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Octopamine and cooperation: octopamine regulates the disappearance of cooperative behaviours between genetically unrelated founding queens in the ant.

ABSTRACT: We investigated whether octopamine (OA) is associated with the disappearance of cooperation in Polyrhachis moesta ant queens. Queens of P. moesta facultatively found the colony with genetically unrelated queens. The founding queens perform frequent food exchange with these non-related queens and partake in cooperative brood rearing, whereas single colony queens exclude non-related queens via aggressive behaviour. Thus, aggression is a factor that reduces cooperation. Given that aggression is generally associated with brain OA in insects, we hypothesized that OA controls the behavioural change in cooperation in the ant queen, via an increase in aggression. To test this hypothesis, we compared the amounts of OA and related substances in the brain between founding and colony queens, and observed the interaction of founding queens following oral OA administration. The brain OA levels in colony queens were significantly higher than those in founding queens. Oral administration of OA to founding queens caused significantly less trophallaxis and allogrooming behaviour than in the control founding queens, but with no significant increase in aggression. These results suggest that OA promotes the disappearance of cooperation in founding queens of P. moesta. This is the first study to reveal the neuroendocrine mechanism of cooperation in ant queens.

SUBMITTER: Koyama S

PROVIDER: S-EPMC4528470 | biostudies-literature | 2015 Jun

REPOSITORIES: biostudies-literature

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Octopamine and cooperation: octopamine regulates the disappearance of cooperative behaviours between genetically unrelated founding queens in the ant.

Koyama Satoshi S Matsui Shingo S Satoh Toshiyuki T Sasaki Ken K

Biology letters 20150601 6

We investigated whether octopamine (OA) is associated with the disappearance of cooperation in Polyrhachis moesta ant queens. Queens of P. moesta facultatively found the colony with genetically unrelated queens. The founding queens perform frequent food exchange with these non-related queens and partake in cooperative brood rearing, whereas single colony queens exclude non-related queens via aggressive behaviour. Thus, aggression is a factor that reduces cooperation. Given that aggression is gen ...[more]

PMID: 26085498

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Project description:AbstractKey social traits, like queen number in eusocial insect colonies, have long been considered plastic, but the recent finding that colony social organization is under strict genetic control in multiple ant lineages challenges this view. This begs the question of which hardwired behavioral mechanism(s) generate alternative forms of social organization during colony development. We addressed this question in the Alpine silver ant, Formica selysi, a species with two social forms determined by a supergene. Queens that carry exclusively the M haplotype are produced by and live in monogyne (= single-queen) colonies, whereas queens that carry at least one copy of the P haplotype are produced by and live in polygyne (= multiple-queen) colonies. With extensive field samplings and laboratory experiments, we show that both types of queens successfully establish colonies independently, without being accompanied by workers, but that they do so in contrasting ways. Monogyne queens were generally intolerant of other queens and founded colonies solitarily, whereas polygyne queens were mutually attracted to each other and mainly founded colonies cooperatively. These associations persisted for months after worker emergence, suggesting that cooperative colony-founding leads to permanent multiple queening. Overall, our study shows that queens of each social form found colonies independently in the field but that P-carrying queens are more likely to cooperate, thereby contributing to perpetuate alternative forms of social organization.Significance statementUnderstanding the genetic and behavioral underpinnings of social organization is a major goal in evolutionary biology. Recent studies have shown that colony social organization is controlled by supergenes in multiple ant lineages. But the behavioral processes linking the genotype of a queen to the type of colony she will form remain largely unknown. Here, we show that in Alpine silver ants, alternative supergene genotypes are associated with different levels of social attraction and tolerance in young queens. These hardwired differences in social traits make queens carrying the P supergene haplotype more prone to cooperate and form durable associations during independent colony-founding. These findings help explain how genetic variants induce alternative forms of social organization during the ontogeny of a colony. They also illustrate how simple phenotypic differences at the individual level can result in large differences at higher levels of organization.Supplementary informationThe online version contains supplementary material available at 10.1007/s00265-021-03105-1.

Project description:One of the fundamental questions in biology is how cooperative and altruistic behaviors evolved. The majority of studies seeking to identify the genes regulating these behaviors have been performed in systems where behavioral and physiological differences are relatively fixed, such as in the honey bee. During colony founding in the monogyne (one queen per colony) social form of the fire ant Solenopsis invicta, newly-mated queens may start new colonies either individually (haplometrosis) or in groups (pleometrosis). However, only one queen (the "winner") in pleometrotic associations survives and takes the lead of the young colony while the others (the "losers") are executed. Thus, colony founding in fire ants provides an excellent system in which to examine the genes underpinning cooperative behavior and how the social environment shapes the expression of these genes. We developed a new whole genome microarray platform for S. invicta to characterize the gene expression patterns associated with colony founding behavior. First, we compared haplometrotic queens, pleometrotic winners and pleometrotic losers. Second, we manipulated pleometrotic couples in order to switch or maintain the social ranks of the two cofoundresses. Haplometrotic and pleometrotic queens differed in the expression of genes involved in stress response, aging, immunity, reproduction and lipid biosynthesis. Smaller sets of genes were differentially expressed between winners and losers. In the second experiment, switching social rank had a much greater impact on gene expression patterns than the initial/final rank. Expression differences for several candidate genes involved in key biological processes were confirmed using qRT-PCR. Our findings indicate that, in S. invicta, social environment plays a major role in the determination of the patterns of gene expression, while the queen's physiological state is secondary. These results highlight the powerful influence of social environment on regulation of the genomic state, physiology and ultimately, social behavior of animals.

Dataset Information

Octopamine and cooperation: octopamine regulates the disappearance of cooperative behaviours between genetically unrelated founding queens in the ant.

Publications

Octopamine and cooperation: octopamine regulates the disappearance of cooperative behaviours between genetically unrelated founding queens in the ant.

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