Genetic, natal and spatial drivers of social phenotypes in wild great tits.

Abstract

In social animals, group dynamics profoundly influence collective behaviours, vital in processes like information sharing and predator vigilance. Disentangling the causes of individual-level variation in social behaviours is crucial for understanding the evolution of sociality. This requires the estimation of the genetic and environmental basis of these behaviours, which is challenging in uncontrolled wild populations. In this study, we partitioned genetic, developmental and spatial environmental variation in repeatable social network traits derived from foraging events. We used a multi-generational pedigree and social data for 1823 individuals with over 800,000 observations from a long-term monitored great tit population. Animal models indicated minimal narrow-sense heritability (2%-3%) in group size choice, further reduced when the spatial location was considered, which itself explains a substantial 30% of the observed variation. Individual gregariousness also had a small genetic component, with a low heritability estimate for degree (<5%). Centrality showed heritability up to 10% in one of 3 years sampled, whereas betweenness showed none, indicating modest genetic variation in individual sociability, but not group-switching tendencies. These findings suggest a small, albeit detectable, genetic basis for individual sociality but pronounced spatial effects. Furthermore, our study highlights the importance of common environment effects (natal origin and brood identity), which essentially negated genetic effects when explicitly accounted for. In addition, we demonstrate that phenotypic resemblance can be a result of similarities beyond shared genes; spatial proximity at birth and natal environmental similarity explained up to 8% of the variation in individual sociability. Our results thus emphasise the role of non-genetic factors, particularly developmental and spatial variation, in shaping individual social behavioural tendencies.