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Context-dependent expression of the foraging gene in field colonies of ants: the interacting roles of age, environment and task.

ABSTRACT: Task allocation among social insect workers is an ideal framework for studying the molecular mechanisms underlying behavioural plasticity because workers of similar genotype adopt different behavioural phenotypes. Elegant laboratory studies have pioneered this effort, but field studies involving the genetic regulation of task allocation are rare. Here, we investigate the expression of the foraging gene in harvester ant workers from five age- and task-related groups in a natural population, and we experimentally test how exposure to light affects foraging expression in brood workers and foragers. Results from our field study show that the regulation of the foraging gene in harvester ants occurs at two time scales: levels of foraging mRNA are associated with ontogenetic changes over weeks in worker age, location and task, and there are significant daily oscillations in foraging expression in foragers. The temporal dissection of foraging expression reveals that gene expression changes in foragers occur across a scale of hours and the level of expression is predicted by activity rhythms: foragers have high levels of foraging mRNA during daylight hours when they are most active outside the nests. In the experimental study, we find complex interactions in foraging expression between task behaviour and light exposure. Oscillations occur in foragers following experimental exposure to 13 L : 11 D (LD) conditions, but not in brood workers under similar conditions. No significant differences were seen in foraging expression over time in either task in 24 h dark (DD) conditions. Interestingly, the expression of foraging in both undisturbed field and experimentally treated foragers is also significantly correlated with the expression of the circadian clock gene, cycle Our results provide evidence that the regulation of this gene is context-dependent and associated with both ontogenetic and daily behavioural plasticity in field colonies of harvester ants. Our results underscore the importance of assaying temporal patterns in behavioural gene expression and suggest that gene regulation is an integral mechanism associated with behavioural plasticity in harvester ants.

SUBMITTER: Ingram KK

PROVIDER: S-EPMC5013789 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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Context-dependent expression of the foraging gene in field colonies of ants: the interacting roles of age, environment and task.

Ingram Krista K KK Gordon Deborah M DM Friedman Daniel A DA Greene Michael M Kahler John J Peteru Swetha S

Proceedings. Biological sciences 20160801 1837

Task allocation among social insect workers is an ideal framework for studying the molecular mechanisms underlying behavioural plasticity because workers of similar genotype adopt different behavioural phenotypes. Elegant laboratory studies have pioneered this effort, but field studies involving the genetic regulation of task allocation are rare. Here, we investigate the expression of the foraging gene in harvester ant workers from five age- and task-related groups in a natural population, and w ...[more]

PMID: 27581876

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Project description:Variation in behaviour among group members often impacts collective outcomes. Individuals may vary both in the task that they perform and in the persistence with which they perform each task. Although both the distribution of individuals among tasks and differences among individuals in behavioural persistence can each impact collective behaviour, we do not know if and how they jointly affect collective outcomes. Here, we use a detailed computational model to examine the joint impact of colony-level distribution among tasks and behavioural persistence of individuals, specifically their fidelity to particular resource sites, on the collective trade-off between exploring for new resources and exploiting familiar ones. We developed an agent-based model of foraging honeybees, parametrized by data from five colonies, in which we simulated scouts, who search the environment for new resources, and individuals who are recruited by the scouts to the newly found resources, i.e. recruits. We varied the persistence of returning to a particular food source of both scouts and recruits and found that, for each value of persistence, there is a different optimal ratio of scouts to recruits that maximizes resource collection by the colony. Furthermore, changes to the persistence of scouts induced opposite effects from changes to the persistence of recruits on the collective foraging of the colony. The proportion of scouts that resulted in the most resources collected by the colony decreased as the persistence of recruits increased. However, this optimal proportion of scouts increased as the persistence of scouts increased. Thus, behavioural persistence and task participation can interact to impact a colony's collective behaviour in orthogonal directions. Our work provides new insights and generates new hypotheses into how variations in behaviour at both the individual and colony levels jointly impact the trade-off between exploring for new resources and exploiting familiar ones.

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.

Project description:Background. Foraging efficiency is critical in determining the success of organisms and may be affected by a range of factors, including resource distance and quality. For social insects such as ants, outcomes must be considered at the level of both the individual and the colony. It is important to understand whether anthropogenic disturbances, such as forestry, affect foraging loads, independent of effects on the quality and distribution of resources. We asked if ants harvest greater loads from more distant and higher quality resources, how individual efforts scale to the colony level, and whether worker loads are affected by stand age. Methods. First, we performed a fine-scale study examining the effect of distance and resource quality (tree diameter and species) on harvesting of honeydew by red wood ants, Formica aquilonia, in terms of crop load per worker ant and numbers of workers walking up and down each tree (ant activity) (study 1). Second, we modelled what the combination of load and worker number responses meant for colony-level foraging loads. Third, at a larger scale, we asked whether the relationship between worker load and resource quality and distance depended on stand age (study 2). Results. Study 1 revealed that seventy percent of ants descending trees carried honeydew, and the percentage of workers that were honeydew harvesters was not related to tree species or diameter, but increased weakly with distance. Distance positively affected load mass in both studies 1 and 2, while diameter had weak negative effects on load. Relationships between load and distance and diameter did not differ among stands of different ages. Our model showed that colony-level loads declined much more rapidly with distance for small diameter than large diameter trees. Discussion. We suggest that a negative relationship between diameter and honeydew load detected in study 1 might be a result of crowding on large diameter trees close to nests, while the increase in honeydew load with distance may result from resource depletion close to nests. At the colony level, our model suggests that very little honeydew was harvested from more distant trees if they were small, but that more distant larger trees continued to contribute substantially to colony harvest. Although forestry alters the activity and foraging success of red wood ants, study 2 showed that it does not alter the fundamental rules determining the allocation of foraging effort.

Dataset Information

Context-dependent expression of the foraging gene in field colonies of ants: the interacting roles of age, environment and task.

Publications

Context-dependent expression of the foraging gene in field colonies of ants: the interacting roles of age, environment and task.

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