Deciphering the Evolution of Neo-Y Chromosomes: Insights from the Spotted Knifejaw Genome

Sex chromosome evolution is one of the most fascinating processes in genomic research, with profound implications for understanding genetic differentiation and adaptation. In our recent study, published in Molecular Biology and Evolution, we assembled chromosome-level genomes for both male and female spotted knifejaw (Oplegnathus punctatus), a marine fish species with a unique X1X2Y sex chromosome system. This work provides a detailed reconstruction of neo-Y chromosome formation and its evolutionary trajectory, contributing valuable knowledge to sex chromosome research.

Key Findings

• Genome Assembly and Sex Chromosome Structure:
  Using PacBio long-read sequencing, Nanopore sequencing, and Hi-C scaffolding, we generated high-contiguity genome assemblies for both sexes. The male genome spans 831 Mb, while the female genome is 764 Mb, closely aligning with cytogenetic observations. Crucially, our assembly includes the full-length sequences of all three sex chromosomes (X1, X2, and neo-Y), enabling an unprecedented evolutionary analysis.

• Evolutionary History of the Neo-Y Chromosome:
  Through comparative analysis, we reconstructed the formation of the neo-Y chromosome, showing that:
  • A large chromosomal inversion occurred ~55 million years ago, suppressing recombination in an ancestral Y chromosome.
  • A subsequent Robertsonian translocation fused the ancestral Y with an autosome, forming the neo-Y chromosome ~48 million years ago.
  • Despite its old age, the neo-Y exhibits only moderate genetic degeneration, retaining a significant proportion of functional genes.
• Functional Gene Annotation and Sex-Specific Expression:
  Transcriptomic profiling of gonads revealed 87 male-biased genes on the sex chromosomes, including key genes involved in spermatogenesis. These findings suggest positive selection for male-beneficial genes, influencing the genetic structure of the neo-Y chromosome.

Reflections

This project marks an important milestone for our genomic research in Qingdao. Following the establishment of BGI-Qingdao, we actively developed long-term collaborations with local research institutions, strengthening joint efforts in genome sequencing and evolutionary genomics. This partnership has allowed us to accelerate project funding applications and streamline scientific publications, paving the way for more extensive studies in marine genomics.

As we analyzed the evolution of the neo-Y chromosome, I was struck by the complexity and unique trajectory of sex chromosome differentiation in teleost fish. Unlike classical mammalian sex chromosomes, the spotted knifejaw’s system demonstrates a prolonged yet incomplete degeneration process, offering rare insights into how genetic recombination, inversion events, and translocations shape sex chromosome evolution. With the foundation of this study in place, our team looks forward to exploring more species with unusual sex-determination systems, further advancing comparative genomics research.

The full text of this study can be accessed online at Molecular Biology and Evolution.