Learning by embryos and the ghost of predation future

Abstract

Most research on the effects of exposure to stressful stimuli during embryonic development has focused on post-embryonic behaviour that appears to be abnormal or maladaptive. Here, we tested whether exposure to some stressful stimuli (predatory cues) can lead to post-embryonic behaviour that is adaptive. When eggs of ringed salamanders (Ambystoma annulatum) were exposed to chemical cues from predators, posthatching larvae showed reduced activity and greater shelter-seeking behaviour; larvae that had been exposed to control cues did not show these behaviours. In addition, wood frog (Rana sylvatica)tadpoles learned to respond to chemical cues from unfamiliar predators with danger based on embryonic conditioning. Therefore, if embryonic experience is a good predictor of future risk, learning associated with exposure to negative stimuli during development may be adaptive.

Alarm substance from adult zebrafish alters early embryonic development in offspring

“…Tollrian 1995) but may have associated costs (Peckarsky et al 2002). Alternatively, the early occurrence of developmental events could relate to later physiological or behavioural traits, as has been demonstrated in tadpoles, which learnt to respond to novel predator cues following exposure as embryos (Mathis et al 2008). The mechanism by which embryos are able to detect alarm substance at such an early stage of development remains unknown.…”

“…Most studies on effects of alarm cues are restricted to juveniles or adults, with effects on early embryonic development virtually unknown. Yet, recent evidence suggests that embryos in the early stages of development may be just as responsive to biotic environmental influences as later developmental stages (Laforsch & Tollrian 2004;Mathis et al 2008).…”

Fear is the mother of invention: anuran embryos exposed to predator cues alter life-history traits, post-hatching behaviour, and neuronal activity patterns

“…In particular, tadpoles show extreme sensitivity to many different environmental stimuli during their development, and phenotypic effects induced by predator cues can be conspicuous. It is well known that developing embryos and tadpoles modify the timing of hatching/ metamorphosis as well as morphology and behaviour in response to the perception of chemical cues of predation (Van Buskirk, 2001;Laurila et al, 2002;Orizaola and Braña, 2004;Ireland et al, 2007;Ferrari and Chivers, 2009;, and this plasticity may result in increased survival (Mathis et al, 2008). In contrast, the neurophysiological changes underlying phenotypic behavioural plasticity induced by predator cues remain largely unexplored (Orr et al, 2007;Whitaker et al, 2011).…”

Convergent evolution of alternative developmental trajectories associated with diapause in African and South American killifish

“…Most studies have focused on the effect of exposure during the juvenile or adult stage [45]. Yet, several recent studies indicate that embryos may be just as responsive to environmental conditions or cues, and this can lead to an adaptive matching between phenotype and the (expected) future environment via effects on post-embryonic behaviour [47] or morphology [48]. Alternative developmental trajectories, or developmental plasticity in general, can induce post-hatching phenotypic differences that have large effects on fitness and are adaptive given predicted future environments [49], but rspb.royalsocietypublishing.org Proc.…”