Parasites: evolution’s neurobiologists

Adamo, Shelley A.

doi:10.1242/jeb.073601

Cited by 148 publications

(191 citation statements)

References 89 publications

(134 reference statements)

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“…"Fatal attraction" has been observed for mammalian hosts that carry the protozoon Toxoplasma gondii: infected mammals enhance their exposure to feline predators, infected males become sexually more attractive to healthy females, and men with latent toxoplasmosis become more risk-taking and aggressive (Poulin, 2010;Hari Dass et al, 2011;Adamo, 2013;Flegr, 2013a;Weinersmith and Faulkes, 2014;Poirotte et al, 2016).…”

Section: "Fatal Attraction" and Manipulating Parasitesmentioning

confidence: 99%

“…Moreover, parasites with a horizontal mode of transmission typically enhance not only aggression, but also other forms of physical contact among the members of their host population (Klein, 2005). In summary, parasites can alter host sexual behavior, including the frequency of mating and the level of promiscuity, and potential molecular mechanisms for this type of manipulation have been described (Klein, 2003;Adamo, 2013Adamo, , 2014. Nevertheless, it seems safe to conclude that STDs are underrepresented in the literature on manipulating parasites.…”

Section: Host Manipulation By Stds-rarely Evolved or Rarely Studied?mentioning

confidence: 99%

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Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Heil

2016

Front. Ecol. Evol.

109

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Parasites must overcome host immunity and change hosts for dispersal. Therefore, seemingly odd behaviors of parasitized animals, like those exhibited by "Zombie ants" or the "fatal attraction" of mammals to their predators, have been explained as the extended phenotype of parasites that manipulate their hosts for transmission enhancement. Manipulation has evolved in all major phylogenetic lineages of parasites but is not ubiquitous. In fact, the real frequency and relevance of manipulation is still matter of debate. Here, I highlight some of the most pertinent questions that arise if we aim at a broader understanding of the ecological relevance and evolutionary trajectory of manipulating parasites. Why are more parasites with a trophic mode of transmission manipulating their host than horizontally transmitted parasites? Why are the causal agents of sexually transmitted diseases (STDs) so rarely reported to manipulate their host? Why do parasites of animals usually manipulate their intermediate host, whereas many pathogens of plants manipulate their final host and then cause a "fatal attraction" of herbivores to the already infected plant? How can we distinguish manipulation effects from adaptive host responses to parasitization? Does manipulation cause a cost to certain parasites that can select against the evolution of manipulation? More emphasis should be put on direct comparisons among parasites of animals, plants, and humans. Manipulation for transmission enhancement should be studied in concert with manipulation for host immunity suppression, the molecular mechanisms that control the manipulation effect need to be deciphered, and we should test for alternative explanations for the observed phenotypic changes. Finally, we should quantify transmission rates and net fitness for manipulating and non-manipulating parasites, in ecologically realistic setups, to identify the forces that select against the evolution of manipulation. Ultimately, parasite net fitness represents the relevant outcome of any manipulation effect.Keywords: immunity, malaria, partner manipulation, pathogen, plant-enemy interaction, STDs, toxoplasmosis "FATAL ATTRACTION" AND MANIPULATING PARASITES Parasites represent a ubiquitous aspect in the life of multicellular organisms (Wood and Johnson, 2015) and most, if not all, of us have experienced how strongly an infection can interfere with our normal activities and well-being. Therefore, it might not appear to be too surprising when parasitized hosts exhibit behavioral alterations (see Glossary) as compared to healthy conspecifics.

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Section: "Fatal Attraction" and Manipulating Parasitesmentioning

confidence: 99%

Section: Host Manipulation By Stds-rarely Evolved or Rarely Studied?mentioning

confidence: 99%

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

Heil

2016

Front. Ecol. Evol.

109

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“…proximate mechanisms [10]), it is less well understood how the altered phenotypes of infected hosts affect other social group members. For instance, parasite infections in social insects change their hosts' chemical signature (e.g.…”

Section: Introductionmentioning

confidence: 99%

The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host

Beros¹,

Jongepier²,

Hagemeier³

et al. 2015

Proc. R. Soc. B.

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Parasites can induce alterations in host phenotypes in order to enhance their own survival and transmission. Parasites of social insects might not only benefit from altering their individual hosts, but also from inducing changes in uninfected group members. Temnothorax nylanderi ant workers infected with the tapeworm Anomotaenia brevis are known to be chemically distinct from nest-mates and do not contribute to colony fitness, but are tolerated in their colonies and well cared for. Here, we investigated how tapeworminfected workers affect colony aggression by manipulating their presence in ant colonies and analysing whether their absence or presence resulted in behavioural alterations in their nest-mates. We report a parasite-induced shift in colony aggression, shown by lower aggression of uninfected nest-mates from parasitized colonies towards conspecifics, potentially explaining the tolerance towards infected ants. We also demonstrate that tapeworm-infected workers showed a reduced flight response and higher survival, while their presence caused a decrease in survival of uninfected nest-mates. This anomalous behaviour of infected ants, coupled with their increased survival, could facilitate the parasites' transmission to its definitive hosts, woodpeckers. We conclude that parasites exploiting individuals that are part of a society not only induce phenotypic changes within their individual hosts, but in uninfected group members as well.

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“…For example, behaviour-parasite feedbacks (discussed below) are often mediated by effects of parasites on host hormone levels [41,42] and, in some cases, appear to involve adaptive parasite manipulation of host neuroendocrine pathways [43,44]. Progress in understanding feedbacks between behaviour and multiple, interacting components of the overall neuroendocrine system should be invaluable for better understanding personalities.…”

mentioning

confidence: 99%