Maternal exposure to predation risk decreases offspring antipredator behaviour and survival in threespined stickleback

Abstract

SUMMARY 1. Adaptive maternal programming occurs when mothers alter their offspring's phenotype in response to environmental information such that it improves offspring fitness. When a mother's environment is predictive of the conditions her offspring are likely to encounter, such transgenerational plasticity enables offspring to be better-prepared for this particular environment. However, maternal effects can also have deleterious effects on fitness. 2. Here, we test whether female threespined stickleback fish exposed to predation risk adaptively prepare their offspring to cope with predators. We either exposed gravid females to a model predator or not, and compared their offspring's antipredator behaviour and survival when alone with a live predator. Importantly, we measured offspring behaviour and survival in the face of the same type of predator that threatened their mothers (Northern pike). 3. We did not find evidence for adaptive maternal programming; offspring of predator-exposed mothers were less likely to orient to the predator than offspring from unexposed mothers. In our predation assay, orienting to the predator was an effective antipredator behaviour and those that oriented, survived for longer. 4. In addition, offspring from predator-exposed mothers were caught more quickly by the predator on average than offspring from unexposed mothers. The difference in antipredator behaviour between the maternal predator-exposure treatments offers a potential behavioural mechanism contributing to the difference in survival between maternal treatments. 5. However, the strength and direction of the maternal effect on offspring survival depended on offspring size. Specifically, the larger the offspring from predator-exposed mothers, the more vulnerable they were to predation compared to offspring from unexposed mothers. 6. Our results suggest that the predation risk perceived by mothers can have long-term behavioural and fitness consequences for offspring in response to the same predator. These stress-mediated maternal effects can have nonadaptive consequences for offspring when they find themselves alone with a predator. In addition, complex interactions between such maternal effects and offspring traits such as size can influence our conclusions about the adaptive nature of maternal effects.

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.…”

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

“…Thus, individuals used here are an unknown combination of full-siblings and unrelated individuals from at least 10 different families. Further details about maternal treatment and rearing methods are in McGhee et al [11].…”

“…Unexposed females were undisturbed. This protocol elevates cortisol in eggs of predator-exposed females [10] and affects offspring anti-predator and shoaling behaviour [10,11]. After at least 7 days in a treatment, when a female became gravid she was stripped of eggs that were artificially fertilized.…”

“…Previous studies in this system have shown that predatorexposure elevates cortisol in female stickleback [13] as well as their eggs [10], and affects offspring behaviour [10,11] and fitness [11].…”

Parental effects enhance risk tolerance and performance in offspring

“…Growing evidence, however, indicates that parental effects, such as the influence of parental provisioning on offspring body size (Reznick et al 1996, Sinervo andDoughty 1996), can operate throughout an offspring's lifetime as well as affect multiple generations (Agrawal et al 1999, Plaistow et al 2006. Moreover, parental exposure to predation risk can affect offspring morphology (e.g., Agrawal et al 1999) and behavior (Storm andLima 2010, McGhee et al 2012), thereby influencing population and community dynamics by changing the foraging success of predators on offspring (Tollrian 1995, Agrawal et al 1999, Storm and Lima 2010, McGhee et al 2012). …”