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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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Very similarly to Figure 3,genes with identified honey orthologs were more highly connected andexpressed, but this relationship also depended on whether the gene wasnurse-upregulated (blue), forager-upregulated (red), ornon-differentially expressed (NDE, gray).Forager-upregulated genes had a higher proportion of identified honey beeorthologs (0.50) relative to nurse-upregulated and non-differentiallyexpressed genes (0.38).DOI:http://dx.doi.org/10.7554/eLife.04775.009
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fig3s1: Very similarly to Figure 3,genes with identified honey orthologs were more highly connected andexpressed, but this relationship also depended on whether the gene wasnurse-upregulated (blue), forager-upregulated (red), ornon-differentially expressed (NDE, gray).Forager-upregulated genes had a higher proportion of identified honey beeorthologs (0.50) relative to nurse-upregulated and non-differentiallyexpressed genes (0.38).DOI:http://dx.doi.org/10.7554/eLife.04775.009

Mentions: We also studied the effects of gene category (i.e., upregulated in nurses orforagers, or not differentially expressed), expression level, and connectivity onwhether a given M. pharaonis gene had an identifiable fire antS. invicta and honey bee A. mellifera orthologs.Overall, genes with orthologs in the fire ant or honey bee had greater connectivityand expression (Figure 3, Figure 3—figure supplement 1). In considering a modelwith both main and interaction effects of behavioral category, expression level, andconnectivity, connectivity had the strongest effect (glm with quasibinomialresiduals: t = 24.5, p < 10−16, for the presence ofS. invicta orthologs; t = 32.2, p <10−16, for the presence of A. melliferaorthologs), with more highly connected genes being more likely to have an ortholog.There were also much smaller interaction effects indicating that nurse-upregulatedgenes had fewer orthologs than expected given their connectivities (i.e.,connectivity had a weaker effect on nurse-upregulated genes than other genes, Figure 3 and Figure 3—figure supplement 1; t = −3.17, p =0.0015 for S. invicta orthologs; t = −2.76, p =0.0057 for A. mellifera orthologs), and forager-upregulated geneshad fewer orthologs than expected given their expression (t = −2.33, p= 0.02 for S. invicta orthologs; t = −2.58, p= 0.0098 for A. mellifera orthologs; Figure 3 and Figure3—figure supplement 1).10.7554/eLife.04775.008Figure 3.Genes with identified fire ant orthologs were more highly connectedand expressed, but this relationship also depended on whether the genewas nurse-upregulated (blue), forager-upregulated (red), ornon-differentially expressed (NDE, gray).


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

Mikheyev AS, Linksvayer TA - Elife (2015)

Very similarly to Figure 3,genes with identified honey orthologs were more highly connected andexpressed, but this relationship also depended on whether the gene wasnurse-upregulated (blue), forager-upregulated (red), ornon-differentially expressed (NDE, gray).Forager-upregulated genes had a higher proportion of identified honey beeorthologs (0.50) relative to nurse-upregulated and non-differentiallyexpressed genes (0.38).DOI:http://dx.doi.org/10.7554/eLife.04775.009
© Copyright Policy
Related In: Results  -  Collection

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

fig3s1: Very similarly to Figure 3,genes with identified honey orthologs were more highly connected andexpressed, but this relationship also depended on whether the gene wasnurse-upregulated (blue), forager-upregulated (red), ornon-differentially expressed (NDE, gray).Forager-upregulated genes had a higher proportion of identified honey beeorthologs (0.50) relative to nurse-upregulated and non-differentiallyexpressed genes (0.38).DOI:http://dx.doi.org/10.7554/eLife.04775.009
Mentions: We also studied the effects of gene category (i.e., upregulated in nurses orforagers, or not differentially expressed), expression level, and connectivity onwhether a given M. pharaonis gene had an identifiable fire antS. invicta and honey bee A. mellifera orthologs.Overall, genes with orthologs in the fire ant or honey bee had greater connectivityand expression (Figure 3, Figure 3—figure supplement 1). In considering a modelwith both main and interaction effects of behavioral category, expression level, andconnectivity, connectivity had the strongest effect (glm with quasibinomialresiduals: t = 24.5, p < 10−16, for the presence ofS. invicta orthologs; t = 32.2, p <10−16, for the presence of A. melliferaorthologs), with more highly connected genes being more likely to have an ortholog.There were also much smaller interaction effects indicating that nurse-upregulatedgenes had fewer orthologs than expected given their connectivities (i.e.,connectivity had a weaker effect on nurse-upregulated genes than other genes, Figure 3 and Figure 3—figure supplement 1; t = −3.17, p =0.0015 for S. invicta orthologs; t = −2.76, p =0.0057 for A. mellifera orthologs), and forager-upregulated geneshad fewer orthologs than expected given their expression (t = −2.33, p= 0.02 for S. invicta orthologs; t = −2.58, p= 0.0098 for A. mellifera orthologs; Figure 3 and Figure3—figure supplement 1).10.7554/eLife.04775.008Figure 3.Genes with identified fire ant orthologs were more highly connectedand expressed, but this relationship also depended on whether the genewas nurse-upregulated (blue), forager-upregulated (red), ornon-differentially expressed (NDE, gray).

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