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Natural selection canalizes expression variation of environmentally induced plasticity-enabling genes.

Shaw JR, Hampton TH, King BL, Whitehead A, Galvez F, Gross RH, Keith N, Notch E, Jung D, Glaholt SP, Chen CY, Colbourne JK, Stanton BA - Mol. Biol. Evol. (2014)

Bottom Line: Gene sets defined by antagonistic interactions between arsenic and salinity show reduced transcriptional variation among individual fish, suggesting unusually accurate and precise regulatory control of these genes, consistent with the hypothesis that they participate in a canalized developmental response.We found that genes participating in this highly canalized and conserved plasticity-enabling response had significantly fewer and less complex associations with transcriptional regulators than genes that respond only to arsenic or salinity.These findings also provide a generalized, conceptual framework of how genes might interact with the environment and evolve toward the development of plastic traits.

View Article: PubMed Central - PubMed

Affiliation: The School of Public and Environmental Affairs, Indiana University, Bloomington The Center for Genomics and Bioinformatics, Indiana University, Bloomington The Mount Desert Island Biological Laboratory, Salisbury Cove, ME Environmental Genomics Group, School of Biosciences, University of Birmingham, Birmingham, United Kingdom joeshaw@indiana.edu.

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Arsenic–seawater interactions reveal phenotypic plasticity-enabling genes. Differences in gene expression (GE) from gill tissue of four male killifish, Fundulus heteroclitus, for each of six treatments were analyzed by measuring quantile normalized log2 expression values using a two-factor linear model that includes two categorical variables (presence of arsenic and time spent in seawater) as well as their interactions. DE genes were defined by P values < 0.05 and fold changes >2 for at least one treatment. The y axis shows differences in GE from freshwater (FW) in units of SD for (A) genes significantly DE at 1 h, (B) genes significantly DE at 24 h, (C) genes with significant interactions between arsenic and salinity at 1 h, and (D) genes with significant interactions between arsenic and salinity at 24 h. Genes upregulated compared with FW appear in red; down in blue. DE genes at 1 h (A) and 24 h (B) diverge from FW, yet the divergence at 1 h (A) is not seen at 24 h (A). Arsenic’s inhibition of gene expression associated with salinity acclimation is seen by observing the interaction gene sets. DE genes of the two treatments, arsenic–seawater 1 h (C) and arsenic–seawater 24 h (D), deviate from expectations of additivity. For example, the arsenic–seawater 1 h DE genes (C) respond to both arsenic and 1 h seawater treatments when compared with FW. An additive model predicts that the combined effect of both arsenic (As) and seawater acclimation at 1 h (SW 1 h) should result in a greater (red) or lesser (blue) GE response (As + 1 h SW). However, this combined effect produces an antagonistic interaction GE pattern that is similar to that observed in a stable environment (FW). Genes showing interaction effects at 24 h (D) recapitulate this pattern.
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msu241-F1: Arsenic–seawater interactions reveal phenotypic plasticity-enabling genes. Differences in gene expression (GE) from gill tissue of four male killifish, Fundulus heteroclitus, for each of six treatments were analyzed by measuring quantile normalized log2 expression values using a two-factor linear model that includes two categorical variables (presence of arsenic and time spent in seawater) as well as their interactions. DE genes were defined by P values < 0.05 and fold changes >2 for at least one treatment. The y axis shows differences in GE from freshwater (FW) in units of SD for (A) genes significantly DE at 1 h, (B) genes significantly DE at 24 h, (C) genes with significant interactions between arsenic and salinity at 1 h, and (D) genes with significant interactions between arsenic and salinity at 24 h. Genes upregulated compared with FW appear in red; down in blue. DE genes at 1 h (A) and 24 h (B) diverge from FW, yet the divergence at 1 h (A) is not seen at 24 h (A). Arsenic’s inhibition of gene expression associated with salinity acclimation is seen by observing the interaction gene sets. DE genes of the two treatments, arsenic–seawater 1 h (C) and arsenic–seawater 24 h (D), deviate from expectations of additivity. For example, the arsenic–seawater 1 h DE genes (C) respond to both arsenic and 1 h seawater treatments when compared with FW. An additive model predicts that the combined effect of both arsenic (As) and seawater acclimation at 1 h (SW 1 h) should result in a greater (red) or lesser (blue) GE response (As + 1 h SW). However, this combined effect produces an antagonistic interaction GE pattern that is similar to that observed in a stable environment (FW). Genes showing interaction effects at 24 h (D) recapitulate this pattern.

Mentions: Analysis of the gene expression data using linear models revealed 496 DE genes with significant (P < 0.05, fold change >+ 2 or <−2) salinity-arsenic interactions. Of these, 367 were uniquely associated with the interaction, that is, they were not significant in any main effect. Linear models detected 203 and 221 DE genes for salinity 1 h and salinity 24 h, respectively (fig. 1A and B). Arsenic alone had a minor effect on gene expression (129 DE genes). A majority (73%) of the 496 DE interaction genes showed reduced expression (supplementary fig. S1, Supplementary Material online) and all of these interactions were antagonistic (i.e., less than additive; fig. 1C and D) producing expression values that more closely resembled those of killifish living in stable freshwater environments.Fig. 1.


Natural selection canalizes expression variation of environmentally induced plasticity-enabling genes.

Shaw JR, Hampton TH, King BL, Whitehead A, Galvez F, Gross RH, Keith N, Notch E, Jung D, Glaholt SP, Chen CY, Colbourne JK, Stanton BA - Mol. Biol. Evol. (2014)

Arsenic–seawater interactions reveal phenotypic plasticity-enabling genes. Differences in gene expression (GE) from gill tissue of four male killifish, Fundulus heteroclitus, for each of six treatments were analyzed by measuring quantile normalized log2 expression values using a two-factor linear model that includes two categorical variables (presence of arsenic and time spent in seawater) as well as their interactions. DE genes were defined by P values < 0.05 and fold changes >2 for at least one treatment. The y axis shows differences in GE from freshwater (FW) in units of SD for (A) genes significantly DE at 1 h, (B) genes significantly DE at 24 h, (C) genes with significant interactions between arsenic and salinity at 1 h, and (D) genes with significant interactions between arsenic and salinity at 24 h. Genes upregulated compared with FW appear in red; down in blue. DE genes at 1 h (A) and 24 h (B) diverge from FW, yet the divergence at 1 h (A) is not seen at 24 h (A). Arsenic’s inhibition of gene expression associated with salinity acclimation is seen by observing the interaction gene sets. DE genes of the two treatments, arsenic–seawater 1 h (C) and arsenic–seawater 24 h (D), deviate from expectations of additivity. For example, the arsenic–seawater 1 h DE genes (C) respond to both arsenic and 1 h seawater treatments when compared with FW. An additive model predicts that the combined effect of both arsenic (As) and seawater acclimation at 1 h (SW 1 h) should result in a greater (red) or lesser (blue) GE response (As + 1 h SW). However, this combined effect produces an antagonistic interaction GE pattern that is similar to that observed in a stable environment (FW). Genes showing interaction effects at 24 h (D) recapitulate this pattern.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4209136&req=5

msu241-F1: Arsenic–seawater interactions reveal phenotypic plasticity-enabling genes. Differences in gene expression (GE) from gill tissue of four male killifish, Fundulus heteroclitus, for each of six treatments were analyzed by measuring quantile normalized log2 expression values using a two-factor linear model that includes two categorical variables (presence of arsenic and time spent in seawater) as well as their interactions. DE genes were defined by P values < 0.05 and fold changes >2 for at least one treatment. The y axis shows differences in GE from freshwater (FW) in units of SD for (A) genes significantly DE at 1 h, (B) genes significantly DE at 24 h, (C) genes with significant interactions between arsenic and salinity at 1 h, and (D) genes with significant interactions between arsenic and salinity at 24 h. Genes upregulated compared with FW appear in red; down in blue. DE genes at 1 h (A) and 24 h (B) diverge from FW, yet the divergence at 1 h (A) is not seen at 24 h (A). Arsenic’s inhibition of gene expression associated with salinity acclimation is seen by observing the interaction gene sets. DE genes of the two treatments, arsenic–seawater 1 h (C) and arsenic–seawater 24 h (D), deviate from expectations of additivity. For example, the arsenic–seawater 1 h DE genes (C) respond to both arsenic and 1 h seawater treatments when compared with FW. An additive model predicts that the combined effect of both arsenic (As) and seawater acclimation at 1 h (SW 1 h) should result in a greater (red) or lesser (blue) GE response (As + 1 h SW). However, this combined effect produces an antagonistic interaction GE pattern that is similar to that observed in a stable environment (FW). Genes showing interaction effects at 24 h (D) recapitulate this pattern.
Mentions: Analysis of the gene expression data using linear models revealed 496 DE genes with significant (P < 0.05, fold change >+ 2 or <−2) salinity-arsenic interactions. Of these, 367 were uniquely associated with the interaction, that is, they were not significant in any main effect. Linear models detected 203 and 221 DE genes for salinity 1 h and salinity 24 h, respectively (fig. 1A and B). Arsenic alone had a minor effect on gene expression (129 DE genes). A majority (73%) of the 496 DE interaction genes showed reduced expression (supplementary fig. S1, Supplementary Material online) and all of these interactions were antagonistic (i.e., less than additive; fig. 1C and D) producing expression values that more closely resembled those of killifish living in stable freshwater environments.Fig. 1.

Bottom Line: Gene sets defined by antagonistic interactions between arsenic and salinity show reduced transcriptional variation among individual fish, suggesting unusually accurate and precise regulatory control of these genes, consistent with the hypothesis that they participate in a canalized developmental response.We found that genes participating in this highly canalized and conserved plasticity-enabling response had significantly fewer and less complex associations with transcriptional regulators than genes that respond only to arsenic or salinity.These findings also provide a generalized, conceptual framework of how genes might interact with the environment and evolve toward the development of plastic traits.

View Article: PubMed Central - PubMed

Affiliation: The School of Public and Environmental Affairs, Indiana University, Bloomington The Center for Genomics and Bioinformatics, Indiana University, Bloomington The Mount Desert Island Biological Laboratory, Salisbury Cove, ME Environmental Genomics Group, School of Biosciences, University of Birmingham, Birmingham, United Kingdom joeshaw@indiana.edu.

Show MeSH
Related in: MedlinePlus