Weak genetic divergence and signals of adaptation obscured by high gene flow in an economically important aquaculture series

Authors: Calla, Bernarda; SONG, JINGWEI - Oregon State University; Thompson, Neil

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/17/2025
Publication Date: 2/5/2025
Citation: Calla, B., Song, J., Thompson, N. 2025. Weak genetic divergence and signals of adaptation obscured by high gene flow in an economically important aquaculture series. BMC Genomics 26, 112. https://doi.org/10.1186/s12864-025-11259-9.
DOI: https://doi.org/10.1186/s12864-025-11259-9

Interpretive Summary: Pacific oysters are an important agricultural product for the U.S. Pacific Coast. Available genetic diversity of Pacific oysters determines their resiliency and adaptability to changing environments. Genetic diversity also determines Pacific oysters’ potential for breeding: crossing of selected individuals or families to improve traits of interest such as survival and growth. Under this view, comprehensive knowledge of the current genetic diversity in Pacific oysters on the U.S. West Coast remains fundamental to the development of practices that maintain health and productivity in this species. This is the first study that uses whole-genome resequencing to evaluate the genetic diversity within and between naturalized and captively reared populations of Pacific oysters along the U.S. Pacific Coast. We identified over 20 million high-confidence SNPs and used those to evaluate population genetic parameters with the aim of cataloguing genetic diversity and to better understand the effects of hatchery rearing and adaptation in this species.

Technical Abstract: The genetic diversity of a population defines its ability to adapt to episodic and fluctuating environmental changes. For species of agricultural value, available genetic diversity also determines their breeding potential. Comprehensive knowledge of the extant gene pool in Pacific oysters (Magallana gigas, previously Crassostrea gigas) remains fundamental to the development of practices that maintain health and productivity in this species. In this study we use whole-genome resequencing to evaluate the genetic diversity within and between naturalized and captively reared populations of Pacific oysters in the US Pacific coast. The analyses included individuals from preserved samples dating to 1998 (Dabob Bay; MBP6) and 2004 (Midori). Two contemporary naturalized populations (Willapa Bay and San Diego Bay), and one domesticated population (MBP30) were also included. We show that despite high heterozygosity, there was very low genetic divergence between populations. The MBP30 population which was reared in captivity for over 25 years was the most genetically distinct population and displayed the least nucleotide diversity, attributable to inbreeding. Unexpectedly, individuals from Willapa Bay and Dabob Bay (MBP6), separated both geographically and temporally, did not show detectable genetic differences. Fifty-nine significant FST outlier sites were identified, the majority of which were individually present in high proportions of the MBP30 samples. Functional annotation of those outlier sites was mined from public data repositories as they might hold clues into hatchery and breeding effects, but more studies would be necessary to conclude on specific pathways affected by these practices. In conclusion, Pacific oysters on the U.S. Pacific coast may hold enough genetic diversity to sustain health and efficient commercial productivity, but captive populations used in breeding programs should be routinely monitored to avoid potential inbreeding depression.