Highly and lowly domesticated endangered fish from a conservation hatchery diverge in their thermal physiology, transcriptome, and methylome

Conservation hatcheries aim to produce fish for supplementation of wild populations, but hatchery environments may drive phenotypic divergence from wild fish. These diverged traits may have reduced fitness in the wild, which could compromise wild population sustainability and evolutionary potential, such as in response to climate change. Delta smelt are a critically endangered fish species that are safeguarded against extinction with a hatchery refuge population. We investigated whether elevated rearing temperature through larval development adjusted upper thermal tolerance limits (acclimation) in Delta smelt, whether upper thermal tolerance and plasticity (acclimation ability) differed between fish with old or recent hatchery ancestry (high or low domestication index; DI), and temperature and DI effects on liver transcriptome and methylome patterns. We observed that elevated rearing temperatures induced higher thermal tolerance (acclimation). Individuals with higher DI also had higher upper thermal tolerances, but high DI families had reduced thermal plasticity between rearing temperatures. This is consistent with domestication causing heritable elevation of upper thermal tolerance but at the cost of reduced thermal plasticity. High and low DI fish were differentiated in both genetic variation and methylome variation, suggesting the influence of both during domestication. But methylome differences distinguishing high and low DI fish did not overlap with temperature-induced methylome changes, and do not appear to be stably inherited in the hatchery. We conclude that domestication selection has altered thermal physiology within the refuge hatchery despite careful genetic management, underpinned by shifts in the transcriptome and methylome. These changes could affect Delta smelt fitness upon reintroduction to habitats that continue to warm, and show that physiological traits can diverge even within carefully genetically managed hatchery populations.