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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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Connectivity, expression, and evolutionary rate for nurse-upregulated(blue), forager-upregulated (red), and non-differentially expressed genes(gray).Overall, connectivity and expression are positively correlated(F) and negatively associated with evolutionary rate(D and E), as expected. At the same time,forager-upregulated genes are much more strongly connected whilenurse-upregulated genes are more loosely connected compared tonon-differentially expressed genes (A); Nurse-upregulated geneshave a small but significant increase in evolutionary rate (C);and both forager- and nurse-upregulated genes are more highly expressed thannon-differentially expressed genes (B). The top panels showresults for all data, while the bottom panels show results only for geneswith S. invicta orthologs that had estimated evolutionaryrates.DOI:http://dx.doi.org/10.7554/eLife.04775.007
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fig2: Connectivity, expression, and evolutionary rate for nurse-upregulated(blue), forager-upregulated (red), and non-differentially expressed genes(gray).Overall, connectivity and expression are positively correlated(F) and negatively associated with evolutionary rate(D and E), as expected. At the same time,forager-upregulated genes are much more strongly connected whilenurse-upregulated genes are more loosely connected compared tonon-differentially expressed genes (A); Nurse-upregulated geneshave a small but significant increase in evolutionary rate (C);and both forager- and nurse-upregulated genes are more highly expressed thannon-differentially expressed genes (B). The top panels showresults for all data, while the bottom panels show results only for geneswith S. invicta orthologs that had estimated evolutionaryrates.DOI:http://dx.doi.org/10.7554/eLife.04775.007

Mentions: Forager-upregulated genes were much more connected than nurse or non-differentiallyexpressed genes, while nurse-upregulated genes were less connected thannon-differentially expressed genes (Figure 2A)(multiple comparison Kruskal–Wallis, p < 0.05). There was a small butsignificant difference in evolutionary rate dN/dS (Figure 2C), with nurse-upregulated genes evolving more rapidly thannon-differentially expressed genes (multiple comparison Kruskal–Wallis, p< 0.05). Nurse and forager genes were also more highly expressed (Figure 2B) than non-differentially expressedgenes (Kruskal–Wallis, p < 0.05), although this last comparison islikely biased because differential expression is more easily detected in highlyexpressed genes.10.7554/eLife.04775.007Figure 2.Connectivity, expression, and evolutionary rate for nurse-upregulated(blue), forager-upregulated (red), and non-differentially expressed genes(gray).


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

Mikheyev AS, Linksvayer TA - Elife (2015)

Connectivity, expression, and evolutionary rate for nurse-upregulated(blue), forager-upregulated (red), and non-differentially expressed genes(gray).Overall, connectivity and expression are positively correlated(F) and negatively associated with evolutionary rate(D and E), as expected. At the same time,forager-upregulated genes are much more strongly connected whilenurse-upregulated genes are more loosely connected compared tonon-differentially expressed genes (A); Nurse-upregulated geneshave a small but significant increase in evolutionary rate (C);and both forager- and nurse-upregulated genes are more highly expressed thannon-differentially expressed genes (B). The top panels showresults for all data, while the bottom panels show results only for geneswith S. invicta orthologs that had estimated evolutionaryrates.DOI:http://dx.doi.org/10.7554/eLife.04775.007
© Copyright Policy
Related In: Results  -  Collection

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

fig2: Connectivity, expression, and evolutionary rate for nurse-upregulated(blue), forager-upregulated (red), and non-differentially expressed genes(gray).Overall, connectivity and expression are positively correlated(F) and negatively associated with evolutionary rate(D and E), as expected. At the same time,forager-upregulated genes are much more strongly connected whilenurse-upregulated genes are more loosely connected compared tonon-differentially expressed genes (A); Nurse-upregulated geneshave a small but significant increase in evolutionary rate (C);and both forager- and nurse-upregulated genes are more highly expressed thannon-differentially expressed genes (B). The top panels showresults for all data, while the bottom panels show results only for geneswith S. invicta orthologs that had estimated evolutionaryrates.DOI:http://dx.doi.org/10.7554/eLife.04775.007
Mentions: Forager-upregulated genes were much more connected than nurse or non-differentiallyexpressed genes, while nurse-upregulated genes were less connected thannon-differentially expressed genes (Figure 2A)(multiple comparison Kruskal–Wallis, p < 0.05). There was a small butsignificant difference in evolutionary rate dN/dS (Figure 2C), with nurse-upregulated genes evolving more rapidly thannon-differentially expressed genes (multiple comparison Kruskal–Wallis, p< 0.05). Nurse and forager genes were also more highly expressed (Figure 2B) than non-differentially expressedgenes (Kruskal–Wallis, p < 0.05), although this last comparison islikely biased because differential expression is more easily detected in highlyexpressed genes.10.7554/eLife.04775.007Figure 2.Connectivity, expression, and evolutionary rate for nurse-upregulated(blue), forager-upregulated (red), and non-differentially expressed genes(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