Bold New World: urbanization promotes an innate behavioral trait in a lizard

Urban environments are novel landscapes that markedly alter animal behavior. Divergence in behavior in response to urbanization may provide advantages in navigation, exploiting resources, and surviving under a novel suite of selective pressures. Relatively few studies, however, have identified population-level behavioral changes in response to urbanization that are not confounded by rearing environment and prior experience (e.g., an urban upbringing). To address this, we used the Australian water dragon (Intellagama lesueurii) to test whether populations under varying levels of urbanization (urban, semi-natural, and natural populations) differ in their innate behavioral traits; acquired either heritably or due to population-specific maternal effects. Eggs were collected from wild mothers and hatched in the lab. Hatchlings were then reared in the lab under standardized conditions (a common-garden experiment). We then assayed individual behavioral traits (boldness, exploration, and neophilia) five times across their first year of development. We compared behavioral traits, as well as their expression (repeatability), between urban, semi-natural, and natural populations. Neophilia and explorative behavior was similar among all populations. However, dragons from semi-natural populations were significantly bolder than those from natural populations. Urban dragons were also bolder than dragons from natural populations, although this trend was not significant because of high variance in boldness. Dragons from semi-natural and urban populations had similar boldness scores, suggesting a potentially biologically relevant difference in boldness between them and natural populations. We also saw some differences in the consistency of the expression of behavior. Boldness in individuals from urban environments was also the only repeatable trait. Overall, our study suggests that boldness is an innate, urban-derived divergent behavioral trait that likely contributes to the success of these lizards in anthropogenically altered environments. SIGNIFICANCE STATEMENT: Lizards from human-modified areas are innately bolder than ones from natural habitats. To determine this, we raised lizards from eggs collected from urban, semi-natural, and natural populations in a standardized environment, removing the effects of prior experience and developmental environment, and examined their behavioral traits over time. The difference we found in boldness was related to their origin population, rather than being shaped through experience, suggesting this trait may be heritable and is being selected for in anthropogenic landscapes. Our study addresses an important gap in studies of urban behavioral ecology by examining behavioral differences among replicated, differently urbanized, sites after experimentally accounting for both rearing environment and prior experience.