Evolution of boldness and exploratory behavior in giant mice from Gough Island

Abstract

Abstract Island populations are hallmarks of extreme phenotypic evolution. Radical changes in resource availability and predation risk accompanying island colonization drive changes in behavior, which Darwin likened to tameness in domesticated animals. Although many examples of animal boldness are found on islands, the heritability of observed behaviors, a requirement for evolution, remains largely unknown. To fill this gap, we profiled anxiety and exploration in island and mainland inbred strains of house mice raised in a common laboratory environment. The island strain was descended from mice on Gough Island, the largest wild house mice on record. Experiments utilizing open environments across two ages showed that Gough Island mice are bolder and more exploratory, even when a shelter is provided. Concurrently, Gough Island mice retain an avoidance response to predator urine. F1 offspring from crosses between these two strains behave more similarly to the mainland strain for most traits, suggesting recessive mutations contributed to behavioral evolution on the island. Our results provide a rare example of novel, inherited behaviors in an island population and demonstrate that behavioral evolution can be specific to different forms of perceived danger. Our discoveries pave the way for a genetic understanding of how island populations evolve unusual behaviors. Significance Organisms on islands are known to behave differently from mainland organisms. An absence of predators and a different set of natural resources are expected to make island organisms less anxious and more exploratory. We raised two groups of house mice, one from Gough Island in the South Atlantic and one from the mainland Eastern USA, in the same laboratory environment to see if behavioral differences between the two groups are heritable. Mice from both groups were placed in novel enclosures that are known to cause anxiety in rodents. We found that mice from the island are bolder and more exploratory in these enclosures but avoid predator odors in the same way as mainland mice. Our results show that boldness and exploration can evolve after island colonization.