Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level

Abstract

SUMMARYIn fishes, performance failure at high temperature is thought to be due to a limitation on oxygen delivery (the theory of oxygen and capacity limited thermal tolerance, OCLTT), which suggests that thermal tolerance and hypoxia tolerance might be functionally associated. Here we examined variation in temperature and hypoxia tolerance among 41 families of Atlantic salmon (Salmo salar), which allowed us to evaluate the association between these two traits. Both temperature and hypoxia tolerance varied significantly among families and there was a significant positive correlation between critical maximum temperature (CT max ) and hypoxia tolerance, supporting the OCLTT concept. At the organ and cellular levels, we also discovered support for the OCLTT concept as relative ventricle mass (RVM) and cardiac myoglobin (Mb) levels both correlated positively with CT max (R 2 =0.21, P<0.001 and R 2 =0.17, P=0.003, respectively). A large RVM has previously been shown to be associated with high cardiac output, which might facilitate tissue oxygen supply during elevated oxygen demand at high temperatures, while Mb facilitates the oxygen transfer from the blood to tissues, especially during hypoxia. The data presented here demonstrate for the first time that RVM and Mb are correlated with increased upper temperature tolerance in fish. High phenotypic variation between families and greater similarity among full-and half-siblings suggests that there is substantial standing genetic variation in thermal and hypoxia tolerance, which could respond to selection either in aquaculture or in response to anthropogenic stressors such as global climate change.

Developmental Hypoxia Has Negligible Effects on Long-Term Hypoxia Tolerance and Aerobic Metabolism of Atlantic Salmon (Salmo salar)

“…For our experiment where DO was decreased at 0.33% min 21 , this represents a difference in mean time to LOE of ∼2.4 min. Such a difference may be negligible because the median time to LOE can vary substantially (up to 114.8 min) between families of Atlantic salmon (Anttila et al 2013). Thus, it is unclear what real-world impacts an effect of such small magnitude would have on fish performance and survival, given the spatial and temporal DO variability often experienced in wild and aquaculture environments.…”

“…Four half-sibling Atlantic salmon families were created by fertilizing eggs from four females with milt from one male, using captive-bred broodstock reared in freshwater at SALTAS. Half-sibling families were used to reduce potential variability in metabolic measurements and hypoxia tolerance between families (Anttila et al 2013). Fertilized eggs were randomly allocated to two replicate mesh isolation baskets (18 cm # 14.5 cm # 5.5 cm) per treatment, with each replicate incubated in separate Heath trays (39 cm # 32 cm # 5.5 cm; Marisource).…”

Atlantic salmon show capability for cardiac acclimation to warm temperatures

“…Thus, because both T max and T arr were similar between populations, cardiac collapse near T crit would be more precipitous in the southern than in the northern population given the larger difference between T arr and T AB for the northern population. Unexplored here, but still needed, is a consideration of transgenerational changes in temperature tolerance (exposure of parental fish to adverse temperatures providing benefits to offspring) and heritability of thermal tolerance, which can occur in fishes 2,24 . Thus, natural selection has the potential to improve thermal tolerance in Atlantic salmon beyond the demonstrated benefits of high thermal plasticity.…”

Indirect genetic effects underlie oxygen-limited thermal tolerance within a coastal population of chinook salmon

“…A switch from aerobic to anaerobic metabolism occurs in fish as temperatures approach their CT max [16], typical of animals experiencing hypoxic conditions. Indeed, CT max and hypoxia tolerance are positively correlated among families of Atlantic salmon (Salmo salar) [40], suggesting a genetic basis for anaerobic capacity. We found that juvenile chinook salmon reach their maximum heart rate (i.e.…”