Variations interindividuelles des performances cognitives et conséquences évolutives chez une population naturelle de mésange charbonnière (Parus major)

Les animaux font face à des changements environnementaux brutaux dus aux modifications de milieux liés à l'activité humaine et aux changements climatiques, et doivent s'ajuster rapidement à leur nouvel environnement. Certains processus cognitifs comme l'innovation et l'apprentissage permettent aux animaux d'intégrer de nouveaux comportements à leur répertoire comportemental (flexibilité comportementale), leur donnant l'opportunité d'intégrer un comportement plus optimal pour s'ajuster. Les performances cognitives varient entre espèces et les individus d'une même population et bien que des études récentes se soient intéressées aux causes des variations interindividuelles des performances cognitives, les conséquences restent peu explorées. Dans cette thèse, les questions des pressions de sélection s'exerçant sur les capacités cognitives sont abordées afin de mieux comprendre l'évolution de ces traits au sein d'une population naturelle de mésange charbonnière Parus major. Un nouveau test de résolution de problème a tout d'abord été présenté à des couples reproducteurs directement en milieu naturel. Les résultats ont montré que les couples les plus performants à résoudre la tâche surpassaient les couples les moins performants sur plusieurs mesures de succès reproducteur. Afin de vérifier que la motivation à nourrir les poussins ne biaisait pas cette relation, la taille de nichée a ensuite été manipulée, ce qui n'a pas affecté la performance subséquente des parents. Les couples innovateurs démontraient un meilleur succès reproducteur quel que soit le changement de la taille de nichée subit, ce qui suggère que cette performance influence bien le succès de reproduction, et non l'inverse. De plus, les couples innovateurs approvisionnaient leurs poussins plus souvent que les couples non innovateurs, suggérant que les innovateurs pourraient exploiter leur habitat de façon plus optimale. Dans un troisième temps, plusieurs caractéristiques morphologiques, dont la coloration des plumes, ont été reliées aux performances de résolution de problème et d'apprentissage. Ces liens, bien que complexes et condition-dépendants, pourraient indiquer un rôle de ces performances lors de la sélection sexuelle. Enfin, afin de tester l'effet du parasite sanguin du paludisme sur les traits comportementaux, un médicament contre le paludisme a été injecté à des femelles reproductrices. Cette injection n'a pas modifié leurs performances cognitives mais a augmenté leur niveau d'activité et d'exploration du nichoir en réponse à la tâche de résolution de problème. Ce parasite sanguin, très présent chez les populations depassereaux, pourrait donc expliquer les variations interindividuelles et interpopulationnelles de certains traits comportementaux en milieu naturel, au même titre que dans nombreux autres systèmes hôte-parasites étudiés. Les travaux présentés dans cette thèse ont permis de détailler pour la première fois la relation entre une performance cognitive et le succès reproducteur chez une population aviaire naturelle, une relation robuste et non influencée par la motivation à nourrir la couvée. Cette performance cognitive est reliée à plusieurs traits morphologiques, mais non à la charge parasitaire. Une meilleure exploitation de l'habitat et habileté à s'occuper des poussins pourrait expliquer cette relation.Animals face a rapidly changing world due to anthropogenic habitat destruction and climate change, forcing them to quickly adjust their behaviour to new environmental conditions. Cognitive processes such as innovation and learning can allow animals to incorporate novel behaviours into their behavioural repertoires and facilitate optimal responses to environmental change. Cognitive performances vary between and within species and although several studies have recently addressed the causes of inter-individual variations in cognitive performance, the fitness consequences of this variation remain poorly explored in natural populations. In my PhD thesis, I investigated different selective pressures acting on innovation and learning performance to better understand the evolution of these traits in a natural population of great tits Parus major. Firstly, I designed a novel problem-solving task that involved opening a trap door to access chicks, and presented it to breeding great tit pairs in their natural habitat. I found that the most efficient birds at solving this task performed better at multiple measures of reproductive success than the less efficient. Secondly, to test whether chick provisioning motivation confounded this relationship, I manipulated brood size and recorded whether this affected the problem-solving performance of the parents. My results showed that this was not the case. Instead, solvers had higher reproductive success whatever the brood size manipulation experienced, supporting the hypothesis that this cognitive performance drives reproductive success rather than the opposite. Problem-solving performance correlates positively with reproductive success both at the early stages of breeding (i.e. number of eggs laid and hatched) and during the nestling rearing period (i.e. number and condition of fledged young). Moreover, solvers seem to provision their young at a higher rate than non-solvers, suggesting that solvers exploit their breeding habitat more efficiently than non-solvers. Thirdly, I found multiple links between morphological traits, among which feather colouration, and problem-solving and learning performances. Although complex and condition-dependent, these links suggest that cognitive performances may be under sexual selective pressures, since they can be signaled by morphological traits shown to be important in great tit mate choice. Finally, injecting breeding females with an anti-malaria drug did not affect their cognitive performances, but increased their level of activity and exploration when presented with the novel problem-solving task. This suggests that the presence of these blood parasites, which are frequent in passerine populations, could partly explain between-individual and between-population variation in certain behavioural traits in natural populations, as previously described in many other host-parasite study systems. In summary, my thesis provides the first detailed analysis of the relationship between cognitive performance and reproductive success in a wild bird population. My studies show that this relationship is robust and not confounded by parents’ motivation to provision their young. This problem-solving performance is also correlated with various morphological traits, but not with parasite load. The relationship between cognitive performance and reproductive success might be mediated through habitat exploitation and chick provisioning skills, but requires further investigation

Selective disappearance of individuals with high levels of glycated haemoglobin in a free-living bird

This work was supported by the ANR (ANR-06-JCJC0082 to B.D.), the CNRS (PEPS INEE and PICS France–Switzerland to B.D.), the French Ministe`re de l’Enseignement Supe´rieur et de la Recherche (PhD fellowship to C.R.), the Re´gion Rhoˆne-Alpes (Explora’doc mobility grant to C.R.), the University of Aberdeen (stipend to C.R.), the L’Ore´al Foundation-UNESCO ‘For Women in Science’ program (fellowship to C.R.) and the Rectors’ Conference of the Swiss Universities (grant to C.R. and P.B.).Peer reviewedPostprin

An Experimental Test of a Causal Link between Problem-Solving Performance and Reproductive Success in Wild Great Tits

This work was supported by a NSERC grant to A.B., a PICS grant from the CNRS (INEE, n° 31520) to B.D., a PhD writing up grant from the FESP (UdM) and a scholarship from the Biological Sciences Department (UdM) to LC and a mobility grant ERASMUS to M.L. We are also grateful to the ABS, the BOU, the BES, the Frank M. Chapman from AMNH and the Fred Cooke from the SCO for awards and research grants attributed to L.C.Peer reviewedPublisher PD

The Role of Cognition in Social Information Use for Breeding Site Selection : Experimental Evidence in a Wild Passerine Population

This work was funded by the ANR (Evol-Cog project, ANR-19-CE02-0007), the Centre National pour la Recherche Scientifique (PICS) and the Region Rhône-Alpes (CIBLE programme) to BD; the NSERC (postdoctoral fellowship), the ABS (student research award), the BOU and the BES (research grants), and the SCO (Fred Cook award) to LC; the Ministère de l'Enseignement Supérieur et de la Recherche, the Department of Ecology and Genetics from Uppsala University and Stiftelsen för Zoologisk Forskning, the Région Auvergne Rhone-Alpes (Explora'Doc mobility grants) and by the University of Lyon (ATER fellowship and IDEX mobility grant) to JM; the Pearcy Sladen Memorial Trust and Carnegie Trust (travel grants), and the BOU and BES (research grants) to PB. The data supporting the findings of this study are openly available in FigShare at http://doi.org/10.6084/m9.figshare.13229081.Peer reviewedPublisher PD

Inter-individual variation in provisioning rate, prey size and number, and links to total prey biomass delivered to nestlings in the Collared Flycatcher (Ficedula albicollis)

Acknowledgements We thank the many students that helped with data collection in the field and data extraction back in the laboratory, and all landowners for access to their forest patches. Funding This work was supported by grants from the CNRS (PICS) and from the ASAB to BD; the NSERC and FRQNT (postdoctoral fellowship), the ABS and the SCO (student awards), the AMNH, the BOU and the BES (research grants) to LC. The datasets generated and/or analysed during the current study are available in the Figshare repository, https://doi.org/10.6084/m9.figshare.14264396.Peer reviewedPublisher PD

Host dispersal shapes the population structure of a tick-borne bacterial pathogen

Birds are hosts for several zoonotic pathogens. Because of their high mobility, especially of longdistance migrants, birds can disperse these pathogens, affecting their distribution and phylogeography. We focused on Borrelia burgdorferi sensu lato, which includes the causative agents of Lyme borreliosis, as an example for tick-borne pathogens, to address the role of birds as propagation hosts of zoonotic agents at a large geographical scale. We collected ticks from passerine birds in 11 European countries. B. burgdorferi s.l. prevalence in Ixodes spp. was 37% and increased with latitude. The fieldfare Turdus pilaris and the blackbird T. merula carried ticks with the highest Borrelia prevalence (92 and 58%, respectively), whereas robin Erithacus rubecula ticks were the least infected (3.8%). Borrelia garinii was the most prevalent genospecies (61%), followed by B. valaisiana (24%), B. afzelii (9%), B. turdi (5%) and B. lusitaniae (0.5%). A novel Borrelia genospecies "Candidatus Borrelia aligera" was also detected. Multilocus sequence typing (MLST) analysis of B. garinii isolates together with the global collection of B. garinii genotypes obtained from the Borrelia MLST public database revealed that: (a) there was little overlap among genotypes from different continents, (b) there was no geographical structuring within Europe, and (c) there was no evident association pattern detectable among B. garinii genotypes from ticks feeding on birds, questing ticks or human isolates. These findings strengthen the hypothesis that the population structure and evolutionary biology of tick-borne pathogens are shaped by their host associations and the movement patterns of these hosts.Peer reviewe

Editorial: Links between cognition and fitness: Mechanisms and constraints in the wild

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