Maternal predator-exposure has lifelong consequences for offspring learning in threespined sticklebacks

Abstract

Learning is an important form of phenotypic plasticity that allows organisms to adjust their behaviour to the environment. An individual's learning performance can be affected by its mother's environment. For example, mothers exposed to stressors, such as restraint and forced swimming, often produce offspring with impaired learning performance. However, it is unclear whether there are maternal effects on offspring learning when mothers are exposed to ecologically relevant stressors, such as predation risk. Here, we examined whether maternal predator-exposure affects adult offsprings' learning of a discrimination task in threespined sticklebacks (Gasterosteus aculeatus). Mothers were either repeatedly chased by a model predator (predator-exposed) or not (unexposed) while producing eggs. Performance of adult offspring from predator-exposed and unexposed mothers was assessed in a discrimination task that paired a particular coloured chamber with a food reward. Following training, all offspring learned the colour-association, but offspring of predator-exposed mothers located the food reward more slowly than offspring of unexposed mothers. This pattern was not driven by initial differences in exploratory behaviour. These results demonstrate that an ecologically relevant stressor (predation risk) can induce maternal effects on offspring learning, and perhaps behavioural plasticity more generally, that last into adulthood.

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

“…Campbell et al, 1992Campbell et al, , 1994Giesing et al, 2011;Mileva et al, 2011), as well as the size, physiology and behaviour of offspring (e.g. McCormick, 1998McCormick, , 2006McCormick, , 2009Giesing et al, 2011;McGhee et al, 2012;Roche et al, 2012;Mommer and Bell, 2013;Eaton et al, 2015;. Maternally derived cortisol, which is deposited to oocytes around the time of vitellogenesis, has been suggested as a potential mediator of the effects of maternal stress on offspring.…”

A female's past experience with predators affects male courtship and the care her offspring will receive from their father

“…Thus, previous predator experiences of mothers can influence offspring traits and survival both directly [12,13,21] and indirectly through how these experiences affect paternal care (this study). Paternal care in this species affects offspring behavioural [26,28,29] and morphological [26] development, brain gene expression [28] and is linked to offspring survival with predators [28].…”

“…Maternal stress during pregnancy or while yolking eggs can have a number of consequences for offspring due to the physiological link between mothers and offspring [9][10][11]. For example, in threespined stickleback (Gasterosteus aculeatus), maternal exposure to high predation risk while yolking eggs has negative consequences for offspring (reared without post-fertilization care): offspring show learning deficits [12], as well as less antipredator behaviour and lower survival when they themselves encounter a predator [13]. Altogether, differential allocation into mating effort and later offspring care by fathers could be in response to cues of their partner's experiences and/or in response to how maternal experiences might affect offspring traits [1,14,15].…”

Iterative development and the scope for plasticity: contrasts among trait categories in an adaptive radiation

“…Although the mechanisms are not well understood, there is emerging evidence that, as has been demonstrated in mammals, maternal stress can impose epigenetic influences on offspring behavior in fish with external fertilization (McCormick, 1998;Giesing et al, 2011;Roche et al, 2012;Mommer and Bell, 2013). In stickleback, the stressor most often studied is exposure to a heterospecific predator.…”

“…In stickleback, the stressor most often studied is exposure to a heterospecific predator. Recent research indicates that repeated exposure to a model predator can cause changes in egg characteristics (higher cortisol levels, larger size and initially higher metabolism; Giesing et al, 2011), has variable effects on offspring antipredator behavior (Giesing et al, 2011;McGhee et al, 2012), can reduce offspring survival and can have a negative influence on performance in a learning discrimination task (Roche et al, 2012). These epigenetic modifications of offspring behavior are likely to be induced by the glucocorticoid stress response of the mother, which could in turn affect responsiveness of this system in offspring, although results to date are equivocal (Mommer and Bell, Figure 3 The proportion of courtships by males from four Alaskan threespine stickleback populations that incorporated or failed to incorporate the zig-zag dance in field and laboratory environments.…”