B Chromosomes Have a Functional Effect on Female Sex Determination in Lake Victoria Cichlid Fishes

Abstract

The endemic cichlid fishes in Lake Victoria are a model system for speciation through adaptive radiation. Although the evolution of the sex-determination system may also play a role in speciation, little is known about the sex-determination system of Lake Victoria cichlids. To understand the evolution of the sex-determination system in these fish, we performed cytogenetic analysis in 11 cichlid species from Lake Victoria. B chromosomes, which are present in addition to standard chromosomes, were found at a high prevalence rate (85%) in these cichlids. In one species, B chromosomes were female-specific. Cross-breeding using females with and without the B chromosomes demonstrated that the presence of the B chromosomes leads to a female-biased sex ratio in this species. Although B chromosomes were believed to be selfish genetic elements with little effect on phenotype and to lack protein-coding genes, the present study provides evidence that B chromosomes have a functional effect on female sex determination. FISH analysis using a BAC clone containing B chromosome DNA suggested that the B chromosomes are derived from sex chromosomes. Determination of the nucleotide sequences of this clone (104.5 kb) revealed the presence of several protein-coding genes in the B chromosome, suggesting that B chromosomes have the potential to contain functional genes. Because some sex chromosomes in amphibians and arthropods are thought to be derived from B chromosomes, the B chromosomes in Lake Victoria cichlids may represent an evolutionary transition toward the generation of sex chromosomes.

Author Summary

The diversity of sex chromosomes among animal species is well known, but how these sex chromosomes emerged during evolutionary history remains to be solved. One hypothesis for the origin of sex chromosomes is that a portion of the sex chromosome was derived from B chromosomes. In about 10% of eukaryotes, B chromosomes are found in addition to standard chromosomes (sex chromosomes and autosomes). B chromosomes have been thought to be selfish genetic elements with no functional effect on the phenotype of individuals and have been thought to lack protein-coding genes. Although B chromosomes share unique features with sex chromosomes, concrete evidence describing which B chromosomes have evolved to gain a function in sex determination has not been reported. In this study, we found that B chromosomes in one cichlid species from Lake Victoria have a functional effect on sex determination. Moreover, we found that they contained multiple protein-coding genes including morphogenetic related genes. These findings support the hypothesis that a portion of the sex chromosomes has been derived from B chromosomes and shed light on the study of the evolution of sex chromosomes.