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Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus).

ABSTRACT: Social insects use odors as cues for a variety of behavioral responses, including nestmate recognition. Past research on nestmate recognition indicates cuticular hydrocarbons are important nestmate discriminators for social insects, but other factors are likely to contribute to colony-specific odors. Here we experimentally tested whether external microbes contribute to nestmate recognition in red harvester ants (Pogonomyrmex barbatus). We changed the external microbiome of ants through topical application of either antibiotics or microbial cultures. We then observed behavior of nestmates when treated ants were returned to the nest. Ants whose external microbiome was augmented with microbial cultures were much more likely to be rejected than controls, but ants treated with antibiotics were not. This result is consistent with the possibility that external microbes are used for nestmate recognition.

SUBMITTER: Dosmann A

PROVIDER: S-EPMC4741111 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus).

Dosmann Andy A Bahet Nassim N Gordon Deborah M DM

PeerJ 20160125

Social insects use odors as cues for a variety of behavioral responses, including nestmate recognition. Past research on nestmate recognition indicates cuticular hydrocarbons are important nestmate discriminators for social insects, but other factors are likely to contribute to colony-specific odors. Here we experimentally tested whether external microbes contribute to nestmate recognition in red harvester ants (Pogonomyrmex barbatus). We changed the external microbiome of ants through topical a ...[more]

PMID: 26855857

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Project description:The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker division of labor. Support for this hypothesis in honeybees is provided by studies demonstrating that the reproductive potential of workers, assessed by the levels of vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honeybees that have a single Vg ortholog and potentially fertile nurses, the genome of the harvester ant Pogonomyrmex barbatus harbors two Vg genes (Pb_Vg1 and Pb_Vg2) and nurses produce infertile trophic eggs. P. barbatus, thus, provides a unique model to investigate whether Vg duplication in ants was followed by subfunctionalization to acquire reproductive and non-reproductive functions and whether Vg reproductive function was co-opted to regulate behavior in sterile workers. To investigate these questions, we compared the expression patterns of P. barbatus Vg genes and analyzed the phylogenetic relationships and molecular evolution of Vg genes in ants. qRT-PCRs revealed that Pb_Vg1 is more highly expressed in queens compared to workers and in nurses compared to foragers. By contrast, the level of expression of Pb_Vg2 was higher in foragers than in nurses and queens. Phylogenetic analyses show that a first duplication of the ancestral Vg gene occurred after the divergence between the poneroid and formicoid clades and subsequent duplications occurred in the lineages leading to Solenopsis invicta, Linepithema humile and Acromyrmex echinatior. The initial duplication resulted in two Vg gene subfamilies preferentially expressed in queens and nurses (subfamily A) or in foraging workers (subfamily B). Finally, molecular evolution analyses show that the subfamily A experienced positive selection, while the subfamily B showed overall relaxation of purifying selection. Our results suggest that in P. barbatus the Vg gene underwent subfunctionalization after duplication to acquire caste- and behavior- specific expression associated with reproductive and non-reproductive functions, supporting the validity of the RGPH in ants.

Project description:BackgroundRecent advances in sociogenomics allow for comparative analyses of molecular mechanisms regulating the development of social behavior. In eusocial insects, one key aspect of their sociality, the division of labor, has received the most attention. Age-related polyethism, a derived form of division of labor in ants and bees where colony tasks are allocated among distinct behavioral phenotypes, has traditionally been assumed to be a product of convergent evolution. Previous work has shown that the circadian clock is associated with the development of behavior and division of labor in honeybee societies. We cloned the ortholog of the clock gene, period, from a harvester ant (Pogonomyrmex occidentalis) and examined circadian rhythms and daily activity patterns in a species that represents an evolutionary origin of eusociality independent of the honeybee.ResultsUsing real time qPCR analyses, we determined that harvester ants have a daily cyclic expression of period and this rhythm is endogenous (free-running under dark-dark conditions). Cyclic expression of period is task-specific; foragers have strong daily fluctuations but nest workers inside the nest do not. These patterns correspond to differences in behavior as activity levels of foragers show a diurnal pattern while nest workers tend to exhibit continuous locomotor activity at lower levels. In addition, we found that foragers collected in the early fall (relative warm, long days) exhibit a delay in the nightly peak of period expression relative to foragers collected in the early spring (relative cold, short days).ConclusionThe association of period mRNA expression levels with harvester ant task behaviors suggests that the development of circadian rhythms is associated with the behavioral development of ants. Thus, the circadian clock pathway may represent a conserved 'genetic toolkit' that has facilitated the parallel evolution of age-related polyethism and task allocation in social insects.

Dataset Information

Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus).

Publications

Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus).

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