Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Abstract

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of par...

The Ecological Importance of Amphipod–Parasite Associations for Aquatic Ecosystems

“…The ecological consequences of parasitism are more evident and documented for the so called "manipulative parasites" and "keystone parasites" [26,39]. Manipulative parasites induce phenotypic or behavioral changes that can render their hosts easy prey for the next host [33,40,41]. As a result, parasites with complex life cycles using trophic transmission can increase their chances to complete the life cycle, with positive implications for their fitness, but can also alter host population structure, the outcome of competition between hosts, and predator-prey dynamics with considerable consequences for the ecosystem [39,42,43].…”

“…Infection of the definitive host occurs when the infected amphipod is consumed by the definitive host [130]. Often, the behavior of the intermediate host is manipulated by the parasite to increase the chance of trophic transmission as soon as the mature cystacanth stage is reached [41,131].…”

Inter-population variation in the intensity of host manipulation by the fish acanthocephalanPomphorhynchus tereticollis: are differences driven by predation risk?

“…The aim of the present study was precisely to investigate whether spatial variation in biotic factors modulates the magnitude of intermediate host manipulation by a fish acanthocephalan parasite. Acanthocephalans are well represented in studies on HPM (Moore, 2002; Fayard et al ., 2019), including reported cases of inter-population variation in the intensity of manipulation. For instance, the intensity of HMP in experimentally-infected G. pulex has been shown to differ according to the geographical origin of P. laevis population (Franceschi et al ., 2010).…”

“…We then quantified HMP on both behavioural and physiological traits. Host manipulation by acanthocephalans is known to be multidimensional (Cézilly et al ., 2013), notably involving traits related to taxis, protection and immune system (Fayard et al ., 2019). Here, we recorded phototaxis and refuge use, two behavioural traits markedly altered by P. tereticollis (Tain et al ., 2006; Perrot-Minnot et al ., 2007).…”

Enhanced Attraction of Arthropod Vectors to Infected Vertebrates: A Review of Empirical Evidence

“…Host manipulation by parasites has been fascinating parasitologists for decades (Thomas et al, 2005), especially when this manipulation results in dramatic changes in host's physiology (Cordaux et al, 2011;Kageyama et al, 2012;Fayard et al, 2020), morphology (Bakker et al, 1997;Yanoviak et al, 2008;Fayard et al, 2020) or behavior (Berdoy et al, 2000;Thomas et al, 2002;Weinersmith, 2019;Fayard et al, 2020). This host exploitation strategy, described in many phylogenetically distant host-parasite systems, usually involves phenotypic changes in the infected host (extended phenotype, Dawkins, 1982).…”