A Behavioral Syndrome Linking Boldness and Flexibility Facilitates Invasion Success in Sticklebacks

Understanding the factors that allow a species to expand its range and adapt to changing habitats is essential for mitigating anthropogenic change. We evaluated how behavior and cognition facilitate colonization of new environments and evolve post establishment during natural biological invasions. Marine threespined sticklebacks are expert colonists with a penchant for invading freshwater environments and rapidly adapting to them. However, the role of behavior in facilitating rapid adaptation in this system has received little attention. By rearing replicate populations of sticklebacks under common garden conditions in the lab, we tested the hypothesis that boldness is favored in dispersers and that neophilia and flexibility are favored in recently-arrived immigrants. We found that dispersing populations comprised bold individuals, while sticklebacks from the invaded region were flexible in their behavior. Moreover, boldness and flexibility were negatively correlated with each another at the individual, family and population levels. Multiple lines of evidence suggest that there is a heritable component to boldness and flexibility, therefore their divergence is likely to be evolutionary in origin. If boldness is favored in invaders during the initial dispersal stage, while flexibility is favored in recent immigrants during the establishment stage, then the link between boldness and flexibility could generate positive correlations between successes during both the dispersal and establishment stages, and therefore play a key role in facilitating colonization success in this important model organism. SIGNIFICANCE STATEMENTFor a species to expand its range, it needs to be good at dispersing and also capable of exploiting resources and adapting to different environments. Therefore, behavioral and cognitive traits such as boldness, neophilia and behavioral flexibility could play key roles in facilitating invasion success. Here, we show that dispersing sticklebacks are bold, while sticklebacks that have recently established in a new region are flexible. Moreover, boldness and flexibility are negatively correlated with one another. If boldness is favored in dispersers while flexibility is favored in immigrants, then this behavioral syndrome could play a heretofore underappreciated role in facilitating rapid adaptation in this important model organism.