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Testing the importance of oxidative stress and dietary antioxidants in linking cognitive traits and fitness in free living animals

Periodic Reporting for period 1 - COSuccess (Testing the importance of oxidative stress and dietary antioxidants in linking cognitive traits and fitness in free living animals)

Période du rapport: 2020-09-01 au 2023-02-28

Because cognitive abilities, such as innovation (i.e. the propensity to invent a new behaviour or to flexibly adjust established behaviours to solve new problems) and learning (i.e. the acquisition of information through experience that may cause a change in behaviour), can help animals to quickly adapt to their changing environments, these abilities are expected to be under strong selection and be key components of species evolutionary success. However, why there is such large inter-individual variation in cognitive abilities, and why and how cognitive abilities are related to fitness remain largely unknown. The aim of this project was to investigate, in a natural bird population, the role of ageing and oxidative stress on inter-individual variation in cognitive performances, and how food (dietary antioxidants), oxidative stress, and cognition interact together in shaping fitness in natural populations.
Overall, this Marie Curie Fellowship was a success at demonstrating that (i) ageing individuals showed a decline in problem-solving performance, potentially via increased oxidative stress with age, (ii) problem-solving performance influenced reproductive success through the ability to find large amount of high quality food in the environment to provision their chicks, and (iii) the experimental supply of food rich in antioxidant during chick growth positively influences the cognitive performance of the same individuals in adulthood. These results confirm the importance of ageing and diet in the inter-individual variation in problem-solving ability and in the link between cognition and fitness.
This project has been performed in a natural population of great tits (Parus major) located on the Swedish island of Gotland. This population is monitored for reproduction and systematically tested for cognitive performance since 2010, providing long-term cognitive and breeding databases and an already implemented system to study the link between chronological age, dietary antioxidants and oxidative stress, cognition and reproductive success.
I started this project by exploring in depths the links between problem-solving performance, provisioning behaviour and reproductive success (objective 2 of this project) using cognitive and reproductive data from 2015, when videos of provisioning behaviours were recorded using IR cameras placed inside the nestbox. I showed that although females were more likely to solve the task, solver males delivered preys at a higher rate and brought more larvae, a particularly nutritious prey, to their chicks, than non-solver males. Paths analyses confirmed that problem-solving performance influenced provisioning, and that provisioning was in turn linked to reproductive success but only in males.
I then investigated how various behavioural traits and individual and extrinsic factors explained individual performance during problem-solving (in addition to the original objective of this project). Using all the data from the cognitive database, I confirmed that females were again more likely to solve the task than males. I also showed that solvers were not only more persistent in contacting the opening parts of the task, but were also more explorative, than non-solvers. Solvers significantly increased this selective persistence toward the solving parts of the task after its first movement, and during successive entrances (until reaching a learning plateau) while non solvers did not significantly change their attention to the solving parts of the task after this cue, providing evidence that associative learning is a key to solve our task.
To disentangle age-related variation in reproductive and cognitive traits driven by demographic effects (i.e. selective appearance or disappearance) from those occurring at the individual level (i.e. senescence per se) (objective 1 of this project), I performed longitudinal analyses on the same individuals measured repeatedly using the cognitive and breeding databases. Results showed that the proportion of solvers in our study population is decreasing with age, and that this decrease is partly explained by within-individual decline in solving performance and selective persistence, thus cognitive senescence.
To test if oxidative stress could shape the link between cognition and reproductive success (objective 3 of this project), I collected blood samples and performed state-of-arts laboratory analyses to gather information on enzymatic and non-enzymatic antioxidant defences and oxidative damage. Analyses of the results are still ongoing, given the important number of samples collected over the multiple years of testing. But these results will shed lights on how chronological age and oxidative stress links cognition and reproduction in wild populations.
Finally, I supplemented parents during reproduction and chicks during development with antioxidants (vitamins E, Quercetin, Coenzyme Q10) naturally present in their diet, and tested the short and long-term influence of dietary antioxidants on cognitive performance and reproductive success (objective 4 of this project). Due to the pandemic situation, this experiment was delayed by one year and is still ongoing thanks to additional funding secured by my project host and project partner. Intermediary results are promising and show that chicks experimentally fed with antioxidants are more likely to be solvers as adults.
The different results of this project should lead to the publications of at least 5 scientific articles. I also disseminated my results to a large audience in Ecology and Evolution through presentations at 3 national and 4 international conferences, 2 symposia on cognition I organised, and a webinar in the Marie Curie/European Commission event ‘Science is Wonderful’.
This project provided the first comprehensive study testing the links between cognition, dietary antioxidants and oxidative stress, and ultimately fitness in a wild population, thanks to the multi-disciplinary innovative methods I used to address my research objective. The results are not only original, but important to understand the responses of natural populations to global changes, since cognition is at the heart of individual behavioural flexibility, which is a major determinant of the ability of individuals to face environmental changes. Moreover, the ageing of the European Union population is likely to be of major significance in the coming decades, and this project shed new lights on the importance of access to dietary antioxidants early in life and at adulthood in mitigating ageing.
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