Academic journal article Genetics

Genetics of Rapid and Extreme Size Evolution in Island Mice

Academic journal article Genetics

Genetics of Rapid and Extreme Size Evolution in Island Mice

Article excerpt

THE 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 is notoriously difficult to demonstrate adaptation (Endler 1986), populations that rapidly evolve to phenotypic extremes following major environmental shifts provide a revealing window into the process. Evidence for adaptive change is often observed in island populations, where the limited geographic scope, sharp boundaries, and simplified biotas of islands facilitate the interpretation of evolutionary patterns (Losos and Ricklefs 2009). Insular mammals show elevated rates of morphological evolution (Pergams and Ashley 2001; Millien 2006) and include several examples of gigantism and dwarfism (Stock 1935; Freudenthal 1972; Roth 1992; Moncunill-Solé et al. 2014). Populations that colonize islands often experience substantial changes in predation risk, competition, and resource availability that together generate strong selection for shifts in body size (Sondaar 1977; Case 1978; Heaney 1978; Lawlor 1982; Lomolino 1985; Lomolino et al. 2012). Although the question of whether island mammals in general follow directional patterns in the evolution of body size (Foster 1964; Van Valen 1973; Lomolino 1985) has inspired debate (Lawlor 1982; Lomolino 1985, 2005; Meiri et al. 2004, 2008, 2011; Lomolino et al. 2005, 2012; Raia and Meiri 2006; Bromham and Cardillo 2007), murid rodents usually evolve larger sizes on islands (Adler and Levins 1994; Meiri et al. 2008). This pattern, combined with the remarkable success of house mice (Mus musculus)incolonizingislandsfrom around the world, positions these rodents as an especially promising system for understanding adaptive size change. Considerable morphological diversity within and among island populations of house mice has been documented, especially in the research of R. J. Berry (Berry 1964, 1965, 1968, 1996; Berry and Jakobson 1975; Berry et al. 1987, 1978a,b, 1979, 1982; Berry and Scriven 2005).

The largest wild house mice in the world reside on Gough Island (GI), a remote volcanic island in the middle of the South Atlantic Ocean (Rowe-Rowe and Crafford 1992). Gough Island mice weigh approximately twice as much as their mainland relatives (Jones et al. 2003). Mice were introduced to Gough Island by teams of seal hunters (Wace 1961; Jones et al. 2003) between 130 and 200 years ago (Verrill 1895; Gray et al. 2014), suggesting that body size evolution has been very rapid.

Gough Island mice belong to the same subspecies as the laboratory mouse (Mus musculus domesticus)(Grayet al. 2014), providing access to an expansive genetic toolkit for investigating their phenotypic evolution. In this article, we focus on the rapid evolution of body size, for two reasons. First, body size is highly correlated with aspects of physiology, life history, morphology, behavior, and ecology (Peters 1983; Calder 1984; Schmidt-Nielsen 1984). …

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