Stress and serial adult metamorphosis: multiple roles for the stress axis in socially regulated sex change

Abstract

Socially regulated sex change in teleost fishes is a striking example of social status information regulating biological function in the service of reproductive success. The establishment of social dominance in sex changing species is translated into a cascade of changes in behavior, physiology, neuroendocrine function, and morphology that transforms a female into a male, or vice versa. The hypothalamic-pituitary-interrenal axis (HPI, homologous to HP-adrenal axis in mammals and birds) has been hypothesized to play a mechanistic role linking status to sex change. The HPA/I axis responds to environmental stressors by integrating relevant external and internal cues and coordinating biological responses including changes in behavior, energetics, physiology, and morphology (i.e., metamorphosis). Through actions of both corticotropin-releasing factor and glucocorticoids, the HPA/I axis has been implicated in processes central to sex change, including the regulation of agonistic behavior, social status, energetic investment, and life history transitions. In this paper, we review the hypothesized roles of the HPA/I axis in the regulation of sex change and how those hypotheses have been tested to date. We include original data on sex change in the bluebanded goby (Lythyrpnus dalli), a highly social fish capable of bidirectional sex change. We then propose a model for HPA/I involvement in sex change and discuss how these ideas might be tested in the future. Understanding the regulation of sex change has the potential to elucidate evolutionarily conserved mechanisms responsible for translating pertinent information about the environment into coordinated biological changes along multiple body axes.

Stress and sex: does cortisol mediate sex change in fish?

“…Research on gonochoristic pejerrey has also come into conflict with the Substrate Competition for Enzymes hypothesis, since results on pejerrey larvae showed that the cortisol treatment was associated with significant increases in 11KT, but not T, during the first 4 weeks (Hattori et al 2009). In combination with data from Frisch et al (2007), an increase in cortisol levels was proposed as part of the trigger initiating sex change in sequential hermaphrodites by Solomon-Lane et al (2013), who argued that this elevation would increase corticotropinreleasing factor (CRF) signaling and activity of HPI axis. Their work on the bidirectional hermaphrodite Lythrypnus dalli (bluebanded goby) showed that cortisol peaked in early stages of sex change during which differences in HPI axis activity were also shown to reflect social status (Solomon-Lane et al 2013).…”

“…In combination with data from Frisch et al (2007), an increase in cortisol levels was proposed as part of the trigger initiating sex change in sequential hermaphrodites by Solomon-Lane et al (2013), who argued that this elevation would increase corticotropinreleasing factor (CRF) signaling and activity of HPI axis. Their work on the bidirectional hermaphrodite Lythrypnus dalli (bluebanded goby) showed that cortisol peaked in early stages of sex change during which differences in HPI axis activity were also shown to reflect social status (Solomon-Lane et al 2013). Most recently, long-term cortisol administration was shown to induce sex change in protogynous three-spot wrasse (Halichoeres trimaculatus; Nozu & Nakamura 2015).…”

“…Precise levels of GCs are necessary for a balanced gonadal function; and increased cortisol (the most important GC) levels due to stress can cause loss of pregnancy and/or have a negative effect on fertility (Nepomnaschy et al 2006, Whirledge & Cidlowski 2010. In recent years, cortisol has been proposed as a key factor linking external environmental stimuli with internal physiological responses during sexual development, whereby environmental stress may initiate a steroidogenic shift at the onset of sex change (Solomon-Lane et al 2013, Nozu & Nakamura 2015. However, the exact role of cortisol or stress in transducing the external signals to elicit physiological responses during sexual development and sex change remains a mystery.…”

Bending Genders: The Biology of Natural Sex Change in Fish

“…4 ). That these factors apparently also mediate agonistic behaviour and social status information implicates the HPI axis in linking social status to sex change in sequential hermaphrodites [Solomon-Lane et al, 2013].…”

“…The stress response, regulated through the hypothalamic-pituitary-interrenal (HPI) axis, modulates processes central to major life-history transitions, including changes in behaviour, metabolism, and growth [Wada, 2008;Solomon-Lane et al, 2013]. Through the actions of corticotropic releasing hormone (CRH) and glucocorticoid steroids (GCs), the HPI axis responds to environmental stressors, with potentially significant effects on gonadal fate ( fig.…”