Genetic divergence of selected and wild populations of Pacific oysters (Crassostrea gigas) on the West Coast of North America

The Molluscan Broodstock Program (MBP) has been selecting Pacific oysters Crassostrea gigas for improved yield for over two decades. Nevertheless, realized gain in yield, the percent difference in least-square mean yield between MBP and pooled control families made from “wild” stock, was reported to be zero in the fifth generation. Among the potential explanations for zero realized gain was that MBP-derived stock had spread or reproduced in bays with extensive oyster farming and contributed to the “wild” broodstock used for the control population. This “MBP = wild” hypothesis was tested by analyses of genetic data from four MBP cohorts and 11 wild populations, including founders of MBP cohorts. A new 2016 sample from Willapa Bay, the primary source of MBP's control families, was genotyped by high-resolution melting (HRM) of 45, SNP-containing PCR amplicons and compared to previous HRM data for a 1996 sample. Average temporal variance in allele frequencies for Willapa Bay implies a small, local, effective population size (Ne = 55, 95% CI, 32–159) with very high gene flow among Pacific Northwest populations (migration rate, m = 0.99, 95% CI, 0.25–1.0). These estimates, which are remarkably consistent with previous estimates, also based on 20-y intervals, for populations in Pipestem Inlet and Dabob Bay, support the general conclusion that the North American Pacific oyster metapopulation is evolving by genetic drift, likely owing to local sweepstakes reproductive processes, with high gene flow maintaining spatial similarity. Direct comparison of MBP and wild populations reveals 7× more genetic divergence between selected and wild populations than among wild populations. Evidence for genetic drift within the Willapa Bay wild population that is uncorrelated with genetic drift in Dabob Bay, together with evidence for genetic drift between MBP and all wild populations studied to date, falsifies the hypothesis that gene flow from MBP-derived commercial stocks to wild populations is responsible for a realized gain in yield of zero. Further analyses of parentage and relatedness in four MBP cohorts suggests that pedigree errors may have contributed to inaccuracies in the selective breeding program and resulted in the observed realized gain in yield of zero. •“Selected oysters = wild controls” does not explain zero realized gain in yield.•Selected stocks and wild populations have diverged by random genetic drift.•Genetic analyses of selected oysters and their parents r