Evol Ecol Res 17: 179-201 (2016)     Full PDF if your library subscribes.

Osmoregulatory physiology and rapid evolution of salinity tolerance
in threespine stickleback recently introduced to fresh water

Jeffrey N. Divino1, Michelle Y. Monette2, Stephen D. McCormick3, Paul H. Yancey4, Kyle G. Flannery4, Michael A. Bell5, Jennifer L. Rollins5, Frank A. von Hippel6 and Eric T. Schultz1

1Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs,  Connecticut, USA,  2Department of Biological and Environmental Sciences, Western Connecticut State University, Danbury, Connecticut, USA,  3USGS, Conte Anadromous Fish Research Center, Turners Falls, Massachusetts, USA,  4Biology Department, Whitman College, Walla Walla, Washington, USA,  5Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York, USA and  6Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, USA

Correspondence: J.N. Divino, Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269-3043, USA. email: jeffrey.divino@uconn.edu


Background: Post-Pleistocene diversification of threespine stickleback in fresh water offers a valuable opportunity to study how changes in environmental salinity shape physiological evolution in fish. In Alaska, the presence of both ancestral oceanic populations and derived landlocked populations, including recent lake introductions, allows us to examine rates and direction of evolution of osmoregulation following halohabitat transition.

Hypotheses: Strong selection for enhanced freshwater tolerance will improve survival of recently lake-introduced stickleback in ion-poor conditions compared with their oceanic ancestors. Trade-offs between osmoregulation in fresh water and seawater will allow members of the ancestral population to survive better in response to seawater challenge, as mediated by upregulating salt-secreting transporters in the gill. Poorer hypo-osmoregulatory performance of derived fish will be marked by higher levels of taurine and other organic osmolytes.

Methods: We reared clutches at a common salinity from an anadromous and a descendant population, Scout Lake, which has been landlocked for only two generations. We challenged 6-week-old juveniles with extreme low and high salinity treatments and sampled fish over 10 days to investigate putative molecular mechanisms underlying differences in halotolerance. We measured whole-body organic osmolyte content as well as gill Na+/K+-ATPase (NKA) activity and Na+/K+/2Cl cotransporter (NKCC) protein abundance. Other juveniles from these populations and also from Cheney Lake, a fourth-generation landlocked descendant, were gradually salt-acclimated to determine maximum halotolerance limits.

Results: Scout Lake stickleback exhibited 67% higher survival in fresh water than the ancestral anadromous population, but individuals from both groups exhibited similar seawater tolerance. Likewise, the gradual salinity threshold for each population was equivalent (71 ppt). Gill NKA activity and NKCC abundance were both higher in seawater-challenged fish, but did not differ between populations. Sticklebacks from both populations responded to acute salinity stress by transiently increasing osmolyte levels in seawater and decreasing them in fresh water.

Conclusion: Enhanced freshwater tolerance has evolved rapidly in recently landlocked stickleback compared with their anadromous ancestors (0.569 haldanes), but the former have retained ancestral seawater-osmoregulatory function.

Keywords: comparative physiology, directional selection, free amino acid, ion balance, osmoregulatory divergence, plasticity, threespine stickleback.

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