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Open Access Research article

Genomic and physiological responses to strong selective pressure during late organogenesis: few gene expression changes found despite striking morphological differences

Goran Bozinovic15*, Tim L Sit2, Richard Di Giulio3, Lauren F Wills3 and Marjorie F Oleksiak14

Author Affiliations

1 Department of Environmental and Molecular Toxicology, North Carolina State University, Box 7633, Raleigh, NC 27695-7633, USA

2 Department of Plant Pathology, North Carolina State University, Box 7342, Raleigh, NC 27695-7342, USA

3 Nicholas School of the Environment, Duke University, A333 LSRC, Box 90328, Durham, NC 27708, USA

4 Rosenstiel School of Marine and Atmospheric Sciences, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA

5 Current Address: Division of Biological Sciences, University of California at San Diego, HSS 1145G, 9500 Gilman Drive, La Jolla, CA 92093, USA

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BMC Genomics 2013, 14:779  doi:10.1186/1471-2164-14-779

Published: 11 November 2013

Abstract

Background

Adaptations to a new environment, such as a polluted one, often involve large modifications of the existing phenotypes. Changes in gene expression and regulation during critical developmental stages may explain these phenotypic changes. Embryos from a population of the teleost fish, Fundulus heteroclitus, inhabiting a clean estuary do not survive when exposed to sediment extract from a site highly contaminated with polycyclic aromatic hydrocarbons (PAHs) while embryos derived from a population inhabiting a PAH polluted estuary are remarkably resistant to the polluted sediment extract. We exposed embryos from these two populations to surrogate model PAHs and analyzed changes in gene expression, morphology, and cardiac physiology in order to better understand sensitivity and adaptive resistance mechanisms mediating PAH exposure during development.

Results

The synergistic effects of two model PAHs, an aryl hydrocarbon receptor (AHR) agonist (β-naphthoflavone) and a cytochrome P4501A (CYP1A) inhibitor (α-naphthoflavone), caused significant developmental delays, impaired cardiac function, severe morphological alterations and failure to hatch, leading to the deaths of reference embryos; resistant embryos were mostly unaffected. Unexpectedly, patterns of gene expression among normal and moderately deformed embryos were similar, and only severely deformed embryos showed a contrasting pattern of gene expression. Given the drastic morphological differences between reference and resistant embryos, a surprisingly low percentage of genes, 2.24% of 6,754 analyzed, show statistically significant differences in transcript levels during late organogenesis between the two embryo populations.

Conclusions

Our study demonstrates important contrasts in responses between reference and resistant natural embryo populations to synergistic effects of surrogate model PAHs that may be important in adaptive mechanisms mediating PAH effects during fish embryo development. These results suggest that statistically significant changes in gene expression of relatively few genes contribute to the phenotypic changes and large morphological differences exhibited by reference and resistant populations upon exposure to PAH pollutants. By correlating cardiac physiology and morphology with changes in gene expression patterns of reference and resistant embryos, we provide additional evidence for acquired resistance among embryos whose parents live at heavily contaminated sites.

Keywords:
Development; Genomics; Embryos; Adaptation; Evolution; Fish; Transcriptomics