Cortisol-Induced Masculinization: Does Thermal Stress Affect Gonadal Fate in Pejerrey, a Teleost Fish with Temperature-Dependent Sex Determination?

Abstract

BackgroundGonadal fate in many reptiles, fish, and amphibians is modulated by the temperature experienced during a critical period early in life (temperature-dependent sex determination; TSD). Several molecular processes involved in TSD have been described but how the animals “sense” environmental temperature remains unknown. We examined whether the stress-related hormone cortisol mediates between temperature and sex differentiation of pejerrey, a gonochoristic teleost fish with marked TSD, and the possibility that it involves glucocorticoid receptor- and/or steroid biosynthesis-modulation.Methodology/Principal FindingsLarvae maintained during the period of gonadal sex differentiation at a masculinizing temperature (29°C; 100% males) consistently had higher cortisol, 11-ketotestoterone (11-KT), and testosterone (T) titres than those at a feminizing temperature (17°C; 100% females). Cortisol-treated animals had elevated 11-KT and T, and showed a typical molecular signature of masculinization including amh upregulation, cyp19a1a downregulation, and higher incidence of gonadal apoptosis during sex differentiation. Administration of cortisol and a non-metabolizable glucocorticoid receptor (GR) agonist (Dexamethasone) to larvae at a “sexually neutral” temperature (24°C) caused significant increases in the proportion of males.Conclusions/SignificanceOur results suggest a role of cortisol in the masculinization of pejerrey and provide a possible link between stress and testicular differentiation in this gonochoristic TSD species. Cortisol role or roles during TSD of pejerrey seem(s) to involve both androgen biosynthesis- and GR-mediated processes. These findings and recent reports of cortisol effects on sex determination of sequential hermaphroditic fishes, TSD reptiles, and birds provide support to the notion that stress responses might be involved in various forms of environmental sex determination.

On the proper rearing density in domesticated zebrafish to avoid unwanted masculinization. Links with the stress response

“…Similar effects were observed in other fish species, i.e. medaka (Hayashi et al, 2010), Japanese flounder and pejerrey (Hattori et al, 2009) -in the latter, fish showed elevated cortisol levels after being exposed to high temperature. In the Southern flounder, the stress caused by the background colour of the tank increased cortisol levels and skewed sex ratios towards males (Mankiewicz et al, 2013).…”

“…In recent years, it has become evident that elevated plasma or whole-body cortisol levels during early development can also affect the process of sex differentiation, resulting in an increase in the number of males in different species, including medaka, Oryzias latipes (Hayashi et al, 2010), pejerrey, Odontesthes bonariensis (Hattori et al, 2009), southern flounder, Paralichthys lethostigma (Mankiewicz et al, 2013), and Japanese flounder, P. olivaceus . However, each one of these studies proposed a distinct, albeit not necessarily mutually exclusive, mechanism on the underlying mechanism responsible for masculinization by cortisol.…”

Demonstration of viability and fertility and development of a molecular tool to identify YY supermales in a fish with both genotypic and environmental sex determination

“…We also noted while performing artificial fertilization that all 1‐year‐old YY males ( n  = 11) had abundant milt production compared to 36.4% (eight of 22) in XY males (unpublished observations), suggesting that the former may attain sexual maturation earlier than the latter. Studies including mRNA quantification of genes involved in amh signaling (such as amhy , amha , and amhr2 ) and measurement of androgens and stress hormones, which are related to sex determination in pejerrey (Fernandino, Hattori, Kishi, Strüssmann, & Somoza, 2012; Hattori, Fernandino, et al., 2009), will be conducted for comparison of thermal sensitivity between XY and YY fish. Similar studies should examine whether amhy has any role in the onset of puberty in this species that could explain the early maturation observed in YY fish.…”

Analysis of Sexually Dimorphic Expression of Genes at Early Gonadogenesis of Pejerrey <i>Odontesthes bonariensis</i> Using a Heterologous Microarray

“…In this species, all-male or all-female populations can be easily obtained by temperature manipulation [Strüss-mann et al, 1997]. Recently, cortisol was proposed as a link between stress and testicular differentiation in pejerrey [Hattori et al, 2009]. Nevertheless, the genes that are differentially expressed during gonadogenesis and potentially participate in the cascade of gonadal differentiation process in pejerrey are largely unknown.…”

“…Some genes have been identified as 'male-specific' such as dmrt1 , amh , sox9 , nr5a1 , cyp11a1 , and cyp11b [Fernandino et al, 2008a;Blasco et al, 2010], whereas others, such as cyp19a1a , show 'female-specific' expression [Karube et al, 2007;Fernandino et al, 2008a]. In addition, previous studies suggest that gonadal apoptosis is associated with masculinization in pejerrey and therefore is absent in gonads at feminizing conditions Hattori et al, 2009]. However, a large-scale analysis of genes potentially involved in gonadogenesis has not been performed in this or any other TSD species.…”