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

Abstract

With global temperatures projected to surpass the limits of thermal tolerance for many species, evaluating the heritable variation underlying thermal tolerance is critical for understanding the potential for adaptation to climate change. We examined the evolutionary potential of thermal tolerance within a population of chinook salmon (Oncorhynchus tshawytscha) by conducting a full-factorial breeding design and measuring the thermal performance of cardiac function and the critical thermal maximum (CT max ) of offspring from each family. Additive genetic variation in offspring phenotype was mostly negligible, although these direct genetic effects explained 53% of the variation in resting heart rate ( f H ). Conversely, maternal effects had a significant influence on resting f H , scope for f H , cardiac arrhythmia temperature and CT max . These maternal effects were associated with egg size, as indicated by strong relationships between the mean egg diameter of mothers and offspring thermal tolerance. Because egg size can be highly heritable in chinook salmon, our finding indicates that the maternal effects of egg size constitute an indirect genetic effect contributing to thermal tolerance. Such indirect genetic effects could accelerate evolutionary responses to the selection imposed by rising temperatures and could contribute to the population-specific thermal tolerance that has recently been uncovered among Pacific salmon populations.

Unusual aerobic performance at high temperatures in juvenile Chinook salmon,Oncorhynchus tshawytscha

“…Literature on critical thermal maximum (CT Max ) and upper incipient lethal temperature (Table 3) show that juvenile Chinook salmon experience mortality when exposed to or held at temperatures above 24°C. Given that CT Max data for these fish range from 26.5 to 28.6°C (Muñoz et al ., 2014; Fangue, N., Baird, S., and Cocherell, D., unpublished), exercise-induced mortality occurred below the CTmax, as might be expected. Moreover, the present population has the highest reported CT Max (28.6°C), which could indicate a local thermal adaptation for this autumn-run population of Chinook in California.…”

Effects of seasonal acclimatization on temperature-dependence of cardiac excitability in the roach, Rutilus rutilus

“…Traditionally, thermal acclimation is divided into resistance acclimation and capacity acclimation (Precht et al, 1955). Acclimation to new thermal conditions could appear as widening of thermal tolerance limits and quantitative changes in physiological performance in order to restore body functions towards their original levels (Hazel and Prosser, 1974).…”

“…Important questions in regard to thermal tolerance of heart function in roach and other fishes are: (1) how does deterioration of heart function appear in the ECG, (2) is it possible to determine the exact temperature for cardiac arrhythmias, and (3) are important, as cardiac arrhythmias in fishes are poorly described and seldom defined, but are, however, sometimes used to make farreaching ecological predictions about the fate and success of fishes in future climates (Munoz et al, 2014). The T BP of in vivo f H , determined as the temperature at which bradycardia started, for winter (19.8±0.5°C) and summer roach (28.1±0.5°C) are close to the upper thermal tolerance limits of 22 and 28°C determined by Cocking for 3°C-and 18°C-acclimated roach, respectively (Cocking, 1959).…”

“…Temperature has profound effects on the physiology of ectothermic animals at all levels of body organization from the whole-body metabolic rate down to the molecular functions (Precht et al, 1955). Most fishes are ectotherms and their body temperature is practically identical to the ambient water temperature; therefore, each organ of the fish will experience all temperature variations of the habitat (Hazel and Prosser, 1974).…”

Indirect genetic effects in behavioral ecology: does behavior play a special role in evolution?

“…The strength and direction of IGEs can also evolve over time and across populations (Chenoweth et al 2010;Bailey and Zuk 2012;Kazancioğlu et al 2012;Edenbrow et al 2017), and associated social selection is predicted to vary accordingly (McGlothlin et al 2010). In recent years, IGEs have been incorporated into animal and plant breeding studies to more accurately predict evolutionary responses in agriculturally valuable traits, such as growth rate, thermal tolerance, and infection risk (Camerlink et al 2013(Camerlink et al , 2014(Camerlink et al , 2015Costa e Silva et al 2013;Anche et al 2014;Muñoz et al 2014;Alemu et al 2016;Baud et al 2017). A substantial literature explores the mathematical approaches used to study IGEs.…”