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Reciprocal relationships between behaviour and parasites suggest that negative feedback may drive flexibility in male reproductive behaviour.

ABSTRACT: Parasites are ubiquitous components of the environment that contribute to behavioural and life-history variation among hosts. Although it is well known that host behaviour can affect parasite infection risk and that parasites can alter host behaviour, the potential for dynamic feedback between these processes is poorly characterized. Using Grant's gazelle (Nanger granti) as a model, we tested for reciprocal effects of behaviour on parasites and parasites on behaviour to understand whether behaviour-parasite feedback could play a role in maintaining variation in male reproductive behaviour. Adult male gazelles either defend territories to attract mates or reside in bachelor groups. Territoriality is highly variable both within- and between-individuals, suggesting that territory maintenance is costly. Using a combination of longitudinal and experimental studies, we found that individual males transition frequently between territorial and bachelor reproductive status, and that elevated parasite burdens are a cost of territoriality. Moreover, among territorial males, parasites suppress aspects of behaviour related to territory maintenance and defence. These results suggest that territorial behaviour promotes the accumulation of parasites in males, and these parasites dampen the very behaviours required for territory maintenance. Our findings suggest that reciprocal feedback between host behaviour and parasitism could be a mechanism maintaining variation in male reproductive behaviour in the system.

SUBMITTER: Ezenwa VO

PROVIDER: S-EPMC4892797 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Reciprocal relationships between behaviour and parasites suggest that negative feedback may drive flexibility in male reproductive behaviour.

Ezenwa Vanessa O VO Snider Matthew H MH

Proceedings. Biological sciences 20160501 1831

Parasites are ubiquitous components of the environment that contribute to behavioural and life-history variation among hosts. Although it is well known that host behaviour can affect parasite infection risk and that parasites can alter host behaviour, the potential for dynamic feedback between these processes is poorly characterized. Using Grant's gazelle (Nanger granti) as a model, we tested for reciprocal effects of behaviour on parasites and parasites on behaviour to understand whether behavi ...[more]

PMID: 27194703

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Project description:BackgroundThe persistence of cooperative relationships is an evolutionary paradox; selection should favor those individuals that exploit their partners (cheating), resulting in the breakdown of cooperation over evolutionary time. Our current understanding of the evolutionary stability of mutualisms (cooperation between species) is strongly shaped by the view that they are often maintained by partners having mechanisms to avoid or retaliate against exploitation by cheaters. In contrast, we empirically and theoretically examine how additional symbionts, specifically specialized parasites, potentially influence the stability of bipartite mutualistic associations. In our empirical work we focus on the obligate mutualism between fungus-growing ants and the fungi they cultivate for food. This mutualism is exploited by specialized microfungal parasites (genus Escovopsis) that infect the ant's fungal gardens. Using sub-colonies of fungus-growing ants, we investigate the interactions between the fungus garden parasite and cooperative and experimentally-enforced uncooperative ("cheating") pairs of ants and fungi. To further examine if parasites have the potential to help stabilize some mutualisms we conduct Iterative Prisoner's Dilemma (IPD) simulations, a common framework for predicting the outcomes of cooperative/non-cooperative interactions, which incorporate parasitism as an additional factor.ResultsIn our empirical work employing sub-colonies of fungus-growing ants, we found that Escovopsis-infected sub-colonies composed of cheating populations of ants or fungi lost significantly more garden biomass than sub-colonies subjected to infection or cheating (ants or fungi) alone. Since the loss of fungus garden compromises the fitness of both mutualists, our findings suggest that the potential benefit received by the ants or fungi for cheating is outweighed by the increased concomitant cost of parasitism engendered by non-cooperation (cheating). IPD simulations support our empirical results by confirming that a purely cooperative strategy, which is unsuccessful in the classic IPD model, becomes stable when parasites are included.ConclusionHere we suggest, and provide evidence for, parasitism being an external force that has the potential to help stabilize cooperation by aligning the selfish interests of cooperative partners in opposition to a common enemy. Specifically, our empirical results and IPD simulations suggest that when two mutualists share a common enemy selection can favor cooperation over cheating, which may help explain the evolutionary stability of some mutualisms.

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Reciprocal relationships between behaviour and parasites suggest that negative feedback may drive flexibility in male reproductive behaviour.

Publications

Reciprocal relationships between behaviour and parasites suggest that negative feedback may drive flexibility in male reproductive behaviour.

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