Characterization and trans-generation dynamics of mitogene pool in the silver carp (Hypophthalmichthys molitrix)

Abstract

Abstract Multicopied mitogenome are prone to mutation during replication often resulting in heteroplasmy. The derived variants in a cell, organ, or an individual animal constitute a mitogene pool. The individual mitogene pool is initiated by a small fraction of the egg mitogene pool. However, the characteristics and relationship between them has not yet been investigated. This study quantitatively analyzed the heteroplasmy landscape, genetic loads, and selection strength of the mitogene pool of egg and hatchling in the silver carp (Hypophthalmichthys molitrix) using high-throughput resequencing. The results showed heteroplasmic sites distribute across the whole mitogenome in both eggs and hatchlings. The dominant substitution was Transversion in eggs and Transition in hatching accounting for 95.23%±2.07% and 85.38%±6.94% of total HP sites, respectively. The total genetic loads were 0.293±0.044 in eggs and 0.228±0.022 in hatchlings (P=0.048). The dN/dS ratio was 58.03±38.98 for eggs and 9.44±3.93 for hatchlings (P=0.037). These results suggest that the mitogenomes were under strong positive selection in eggs with tolerance to variants with deleterious effects, while the selection was positive but much weaker in hatchlings showing marked quality control. Based on these findings, we proposed a trans-generation dynamics model to explain differential development mode of the two mitogene pool between oocyte maturation and ontogenesis of offspring. This study sheds light on significance of mitogene pool for persistence of populations and subsequent integration in ecological studies and conservation practices.