ABSTRACT
BACKGROUND: The factors determining sex are diverse in vertebrates and especially so in teleost fishes. Only a handful of master sex-determining genes have been identified, however great efforts have been undertaken to characterize the subsequent genetic network of sex differentiation in various organisms. East African cichlids offer an ideal model system to study the complexity of sexual development, since many different sex-determining mechanisms occur in closely related species of this fish family. Here, we investigated the sex-determining system and gene expression profiles during male development of Astatotilapia burtoni, a member of the rapidly radiating and exceptionally species-rich haplochromine lineage. RESULTS: Crossing experiments with hormonally sex-reversed fish provided evidence for an XX-XY sex determination system in A. burtoni. Resultant all-male broods were used to assess gene expression patterns throughout development of a set of candidate genes, previously characterized in adult cichlids only. CONCLUSIONS: We could identify the onset of gonad sexual differentiation at 11-12 dpf. The expression profiles identified wnt4B and wt1A as the earliest gonad markers in A. burtoni. Furthermore we identified late testis genes (cyp19a1A, gsdf, dmrt1 and gata4), and brain markers (ctnnb1A, ctnnb1B, dax1A, foxl2, foxl3, nanos1A, nanos1B, rspo1, sf-1, sox9A and sox9B).
Subject(s)
Cichlids/genetics , Gene Expression Regulation, Developmental , Sex Determination Processes , Animals , Base Sequence , Binding Sites , Cichlids/metabolism , Female , Fish Proteins/genetics , Fish Proteins/metabolism , Gene Regulatory Networks , Genetic Markers , Male , Organ Specificity , Sex Differentiation , Transcription Factors/genetics , Transcription Factors/metabolism , TranscriptomeABSTRACT
Teleost fishes are the most species-rich clade of vertebrates and feature an overwhelming diversity of sex-determining mechanisms, classically grouped into environmental and genetic systems. Here, we review the recent findings in the field of sex determination in fish. In the past few years, several new master regulators of sex determination and other factors involved in sexual development have been discovered in teleosts. These data point toward a greater genetic plasticity in generating the male and female sex than previously appreciated and implicate novel gene pathways in the initial regulation of the sexual fate. Overall, it seems that sex determination in fish does not resort to a single genetic cascade but is rather regulated along a continuum of environmental and heritable factors.
Subject(s)
Fishes/genetics , Sex Determination Processes , Animals , Biological Evolution , Female , Fishes/classification , Fishes/physiology , Gene-Environment Interaction , Genetic Variation , MaleABSTRACT
Sex determination mechanisms are highly variable across teleost fishes and sexual development is often plastic. Nevertheless, downstream factors establishing the two sexes are presumably conserved. Here, we study sequence evolution and gene expression of core genes of sexual development in a prime model system in evolutionary biology, the East African cichlid fishes. Using the available five cichlid genomes, we test for signs of positive selection in 28 genes including duplicates from the teleost whole-genome duplication, and examine the expression of these candidate genes in three cichlid species. We then focus on a particularly striking case, the A- and B-copies of the aromatase cyp19a1, and detect different evolutionary trajectories: cyp19a1A evolved under strong positive selection, whereas cyp19a1B remained conserved at the protein level, yet is subject to regulatory changes at its transcription start sites. Importantly, we find shifts in gene expression in both copies. Cyp19a1 is considered the most conserved ovary-factor in vertebrates, and in all teleosts investigated so far, cyp19a1A and cyp19a1B are expressed in ovaries and the brain, respectively. This is not the case in cichlids, where we find new expression patterns in two derived lineages: the A-copy gained a novel testis-function in the Ectodine lineage, whereas the B-copy is overexpressed in the testis of the speciest-richest cichlid group, the Haplochromini. This suggests that even key factors of sexual development, including the sex steroid pathway, are not conserved in fish, supporting the idea that flexibility in sexual determination and differentiation may be a driving force of speciation.
