Deciphering male influence in gynogenetic Pengze crucian carp (Carassius auratus var. pengsenensis): insights from Nanopore sequencing of structural variations

Abstract

In this study, we investigate gynogenetic reproduction in Pengze Crucian Carp (Carassius auratus var. pengsenensis) using third-generation Nanopore sequencing to uncover structural variations (SVs) in offspring. Our objective was to understand the role of male genetic material in gynogenesis by examining the genomes of both parents and their offspring. We discovered a notable number of male-specific structural variations (MSSVs): 1,195 to 1,709 MSSVs in homologous offspring, accounting for approximately 0.52%–0.60% of their detected SVs, and 236 to 350 MSSVs in heterologous offspring, making up about 0.10%–0.13%. These results highlight the significant influence of male genetic material on the genetic composition of offspring, particularly in homologous pairs, challenging the traditional view of asexual reproduction. The gene annotation of MSSVs revealed their presence in critical gene regions, indicating potential functional impacts. Specifically, we found 5 MSSVs in the exonic regions of protein-coding genes in homologous offspring, suggesting possible direct effects on protein structure and function. Validation of an MSSV in the exonic region of the polyunsaturated fatty acid 5-lipoxygenase gene confirmed male genetic material transmission in some offspring. This study underscores the importance of further research on the genetic diversity and gynogenesis mechanisms, providing valuable insights for reproductive biology, aquaculture, and fostering innovation in biological research and aquaculture practices.