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Division of labour promotes the spread of information in colony emigrations by the ant Temnothorax rugatulus.

ABSTRACT: The fitness of group-living animals often depends on how well members share information needed for collective decision-making. Theoretical studies have shown that collective choices can emerge in a homogeneous group of individuals following identical rules, but real animals show much evidence for heterogeneity in the degree and nature of their contribution to group decisions. In social insects, for example, the transmission and processing of information is influenced by a well-organized division of labour. Studies that accurately quantify how this behavioural heterogeneity affects the spread of information among group members are still lacking. In this paper, we look at nest choices during colony emigrations of the ant Temnothorax rugatulus and quantify the degree of behavioural heterogeneity of workers. Using clustering methods and network analysis, we identify and characterize four behavioural castes of workers-primary, secondary, passive and wandering-covering distinct roles in the spread of information during an emigration. This detailed characterization of the contribution of each worker can improve models of collective decision-making in this species and promises a deeper understanding of behavioural variation at the colony level.

SUBMITTER: Valentini G

PROVIDER: S-EPMC7209055 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Temnothorax rugatulus ant colonies consistently vary in nest structure across time and context.

Project description:A host of animals build architectural constructions. Such constructions frequently vary with environmental and individual/colony conditions, and their architecture directly influences behavior and fitness. The nests of ant colonies drive and enable many of their collective behaviors, and as such are part of their 'extended phenotype'. Since ant colonies have been recently shown to differ in behavior and life history strategy, we ask whether colonies differ in another trait: the architecture of the constructions they create. We allowed Temnothorax rugatulus rock ants, who create nests by building walls within narrow rock gaps, to repeatedly build nest walls in a fixed crevice but under two environmental conditions. We find that colonies consistently differ in their architecture across environments and over nest building events. Colony identity explained 12-40% of the variation in nest architecture, while colony properties and environmental conditions explained 5-20%, as indicated by the condition and marginal R2 values. When their nest boxes were covered, which produced higher humidity and lower airflow, colonies built thicker, longer, and heavier walls. Colonies also built more robust walls when they had more brood, suggesting a protective function of wall thickness. This is, to our knowledge, the first study to explicitly investigate the repeatability of nestbuilding behavior in a controlled environment. Our results suggest that colonies may face tradeoffs, perhaps between factors such as active vs. passive nest defense, and that selection may act on individual construction rules as a mechanisms to mediate colony-level behavior.

| S-EPMC5479500 | biostudies-literature

Histone acetylation regulates the expression of genes involved in worker reproduction in the ant Temnothorax rugatulus.

Project description:BackgroundIn insect societies, queens monopolize reproduction while workers perform tasks such as brood care or foraging. Queen loss leads to ovary development and lifespan extension in workers of many ant species. However, the underlying molecular mechanisms of this phenotypic plasticity remain unclear. Recent studies highlight the importance of epigenetics in regulating plastic traits in social insects. Thus, we investigated the role of histone acetylation in regulating worker reproduction in the ant Temnothorax rugatulus. We removed queens from their colonies to induce worker fecundity, and either fed workers with chemical inhibitors of histone acetylation (C646), deacetylation (TSA), or the solvent (DMSO) as control. We monitored worker number for six weeks after which we assessed ovary development and sequenced fat body mRNA.ResultsWorkers survived better in queenless colonies. They also developed their ovaries after queen removal in control colonies as expected, but not in colonies treated with the chemical inhibitors. Both inhibitors affected gene expression, although the inhibition of histone acetylation using C646 altered the expression of more genes with immunity, fecundity, and longevity functionalities. Interestingly, these C646-treated workers shared many upregulated genes with infertile workers from queenright colonies. We also identified one gene with antioxidant properties commonly downregulated in infertile workers from queenright colonies and both C646 and TSA-treated workers from queenless colonies.ConclusionOur results suggest that histone acetylation is involved in the molecular regulation of worker reproduction, and thus point to an important role of histone modifications in modulating phenotypic plasticity of life history traits in social insects.

| S-EPMC8642982 | biostudies-literature

Parallel vs. comparative evaluation of alternative options by colonies and individuals of the ant Temnothorax rugatulus.

Project description:Both a single ant and the colony to which it belongs can make decisions, but the underlying mechanisms may differ. Colonies are known to be less susceptible than lone ants to "choice overload", whereby decision quality deteriorates with increasing number of options. We probed the basis of this difference, using the model system of nest-site selection by the ant Temnothorax rugatulus. We tested the applicability of two competing models originally developed to explain information-processing mechanisms in vertebrates. The Tug of War model states that concurrent alternatives are directly compared, so that choosing between two alternatives takes longer than accepting a single one. In contrast, the Sequential Choice Model assumes that options are examined in parallel, and action takes place once any option reaches a decision criterion, so that adding more options shortens time to act. We found that single ants matched the Tug of War model while colonies fitted the Sequential Choice model. Our study shows that algorithmic models for decision-making can serve to investigate vastly different domains, from vertebrate individuals to both individuals and colonies of social insects.

| S-EPMC6109163 | biostudies-literature

Individual experience influences reconstruction of division of labour under colony disturbance in a queenless ant species.

Project description:BackgroundDivision of labour (DOL) is ubiquitous across biological hierarchies. In eusocial insects, DOL is often characterized by age-related task allocation, but workers can flexibly change their tasks, allowing for DOL reconstruction in fluctuating environments. Behavioural change driven by individual experience is regarded as a key to understanding this task flexibility. However, experimental evidence for the influence of individual experience is remains sparse. Here we tested the effect of individual experience on task choice in the queenless ponerine ant, Diacamma cf. indicum from Japan.ResultsWe confirmed that both nurses and foragers shifted to vacant tasks when the colony composition was biased to one or the other. We also found that nurses which are induced to forage readily revert to nursing when reintroduced into balanced colonies. In contrast, foragers which are induced to revert to nursing very rarely return to a foraging role, even 19 days post reintroduction to their original colony.ConclusionsTaken together, our results suggest that individual experience decreases the response threshold of original foragers, as they continue to be specialist nurses in a disturbed colony. However, original nurses do not appear strongly affected by having forager experience and revert to being nurses. Therefore, while individual experience does have an effect, other factors, such as reproductive ability, are clearly required to understand DOL maintenance in fluctuating environments.

| S-EPMC9202139 | biostudies-literature

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| PRJNA656927 | ENA

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Project description:Temnothorax rugatulus overview

| PRJNA606111 | ENA

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Project description:Effects of fertility and immune challenge on Temnothorax rugatulus gut bacterial communities

| PRJNA513968 | ENA

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Project description:Temnothorax rugatulus Raw sequence reads

| PRJNA955004 | ENA

How can ant queens live so long? Genes of multiple longevity pathways change expression with age in the ant Temnothorax rugatulus

Project description:Senescence is manifested by an increase in oxidative stress and a decline in biological functions with age. In most organisms, body maintenance is traded-off with reproduction. The negative relationship between longevity and fecundity is also evident on the molecular level, yet the proximate mechanisms remain poorly understood. Apparently by-passing this trade-off, social insect queens are both extremely long-lived (up to 30 years in some ants) and highly fecund compared to workers. Here, we study changes in gene expression with age and fecundity in queens to determine how the trade-off between those two traits is reshaped. We analyse tissue-specific gene expression in young founding queens and old, highly fecund queens of the ant Temnothorax rugatulus. More genes altered their expression with age in the fat body than in the brain. Despite strong differences in ovary development, few fecundity genes were differentially expressed. However, many longevity genes involved in well-known pathways or lifespan-associated biological processes changed their expression with age indicating that multiple longevity mechanisms are activated successively throughout a queens’ life. Young queens invested in immunity (i.e. activation of the Toll signalling pathway) and resistance against environmental and physiological stress associated with the founding phase (i.e. down regulation of the TOR pathway), while established older queens up-regulate anti-aging mechanisms (i.e. up-regulation of catalase, superoxide dismutase, heat shock 70 kDa proteins). Finally, we identified a number of candidate genes and pathways, potentially involved in reshaping the fertility-longevity trade-off in social insects, shedding light on how this is achieved on a proximate level.

2018-03-06 | GSE111415 | GEO

Colony size predicts division of labour in attine ants.

Project description:Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size-complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen-worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size-complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.

| S-EPMC4173680 | biostudies-literature

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