Early social isolation disrupts adult personality expression in group-living mites

Animal personalities are characterized by intra-individual consistency and consistent inter-individual variability in behaviour across time and contexts. Personalities abound in animals, ranging from sea anemones to insects, arachnids, birds, fish and primates, yet the pathways mediating personality formation and expression remain elusive. Social conditions during the early postnatal period are known determinants of mean behavioural trait expressions later in life, but their relevance in shaping personality trajectories is unknown. Here, we investigated the consequences of early social isolation on adult personality expression in plant-inhabiting predatory mites Phytoseiulus persimilis. These mites are adapted to live in groups. We hypothesized that transient experience of social isolation early in life, that is, deprivation of any social contact during a sensitive window in the post-hatching phase, has enduring adverse effects on adult personality expression. Newly hatched mites were transiently reared in isolation or in groups and tested as adults for repeatability of various within-group behaviours, such as movement patterns and mutual interactions including sociability, defined as the propensity to associate and interact benignly with conspecifics, and activity patterns when alone. Groups composed of individuals with the same or different early-life experiences were repeatedly videotaped and individual behaviours were automatically analysed using AnimalTA. Social experiences early in life had persistent effects on mean behavioural traits as well as adult personality expression, as measured by intraclass correlation coefficients (indicating repeatability). On average, isolation-reared females moved at higher speeds, meandered less, kept greater distances from others and had fewer immediate neighbours than group-reared females. Group-reared females were highly repeatable in inter-individual distance, moving speed, meandering and area explored, whereas isolation-reared females were repeatable only in the number of immediate neighbours. Activity, quantified as the proportion of time spent moving within groups, was only repeatable in group-reared females, whereas activity, quantified as the proportion of time spent moving when alone, was only repeatable in females reared in isolation. Strikingly, also the early-life experiences of male mates influenced personality expression of mated females, with isolation-reared males boosting the repeatability of behavioural traits of group-reared females. Overall, our study provides evidence that a transient phase of social isolation during a critical period early in life has lasting effects that extend into adulthood, impairing adult personality expression. These effects should cascade upward, changing the phenotypic composition and diversity within populations.