Conflicts over host manipulation between different parasites and pathogens: Investigating the ecological and medical consequences

Abstract

When parasites have different interests in regard to how their host should behave this can result in a conflict over host manipulation, i.e. parasite induced changes in host behaviour that enhance parasite fitness. Such a conflict can result in the alteration, or even complete suppression, of one parasite's host manipulation. Many parasites, and probably also symbionts and commensals, have the ability to manipulate the behaviour of their host. Non‐manipulating parasites should also have an interest in host behaviour. Given the frequency of multiple parasite infections in nature, potential conflicts of interest over host behaviour and manipulation may be common. This review summarizes the evidence on how parasites can alter other parasite's host manipulation. Host manipulation can have important ecological and medical consequences. I speculate on how a conflict over host manipulation could alter these consequences and potentially offer a new avenue of research to ameliorate harmful consequences of host manipulation.

Behavior out of control: Experimental evolution of resistance to host manipulation

“…By contrast, host manipulation changed within a few generation in a similar experiment in which only the parasite was under selection (Hafer-Hahmann, 2019). It fits well, however, with previous speculations that rather than actually resisting host manipulation, hosts could alter their baseline behavior to counter and accommodate host manipulation by a very prevalent and co-evolved parasite, but resulting in a suboptimal phenotype in the absence of this parasite (Hafer, 2016;Read & Braithwaite, 2012;Weinersmith & Earley, 2016). In infected copepods, this altered level of activity was decreased by not yet infective parasites and increased by infective parasites.…”

“…In order to avoid being attacked by the perceived predator, copepods should reduce their activity following this "attack" (Benesh, 2010a;Hafer & Benesh, 2015;Hafer & Milinski, 2015, 2016Hammerschmidt et al, 2009). In order to avoid being attacked by the perceived predator, copepods should reduce their activity following this "attack" (Benesh, 2010a;Hafer & Benesh, 2015;Hafer & Milinski, 2015, 2016Hammerschmidt et al, 2009).…”

“…Copepod behavior was recorded using a device that dropped the plate with copepods by about 3mm in a standardized manner to simulate a predator attack. In order to avoid being attacked by the perceived predator, copepods should reduce their activity following this "attack" (Benesh, 2010a;Hafer & Benesh, 2015;Hafer & Milinski, 2015, 2016Hammerschmidt et al, 2009). At the beginning of each trial, I placed a plate on the apparatus, let it rest for one minute and then dropped it.…”

Viral infections in fire ants lead to reduced foraging activity and dietary changes

“…Both allo-grooming and secretion of antibiotic compounds are two often cited examples reported in social insects 1 – 4 . Conversely, some pathogens have been reported to alter host behavior to favor their own transmission and enhance their replication and virulence 5 . Studies of non-social insects have reported reduced feeding (anorexia) and changes in dietary macronutrient preference in pathogen-challenged individuals, both of which are associated with an enhanced ability to cope with pathogen infections likely via starvation of resident pathogens from essential macronutrients or trade-offs in energy allocation 6 .…”

Adaptive parasitic manipulation as exemplified by acanthocephalans

“…In contrast, it is more difficult to assess how benefits and costs are traded off against each other. Costs entails energetic effort of the parasite, final host resistance to manipulation (Mazzi & Bakker, 2003; see previous section), intermediate host mortality (Mazzi & Bakker, 2003), conflict over manipulation when infected with different parasite stages of the same species or different parasite species with contrasting interests (Hafer, 2016;Hafer & Milinski, 2015, or transmission to dead-end hosts (e.g., Poulin et al, 2005). Milinski (1990) distinguishes two ways in which parasites can influence host's decision-making.…”