Genetics of Rapid and Extreme Size Evolution in Island Mice

Abstract

Abstract Organisms on islands provide a revealing window into the process of adaptation. Populations that colonize islands often evolve substantial differences in body size from their mainland relatives. Although the ecological drivers of this phenomenon have received considerable attention, its genetic basis remains poorly understood. We use house mice (subspecies: Mus musculus domesticus) from remote Gough Island to provide a genetic portrait of rapid and extreme size evolution. In just a few hundred generations, Gough Island mice evolved the largest body size among wild house mice from around the world. Through comparisons with a smaller-bodied wild-derived strain from the same subspecies (WSB/EiJ), we demonstrate that Gough Island mice achieve their exceptional body weight primarily by growing faster during the 6 weeks after birth. We use genetic mapping in large F2 intercrosses between Gough Island mice and WSB/EiJ to identify 19 quantitative trait loci (QTL) responsible for the evolution of 16-week weight trajectories: 8 QTL for body weight and 11 QTL for growth rate. QTL exhibit modest effects that are mostly additive. We conclude that body size evolution on islands can be genetically complex, even when substantial size changes occur rapidly. In comparisons to published studies of laboratory strains of mice that were artificially selected for divergent body sizes, we discover that the overall genetic profile of size evolution in nature and in the laboratory is similar, but many contributing loci are distinct. Our results underscore the power of genetically characterizing the entire growth trajectory in wild populations and lay the foundation necessary for identifying the mutations responsible for extreme body size evolution in nature.