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Species-specific ant brain manipulation by a specialized fungal parasite.
BMC Evol Biol. 2014 Aug 29; 14:166.BE

Abstract

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.

Authors

No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

25085339

Citation

de Bekker, Charissa, et al. "Species-specific Ant Brain Manipulation By a Specialized Fungal Parasite." BMC Evolutionary Biology, vol. 14, 2014, p. 166.
de Bekker C, Quevillon LE, Smith PB, et al. Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evol Biol. 2014;14:166.
de Bekker, C., Quevillon, L. E., Smith, P. B., Fleming, K. R., Ghosh, D., Patterson, A. D., & Hughes, D. P. (2014). Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evolutionary Biology, 14, 166. https://doi.org/10.1186/s12862-014-0166-3
de Bekker C, et al. Species-specific Ant Brain Manipulation By a Specialized Fungal Parasite. BMC Evol Biol. 2014 Aug 29;14:166. PubMed PMID: 25085339.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Species-specific ant brain manipulation by a specialized fungal parasite. AU - de Bekker,Charissa, AU - Quevillon,Lauren E, AU - Smith,Philip B, AU - Fleming,Kimberly R, AU - Ghosh,Debashis, AU - Patterson,Andrew D, AU - Hughes,David P, Y1 - 2014/08/29/ PY - 2014/07/16/received PY - 2014/07/18/accepted PY - 2014/8/3/entrez PY - 2014/8/3/pubmed PY - 2014/12/17/medline SP - 166 EP - 166 JF - BMC evolutionary biology JO - BMC Evol. Biol. VL - 14 N2 - 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. SN - 1471-2148 UR - https://www.unboundmedicine.com/medline/citation/25085339/Species_specific_ant_brain_manipulation_by_a_specialized_fungal_parasite_ L2 - https://bmcevolbiol.biomedcentral.com/articles/10.1186/s12862-014-0166-3 DB - PRIME DP - Unbound Medicine ER -