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Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs)

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Abstract

In this study, we describe remarkable intraspecific variation in sensitivity to the broadly distributed pollutants, polychlorinated biphenyls (PCBs), among wild populations of the nonmigratory estuarine Atlantic killifish (Fundulus heteroclitus). Variation among killifish populations was characterized in 28-day laboratory challenges using embryonic and larval life stages and the highly toxic, dioxin-like PCB congener, 3,3′4,4′,5-hexachlorobiphenyl (PCB126). In summarizing results for 24 populations, we show that killifish populations vary over four orders of magnitude in their sensitivity to PCB126 and that this variation is adaptive to the magnitude of contamination at their residence site. The four least-sensitive killifish populations reside in US Atlantic coast urban harbors >100 km apart from one another: New Bedford, MA, Bridgeport, CT, Newark, NJ, and Norfolk, VA, USA. Prior studies examining all but the CT population have shown that these killifish are relatively insensitive to local contaminants, with mixed evidence concerning the heritability of this trait. We show here that tolerance to PCB126 is extreme, with some mechanistic similarities among these four killifish populations. However, these populations do not respond identically to each other, and in at least one population, tolerance appears to degrade over the F1 and F2 generations tested. Complementary ongoing studies using molecular approaches provide opportunity to identify unique and shared mechanisms of tolerance in these independently evolving populations and explore the adaptive benefits and costs of contemporary evolutionary responses in the wild.

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Acknowledgements

We appreciate the assistance and encouragement of the staff at Bloodroot Restaurant (Bridgeport, CT), Peter Van Veld (Virginia Institute of Marine Sciences, VA), the technical support of Jane Copeland and James Heltshe, CSC Corporation, as well as helpful advice from reviewers of early drafts, Ruth Gutjahr-Gobell, Marguerite Pelletier, and Eric Waits, US Environmental Protection Agency. We also acknowledge the assistance of anonymous reviewers contributing to the final version of this manuscript. This is contribution number AED-09-014 of the US Environmental Protection Agency, Office of Research and Development, National Health and Environmental Effects Research Laboratory, Atlantic Ecology Division. This manuscript has been reviewed and approved for publication by the US EPA. Approval does not signify that the contents necessarily reflect the views and policies of the US EPA. Mention of trade names, products, or services does not convey and should not be interpreted as conveying official US EPA approval, endorsement, or recommendation.

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  1. Atlantic Ecology Division, National Health and Environmental Effects Research Laboratory, Office of Research and Development, US Environmental Protection Agency, 27 Tarzwell Drive, Narragansett, RI, 02882, USA

    Diane E. Nacci, Denise Champlin & Saro Jayaraman

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  1. Diane E. Nacci
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  2. Denise Champlin
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  3. Saro Jayaraman
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Correspondence to Diane E. Nacci.

Appendix

Appendix

Table 3 Characteristics of previously unpublished early life stage exposure-lethality models that describe tolerance to 3,3′4,4′,5-pentachloro biphenyl (PCB126) for progeny of F. heteroclitus from those sites described in Table 1
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Nacci, D.E., Champlin, D. & Jayaraman, S. Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs). Estuaries and Coasts 33, 853–864 (2010). https://doi.org/10.1007/s12237-009-9257-6

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