Aggregation of Infective Stages of Parasites as an Adaptation and Its Implications for the Study of Parasite-Host Interactions

Abstract

The causes and consequences of aggregation among conspecifics have received much attention. For infecting macroparasites, causes include variation among hosts in susceptibility and whether infective stages are aggregated in the environment. Here, we link these two phenomena and explore whether aggregation of infective stages in the environment is adaptive to parasites encountering host condition-linked defenses and what effect such aggregations have for parasite-host interactions. Using simulation models, we show that parasite fitness is increased by aggregates attacking a host, particularly when investment into defenses is high. The fitness benefit of aggregation remains despite inclusion of factors that should curb the benefits of aggregation, namely, mortality of low-condition hosts (those hosts expected to be most susceptible to parasitism) and costs of high coinfection. For sample sizes common in studies, aggregation of infective stages reduces the likelihood of detecting host condition-parasitism relations, even when host condition is the only other factor in models affecting parasitism. Thus, it is not surprising that the expected inverse relations between host condition and parasitism, commonly a premise in studies of parasite-host interactions, are inconsistently found. An understanding of how parasites encounter hosts is thus needed for developing theory for parasite-host ecological and evolutionary interactions.

Risk taking of educated nematodes

“…Parasitic nematodes have evolved many means to address these risks in order to overcome and influence host behavior [ 10 ]. One of the most successful infection strategies involves overwhelming the host immune system through group attack [ 11 ]. This type of behavior is seen perhaps most clearly in insect parasitic nematodes, called entomopathogenic nematodes, where large numbers of pathogens are required to overcome a host’s immune system [ 12 , 13 ].…”

Whether larval amphibians school does not affect the parasite aggregation rule: testing the effects of host spatial heterogeneity in field and experimental studies

“…phototaxis) to maximize their chances of host encounter, and others use host‐generated cues to actively search (Haas , Sukhdeo and Sukhdeo ) – both general strategies could result in spatial aggregations. If over‐dispersion benefits some macroparasites (Jaenike , May and Woolhouse ), one would further expect motile infective stages to show aggregating behavior in the absence of external stimuli (Morrill and Forbes ). Although high degrees of aggregation have been observed with entomopathogenic nematodes, there is an overall lack of study regarding the expected distributions of parasite infective stages in the environment (Morrill and Forbes ).…”

“…If over‐dispersion benefits some macroparasites (Jaenike , May and Woolhouse ), one would further expect motile infective stages to show aggregating behavior in the absence of external stimuli (Morrill and Forbes ). Although high degrees of aggregation have been observed with entomopathogenic nematodes, there is an overall lack of study regarding the expected distributions of parasite infective stages in the environment (Morrill and Forbes ). As such, the possible contributions of temporal and spatial heterogeneity in the distributions of infected snails and cercariae require further study.…”

“…Intermediate values of over‐dispersion may help to maximize parasite fitness when prevalence is low by increasing within‐host co‐occurrence of males and females while limiting the risk of parasite‐induced host mortality (May and Woolhouse , Jaenike ). However, the ubiquity of aggregated infections even among larval or non‐reproductive parasite stages suggests broader underlying drivers, and recent simulation models show that parasite fitness is increased when their infectious stages attack hosts as aggregations rather than singly, especially when hosts invest heavily in defence (Morrill and Forbes ).…”

Identifying sources of variation in parasite aggregation

“…The search for biological predictors of parasite aggregation must recognize that aggregation is a phenomenon of both the parasite and host species. Factors promoting aggregation such as reproduction and recruitment of parasites on hosts ( Grear & Hudson, 2011 ), attraction of infective stages of parasites to one another and environmental aggregation ( Morrill & Forbes, 2016 ), and host condition-linked immunity ( Morrill & Forbes, 2012 ) must be considered alongside factors reducing aggregation such as density-dependent mortality of parasites ( Anderson & May, 1978 ; Luong, Vigliotti & Hudson, 2011 ) and parasite-induced host mortality ( Anderson & Gordon, 1982 ). Such factors can be variably important in determining the degree of parasite aggregation observed, both within and across species associations.…”