Insect societies fight back: the evolution of defensive traits against social parasites

Grüter, Christoph; Jongepier, Evelien; Foitzik, Susanne

doi:10.1098/rstb.2017.0200

Cited by 38 publications

(34 citation statements)

References 137 publications

(186 reference statements)

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“…Larvae consumed social parasite eggs at a significantly higher rate than those of non-parasites. This suggests that larvae participate in post-infection defence by selectively removing parasite eggs, thus acting as a second line of defence, and potentially improving colony survival [17,[24][25][26]57]. Earlier studies have shown, that while workers of social insect hosts destroy social parasite eggs [24][25][26]29,58,59], workers of many ant species forgo discrimination between nest-mate and non-nest-mate eggs [60][61][62][63].…”

Section: Discussionmentioning

confidence: 99%

The possible role of ant larvae in the defence against social parasites

et al. 2019

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Temporary social parasite ant queens initiate new colonies by entering colonies of host species, where they begin laying eggs. As the resident queen can be killed during this process, host colonies may lose their entire future reproductive output. Selection thus favours the evolution of defence mechanisms, before and after parasite intrusion. Most studies on social parasites focus on host worker discrimination of parasite queens and their offspring. However, ant larvae can also influence brood composition by consuming eggs. This raises the question whether host larvae can aid in preventing colony takeover by consuming eggs laid by parasite queens. To test whether larvae could play a role in anti-parasite defence, we compared the rates at which larvae of a common host species, Formica fusca , consumed eggs laid by social parasite, non-parasite, nest-mate, or conspecific non-nest-mate queens. Larvae consumed social parasite eggs more than eggs laid by a heterospecific non-parasite queen, irrespective of the chemical distance between the egg cuticular profiles. Also, larvae consumed eggs laid by conspecific non-nest-mate queens more than those laid by nest-mate queens. Our study suggests that larvae may act as players in colony defence against social parasitism, and that social parasitism is a key factor shaping discrimination behaviour in ants.

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Section: Discussionmentioning

confidence: 99%

The possible role of ant larvae in the defence against social parasites

et al. 2019

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“…Some of the best experimental models of parasite avoidance behaviour may be the social insects, which are also some of the most strategic fighters when it comes to combatting social parasites. In their review, Grü ter et al [30] show the different defence traits that social insects such as ants, termites, social wasps and bees have evolved to interrupt the entry and establishment of parasites into the colony. These strategies involve several steps; firstly, the avoidance of contacting parasites or being detected by them (e.g.…”

Section: (A) Strategiesmentioning

confidence: 99%

Evolution of pathogen and parasite avoidance behaviours

Sarabian

Curtis

McMullan

2018

Phil. Trans. R. Soc. B

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All free-living animals are subject to intense selection pressure from parasites and pathogens resulting in behavioural adaptations that can help potential hosts to avoid falling prey to parasites. This special issue on the evolution of parasite avoidance behaviour was compiled following a Royal Society meeting in 2017. Here we have assembled contributions from a wide range of disciplines including genetics, ecology, parasitology, behavioural science, ecology, psychology and epidemiology on the disease avoidance behaviour of a wide range of species. Taking an interdisciplinary and cross-species perspective allows us to sketch out the strategies, mechanisms and consequences of parasite avoidance and to identify gaps and further questions. Parasite avoidance strategies must include avoiding parasites themselves and cues to their presence in conspecifics, heterospecifics, foods and habitat. Further, parasite avoidance behaviour can be directed at constructing parasite-retardant niches. Mechanisms of parasite avoidance behaviour are generally less well characterized, though nematodes, rodents and human studies are beginning to elucidate the genetic, hormonal and neural architecture that allows animals to recognize and respond to cues of parasite threat. While the consequences of infection are well characterized in humans, we still have much to learn about the epidemiology of parasites of other species, as well as the trade-offs that hosts make in parasite defence versus other beneficial investments like mating and foraging. Finally, in this overview we conclude that it is legitimate to use the word disgust' to describe parasite avoidance systems, in the same way that 'fear' is used to describe animal predator avoidance systems. Understanding disgust across species offers an excellent system for investigating the strategies, mechanisms and consequences of behaviour and could be a vital contribution towards the understanding and conservation of our planet's ecosystems.This article is part of the Theo Murphy meeting issue 'Evolution of pathogen and parasite avoidance behaviours'.

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“…I do not discuss the strategies of parasites that take direct control of the host's muscles (as it has been suggested in the case of the antinfecting fungus Ophiocordyceps unilateralis; Fredericksen et al 2017); target sensory receptors; and indirectly affect behavior by depleting energetic reserves, castrating/sterilizing the host, or altering sex determination (see Adamo 2012;Lafferty and Shaw 2013). Also excluded is manipulation through sensory cues and signals, as practiced by brood parasites in birds (e.g., cuckoos; Langmore and Spottiswoode 2012) and social parasites in insects (e.g., beetles that parasitize ant colonies; Grüter et al 2018). Before addressing specific mechanisms, however, it is useful to briefly consider the functions of manipulation from the perspective of parasites.…”

Section: Hijacking the Brain: Parasitementioning

confidence: 99%

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

Giudice¹

2019

The Quarterly Review of Biology

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keywords behavior, brain evolution, hormones, neurobiology, parasite-host interactions, parasite manipulation abstract The ability of parasites to manipulate host behavior to their advantage has been studied extensively, but the impact of parasite manipulation on the evolution of neural and endocrine mechanisms has remained virtually unexplored. If selection for countermeasures has shaped the evolution of nervous systems, many aspects of neural functioning are likely to remain poorly understood until parasites-the brain's invisible designers-are included in the picture. This article offers the first systematic discussion of brain evolution in light of parasite manipulation. After reviewing the strategies and mechanisms employed by parasites, the paper presents a taxonomy of host countermeasures with four main categories, namely: restrict access to the brain; increase the costs of manipulation; increase the complexity of signals; and increase robustness. For each category, possible examples of countermeasures are explored, and the likely evolutionary responses by parasites are considered. The article then discusses the metabolic, computational, and ecological constraints that limit the evolution of countermeasures. The final sections offer suggestions for future research and consider some implications for basic neuroscience and psychopharmacology. The paper aims to present a novel perspective on brain evolution, chart a provisional way forward, and stimulate research across the relevant disciplines.

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Insect societies fight back: the evolution of defensive traits against social parasites

Cited by 38 publications

References 137 publications

The possible role of ant larvae in the defence against social parasites

The possible role of ant larvae in the defence against social parasites

Evolution of pathogen and parasite avoidance behaviours

Invisible Designers: Brain Evolution Through the Lens of Parasite Manipulation

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