Three-way crossed scallops between Argopecten irradians irradians, A. i. concentricus and A. purpuratus exhibit strong heterosis in growth, survival and temperature tolerance

The bay scallops, including the northern subspecies Argopecten irradians irradians (NN) and southern subspecies A. i. concentricus (SS), are economically important cultured bivalves in China. Due to their hermaphroditic nature, the currently farmed bay scallops often suffered from significant inbreeding depression characterized by slow growth, high mortality and low-stress tolerance, especially in the hot summers. In this study, to further improve the production performance and stress resistance of bay scallops, we first conducted a two-way intraspecific hybridization between the two subspecies of the bay scallops (NN and SS), and then hybridized the two-way hybrids with the Peruvian scallop, A. purpuratus (PP) and obtained two three-way hybrids, NSP and SNP. During embryonic and larval stages, both two three-way hybrids exhibited higher fertilization rate, hatching rate and metamorphosis rate, larger initial D-larvae size, and faster embryonic development and larvae growth than those of their parental stocks. The two three-way crossed hybrids displayed excellent heterosis in both growth and survival at larval stage. Both egg origin and mating strategy had significant effects on growth at the larval stage, while the survival rate was mainly dictated by mating strategy. At adult grow-out stage, the heteroses in NSP and SNP cohorts were 12.36 and 19.92 in shell height, 40.37 and 53.27 in whole body weight, and 13.73 and 21.13 in survival rate at harvest, respectively. Moreover, temperature stress tolerance was significantly improved in the three-way crossed scallops. The gonads of most three-way crossed hybrids seemed to be morphologically and functionally females, although the fertility of eggs was very low, suggesting that more energy would be allocated for growth and survival. Notably, the genetic diversity was increased in both three-way hybrids. Therefore, the three-way crossed scallops are potentially precious breeding material for selecting new scallop strains and can be potentially widely cultured along both the southern and northern China coasts.