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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: We observe that natural selection acts to preserve canalized gene expression in populations of killifish that are most tolerant to abrupt salinity change and that these populations show the least variability in their transcription of genes enabling plasticity of the gill.Collectively these findings, which are drawn from the relationships between environmental challenge, plasticity, and canalization among populations, suggest that the selective processes that facilitate phenotypic plasticity do so by targeting the regulatory networks that gives rise to the response.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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Plasticity in gene expression and physiology are canalized. Box plots illustrate the data range (whiskers are 1.5 times interquartile range), interquartile range (box), and median (line). Unique letters indicate significance, as defined below for each plot. (A) Genes revealed through the combined sets of arsenic and seawater interactions exhibit reduced interindividual variation as evidenced by their significantly lower coefficient of variation (COV; Wilcoxon rank sum test; n = 496 interaction genes, 365 main effects genes; P < 2 e-16) compared with the combined main effects of arsenic, seawater 1 h, and seawater 24 h. (B) The reduced variation in putative phenotypic plasticity gene expression observed in the unique interaction gene set persists across the time-course of acclimation as revealed by the distribution of their SD. Wilcoxon rank sum tests identified significant differences (P < 5.8 e-6) between time points in interindividual variation of interaction gene expression. (C) Significant differences in interaction gene expression variation (SD) were observed between freshwater and mesohaline populations (P < 0.03) and freshwater and coastal populations (P < 0.001) using Wilcoxon rank sum tests. The expression of these genes is more accurately and precisely regulated in the freshwater population and variation increases with salinity of native environments (freshwater<mesohaline<coastal). (D) The functional significance of the canalized gene expression is explored by comparing interindividual variation in plasma chloride levels between the three populations during the early stages (0–24 h) that reflect the onset of acclimation. Variation in the distribution of plasma chloride levels is significantly lower in the freshwater population (n = 17 fish per population, modified robust Levene’s test, P < 0.04).
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msu241-F2: Plasticity in gene expression and physiology are canalized. Box plots illustrate the data range (whiskers are 1.5 times interquartile range), interquartile range (box), and median (line). Unique letters indicate significance, as defined below for each plot. (A) Genes revealed through the combined sets of arsenic and seawater interactions exhibit reduced interindividual variation as evidenced by their significantly lower coefficient of variation (COV; Wilcoxon rank sum test; n = 496 interaction genes, 365 main effects genes; P < 2 e-16) compared with the combined main effects of arsenic, seawater 1 h, and seawater 24 h. (B) The reduced variation in putative phenotypic plasticity gene expression observed in the unique interaction gene set persists across the time-course of acclimation as revealed by the distribution of their SD. Wilcoxon rank sum tests identified significant differences (P < 5.8 e-6) between time points in interindividual variation of interaction gene expression. (C) Significant differences in interaction gene expression variation (SD) were observed between freshwater and mesohaline populations (P < 0.03) and freshwater and coastal populations (P < 0.001) using Wilcoxon rank sum tests. The expression of these genes is more accurately and precisely regulated in the freshwater population and variation increases with salinity of native environments (freshwater<mesohaline<coastal). (D) The functional significance of the canalized gene expression is explored by comparing interindividual variation in plasma chloride levels between the three populations during the early stages (0–24 h) that reflect the onset of acclimation. Variation in the distribution of plasma chloride levels is significantly lower in the freshwater population (n = 17 fish per population, modified robust Levene’s test, P < 0.04).

Mentions: To assess differences in interindividual gene expression variation we compared the coefficient of variation (COV) of the interaction genes to the COV of all other DE genes (i.e., main effects). Variation in the expression of these putative plasticity-enabling genes among individual fish was reduced compared with those from the main effects gene set (Wilcoxon rank sum test, P < 2 e-16; fig. 2A). The COV for the DE interaction gene set was only 83% as large as the COV for the DE main effects gene set. In addition, interindividual variation in gene expression for the 367 uniquely interaction DE genes (1 and 24 h) differed between the three experimental time points (Wilcoxon rank sum tests, P < 5.8 e-06). Maximum variation was observed in freshwater, a reduction in variation occurred during the early onset of plasticity (1 h), and variation increased again after 24 h as the fish initially acclimate to seawater (fig. 2B).Fig. 2.


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)

Plasticity in gene expression and physiology are canalized. Box plots illustrate the data range (whiskers are 1.5 times interquartile range), interquartile range (box), and median (line). Unique letters indicate significance, as defined below for each plot. (A) Genes revealed through the combined sets of arsenic and seawater interactions exhibit reduced interindividual variation as evidenced by their significantly lower coefficient of variation (COV; Wilcoxon rank sum test; n = 496 interaction genes, 365 main effects genes; P < 2 e-16) compared with the combined main effects of arsenic, seawater 1 h, and seawater 24 h. (B) The reduced variation in putative phenotypic plasticity gene expression observed in the unique interaction gene set persists across the time-course of acclimation as revealed by the distribution of their SD. Wilcoxon rank sum tests identified significant differences (P < 5.8 e-6) between time points in interindividual variation of interaction gene expression. (C) Significant differences in interaction gene expression variation (SD) were observed between freshwater and mesohaline populations (P < 0.03) and freshwater and coastal populations (P < 0.001) using Wilcoxon rank sum tests. The expression of these genes is more accurately and precisely regulated in the freshwater population and variation increases with salinity of native environments (freshwater<mesohaline<coastal). (D) The functional significance of the canalized gene expression is explored by comparing interindividual variation in plasma chloride levels between the three populations during the early stages (0–24 h) that reflect the onset of acclimation. Variation in the distribution of plasma chloride levels is significantly lower in the freshwater population (n = 17 fish per population, modified robust Levene’s test, P < 0.04).
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Related In: Results  -  Collection

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msu241-F2: Plasticity in gene expression and physiology are canalized. Box plots illustrate the data range (whiskers are 1.5 times interquartile range), interquartile range (box), and median (line). Unique letters indicate significance, as defined below for each plot. (A) Genes revealed through the combined sets of arsenic and seawater interactions exhibit reduced interindividual variation as evidenced by their significantly lower coefficient of variation (COV; Wilcoxon rank sum test; n = 496 interaction genes, 365 main effects genes; P < 2 e-16) compared with the combined main effects of arsenic, seawater 1 h, and seawater 24 h. (B) The reduced variation in putative phenotypic plasticity gene expression observed in the unique interaction gene set persists across the time-course of acclimation as revealed by the distribution of their SD. Wilcoxon rank sum tests identified significant differences (P < 5.8 e-6) between time points in interindividual variation of interaction gene expression. (C) Significant differences in interaction gene expression variation (SD) were observed between freshwater and mesohaline populations (P < 0.03) and freshwater and coastal populations (P < 0.001) using Wilcoxon rank sum tests. The expression of these genes is more accurately and precisely regulated in the freshwater population and variation increases with salinity of native environments (freshwater<mesohaline<coastal). (D) The functional significance of the canalized gene expression is explored by comparing interindividual variation in plasma chloride levels between the three populations during the early stages (0–24 h) that reflect the onset of acclimation. Variation in the distribution of plasma chloride levels is significantly lower in the freshwater population (n = 17 fish per population, modified robust Levene’s test, P < 0.04).
Mentions: To assess differences in interindividual gene expression variation we compared the coefficient of variation (COV) of the interaction genes to the COV of all other DE genes (i.e., main effects). Variation in the expression of these putative plasticity-enabling genes among individual fish was reduced compared with those from the main effects gene set (Wilcoxon rank sum test, P < 2 e-16; fig. 2A). The COV for the DE interaction gene set was only 83% as large as the COV for the DE main effects gene set. In addition, interindividual variation in gene expression for the 367 uniquely interaction DE genes (1 and 24 h) differed between the three experimental time points (Wilcoxon rank sum tests, P < 5.8 e-06). Maximum variation was observed in freshwater, a reduction in variation occurred during the early onset of plasticity (1 h), and variation increased again after 24 h as the fish initially acclimate to seawater (fig. 2B).Fig. 2.

Bottom Line: We observe that natural selection acts to preserve canalized gene expression in populations of killifish that are most tolerant to abrupt salinity change and that these populations show the least variability in their transcription of genes enabling plasticity of the gill.Collectively these findings, which are drawn from the relationships between environmental challenge, plasticity, and canalization among populations, suggest that the selective processes that facilitate phenotypic plasticity do so by targeting the regulatory networks that gives rise to the response.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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Related in: MedlinePlus