Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Abstract

Interest in how parasites shape host behaviour has increased dramatically in recent years. The main focus of behavioural ecologists has been on the negative effects of parasites on host behaviour. However, there are instances in which infected hosts express more adaptive behavioural phenotypes and have higher fitness relative to uninfected hosts, suggesting that it is sometimes beneficial to be parasitized. For example, hosts can exhibit evolved dependence, wherein the host coevolves with and comes to depend on parasites for the expression of adaptive host behaviours. Additionally, 'conditionally helpful parasites' modify the host phenotype in ways that benefit the host under particular conditions. These scenarios have been explored in the context of bacterial or fungal symbionts, but have been relatively unstudied with regard to metazoan parasites (e.g. trematodes, acanthocephalans, nematodes and cestodes). We explore how these scenarios apply to hosts infected by metazoan parasites, and consider implications for research in behavioural ecology. We examine conditions under which infection should result in more adaptive host behavioural phenotypes, and the implications for host fitness and evolution. We then discuss the implications of conditionally helpful parasites and parasites for which hosts have evolved dependence for laboratory studies of host behaviour and for conservation and reintroduction programmes.

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.…”

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

“…There is evidence that, in the early phase of the infection, spinyheaded worms protect their gammarid hosts by making them less susceptible to predation (Dianne et al 2011). Other conditionally helpful parasites may increase their host's mating success or help prevent infections by other and potentially more harmful parasites (see Fellous and Salvaudon 2009;Weinersmith and Earley 2016). The net effect on the host's fitness is still likely to be negative in most cases, but may turn positive if ecological conditions put a premium on the specific phenotype induced by the parasite.…”

“…The net effect on the host's fitness is still likely to be negative in most cases, but may turn positive if ecological conditions put a premium on the specific phenotype induced by the parasite. For example, heightened antipredator behaviors may provide a net benefit if predation risk is especially severe; enhanced immunity from other parasites may be a crucial advantage under high pathogen threat (see Weinersmith and Earley 2016).…”

“…Negative feedback is a basic building block of robust systems; it is also a general purpose strategy with little functional specificity. More sophisticated forms of reactive robustness can be implemented by specialized mechanisms designed to detect manipulation attempts and respond in flexible, strategic ways (see Weinersmith and Earley 2016;Massey and Mishra 2018). The first question to ask is: How can the brain detect a manipulation attempt?…”

“…Some apparently "paradoxical" effects-e.g., increasing dopamine makes rats more fearful rather than less-are consistent with the existence of compensatory mechanisms that get triggered by sudden, anomalous changes in brain biochemistry. What I am suggesting is that those mechanisms may be more than general purpose homeostatic devices (e.g., Adamo 2013); instead, some of their features may be specifically designed to detect and respond to parasite intrusions (for a similar argument see Weinersmith and Earley 2016).…”