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Predation risk during early ontogeny can impact developmental trajectories and permanently alter adult phenotypes. Such phenotypic plasticity often leads to adaptive changes in traits involved in anti-predator responses. While plastic changes in cognition may increase survival, it remains unclear whether early predation experience shapes cognitive investment and drives developmental plasticity in cognitive abilities. Here, we show that predation risk during early ontogeny induces developmental plasticity in two cognitive domains. We reared female guppies (Poecilia reticulata) with and without predator cues and tested their adult cognitive abilities. We found that females reared under simulated predation took longer to learn a simple association task, yet outperformed animals reared without predation threat in a reversal learning task testing cognitive flexibility. These results show that predation pressure during ontogeny shapes adult cognitive abilities, which we argue is likely to be adaptive. Our study highlights the important role of predator-mediated developmental plasticity on cognitive investment in natural populations and the general role of plasticity in cognitive performance.

Predation risk during early ontogeny can impact developmental trajectories and permanently alter adult phenotypes. Such phenotypic plasticity often leads to adaptive changes in traits involved in anti-predator responses. While plastic changes in cognition may increase survival, it remains unclear whether early predation experience shapes cognitive investment and drives developmental plasticity in cognitive abilities. Here, we show that predation risk during early ontogeny induces developmental plasticity in two cognitive domains. We reared guppies (Poecilia reticulata) with and without predator cues and tested their adult cognitive abilities. We found that animals reared under simulated predation took longer to learn a simple association task, yet outperformed animals reared without predation threat in a reversal learning task testing cognitive flexibility. These results show that predation pressure during ontogeny shapes adult cognitive abilities, which we argue is likely to be adaptive. Our study highlights the important role of predator-mediated developmental plasticity on cognitive investment in natural populations and the general role of plasticity in cognitive performance.

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1.Phenotypic plasticity requires animals to acquire reliable environmental information. When multiple sources of information agree, cues should be perceived as reliable and induce a relatively strong response. Conversely, where stimuli conflict, animals must weigh the accuracy of the sources of information and responses should be reduced. 2.Availability of reliable information is often considered a limitation on plasticity, yet how animals integrate seemingly contradictory or incomplete information remains enigmatic, as empirical tests are scarce. 3.We tested how incomplete information determines phenotypic plasticity by simulating predation risk during early ontogeny of guppies (Poecilia reticulata). We exposed guppy fry to a combination of visual and/or olfactory cues of the predatory pike cichlid (Crenicichla alta), and monitored growth of the body and brain. After five weeks of exposure, guppies were returned to common no-risk conditions and their activity rates were monitored for four weeks post-treatment. 4.Visual predator exposure more strongly affected development; reducing body size of adult males and increasing brain size in females. However, there was little evidence for the hypothesised additive effect, with the combined treatment not inducing a larger effect than when only receiving olfactory or visual treatments. 5.While there was consistent individual variation in activity rates, this was unaffected by developmental risk and uncorrelated with the growth parameters. 6.Our results demonstrate the differential reliability of cues during development. Visual exposure to a predator was a highly reliable environmental cue, while environmental certainty was unaffected by combined stimuli.