# Evidence for Paternal Mitochondrial DNA Leakage in Diploid Hybrid Fish Lineages

## TL;DR

This study shows that distant hybridization in fish leads to unstable mitochondrial DNA, with random paternal leakage followed by selective elimination to stabilize hybrid offspring.

## Contribution

The study reveals paternal mitochondrial DNA leakage and selective elimination in hybrid fish lineages, offering new insights into hybrid adaptability and mitochondrial evolution.

## Key findings

- Paternal mtDNA leakage occurs randomly in first-generation hybrid fish.
- Selective pressure eliminates incompatible mtDNA variations in hybrid lineages.
- Subsequent self-crossing reduces structural variation in mitochondrial genomes.

## Abstract

Distant hybridization can induce rapid changes in the genotype and phenotype of offspring. Compared to the nuclear genome, the mitochondrial genome often possesses greater potential for cross-species introgression. This distinction facilitates the more stable transmission of mitochondrial DNA (mtDNA) in hybrid offspring, directly regulates their adaptability, and provides a key driving force for species evolution. Here, through an analysis of complete mitochondrial genome genetic variation in offspring from distant hybridization between female common carp and male blunt snout bream, we reveal that the mitochondrial genomes in first-generation hybrid species are unstable under the impact of distant hybridization shock, exhibiting paternal mtDNA leakage with randomness. However, to establish viable offspring under the impact of distant hybridization shock, strong selective pressure activates a selective elimination mechanism within the mitochondria, purging incompatible mtDNA genetic variations from the first-generation hybrid lineages, thereby achieving a new state of stability. This study provides an ideal model for elucidating the regulatory mechanisms by which paternal mitochondrial DNA leakage influences hybrid species adaptability, holding significant implications for both mitochondrial genome evolution research in distant hybrid species and the practice of fish genetic breeding.

Distant hybridization induces genomic instability in offspring, driving the occurrence of gene recombination and mutation. Analysis of the genomic genetic composition can be used to infer the genetic evolutionary relationships between species. Based on the improved diploid carp (IDC) and the improved diploid scattered mirror carp (IDMC) lineages derived from distant hybridization between female common carp and male blunt snout bream, this study analyzed the genetic variation in their mitochondrial genomes to investigate the impact of distant hybridization on mitochondrial DNA (mtDNA) structural variation. Analysis of complete mitochondrial genome sequence structure and composition revealed subtle structural divergence across generations in both the IDC and IDMC lineages. Analysis of the protein-coding gene sequence structure demonstrated mitochondrial genome structure instability in nascent hybrid diploid lineages. Yet, subsequent self-crossing significantly narrowed the range of structural variation within each lineage. Furthermore, analysis of the genetic variation in the mitochondrial genome sequence structure revealed that paternal base insertions occurred in both F1 lineages, accompanied by mutations predominantly consistent with those in crucian carp. The results of this study also indicated that the strictness of the paternal mtDNA elimination mechanism varied significantly among polymorphic individuals across different generations of the hybrid lineages, reflecting the randomness of paternal leakage.