Transcriptional evolution underlying vertebrate sexual development

Abstract

Explaining the diversity of vertebrate sex-determining mechanisms ranging from genotypic (GSD) to temperature-dependent (TSD) remains a developmental and evolutionary conundrum. Using a phylogenetic framework, we explore the transcriptional evolution during gonadogenesis of several genes involved in sexual development, combining novel data from Chrysemys picta turtles (TSD) and published data from other TSD and GSD vertebrates. Our novel C. picta dataset underscores Sf1 and Wt1 as potential activators of the thermosensitive period and uncovered the first evidence of Dax1 involvement in male development in a TSD vertebrate. Contrasting transcriptional profiles revealed male-biased Wt1 expression in fish while monomorphic expression is found in tetrapods but absent in turtles. Sf1 expression appears highly labile with transitions among testicular, ovarian, and non-sex-specific gonadal formation patterns among and within lineages. Dax1's dual role in ovarian and testicular formation is found in fish and mammals but is dosage-sensitive exclusively in eutherian mammals due to its X-linkage in this group. Contrastingly, Sox9 male-biased and Aromatase female-biased expression appear ancestral and virtually conserved throughout vertebrates despite significant heterochronic changes in expression as other elements likely replaced their function in early gonadogenesis. Finally, research avenues are highlighted to further study the evolution of the regulatory network of sexual development. Developmental Dynamics 242:307-319,

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

“…This difference represents just a fraction (8%) of the ∼15,000 DETs that were differentially expressed between untreated females (FCT) and males (MCT), which, in turn, account for a significant part of the estimated number of protein-coding genes (>25,000) in zebrafish. In fish, masculinization by elevated temperature usually involves down-regulation of profemale genes, such as cyp19a1a and foxl2, and up-regulation of promale genes, such as dmrt1 or amh (8)(9)(10)(11)(12)(13)(14). In accordance with this general pattern, the FHT2 females with a male-like gonadal transcriptome exhibited down-regulation of both key profemale genes such as cyp19a1a and vtg5 as well as downregulation of profemale pathways such as oocyte meiosis, progesterone-mediated oocyte maturation, canonical Wnt signaling (28,53), and Fanconi anemia (26).…”

Genetics of Sexual Development: An Evolutionary Playground for Fish

“…Interestingly, steroid hormones, or the regulation of their production, are a putative link between ESD and GSD (Nakamura 2010;Angelopoulou et al 2012), with cyp19a1 being a prime candidate (Valenzuela et al 2013). NavarroMartín et al (2011) have recently investigated the methylation levels of the aromatase (cyp19a1A) promoter in the European sea bass, Dicentrarchus labrax, a species with a polygenic SD system influenced by temperature (Vandeputte et al 2007).…”

Molecular Cytogenetic Search for Cryptic Sex Chromosomes in Painted Turtles <b><i>Chrysemys picta</i></b>

“…Data on sex determination was collected from the literature [Olmo, 2005;Olmo and Signorino, 2005;Vogt, 2008;Leaché and Sites, 2009;Paez et al, 2009;Pokorná and Kratochvíl, 2009;Shibaike et al, 2009;Bernhard, 2010;Okada et al, 2010;Zhang et al, 2010;Hare et al, 2011;Valenzuela and Adams, 2011;Inamdar et al, 2012;Rojo et al, 2012;Tang et al, 2012;Valenzuela et al, 2013]. Lizards are paraphyletic with snakes nested within this clade.…”