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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 identified modules vary in expression pattern, composition ofnurse-upregulated and forager-upregulated genes, and the proportion ofconserved genes with identified fire ant orthologs.The total number of genes, number of nurse-upregulated genes, andforager-upregulated genes are shown, along with the proportion ofidentified fire ant orthologs and prominent gene ontology terms enrichedfor each module (see Supplementary file 4 for the full GO enrichmentprofiles for each module). Both the module number and associated modulecolor are shown on the left.DOI:http://dx.doi.org/10.7554/eLife.04775.006
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fig1s3: The identified modules vary in expression pattern, composition ofnurse-upregulated and forager-upregulated genes, and the proportion ofconserved genes with identified fire ant orthologs.The total number of genes, number of nurse-upregulated genes, andforager-upregulated genes are shown, along with the proportion ofidentified fire ant orthologs and prominent gene ontology terms enrichedfor each module (see Supplementary file 4 for the full GO enrichmentprofiles for each module). Both the module number and associated modulecolor are shown on the left.DOI:http://dx.doi.org/10.7554/eLife.04775.006

Mentions: The number of modules produced by WGCNA can vary based on several thresholdingparameters, which we left as defaults (Supplementary file 2, pages 20–21). These settingsresulted in 14 co-expression modules, ranging in size from 83 to 4218 genes (Figure 1C; Figure 1—figure supplement 3). A module's overall expressioncan be characterized by its eigengene. Correlations between eigengenes and traits inthe original data suggest the involvement of corresponding modules in these traits.Eigengenes in two of the modules—1 and 14, which contained the most nurse andforager genes, respectively—were strongly correlated with worker age, althoughin opposite directions, suggesting their role in aging and age-based division oflabor (r = −0.95, r = 0.91 and with FDR-adjusted p-values0.0038, 0.023, respectively) (Supplementary file 2, page 24). Other modules showed complex patterns ofage and behavior specific expression, with most of them showing a peak in expressiononce or twice during the lifetime of a worker (Supplementary file 2, page26). Interestingly, most module eigengenes switched signs during the period between 9and 12 days, corresponding to the behavioral transition from nursing to foraging. Inother words, there appeared to be a major reprogramming step, where modules initiallyshowing low expression became up-regulated, while modules initially showing highexpression were down-regulated.


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

Mikheyev AS, Linksvayer TA - Elife (2015)

The identified modules vary in expression pattern, composition ofnurse-upregulated and forager-upregulated genes, and the proportion ofconserved genes with identified fire ant orthologs.The total number of genes, number of nurse-upregulated genes, andforager-upregulated genes are shown, along with the proportion ofidentified fire ant orthologs and prominent gene ontology terms enrichedfor each module (see Supplementary file 4 for the full GO enrichmentprofiles for each module). Both the module number and associated modulecolor are shown on the left.DOI:http://dx.doi.org/10.7554/eLife.04775.006
© Copyright Policy
Related In: Results  -  Collection

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

fig1s3: The identified modules vary in expression pattern, composition ofnurse-upregulated and forager-upregulated genes, and the proportion ofconserved genes with identified fire ant orthologs.The total number of genes, number of nurse-upregulated genes, andforager-upregulated genes are shown, along with the proportion ofidentified fire ant orthologs and prominent gene ontology terms enrichedfor each module (see Supplementary file 4 for the full GO enrichmentprofiles for each module). Both the module number and associated modulecolor are shown on the left.DOI:http://dx.doi.org/10.7554/eLife.04775.006
Mentions: The number of modules produced by WGCNA can vary based on several thresholdingparameters, which we left as defaults (Supplementary file 2, pages 20–21). These settingsresulted in 14 co-expression modules, ranging in size from 83 to 4218 genes (Figure 1C; Figure 1—figure supplement 3). A module's overall expressioncan be characterized by its eigengene. Correlations between eigengenes and traits inthe original data suggest the involvement of corresponding modules in these traits.Eigengenes in two of the modules—1 and 14, which contained the most nurse andforager genes, respectively—were strongly correlated with worker age, althoughin opposite directions, suggesting their role in aging and age-based division oflabor (r = −0.95, r = 0.91 and with FDR-adjusted p-values0.0038, 0.023, respectively) (Supplementary file 2, page 24). Other modules showed complex patterns ofage and behavior specific expression, with most of them showing a peak in expressiononce or twice during the lifetime of a worker (Supplementary file 2, page26). Interestingly, most module eigengenes switched signs during the period between 9and 12 days, corresponding to the behavioral transition from nursing to foraging. Inother words, there appeared to be a major reprogramming step, where modules initiallyshowing low expression became up-regulated, while modules initially showing highexpression were down-regulated.

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