence. The second part is a truncated negative binomial model that estimates infection intensity, as many parasitic infections show a negative binomial distribution (Pennycuick, 1971; Tinsley et al., 2020). The hurdle model was initially fit using all main effects (i.e.…”