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Novel cooperative antipredator tactics of an ant specialized against a snake.

ABSTRACT: Eusocial insects can express surprisingly complex cooperative defence of the colony. Brood and reproductive castes typically remain in the nest and are protected by workers' various antipredator tactics against intruders. In Madagascar, a myrmicine ant, Aphaenogaster swammerdami, occurs sympatrically with a large blindsnake, Madatyphlops decorsei. As blindsnakes generally specialize on feeding on termites and ants brood by intruding into the nest, these snakes are presumably a serious predator on the ant. Conversely, a lamprophiid snake, Madagascarophis colubrinus, is considered to occur often in active A. swammerdami nests without being attacked. By presenting M. colubrinus, M. decorsei and a control snake, Thamnosophis lateralis, at the entrance of the nest, we observed two highly specialized interactions between ants and snakes: the acceptance of M. colubrinus into the nest and the cooperative evacuation of the brood from the nest for protection against the ant-eating M. decorsei. Given that M. colubrinus is one of the few known predators of blindsnakes in this area, A. swammerdami may protect their colonies against this blindsnake by two antipredator tactics, symbiosis with M. colubrinus and evacuation in response to intrusion by blindsnakes. These findings demonstrate that specialized predators can drive evolution of complex cooperative defence in eusocial species.

SUBMITTER: Jono T

PROVIDER: S-EPMC6731735 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Novel cooperative antipredator tactics of an ant specialized against a snake.

Jono Teppei T Kojima Yosuke Y Mizuno Takafumi T

Royal Society open science 20190814 8

Eusocial insects can express surprisingly complex cooperative defence of the colony. Brood and reproductive castes typically remain in the nest and are protected by workers' various antipredator tactics against intruders. In Madagascar, a myrmicine ant, <i>Aphaenogaster swammerdami</i>, occurs sympatrically with a large blindsnake, <i>Madatyphlops decorsei</i>. As blindsnakes generally specialize on feeding on termites and ants brood by intruding into the nest, these snakes are presumably a seri ...[more]

PMID: 31598235

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Project description:BACKGROUND: A compelling demonstration of adaptation by natural selection is the ability of parasites to manipulate host behavior. One dramatic example involves fungal species from the genus Ophiocordyceps that control their ant hosts by inducing a biting behavior. Intensive sampling across the globe of ants that died after being manipulated by Ophiocordyceps suggests that this phenomenon is highly species-specific. We advance our understanding of this system by reconstructing host manipulation by Ophiocordyceps parasites under controlled laboratory conditions and combining this with field observations of infection rates and a metabolomics survey. RESULTS: We report on a newly discovered species of Ophiocordyceps unilateralis sensu lato from North America that we use to address the species-specificity of Ophiocordyceps-induced manipulation of ant behavior. We show that the fungus can kill all ant species tested, but only manipulates the behavior of those it infects in nature. To investigate if this could be explained at the molecular level, we used ex vivo culturing assays to measure the metabolites that are secreted by the fungus to mediate fungus-ant tissue interactions. We show the fungus reacts heterogeneously to brains of different ant species by secreting a different array of metabolites. By determining which ion peaks are significantly enriched when the fungus is grown alongside brains of its naturally occurring host, we discovered candidate compounds that could be involved in behavioral manipulation by O. unilateralis s.l.. Two of these candidates are known to be involved in neurological diseases and cancer. CONCLUSIONS: The integrative work presented here shows that ant brain manipulation by O. unilateralis s.l. is species-specific seemingly because the fungus produces a specific array of compounds as a reaction to the presence of the host brain it has evolved to manipulate. These studies have resulted in the discovery of candidate compounds involved in establishing behavioral manipulation by this specialized fungus and therefore represent a major advancement towards an understanding of the molecular mechanisms underlying this phenomenon.

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Novel cooperative antipredator tactics of an ant specialized against a snake.

Publications

Novel cooperative antipredator tactics of an ant specialized against a snake.

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