Egg hormones in a highly fecund vertebrate: do they influence offspring social structure in competitive conditions?

Abstract

Summary1. Social status can vary considerably among individuals and has significant implications for performance. In addition to a genetic component, social status may be influenced by environmental factors including maternal effects such as prenatal hormone exposure. Maternal effects on traits determining social status have previously been examined in species where mothers provide parental care for relatively few offspring and therefore directly influence postnatal development. However, the generality of conclusions arising from these investigations is unclear because species that employ different reproductive strategies have not been studied. 2. We investigated the hypothesis that egg steroid hormone levels influence the social status of juvenile brown trout (Salmo trutta). We manipulated intra-clutch levels of cortisol and testosterone in eggs from 15 mothers using dilute hormone baths at the time of fertilization and examined their effects on traits that correlate with social status in juveniles [including standard body size, aggression, competitive ability and standard metabolic rate (SMR)]. 3. Hormone treatment did not affect whole-animal or mass-corrected SMR at the critical developmental stage when juveniles switch from reliance on a maternally provisioned yolk sac to independent feeding. However, juveniles from cortisol-treated eggs were smaller at this developmental stage. They were also less aggressive than, and subordinate to, fish from untreated eggs in socially competitive conditions, even after correcting for the observed effect of cortisol on body size. Egg testosterone treatment resulted in a likely pharmacological or toxicological dose with subsequent effects on both body size and behaviour in independently feeding juveniles. 4.Results from this study demonstrate that variation in the amount of cortisol deposited in eggs by spawning females influences juvenile social status and performance. The effects of elevated egg cortisol in fish are similar to the actions of embryonic glucocorticoids reported in other vertebrate taxa with very different reproductive strategies, suggesting a widespread mechanism for the effects of maternal stress on offspring. Possible adaptive aspects of this relationship are discussed.

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

“…Maternal cortisol plays an important organizational role during early development in fish, and cortisol treatment of eggs or embryos alters both physiology and behaviour of the developing young (e.g. Sloman, 2010;Burton et al, 2011;Li et al, 2012;Nesan and Vijayan, 2012;Colson et al, 2015;. However, programming of offspring is probably more complex than the action of cortisol alone, because previous studies have found effects of maternal stress even in the absence of increased embryo cortisol levels -for example, on egg size in Neolamprologus pulcher (Mileva et al, 2011) and on swim performance in Oncorhynchus nerka (Sopinka et al, 2014).…”

State-dependent behavior and alternative behavioral strategies in brown trout (Salmo trutta L.) fry

“…Still, artificial selection programs seem to be able to create genetic strains with altered aggression levels compared to wild salmonid populations, indicating that there actually is a genetic component for the behavioral expression (Huntingford and Adams 2005). Substantial among-sibling variation in behavior has previously been found in brown trout, attributed to the location of the eggs in the egg sac and possibly pre-natal hormone exposure (Burton et al 2011, 2013). Thus, behavioral strategies of individual fry may be depending on embryonal environment, which can vary within females (Jonsson and Jonsson 2014).…”

The association between parental life history and offspring phenotype

“…Standard metabolic rate (SMR, usually measured in terms of oxygen consumption) is the minimal maintenance metabolic rate of an ectotherm in a postabsorptive and inactive state (so is the equivalent of the basal metabolic rate of an endotherm), and is an integrated measure of the energy expenditure involved in tissue maintenance and organism homeostasis. After controlling for temperature, body size and other sources of variation, SMR often differs by a factor of 2 or 3 between individuals of the same age, sex and species held in similar conditions (Burton et al, 2011). Aerobic scope (AS) is the difference between an animal's SMR and its maximum possible aerobic metabolic rate (MMR) under the same environmental conditions, so that AS represents the capacity of the animal to increase its rate of aerobic metabolism (Fry, 1957(Fry, , 1971).…”