Hybrid sterility in hermaphroditic Argopecten scallops: Mutated mitochondrial genes and abnormal expression of nuclear genes

Abstract

Bay scallops (Argopecten irradians) are a commercially important bivalve species for fisheries and aquaculture in China, the USA, Peru and Chile, but their small size and serious inbreeding depression restrict the sustainable development of their aquaculture. We successfully hybridized bay scallops with Peruvian scallops (Argopecten purpuratus), and the F1 hybrids showed significant heterosis in growth, but the majority of them were sterile. Nevertheless, Argopecten scallops are typical hermaphroditic animals, resulting in a low proportion of interspecific hybrids. Hybrid sterility restricts the utilization of Argopecten scallop resources and causes reproductive isolation in speciation. However, the underlying mechanism of hybrid sterility remains unexplored in hermaphroditic scallops. In this study, we investigated the mechanism of hybrid sterility in hermaphroditic Argopecten scallops by examining mutations in mitochondrial genes and the expression of nuclear genes. Our results showed that the ATP content in the gonads of F1 hybrid scallops was significantly lower than that in their parents, indicating that energy deficiency may be an immediate cause of sterility in F1 hybrid scallops. Thirteen SNPs were detected in five mitochondrial genes of F1 hybrids, and 92.3% of which were transitions that could change the hydrophobicity of amino acids and protein structures, and the allele frequencies of the SNP loci were significantly different between sterile hybrids and fertile scallops. Abnormal interaction between the mitochondrial and nuclear genes might contribute to hybrid sterility through the following pathways: (1) inhibition of oocyte maturation by enhanced expression of Mfn2; (2) cell cycle arrest in G1 phase of oocytes by inhibited expression of CDK2; (3) cell apoptosis induced by mitochondrial apoptosis; (4) insufficient energy supply from abnormal mitochondria, and (5) mitochondrial dysfunction resulting from abnormal expression of other nuclear genes. The present results provide more information for understanding the mechanism of hybrid sterility in hermaphroditic animals and benefit extensive hybrid breeding.