Genetics of Rapid and Extreme Size Evolution in Island Mice

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 F 2 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.KEYWORDS island syndrome; island evolution; phenotypic extreme; body size; complex trait T HE question of how organisms adapt to new environments continues to captivate biologists. Because adaptation requires genetic change, discovering the mutations responsible for adaptive phenotypes is a key step toward understanding the mechanisms of this process. There is a growing list of traits for which adaptive differences in nature have been directly traced to specific genes. Examples include adaptive coloration in pocket mice (Nachman et al. 2003), deer mice (Hoekstra et al. 2006), Drosophila melanogaster (Rebeiz et al. 2009), and peppered moths (van't Hof et al. 2011); armor plate patterning and pelvic spine reduction in stickleback fish (Colosimo et al. 2005;Chan et al. 2010;Jones et al. 2012); and defense chemistry in Boechera stricta (Prasad et al. 2012). Despite these advances, the genetic architecture of adaptation in nature remains poorly understood. Most progress has focused on traits with simple genetic bases, where one or a few loci explain observed phenotypic variation (Rockman 2012). But the majority of trait differences between populations inhabiting contrasting environments are quantitative, suggesting that adaptation often involves more complex inheritance.While it ...

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“…However, there have been studies on the house mouse (Mus musculus) that examine the genetics of body size. Gray et al (2015) found that insular M. musculus on Gough Island in the Atlantic Ocean attain their unusually large body size through accelerated growth in the first 6 weeks of life. They identified 19 quantitative trait loci (QTLs) that were responsible for this increased growth rate (11 QTLs, 3-20% of variance) and overall larger body size (8 QTLs, 6-24% of variance) (Gray et al 2015).…”

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