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Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns.

Mikheyev AS, Linksvayer TA - Elife (2015)

Bottom Line: To begin to reconcile these perspectives, we studied how the evolutionary conservation of genes associated with social behavior depends on regulatory context, and whether genes associated with social behavior exist in distinct regulatory and evolutionary contexts.However, compared to the rest of the genome, forager-upregulated genes were much more highly connected and conserved, while nurse-upregulated genes were less connected and more evolutionarily labile.Our results indicate that the genetic architecture of social behavior includes both highly connected and conserved components as well as loosely connected and evolutionarily labile components.

View Article: PubMed Central - PubMed

Affiliation: Ecology and Evolution Unit, Okinawa Institute of Science and Technology, Okinawa, Japan.

ABSTRACT
Studies of the genetic basis and evolution of complex social behavior emphasize either conserved or novel genes. To begin to reconcile these perspectives, we studied how the evolutionary conservation of genes associated with social behavior depends on regulatory context, and whether genes associated with social behavior exist in distinct regulatory and evolutionary contexts. We identified modules of co-expressed genes associated with age-based division of labor between nurses and foragers in the ant Monomorium pharaonis, and we studied the relationship between molecular evolution, connectivity, and expression. Highly connected and expressed genes were more evolutionarily conserved, as expected. However, compared to the rest of the genome, forager-upregulated genes were much more highly connected and conserved, while nurse-upregulated genes were less connected and more evolutionarily labile. Our results indicate that the genetic architecture of social behavior includes both highly connected and conserved components as well as loosely connected and evolutionarily labile components.

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The location of age-marked workers also changed as the workers aged,from the nest area over the brood to outside the nest.Boxplots show the distribution of age with the mean and sample size foreach category.DOI:http://dx.doi.org/10.7554/eLife.04775.005
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fig1s2: The location of age-marked workers also changed as the workers aged,from the nest area over the brood to outside the nest.Boxplots show the distribution of age with the mean and sample size foreach category.DOI:http://dx.doi.org/10.7554/eLife.04775.005

Mentions: We tracked cohorts of age-marked workers and recorded their behavior and locationinside and outside the nest. In order to identify differentially expressed genesassociated with age-based division of labor, we collected age-marked workers andworkers observed performing specific behaviors. The observed location of workers fromdifferent age classes changed with both nest location and behavior (glm withquasipoisson errors and log link, both p < 0.01) (Figure 1, Figure1—figure supplements 1, 2). In concordance with the expected patternof age polyethism, the average age of workers observed in the different locationsincreased as distance from the brood area increased (Figure 1—figure supplement 2). Of the 15 behaviorsobserved more than 15 total times (Supplementary file 1), the likelihood of observing workersperforming the behaviors ‘nurse’, ‘groom’,‘rest’, ‘trophallaxis’, ‘walk’, and‘forage’ depended on worker age (Figure1A; glm with binomial errors and logit link, all nominal p < 0.0002,α = 0.003, controlling for multiple testing). Nursing and foraging wereat the two extremes: the average age of workers observed nursing was 6.94 days andthe average age of workers observed foraging (i.e., in the act of collecting food)was 13.04 days. There appeared to be a marked transition from nursing to foragingbetween 9 and 12 days of age (Figure 1A), with75% of nursing observations made for workers less than 10 days old and 75% offoraging observations made for workers over 10 days old (Figure 1—figure supplement 1).10.7554/eLife.04775.003Figure 1.Behavioral and transcriptional changes associated with worker age andbehavior.


Genes associated with ant social behavior show distinct transcriptional and evolutionary patterns.

Mikheyev AS, Linksvayer TA - Elife (2015)

The location of age-marked workers also changed as the workers aged,from the nest area over the brood to outside the nest.Boxplots show the distribution of age with the mean and sample size foreach category.DOI:http://dx.doi.org/10.7554/eLife.04775.005
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383337&req=5

fig1s2: The location of age-marked workers also changed as the workers aged,from the nest area over the brood to outside the nest.Boxplots show the distribution of age with the mean and sample size foreach category.DOI:http://dx.doi.org/10.7554/eLife.04775.005
Mentions: We tracked cohorts of age-marked workers and recorded their behavior and locationinside and outside the nest. In order to identify differentially expressed genesassociated with age-based division of labor, we collected age-marked workers andworkers observed performing specific behaviors. The observed location of workers fromdifferent age classes changed with both nest location and behavior (glm withquasipoisson errors and log link, both p < 0.01) (Figure 1, Figure1—figure supplements 1, 2). In concordance with the expected patternof age polyethism, the average age of workers observed in the different locationsincreased as distance from the brood area increased (Figure 1—figure supplement 2). Of the 15 behaviorsobserved more than 15 total times (Supplementary file 1), the likelihood of observing workersperforming the behaviors ‘nurse’, ‘groom’,‘rest’, ‘trophallaxis’, ‘walk’, and‘forage’ depended on worker age (Figure1A; glm with binomial errors and logit link, all nominal p < 0.0002,α = 0.003, controlling for multiple testing). Nursing and foraging wereat the two extremes: the average age of workers observed nursing was 6.94 days andthe average age of workers observed foraging (i.e., in the act of collecting food)was 13.04 days. There appeared to be a marked transition from nursing to foragingbetween 9 and 12 days of age (Figure 1A), with75% of nursing observations made for workers less than 10 days old and 75% offoraging observations made for workers over 10 days old (Figure 1—figure supplement 1).10.7554/eLife.04775.003Figure 1.Behavioral and transcriptional changes associated with worker age andbehavior.

Bottom Line: To begin to reconcile these perspectives, we studied how the evolutionary conservation of genes associated with social behavior depends on regulatory context, and whether genes associated with social behavior exist in distinct regulatory and evolutionary contexts.However, compared to the rest of the genome, forager-upregulated genes were much more highly connected and conserved, while nurse-upregulated genes were less connected and more evolutionarily labile.Our results indicate that the genetic architecture of social behavior includes both highly connected and conserved components as well as loosely connected and evolutionarily labile components.

View Article: PubMed Central - PubMed

Affiliation: Ecology and Evolution Unit, Okinawa Institute of Science and Technology, Okinawa, Japan.

ABSTRACT
Studies of the genetic basis and evolution of complex social behavior emphasize either conserved or novel genes. To begin to reconcile these perspectives, we studied how the evolutionary conservation of genes associated with social behavior depends on regulatory context, and whether genes associated with social behavior exist in distinct regulatory and evolutionary contexts. We identified modules of co-expressed genes associated with age-based division of labor between nurses and foragers in the ant Monomorium pharaonis, and we studied the relationship between molecular evolution, connectivity, and expression. Highly connected and expressed genes were more evolutionarily conserved, as expected. However, compared to the rest of the genome, forager-upregulated genes were much more highly connected and conserved, while nurse-upregulated genes were less connected and more evolutionarily labile. Our results indicate that the genetic architecture of social behavior includes both highly connected and conserved components as well as loosely connected and evolutionarily labile components.

Show MeSH