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Relaxed selection causes microevolution of seawater osmoregulation and gene expression in landlocked Alewives

  • Physiological ecology - Original research
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Abstract

Ecological transitions from marine to freshwater environments have been important in the creation of diversity among fishes. Evolutionary changes associated with these transitions likely involve modifications of osmoregulatory function. In particular, relaxed selection on hypo-osmoregulation should strongly affect animals that transition into novel freshwater environments. We used populations of the Alewife (Alosa pseudoharengus) to study evolutionary shifts in hypo-osmoregulatory capacity and ion regulation associated with freshwater transitions. Alewives are ancestrally anadromous, but multiple populations in Connecticut have been independently restricted to freshwater lakes; these landlocked populations complete their entire life cycle in freshwater. Juvenile landlocked and anadromous Alewives were exposed to three salinities (1, 20 and 30 ppt) in small enclosures within the lake. We detected strong differentiation between life history forms: landlocked Alewives exhibited reduced seawater tolerance and hypo-osmoregulatory performance compared to anadromous Alewives. Furthermore, gill Na+/K+-ATPase activity and transcription of genes for seawater osmoregulation (NKCC—Na+/K+/2Cl− cotransporter and CFTR—cystic fibrosis transmembrane conductance regulator) exhibited reduced responsiveness to seawater challenge. Our study demonstrates that adaptations of marine-derived species to completely freshwater life cycles involve partial loss of seawater osmoregulatory performance mediated through changes to ion regulation in the gill.

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Acknowledgments

We thank Dr. David M. Post, Andrew Jones, and Megan Cruz for their help collecting juvenile Alewives. We thank Dr. Arne K. Christensen for assisting in gill tissue sample collection, and Michael O’Dea for assisting in sample collection and for running Na+/K+-ATPase activity assays. We also thank Emily Funk for assisting with real-time quantitative PCR assays. Many thanks to Carl Schlichting, Mark Urban, Brian G. Walker, Alejandro Rico-Guevara, Jeffrey Divino, and two anonymous reviewers for providing helpful comments on the manuscript. This study was funded by Connecticut Sea Grant, the University of Connecticut Center for Environmental Science and Engineering, the American Museum of Natural History Lerner Gray Fund, the University of Connecticut Department of Ecology and Evolutionary Biology, and Sigma Xi Grants-in-Aid of Research. The authors declare no conflicts of interest. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Unit 3043, Storrs, CT, 06269, USA

    Jonathan P. Velotta & Eric T. Schultz

  2. USGS, Conte Anadromous Fish Research Center, Turners Falls, MA, 01376, USA

    Stephen D. McCormick

  3. Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT, 06269, USA

    Rachel J. O’Neill

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  1. Jonathan P. Velotta
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  4. Eric T. Schultz
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Correspondence to Jonathan P. Velotta.

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Communicated by Steve Swearer.

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Velotta, J.P., McCormick, S.D., O’Neill, R.J. et al. Relaxed selection causes microevolution of seawater osmoregulation and gene expression in landlocked Alewives. Oecologia 175, 1081–1092 (2014). https://doi.org/10.1007/s00442-014-2961-3

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