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Regulation of harvester ant foraging as a closed-loop excitable system.

ABSTRACT: Ant colonies regulate activity in response to changing conditions without using centralized control. Desert harvester ant colonies forage for seeds, and regulate foraging to manage a tradeoff between spending and obtaining water. Foragers lose water while outside in the dry air, but ants obtain water by metabolizing the fats in the seeds they eat. Previous work shows that the rate at which an outgoing forager leaves the nest depends on its recent rate of brief antennal contacts with incoming foragers carrying food. We examine how this process can yield foraging rates that are robust to uncertainty and responsive to temperature and humidity across minute-to-hour timescales. To explore possible mechanisms, we develop a low-dimensional analytical model with a small number of parameters that captures observed foraging behavior. The model uses excitability dynamics to represent response to interactions inside the nest and a random delay distribution to represent foraging time outside the nest. We show how feedback from outgoing foragers returning to the nest stabilizes the incoming and outgoing foraging rates to a common value determined by the volatility of available foragers. The model exhibits a critical volatility above which there is sustained foraging at a constant rate and below which foraging stops. To explain how foraging rates adjust to temperature and humidity, we propose that foragers modify their volatility after they leave the nest and become exposed to the environment. Our study highlights the importance of feedback in the regulation of foraging activity and shows how modulation of volatility can explain how foraging activity responds to conditions and varies across colonies. Our model elucidates the role of feedback across many timescales in collective behavior, and may be generalized to other systems driven by excitable dynamics, such as neuronal networks.

SUBMITTER: Pagliara R

PROVIDER: S-EPMC6294393 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Regulation of harvester ant foraging as a closed-loop excitable system.

Pagliara Renato R Gordon Deborah M DM Leonard Naomi Ehrich NE

PLoS computational biology 20181204 12

Ant colonies regulate activity in response to changing conditions without using centralized control. Desert harvester ant colonies forage for seeds, and regulate foraging to manage a tradeoff between spending and obtaining water. Foragers lose water while outside in the dry air, but ants obtain water by metabolizing the fats in the seeds they eat. Previous work shows that the rate at which an outgoing forager leaves the nest depends on its recent rate of brief antennal contacts with incoming for ...[more]

PMID: 30513076

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Project description:BackgroundThe division of labor in social insect colonies involves transitions by workers from one task to another and is critical to the organization and ecological success of colonies. The differential regulation of genetic pathways is likely to be a key mechanism involved in plasticity of social insect task behavior. One of the few pathways implicated in social organization involves the cGMP-activated protein kinase gene, foraging, a gene associated with foraging behavior in social insect species. The association of the foraging gene with behavior is conserved across diverse species, but the observed expression patterns and proposed functions of this gene vary across taxa. We compared the protein sequence of foraging across social insects and explored whether the differential regulation of this gene is associated with task behaviors in the harvester ant, Pogonomyrmex occidentalis.ResultsPhylogenetic analysis of the coding region of the foraging gene reveals considerable conservation in protein sequence across insects, particularly among hymenopteran species. The absence of amino acid variation in key active and binding sites suggests that differences in behaviors associated with this gene among species may be the result of changes in gene expression rather than gene divergence. Using real time qPCR analyses with a harvester ant ortholog to foraging (Pofor), we found that the brains of harvester ant foragers have a daily fluctuation in expression of foraging with mRNA levels peaking at midday. In contrast, young workers inside the nest have low levels of Pofor mRNA with no evidence of daily fluctuations in expression. As a result, the association of foraging expression with task behavior within a species changes depending on the time of day the individuals are sampled.ConclusionsThe amino acid protein sequence of foraging is highly conserved across social insects. Differences in foraging behaviors associated with this gene among social insect species are likely due to differences in gene regulation rather than evolutionary changes in the encoded protein. The task-specific expression patterns of foraging are consistent with the task-specific circadian rhythms observed in harvester ants. Whether the molecular clock plays a role in regulating foraging gene expression (or vice versa) remains to be determined. Our results represent the first time series analysis of foraging gene expression and underscore the importance of assaying time-related expression differences in behavioral studies. Understanding how this gene is regulated within species is critical to explaining the mechanism by which foraging influences behavior.

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Regulation of harvester ant foraging as a closed-loop excitable system.

Publications

Regulation of harvester ant foraging as a closed-loop excitable system.

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