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Multi-level Selection in a Heterogeneous Environment

Final Report Summary - SHE (Multi-level Selection in a Heterogeneous Environment)

Our project SHE investigated the extent to which phenotypic and genetic diversity in the wild is modulated by recent drivers of rapid environmental change (habitat fragmentation and climate), and how it can interfere with processes of evolutionary adaptation. We integrated measures of selection at multiple levels (selection acting on phenotypic variation, additive genetic variation and genomic variation) for multiple potentially correlated traits (morphology, life-history, sexual character and behavior) and across space and time, using data collected during long-term monitoring projects of blue tits Cyanistes caeruleus and great tits Parus major in multiple study sites.
First, a phenotypic approach investigated covariances between phenotypes and relative fitness, to measure present selection on combinations of traits, and explore spatio-temporal fluctuations of selection. We demonstrated that climate change, and in particular extreme climatic events, increases the force of selection acting on avian timing of breeding. We also revealed that the urban environment imposes novel selection on bird morphology and life history. Although it is pervasively assumed that climate change and the urban environment both induce new selection on wild organisms, these are one of the first evidence confirming this prediction.
Second, we conducted quantitative genetic analyses using both long-term pedigree data and experimental (e.g. cross-fostering) approaches on behavior, colour ornamentation, morphology and life history of blue tits. We revealed that most colour ornament traits in this species are heritable, and that colours expressed in males and females are linked by strong cross-sex genetic colourations, possibly influencing strongly the evolution of colour in females. A thorough investigation on the variability, heritability and natural selection of phenological plasticity in a wild bird highlighted the importance of integrating ecological mechanisms shaping variation in plasticity if we are to understand how global change will affect plasticity and its consequences for population biology. The multi-trait approach was used to compare G matrices across populations at different spatial scale. It also revealed that behavioural syndromes are linked with a wider pace-of-life syndrome, and can vary across contrasted habitats because of heterogeneous selection across the landscape.
Third, an ecological genomics approach analyzed the genomic regions found to be associated with phenotypic variation in terms of genetic structure, genetic diversity patterns and footprints of selection, thereby providing insights into past selection that has shaped phenotypic variation. These genomic studies brought novel insight into local adaptation in a heterogeneous landscape (blue tits in Corsica) and in the urban habitat (great tits in Montpellier). In particular genome scans across the whole genome and in the epigenome found footprints of divergent selection along the urbanization gradient. Our findings open exciting perspectives for broader investigations of (epi)genomic bases related to adaptation in urban environment, notably in relation to avian personality and metabolism.
The forces and originality of this project included a/ the use of multiple long term datasets in different populations of the same species, in two contexts of environmental change of anthropogenic origin (climate change and urbanization), b/ the integration of different characters (behavior, life history, physiology) in the study of pace-of-life syndromes, c/ the combined use of expertise from the fields of Evolutionary Biology, Behaviour Ecology, Physiology, (Epi)Genomics, Quantitative Genetics, Biogeography, Remote Sensing and Biostatitics, and finally d/ the important outreach effort in link with local communities, in particular schools.