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

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.

Scavengingvshunting affects behavioral traits of an opportunistic carnivore

“…Individuals who failed to adjust quickly would likely struggle in response to shifting resources, highlighting that shifts in resource availability can be a strong selection pressure for inherently bold, innovative, persistent, or flexible individuals. The understanding of the heritability of these behavioral traits is still developing, but research has identified genetic correlations with boldness in multiple vertebrate species ( Bubac et al, 2021 ; Stratton, Nolte & Payseur, 2021 ) and differential heritability among different behaviors in donkeys ( Equus asinus ; Navas González et al., 2019 ). Therefore, environmental changes that select for bold, innovative, or persistent individuals paired with the heritability of these traits could result in shifts in behavior at the population level over time.…”

Genetics of behavioural evolution in giant mice from Gough Island

“…To generate F2 mice, we conducted intercrosses between inbred strains of GI mice (produced in our laboratory) and mainland mice, the same strains used by Stratton et al . [ 20 ]. In 2009, GI mice were live-caught and shipped to the University of Wisconsin School of Veterinary Medicine Charmany Instructional Facility, where a breeding colony was established [ 27 ].…”

“…Husbandry and weighing protocols were identical to those applied by Stratton et al . [ 20 ] (see electronic supplementary material, file S1). F1s were generated by crossing mice from the GI strain and the mainland strain in both maternal directions ( figure 1 d ).…”

“…A striking example of an insular population with documented, heritable changes in behaviour is the house mice that invaded Gough Island (hereafter ‘GI’) [ 20 ], a remote island in the middle of the South Atlantic. These mice belong to the subspecies Mus musculus domesticus [ 21 ] and colonized the remote island probably via sailing vessels from Western Europe [ 22 , 23 ] a few hundred to a few thousand generations ago [ 24 , 25 ].…”

“…In the winter, GI mice predate on seabird populations, consuming an estimated 2 million chicks and/or eggs per year [ 31 ]. Following expectations for island colonizers and corresponding to their novel predatory behaviour, GI mice are bolder and more exploratory in novel environments compared with mainland conspecifics [ 20 ]. A genetic investigation of these behavioural changes promises to provide insight into long-standing questions about behavioural evolution.…”