The evolutionary consequences for seawater performance and its hormonal control when anadromous Atlantic salmon become landlocked

Abstract

Populations of anadromous fish have become landlocked in relatively recent geological history (<14,000 years), but the evolutionary impacts of this altered lifecycle on traits underlying seawater performance have not been established. In order to examine the effects of relaxed selection on seawater traits, anadromous and landlocked Atlantic salmon were reared under identical conditions and examined for differences in seawater performance and its underlying physiological and endocrine control during the time of spring downstream migration. Salinity tolerance, survival and initial growth in seawater were greater in anadromous than in landlocked salmon. Abundance of the seawater isoform of gill Na⁺/K⁺-ATPase increased in spring in both strains but was greater in anadromous salmon. Hormones associated with seawater acclimation (adrenocorticotropic hormone, cortisol and growth hormone) increased in spring in both strains but were higher in anadromous salmon, whereas plasma thyroid hormones did not differ. Hypothalamic urotensin I mRNA levels also increased in spring and were higher in the anadromous strain. The results provide evidence that salinity tolerance and associated physiological traits are regulated by seasonal stimulation of the hypothalamic-pituitary-interrenal axis, and that relaxed selection on seawater entry traits has decreased this stimulation in landlocked salmon.

Figure 1

Whole body mass (a), condition factor (100 · (mass^. length⁻³)) (b), plasma chloride (c), abundance of gill NKAα1b (d) and NKAα1a (e) and NKA activity (f) in juvenile anadromous and landlocked juvenile Atlantic salmon in freshwater (a,b,d–f) or after 24 h seawater challenge (c; 35 ppt). Values are mean ± standard error of 10–12 individuals. For plasma chloride, gill NKA activity and NKAα1b there was a significant effect of time (p < 0.0001), strain (p < 0.0001) and a significant interaction (p < 0.02). For gill NKAα1a there was a significant effect of time (p = 0.0036), no effect of strain (p = 0.82) but a significant interaction (p = 0.019). Asterisk indicates significant difference from the landlocked strain at the same time period (p < 0.05, Neuman-Keuls test).

Figure 2

Plasma ACTH (a), cortisol (b), GH (c), IGF-I (d), thyroxine (T₄; e) and triiodothyronine (T₃; f) levels in juvenile anadromous and landlocked Atlantic salmon in freshwater. Values are mean ± standard error of 10–12 individuals. For plasma cortisol, ACTH and GH levels there was a significant effect of time (p < 0.0001), strain (p < 0.0001) and a significant interaction (p < 0.02). For plasma IGF-I and T₄ levels there was a significant effect of time (p < 0.0001), no effect of strain (p > 0.8) but a significant interaction (p < 0.026). For plasma T₃ there was a significant effect of time (p < 0.0001) and strain (p = 0.005) and no significant interaction (p = 0.15). Asterisk indicates significant difference from the landlocked strain at the same time period (p < 0.05, Neuman-Keuls test).

Figure 3

Pituitary mRNA levels for the 3 known isoforms of pro-opiomelanocortin (POMC; the precursor of ACTH), pomc-a1 (a), pomc-a2 (b) and pomc-b (c), and pc1 (d) and pc2 (e) mRNA levels in juvenile anadromous and landlocked Atlantic salmon in freshwater. Values are relative to the housekeeping gene ef1α and are the mean ± standard error of 6–9 individuals. Results of two-way ANOVA are noted in the figure. Asterisk indicates significant difference from the landlocked strain at the same time period (p < 0.05, Neuman-Keuls test).

Figure 4

Hypothalamic (HYP) urotensin I (uts1; a) and corticotropin-releasing factor (crf; b) and preoptic area (POA) uts1 (c) and crf (d) mRNA levels in juvenile anadromous and landlocked Atlantic salmon in freshwater. Values are relative to the housekeeping gene ef1α and are the mean ± standard error of 8–10 individuals. Results of two-way ANOVA are noted in the figure. Asterisk indicates significant difference from the landlocked strain at the same time period (p < 0.05, Neuman-Keuls test).