Convergence and divergence in gene expression among natural populations exposed to pollution

Abstract

Background: Natural populations of the teleost fish Fundulus heteroclitus tolerate a broad range of environmental conditions including temperature, salinity, hypoxia and chemical pollutants. Strikingly, populations of Fundulus inhabit and have adapted to highly polluted Superfund sites that are contaminated with persistent toxic chemicals. These natural populations provide a foundation to discover critical gene pathways that have evolved in a complex natural environment in response to environmental stressors.

Results: We used Fundulus cDNA arrays to compare metabolic gene expression patterns in the brains of individuals among nine populations: three independent, polluted Superfund populations and two genetically similar, reference populations for each Superfund population. We found that up to 17% of metabolic genes have evolved adaptive changes in gene expression in these Superfund populations. Among these genes, two (1.2%) show a conserved response among three polluted populations, suggesting common, independently evolved mechanisms for adaptation to environmental pollution in these natural populations.

Conclusion: Significant differences among individuals between polluted and reference populations, statistical analyses indicating shared adaptive changes among the Superfund populations, and lack of reduction in gene expression variation suggest that common mechanisms of adaptive resistance to anthropogenic pollutants have evolved independently in multiple Fundulus populations. Among three independent, Superfund populations, two genes have a common response indicating that high selective pressures may favor specific responses.

Figure 1

Sampling and Experimental Design. A) Map of sampling sites, USA, showing polluted Superfund Sites (diamonds, B, E and H) and reference sites (circles). Dashed triangles show the population comparisons illustrated in (B). Superfund sites have text labels. Site names, latitudes and longitudes are in Additional file 2. B) Loop design showing 5 individuals (1–5) from a polluted Superfund population (shaded diamond) hybridized with 5 individuals from each of two reference sites (circles). This experiment used 3 loops and 15 individuals per loop for a total of 45 individuals hybridized to 45 arrays. Each individual is labeled with both Cy3 and Cy5 dyes. Spots are replicated 4 times per array.

Figure 2

Venn Diagram showing numbers of significant genes (p < 0.01) for each polluted versus reference sites comparison. Two genes are significantly different in all three polluted populations compared to their respective reference populations. NBH = New Bedford Harbor comparison, Newark = Newark Bay comparison, ER = Elizabeth River comparison.

Figure 3

All polluted sites versus all reference sites. Heat map, p-values, and gene expression increased (red) and decreased (green) in a comparison of all polluted sites (P) versus all reference sites (R).