Heritable Genetic Effects Caused by a Single Generation of Captive Breeding

ABSTRACT Understanding the genetic effects of captive breeding is critical for successful fisheries management and conservation efforts. Recent work has demonstrated that genetic adaptation to captivity, with resulting loss of fitness in the wild environment, can occur in as little as a single generation. To understand the genetic changes underlying such rapid adaptation, we performed crosses within and between first‐generation hatchery and natural‐origin steelhead ( Oncorhynchus mykiss ), raised their offspring in a common environment, and used RNA‐seq to examine global patterns of gene expression in those offspring. We found: (i) substantial transcriptomic evidence (hundreds of differentially expressed genes; DEGs) of genetic change induced by a single generation in the captive environment, where the majority of DEGs were upregulated in the offspring of first‐generation hatchery fish (75%), (ii) reciprocal crosses revealed that the differentially expressed genes could not be explained by maternal/paternal effects, chance differences in the background levels of gene expression among unrelated families, or other potential explanations, and (iii) the majority of DEGs are related to growth, development, behavior, immune response, and metabolism. These results demonstrate that a single generation of captive breeding results in the heritable activation of hundreds of genes with consequences for stocking or reintroduction efforts.