Reconstruction of the Origin of a Neo-Y Sex Chromosome and Its Evolution in the Spotted Knifejaw,Oplegnathus punctatus

Abstract

Sex chromosomes are a peculiar constituent of the genome because the evolutionary forces that fix the primary sex-determining gene cause genic degeneration and accumulation of junk DNA in the heterogametic partner. One of the most spectacular phenomena in sex chromosome evolution is the occurrence of neo-Y chromosomes, which lead to X1X2Y sex-determining systems. Such neo-sex chromosomes are critical for understanding the processes of sex chromosome evolution because they rejuvenate their total gene content. We assembled the male and female genomes at the chromosome level of the spotted knifejaw (Oplegnathus punctatus), which has a cytogenetically recognized neo-Y chromosome. The full assembly and annotation of all three sex chromosomes allowed us to reconstruct their evolutionary history. Contrary to other neo-Y chromosomes, the fusion to X2 is quite ancient, estimated at 48 Mya. Despite its old age and being even older in the X1 homologous region which carries a huge inversion that occurred as early as 55-48 Mya, genetic degeneration of the neo-Y appears to be only moderate. Transcriptomic analysis showed that sex chromosomes harbor 87 genes, which may serve important functions in the testis. The accumulation of such male-beneficial genes, a large inversion on the X1 homologous region and fusion to X2 appear to be the main drivers of neo-Y evolution in the spotted knifejaw. The availability of high-quality assemblies of the neo-Y and both X chromosomes make this fish an ideal model for a better understanding of the variability of sex determination mechanisms and of sex chromosome evolution.

Chromosome-Level Assembly of the Southern Rock Bream (Oplegnathus fasciatus) Genome Using PacBio and Hi-C Technologies

“…The total length of assembly contained 24 chromosomes (the lengths ranged from 18.22 to 37.18 Mb) was 723.22 Mb, and the integration efficiency was 98.67% (Table 1 and Supplementary Table S2). The genome sizes of O. fasciatus (733.99 Mb) were similar with two closely related Perciformes species i.e., L. crocea (723.86 Mb) (Chen et al, 2019a) and Oplegnathus punctatus (718 Mb) (Li et al, 2021). To further verify the integrality of the assembled genome, the reads from the short-insert library were re-mapped onto the assembled genome using BWA (version 0.7.17).…”

Sex determination mechanisms and sex control approaches in aquaculture animals

“…The ancestral X (X 1 ) and Y chromosomes evolved from a pair of autosomes over 60 Mya, and recombination was further suppressed by an inversion approximately 55 Mya. Finally, the Y chromosome was fused to the X 2 chromosome via Robertsonian translocation at 48 Mya, leading to neo-Y sex chromosome (Li et al, 2021a). Compared with the ancient time of neo-Y chromosome formation in spotted knifejaw, the neo-sex chromosome occurred much more recent in Japanese threespine stickleback fish (G. aculeatus), which were estimated to 1.5-2 Mya.…”

Identification of Male-Specific Molecular Markers by Recombination of RhoGEF10 Gene in Spotted Knifejaw (Oplegnathus punctatus)

“…Since O. punctatus is a native natural species in China, the development and sustainable use of its resources are more long-lasting, and the breeding prospects are extremely broad. The karyotype of female O. punctatus is 2 n = 48 with genetic sex type (X1X1X2X2), and the karyotype of the male is 2 n = 47 with one large metacentric Y chromosome in male individuals of O. punctatus chromosome and genetic sex type (X1X2Y) [ 4 , 5 , 6 ]. The spotted knifejaw has significant male and female growth dimorphism in the breeding process, male individuals grow faster than female fish, the preparation of O. punctatus Kaohsiung fry and the all-male fry will promote the quality and efficiency of O. punctatus breeding industry, and the development of rapid genetic sex identification technology for grouper fry will help the reserve of excellent male germplasm of O. punctatus [ 7 ].…”