Mitochondrial mutations and sterility in the interspecific hybrids of the hermaphroditic Argopecten scallops

Abstract

The sterility of hybrids from interspecific hybridization limits speciation, which widely exists in interspecific hybrids of hermaphroditic plants and also been found in the F1 hybrids of hermaphroditic Argopecten scallops. However, the underlying mechanism of sterility remained unexplored in hermaphroditic animals. In this study, we firstly investigated the mechanism of sterility in the interspecific F1 hybrids of Argopecten scallops by examining the mutations in mitochondrial genes and expressions of nuclear genes. Our results showed that the ATP content in gonads of F1 hybrids was significantly lower than their parents, indicating that energy deficiency may be an immediate cause of sterility in F1 hybrids. The SNP variation types of transition in mitochondrial genes (CYTB, ND4, ND2, ATP6, and COX2) could change their hydrophobicity of amino acids and protein structures, which might contribute to sterility in F1 hybrids. The mutations and rearrangements of mitochondrial genes and abnormal expression of nuclear genes were found in F1 hybrids. Abnormal interaction between the mitochondrial and nuclear genes might contribute to sterility of the F1 hybrids 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 resulted from abnormal expression of other nuclear genes. The mechanism of sterility in interspecific hybrids of hermaphroditic animals would provide more information for understanding the reproductive isolation and exploitation of heterosis.

On The Origin of Speciation

“…Spermatocytes of mutant mice with partial deletion of mtDNA exhibit meiotic arrest (Nakada et al, 2006). As mentioned above, interspecific hybrid F1 gonads of scallops indicate that cell cycle arrest due to ATP depletion is the direct cause of hybrid sterility (Yu et al 2022). Dmc1 that causes meiotic arrest due to synaptic failure by the defect is ATP-dependent (Pittman et al, 1998).…”

“…Hayashida et al 2009 showed by TUMEL assay using confocal fluorescence microscopic image that spermatocytes of mouse hybrid sterility testis have mtDNA disruption, but not nuclei. Recently, Yu et al, 2022 showed that the direct cause of hybrid sterility in scallops is cell cycle arrest due to ATP depletion in interspecific hybrid F1 gonads. Mutations, rearrangements, depletions, etc.…”