Ecological relationships refer to interactions between organisms within their environment and are classified according to the outcomes for each partner (positive, negative, or neutral effects). The Red Queen hypothesis (Van Valen, 1973) stated that biotic interactions are key drivers of evolution through adaptation and counteracting adaptations in interacting species. Selection favors hosts that are able to avoid or resist infection (resistance) or attenuate the parasite-induced damages (tolerance), whereas parasites evolve to impede the host’s strategies to detect, reject, or neutralize them. Such strategies are costly (Rigby et al., 2002) and are selected as long as the reduction in damages outweighs the cost of parasites’ resistance or tolerance (Sheldon and Verhulst, 1996).

Instead of a binary view of parasites and mutualists, interactions between hosts and symbionts can be addressed as a continuum from mutualism to parasitism according to the outcomes for each partner’s fitness (beneficial or harmful effects, Thomas et al., 2000; Leung and Poulin, 2008). In this context, parasites may evolve to be less deleterious to their host because of direct advantages for the transmission, reproduction, and survival of parasites. For instance, parasites may temporally improve antipredator behavior (“bodyguard manipulation,” Maure et al., 2013), especially in the intermediate host, to avoid non-host predators or postpone host mortality until parasites reach an infective stage and survive predation by a definitive host (Médoc et al., 2009). Some parasites species may also endorse a protective role for the host against lethal parasitoids (Sternberg et al., 2011) due to within-host competition. Feather mites can play a commensalistic–mutualistic role by feeding mainly on fungi including pathogenic ones and thus by cleaning host feathers (Dona et al., 2019). Finally, vertically transmitted parasites may enhance the short-term reproductive output of the host (Haine et al., 2004).

In addition, indirect consequences, which are unrelated to parasites’ fitness, may provide hosts with unexpected advantages in specific environments. Fellous and Salvaudon (2009) have proposed the term “conditionally helpful parasites” and have postulated that adverse environmental conditions seem to drive transitions along the parasite–mutualist continuum. For instance, shell-degrading endoliths attenuate the mortality of mussels during heat stress because of shell discoloration (Zardi et al., 2016). Trypanosoma otospermophili confers advantages to young of the year on Richardson’s ground squirrels (Spermophilus richardsonii) in a pyridoxine-deficient environment through the synthesis of vitamin B6 (i.e., pyridoxine, Munger and Holmes, 1988). This possible shift toward mutualism is more likely to occur for mild parasites with low-intensity infection, causing few damages (Fellous and Salvaudon, 2009).

Environmental pollution is a major and worldwide issue, which is likely to affect both hosts and parasites. During recent years, a couple of studies have yielded exciting results on the potential benefits of helminth parasites for hosts exposed to pollutants (Sánchez et al., 2016; Sures et al., 2017; Morrill et al., 2019; Molbert et al., 2020, 2021). This review aims to explore the potential effect of toxic chemicals in shifting interspecific relationships from parasitic to mutualistic. We review (i) the large body of studies showing that some parasites can accumulate pollutants and we discuss possible mechanisms. We then investigate the potential consequences of parasitism on (ii) the pollutant burden of the host and (iii) the costs and benefits for hosts in contaminated environments. In addition, we explore (iv) costs and benefits for parasites. We construct (v) a conceptual framework and we consider (vi) the consequences at the population and community levels. Finally, (vii) we propose future research directions.

Several studies have reported additive and synergistic interactions between parasitism and pollution (Bustnes et al., 2006; Marcogliese and Pietrock, 2011), since some toxic chemicals may induce oxidative stress, depress the immune system, or disrupt endocrine functions, that may, in turn, favor parasitic infection and exacerbate their pathogenicity (Jobling and Tyler, 2003; Marcogliese, 2005; Morley et al., 2006; Sures, 2006). Joint effects of parasitism and pollution on host fitness are highly complex (Sures, 2008) and depend on the level of parasitism, as well as the level and mode of action of the environmental pollutant.

Recent findings suggest that some parasites, through their noteworthy ability to uptake pollutants, provide substantial benefits to their host. The first evidence came from an experimentally manipulated arsenic levels study under controlled conditions: arsenic-induced damages were attenuated in Artemia parthenogenetica infected by intestinal cestodes compared with uninfected ones (Sánchez et al., 2016). Acute mortality was reduced, the number of lipid droplets increased, and anti-oxidative defense mechanisms (catalase and glutathione reductase activity) were enhanced, without oxidative damage in parasitized compared with unparasitized Brine shrimps (Sánchez et al., 2016). Morrill et al. (2019) suggested that common eiders Somateria mollissima may benefit from intestinal helminths when exposed to lead: hens treated with an antihelminthic were more prone to being resighted the following year, with decreasing blood lead levels. Moreover, African common toads infected by the intestinal nematodes Amplicaecum africanum were not only less contaminated by trace metals (cadmium, lead, copper, nickel, and chromium) but also had less severe alterations of the intestinal mucosa and higher antioxidant activities (glutathione peroxidase, superoxide dismutase, and catalase) compared with uninfected conspecifics (Akinsanya et al., 2020). When infected by intestinal cestodes (C. laticeps), breams were in better body condition and less contaminated by PCBs (Brázová et al., 2021). Chubs infected by acanthocephalans exhibited lower oxidative damage than uninfected ones when naturally exposed to organic micropollutants (Molbert et al., 2020) and experimentally exposed to PAH (Molbert et al., 2021). Although these descriptive and experimental studies are still scarce, they support the hypothesis that some intestinal helminths, at low-intensity infections, could be less detrimental or even helpful for hosts exposed to trace metal elements or organic pollutants.

Pollutant exposure can directly or indirectly induce a wide array of costs and benefits for parasites (Marcogliese, 2005). First, toxic chemicals affect species differently and can be more deleterious for parasites compared with vertebrate hosts (Blanar et al., 2010) because of (i) a weaker tolerance to particular xenobiotics (e.g., fungicide, Hanlon and Parris, 2012) and (ii) the bioaccumulation rate and less efficient metabolization and excretion processes (Livingstone, 1998). Free-living stages and ectoparasites may also be particularly vulnerable to environmental pollution (Pietrock and Marcogliese, 2003; Blanar et al., 2009). As an example, abnormal attachment clamps were observed more frequently in parasites (diplozoons) from the gills of chubs and breams caught in the most polluted sites (Šebelová et al., 2002), suggesting pollution-induced morphological impairments. Harmful effects of the pollutant burden on parasites can lead to a lower infestation by parasites and/or higher mortality of adult forms in highly contaminated hosts, which could be indirectly beneficial for the host. In such a context, one may predict that parasites would adapt faster than their host under this toxic selection pressure because of the shorter generation time. However, such rapid microevolution was not demonstrated by a multigenerational experimental exposure to a globally marketed and used pesticide (Cuco et al., 2020).

On the other hand, pollution-tolerant parasites may benefit from environmental pollution since toxic compounds can impair the physiology and, particularly, the immune defenses of the host (Jokinen et al., 1995), thus weakening resistance to parasites (Valtonen et al., 1997). For instance, experimental exposure at sublethal concentrations to carbaryl, a neurotoxic pesticide, synergistically interacts with parasitism by enhancing parasite virulence (Coors et al., 2008). The impacts of pollutants’ bioaccumulation on parasites appear to be complex and context-dependent (Rohr et al., 2008). For instance, in a terrestrial host-parasite system, the establishment of the tapeworm Hymenolepis diminuta in beetles was either increased or reduced by the exposure to an insecticide depending on the timing of the contamination (Dhakal et al., 2020).

Finally, environmental pollution can positively or negatively impact the presence, density, or resistance of intermediate and final hosts (Valtonen et al., 1997), thus compromising parasite life cycles. Evaluating potential ecotoxicological consequences on parasites’ transmission, reproduction, or survival is thus a complex issue (Khan and Thulin, 1991; Sures et al., 2017). It is noteworthy that adverse impacts of pollutants on parasites could have cascading effects on ecological processes, ecosystem functioning, and services (Gómez and Nichols, 2013; Davis and Prouty, 2019).

We propose a conceptual framework and we argue that parasites can be helpful (positive outcome for the host’s fitness) when the costs of parasitism (level of infestation and pathogenicity) are negligible compared with the benefits of pollutant sequestration (depending on the accumulation rate and toxicity for the host). The interaction may drastically change depending on levels of parasitism (or pathogenicity) and pollutant levels. When hosts experience high aggregation of parasites, their pathogenicity likely outweighs the potential benefits of pollutants sequestration (Figure 1). When environmental contamination exceeds the ability of parasites to sequester pollutants, ecotoxicological effects may be exacerbated by parasitism (Figure 1). This simplified model implies only one type of pollutant and one parasite species (Figure 1). We summarize the main environmental and ecological factors that can influence the host-parasite interaction in polluted environments (Figure 2), including (i) the type of pollutants’ mixture, their probabilities of occurrence, and their chemical properties (accumulation, metabolization, differential toxicity among species, etc.), (ii) the nature and intensity of parasites, tolerance to pollutants, the ability to sequester pollutants, life cycle (number of obligatory hosts), diversity of parasites’ species, and dynamics of co-infection, and (iii) host tolerance and resistance to parasites, tolerance to pollutants, individual traits (sex, age, body length, trophic ecology, etc.), and inter- and intra-specific relationships. All these biotic and abiotic factors can interact and it may be difficult to establish some predictions.

Could context-dependent outcomes in host-parasite interactions have some impact on the dynamics and community structures of the host and parasite populations? This has been discussed for mutualistic interactions: costs, benefits, and thus net effects greatly vary in space and time, affecting geographical disparities in community structures as well as the rate of evolutionary change (Bronstein, 1994; Hay et al., 2004).

The consequences of context-dependent helpful parasites on host populations and communities have not been studied to the best of our knowledge. One may predict that, in a population facing environmental pollution, parasitism could be beneficial at a low-intensity infection but becomes detrimental as the parasite load increases.

In a quantitative meta-analysis, the effects of environmental pollution on parasite populations and communities have been explored (Blanar et al., 2009). Surprisingly, contaminants caused more damage to (i) monoxenous (single obligatory host in the life cycle) parasite taxa than to heteroxenous (at least two hosts) taxa and (ii) directly exposed (ectoparasites) than indirectly exposed (endo-) parasites (Blanar et al., 2009). These findings conflict with the assumptions of (i) stronger effects on parasites with complex life cycles due to potential altered transmission in intermediate hosts and (ii) an amplifying effect of pollutant bioaccumulation from the host gastrointestinal tract. While meta-analyses unveil the general pattern among functional groups, some specific responses have been evidenced depending on parasite ecology, pollutant levels, and direct and indirect mechanisms (Sures et al., 2017). For instance, parasite diversity and biomass of helminth species in fish, were much lower in a historically contaminated site (Oros and Hanzelová, 2009) not because of changes in fish communities or ecotoxicological effects of pollutant sequestration but probably as a consequence of pollution-related decline of intermediate hosts.

This review aimed to identify whether environmental contamination can modulate the direction and strength of host-parasite interactions. We argue that two conditions must be met to elicit a transition from parasitism to mutualism: (i) pollutant sequestration by parasites should provide greater advantages for the host than the cost of infection (Figure 1) and (ii) pollutant levels should not be deleterious for both partners (and intermediate host) to avoid profound changes in host–parasite interactions. Reciprocal and complex relationships are expected among pollutants, parasites, and hosts (Figure 2). As previously discussed, transversal studies could lead to biased assessments because of confounding factors. Hence, longitudinal studies must be favored to evaluate the long-term consequences of pollution and parasitism on host health as well as the effect of pollution on parasites’ establishment and development. In addition, appropriate experimental approaches are required to confirm the causal relationship: a simultaneous manipulation of parasitism and chemical exposure would be an elegant design. In addition, endoscopic procedures could be used to conduct the long-term monitoring of intestinal parasites in hosts experimentally exposed to contaminants. This method has been recently developed for seabirds to monitor intestinal parasitic infections without sacrificing hosts (Carravieri et al., 2020). This approach would thus allow assessing impacts of experimentally increased pollutant exposure on the infection rate and the developmental rate of parasites, as well as on the joint effect of parasitism (at different levels) and pollution (at different levels) on host health.

At the population level, it would be crucial to compare the host infection status according to environmental pollution without sacrificing individuals. A non-lethal and non-invasive method is the use of urine DNA (uDNA, Duval et al., 2021), but it requires methodological developments to be extended to several parasite species. This opens new avenues for research on parasitism in host populations exposed to environmental contamination.

AG drafted the initial version of the manuscript. NM contributed to the revising of the manuscript. Both authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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