Prenatal Stress Exposure Generates Higher Early Survival and Smaller Size without Impacting Developmental Rate in a Pacific Salmon

Abstract

Prenatal exposure to elevated glucocorticoids can act as a signal of environmental stress, resulting in modifications to offspring phenotype. While "negative" phenotypic effects (i.e., smaller size, slower growth) are often reported, recent research coupling phenotype with other fitness-related traits has suggested positive impacts of prenatal stress. Using captive Chinook salmon (Oncorhynchus tshawytscha), we treated eggs with biologically relevant cortisol levels-low (300 ng mL ), high (1,000 ng mL ), or control (0 ng mL )-to examine the early-life impacts of maternally transferred stress hormones on offspring. Specifically, we measured early survival, rate of development, and multiple measures of morphology. Low and high cortisol dosing of eggs resulted in significantly higher survival compared to controls (37% and 24% higher, respectively). Fish reared from high dose eggs were structurally smaller compared to control fish, but despite this variation in structural size, exposure to elevated cortisol did not impact developmental rate. These results demonstrate that elevations in egg cortisol can positively influence offspring fitness through an increase in early survival while also altering phenotype at a critical life-history stage. Overall, these results suggest that exposure to prenatal stress may not always produce apparently negative impacts on offspring fitness and further proposes that complex phenotypic responses should be examined in relevant environmental conditions.

Phenotypic integration of behavioural and physiological traits is related to variation in growth among stocks of Chinook salmon

“…Packed red blood cells were then separated from plasma via centrifugation at 14,000 rpm (13,331 g) and plasma was stored at -80˚C until further analyses. Baseline plasma cortisol was determined using a cortisol enzyme-linked immunosorbent assay (Cayman Chemical, MI, USA) optimized in-house for use in juvenile Chinook salmon (Capelle et al 2016). Samples were run in triplicate across fourteen assay plates at 1:20 dilution.…”

Exposure to exogenous egg cortisol does not rescue juvenile Chinook salmon body size, condition, or survival from the effects of elevated water temperatures

“…In Atlantic salmon ( Salmo salar ) where mothers received cortisol injections and eggs were incubated under mild hyperthermia (+2°C), there were no effects on offspring survival (Eriksen, Bakken, Espmark, Braastad, & Salte, ; Eriksen, Espmark, Braastad, Salte, & Bakken, ). However, although under benign environments some studies have reported either lower ( Oncorhynchus mykiss : Li, Bureau, King, & Leatherland, ) and even higher ( O. tshawytscha : Capelle et al, ) early survival for offspring exposed to elevated egg cortisol, the majority of studies have reported no effect across a diversity of fish species ( Danio rerio : Nesan & Vijayan, ; Salmo trutta : Sloman, ; O. kisutch , O. keta , O. nerka : Sopinka et al, ; Sopinka, Hinch, Healy, Harrison, & Patterson, ; O. kisutch : Stratholt, Donaldson, & Liley, ). Considering these contrasting results both within and across fish species, it may not be surprising that exposure to elevated egg cortisol was incapable of ameliorating survival of elevated water temperatures.…”

“…After 2 min (when sperm should no longer be motile), we added river water mixed to 1,000 ng/ml concentration of cortisol (H4001; Sigma‐Aldrich Canada Co) dissolved in 90% ethanol (HPLC grade; Sigma‐Aldrich Canada Co) or 0 ng/ml control solution (ethanol and water only) for a 2‐hr incubation. These concentrations and exposure times were chosen as they have been shown in previous published studies to result in biologically relevant elevations of cortisol in the eggs (i.e., within 2 SD of control: Burton, Hoogenboom, Armstrong, Groothuis, & Metcalfe, ; Capelle, Semeniuk, Sopinka, Heath, & Love, ; Sopinka et al, ; Sopinka, Hinch, Healy, Raby, & Patterson, ). After the 2‐hr exposure, we rinsed the eggs using dechlorinated water, and removed three eggs from each cortisol replicate to verify the effectiveness of the cortisol manipulation.…”

“…Briefly, we sampled three eggs from each treatment (unfertilized, control‐dosed, and cortisol‐dosed) for each of the 15 females ( N = 45). We weighed, and blended eggs in 1.2 ml assay buffer, and then extracted the cortisol according to protocol as detailed in Capelle et al (). Samples were stored in –80°C freezer until use in assay.…”

Pre‐ and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens

“…Similarly, nestlings hatching from corticosterone‐injected eggs in our study population were lighter than control nestlings at hatching, but, through compensatory growth, were heavier near the time of nest‐leaving (Strange et al., ), a likely positive effect; however, there are often long‐term costs to compensatory growth (Grace, Froud, Meillère, & Angelier, ; Metcalfe & Monaghan, ; Monaghan, ). There is evidence of positive effects of prenatal corticosterone or cortisol exposure in a variety of taxa (Capelle, Semeniuk, Sopinka, Heath, & Love, ; Meylan & Clobert, ). The immediate cause for these prenatal effects is most likely the maternal corticosterone and other possible compounds associated with elevated maternal corticosterone that were transferred to the eggs.…”