Programming of the hypothalamic-pituitary-interrenal axis by maternal social status in zebrafish (Danio rerio)

Abstract

The present study examined the effects of maternal social status, with subordinate status being a chronic stressor, on development and activity of the stress axis in zebrafish embryos and larvae. Female zebrafish were confined in pairs for 48 h to establish dominant/subordinate hierarchies; their offspring were reared to 144 hours post-fertilization (hpf) and sampled at five time points over development. No differences were detected in maternal cortisol contribution, which is thought to be an important programmer of offspring phenotype. However, once zebrafish offspring began to synthesize cortisol de novo (48 hpf), larvae of dominant females exhibited significantly lower baseline cortisol levels than offspring of subordinate females. These lower cortisol levels may reflect reduced hypothalamic-pituitary-interrenal (HPI) axis activity, because corticotropin-releasing factor (crf) and cytochrome p450 side chain cleavage enzyme (p450scc) mRNA levels also were lower in larvae from dominant females. Moreover, baseline mRNA levels of HPI axis genes continued to be affected by maternal social status beyond 48 hpf. At 144 hpf, stress-induced cortisol levels were significantly lower in offspring of subordinate females. These results suggest programming of stress axis function in zebrafish offspring by maternal social status, emphasizing the importance of maternal environment and experience on offspring stress axis activity.

Glucocorticoids in Fish Eggs: Variation, Interactions with the Environment, and the Potential to Shape Offspring Fitness

“…Does maternal social status or stress-coping style regulate egg cortisol content? Egg cortisol content did not differ between dominant and subordinate zebrafish (Jeffrey and Gilmour 2016). This was contrary to the authors' predictions, given that subordinate fish have chronically elevated plasma cortisol (Sloman et al 2001) and thus one would expect elevation of egg cortisol to align with elevated maternal cortisol (Stratholt et al 1997).…”

“…There are several methods used to manipulate egg cortisol levels in vivo. Maternal environments can be altered and egg cortisol can be quantified (e.g., exposure of females to a physical stressor [Stratholt et al 1997;Sopinka et al 2014;Ghio et al 2016], exposure of females to conspecific competition [McCormick 2006[McCormick , 2009Jeffrey and Gilmour 2016], and exposure of females to anthropogenic noise [Sierra-Flores et al 2015]). Given that steroids are lipophilic, egg cortisol concentrations can be indirectly manipulated with an intraperitoneal injection of cortisol emulsified incocoa butteroroil (Eriksen et al 2006).…”

“…Despite an enthusiastic interest in determining how elevations in egg cortisol shape offspring phenotype (table 2), the evidence Effects of Egg Glucocorticoids on the Progeny of Fishes 25 to date indicating that maternal stressor exposure modifies egg cortisol levels is ambiguous. There are as many studies that have found differences (e.g., Stratholt et al 1997;McCormick 2006McCormick , 2009Sierra-Flores et al 2015) as there are that have not (e.g., Contreras-Sánchez 1996;Mileva et al 2010;Sopinka et al 2014;Jeffrey and Gilmour 2016;Ghio et al 2016). There are physiological or biochemical (e.g., maternal and embryonic metabolism of cortisol; see sec.…”

Oxytocin-mediated social preference and socially reinforced reward learning in the miniature fishDanionella cerebrum

“…One exception is a tendency to form loose shoals that has been seen in some studies as early as 7 dpf [13], but it is nonetheless clear that even this simple form of social interaction is not mature until much later [30]. Since zebrafish do not become gendered until metamorphosis occurs at approximately 21 -30 dpf [24], it is unsurprising that courtship behaviors, aggression, and the formation of social hierarchies only occur at adulthood [10,37,38]. Other social phenomena, such as the behavioral response to an alarm pheromone given off by injured conspecifics, have similarly been shown to appear only around sexual maturity [15].…”

Exposure to boat noise in the field yields minimal stress response in wild reef fish

“…To obtain whole-body cortisol levels for each fish, we generally followed the procedures outlined in Sopinka et al (2014), Jeffrey & Gilmour (2016), and Redfern et al (2017). Individual fish were removed from their respective frozen bags and the proximal portion of each fish (anterior of midway between the operculum and pelvic girdle) was removed using a serrated duct knife.…”