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

Wild and captive vertebrates face multiple stressors that all have the potential to induce chronic maternal stress (i.e., sustained, elevated plasma glucocorticoids), resulting in embryo exposure to elevated maternally derived glucocorticoids. In oviparous taxa such as fish, maternally derived glucocorticoids in eggs are known for their capacity to shape offspring phenotype. Using a variety of methodologies, scientists have quantified maternally derived levels of egg cortisol, the primary glucocorticoid in fishes, and examined the cascading effects of egg cortisol on progeny phenotype. Here we summarize and interpret the current state of knowledge on egg cortisol in fishes and the relationships linking maternal stress/state to egg cortisol and offspring phenotype/fitness. Considerable variation in levels of egg cortisol exists across species and among females within a species; this variation is hypothesized to be due to interspecific differences in reproductive life history and intraspecific differences in female condition. Outcomes of experimental studies manipulating egg cortisol vary both inter- and intraspecifically. Moreover, while exogenous elevation of egg cortisol (as a proxy for maternal stress) induces phenotypic changes commonly considered to be maladaptive (e.g., smaller offspring size), emerging work in other taxa suggests that there can be positive effects on fitness when the offspring's environment is taken into account. Investigations into (i) mechanisms by which egg cortisol elicits phenotypic change in offspring (e.g., epigenetics), (ii) maternal and offspring buffering capacity of cortisol, and (iii) factors driving natural variation in egg cortisol and how this variation affects offspring phenotype and fitness are all germane to discussions on egg glucocorticoids as signals of maternal stress.

Maternal programming of offspring hypothalamic-pituitary-interrenal axis in wild sockeye salmon (Oncorhynchus nerka).

In fishes, maternal exposure to a stressor can influence offspring size and behavior. However, less is known about how maternal stress influences physiological processes in offspring, such as function of the hypothalamic-pituitary-interrenal (HPI) axis. We examined the impact of chronic maternal exposure to an acute chase stressor on the stress response/HPI activity of progeny in wild sockeye salmon (Oncorhynchus nerka). Resting plasma cortisol and brain preoptic area (POA) corticotropin-releasing factor (CRF) mRNA levels did not vary between offspring reared from undisturbed, control females and offspring reared from females exposed to the stressor. However, resting levels of POA glucocorticoid receptors (GR1 and GR2), and head kidney melanocortin 2 receptor (MC2R), steroidogenic acute regulatory protein (StAR), and cytochrome P450 side chain cleavage enzyme (P450scc) were elevated in offspring reared from stressor-exposed females. Offspring reared from stressor-exposed females had lower plasma cortisol levels 1-h after an acute chase stressor compared to cortisol levels in offspring reared from control females. In offspring reared from chased females, mRNA levels of genes associated with cortisol biosynthesis were reduced in the head kidney post-chase. In offspring reared from control females, mRNA levels in the head kidney did not vary pre- to post-chase. Together, the results of the present study suggest maternal programming of progeny with respect to baseline and stressor-induced mediators of HPI axis activity.

Mother knows best, even when stressed? Effects of maternal exposure to a stressor on offspring performance at different life stages in a wild semelparous fish.

The environment mothers are exposed to has resonating effects on offspring performance. In iteroparous species, maternal exposure to stressors generally results in offspring ill-equipped for survival. Still, opportunities for future fecundity can offset low quality offspring. Little is known, however, as to how intergenerational effects of stress manifest in semelparous species with only a single breeding episode. Such mothers would suffer a total loss of fitness if offspring cannot survive past multiple life stages. We evaluated whether chronic exposure of female sockeye salmon (Oncorhynchus nerka) to a chase stressor impaired offspring performance traits. Egg size and early offspring survival were not influenced by maternal exposure to the repeated acute stressor. Later in development, fry reared from stressed mothers swam for shorter periods of time but possessed a superior capacity to re-initiate bouts of burst swimming. In contrast to iteroparous species, the mechanisms driving the observed effects do not appear to be related to cortisol, as egg hormone concentrations did not vary between stressed and undisturbed mothers. Sockeye salmon appear to possess buffering strategies that protect offspring from deleterious effects of maternal stress that would otherwise compromise progeny during highly vulnerable stages of development. Whether stressed sockeye salmon mothers endow offspring with traits that are matched or mismatched for survival in the unpredictable environment they encountered is discussed. This study highlights the importance of examining intergenerational effects among species-specific reproductive strategies, and across offspring life history to fully determine the scope of impact of maternal stress.

Does among-population variation in burst swimming performance of sockeye salmon Oncorhynchus nerka fry reflect early life migrations?

Using a fixed-speed test, burst swimming performance was found to vary among nine populations of emergent sockeye salmon Oncorhynchus nerka fry reared in a common-garden environment. No consistent relationship was, however, detected between difficulty of fry migration (upstream v. downstream) to rearing areas and total burst swimming duration or bursting rate.

Does proximity to aquatic pollution affect reproductive traits in a wild-caught intertidal fish?

How chronic exposure to aquatic pollution affects reproductive traits was assessed in nesting wild-caught plainfin midshipman Porichthys notatus in areas with low and high contaminant exposure on Vancouver Island, British Columbia. Males in high-exposure areas had a greater degree of testicular asymmetry, sperm with shorter heads and fewer live eggs in their nests. The results of this study provide important insights into the potential consequences of contaminant exposure on the reproductive physiology of wild-caught fishes.

Liver size reveals social status in the African cichlid Neolamprologus pulcher.

Wild groups (n = 167) of the cooperatively breeding Lake Tanganyika cichlid, Neolamprologus pulcher, were used to investigate how social status and sex influence liver investment. In contrast to expectations, males and females (controlling for body size) had similar liver investment and subordinates (both sexes) had relatively larger livers compared with dominants. Three hypotheses were considered for why social status results in liver size disparity: liver mass might reflect status-dependent differences in (1) energy expenditure, (2) energy storage and (3) energy acquisition. First, dominants performed more energetically costly behaviours (e.g. social policing and care) compared with subordinates, supporting the notion that energy expenditure drives liver investment. Moreover, dominants in large groups (with many subordinates to monitor) and those holding multiple territories (with large areas to patrol), tended to have smaller livers. Second, subordinates did not appear to use the liver as a strategic energy storage organ. In laboratory and field experiments, subordinates ascending in rank had similar or larger livers during periods of rapid growth compared with non-ascending controls. Third, although subordinates fed more frequently than dominants, a negative relationship was found between feeding rates and liver size. Hence, these results contrast with previous liver studies and suggest that liver investment patterns were linked to status-driven differences in energy expenditure but not to energy intake or storage in N. pulcher.