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

Abstract

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.

Figure 1

Study animals (line drawings by K.E. McGhee).

Figure 2

Survival time interacted with offspring size: for offspring of predator-exposed mothers, survival time decreased with offspring standard length. Shown are means ± SE with 24 ± 2 offspring contributing to each mean on average. Note that this figure is only illustrative - the analyses were conducted using standard length as a continuously distributed covariate.

Figure 3

Orienting at the pike was an effective antipredator behaviour and differed between maternal predator-exposure treatments. (A) A greater proportion of offspring from unexposed mothers oriented to the predator than did offspring from predator-exposed mothers. (B) Stickleback that oriented to the predator survived for longer than those that did not orient to the predator. Shown are means ± SE. * indicates P = 0.016.