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B R I E F C O M M U N I C AT I O N doi:1111/j.1558-5646.00976.x THE SELECTIVE ADVANTAGE OF CRYPSIS IN MICE Sacha N. Vignieri,1,2 Joanna G. Larson,1...

In the article "The Selective advantage of crypsis in mice," how was the fitness of different coat colors in the beach mice, Peromyscus polionotus, determined? Which type of natural selection was maintaining variation among beach mice populations in coat color and how did the study demonstrate this particular action of natural selection? 

BRIEF COMMUNICATION doi:10.1111/j.1558-5646.2010.00976.x THE SELECTIVE ADVANTAGE OF CRYPSIS IN MICE Sacha N. Vignieri, 1 , 2 Joanna G. Larson, 1 and Hopi E. Hoekstra 1 1 Department of Organismic and Evolutionary Biology and The Museum of Comparative Zoology, Harvard University, 26 Oxford St, Cambridge, Massachusetts 02138 2 E-mail: [email protected] Received October 7, 2009 Accepted January 29, 2010 The light color of mice that inhabit the sandy dunes of Florida’s coast have served as a textbook example of adaptation for nearly a century, despite the fact that the selective advantage of crypsis has never been directly tested or quanti±ed in nature. Using plasticine mouse models of light and dark color, we demonstrate a strong selective advantage for mice that match their local background substrate. Further our data suggest that stabilizing selection maintains color matching within a single habitat, as models that are both lighter and darker than their local environment are selected against. These results provide empirical evidence in support of the hypothesis that visual hunting predators shape color patterning in Peromyscus mice and suggest a mechanism by which selection drives the pronounced color variation among populations. KEY WORDS: Adaptation, camou²age, natural selection, Peromyscus , plasticine model, stabilizing selection. One-hundred fifty years ago in The Origin of Species ,Cha r les Darwin famously proposed his theory of evolution by natural se- lection. To build the argument for natural selection, Darwin often relied on intuitive examples: “when we see ... the alpine ptarmi- gan white in winter, the red grouse the color of heather, and the black-grouse of peaty earth, we must believe that these tints are of service ... in preserving them from danger” (Darwin 1859). Perhaps inspired by Darwin’s intuition that camouflage confers a survival advantage, color variation became the focus of many of the early studies of adaptation. In particular, studies on color matching in Peromyscus mice were instrumental in documenting natural selection in the wild—strong correlations between local soil color and dorsal coat color were repeatedly found among pop- ulations (e.g., Dice 1940). Further, JBS Haldane (1948) demon- strated theoretically that spatially varying selection could lead to and maintain locally adapted phenotypes, again using Peromyscus color matching as the prime empirical example. These few early studies were broadly seen as evidence that selection could drive color matching in a variety of taxa. Despite nearly a century of work on this system, however, a direct and empirical quantification of the selective advantage for color matching in a natural setting is still lacking. Enclosure experiments have been suggestive, albeit contrived—these stud- ies often use unnatural densities of mice, extreme color variants, and/or largely depend on the personalities of one or two individ- ual predators (“the long horned owl was very shy and erratic in his behavior,” whereas “the barn owl was a much more consistent worker”; Dice 1949). Moreover, even with enclosure experiments and more traditional common-garden approaches, it is difficult to disentangle direct selection on color (due to crypsis) from selec- tion on other traits (e.g., odor, activity level, or escape behavior) that may be correlated with color. To address these concerns, recent research has taken a novel experimental approach—using photographs (Webster et al. 2009), manipulated prey (Cuthill et al. 2005; Ioannou and Krause 2009), and computer-generated images (Kiltie and Laine 1992; Chlao et al. 2007)—to empirically test hypotheses about the adaptive significance and function of ani- mal color (Stevens and Merilaita 2009). Similar to these studies, here we expose predators to prey models to directly estimate the selective advantage of camouflage in nature. The use of plasticine models to address questions in evo- lutionary biology was pioneered by Brodie (1993) and since has 1 C ° 2010 The Author(s). Evolution
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BRIEF COMMUNICATION been used to document predation in reptile and amphibian species. These studies have demonstrated how variation in aposematism (e.g., Kuchta 2005; Saporito et al. 2007; Noonan and Comeault 2009), Batesian mimicry (e.g., Brodie and Janzen 1995; Pfennig et al. 2001), body shape (e.g., Shepard 2007), and sexual sig- naling (e.g., Husak et al. 2006) affect predation rates. Although simple, this method has several advantages. First, because plas- ticine preserves evidence of predation attempts (i.e., tooth, beak or claw imprints), it is possible to quantify both predation rate and predator type. Moreover, using models, we can deploy a large, and biologically realistic, number of individuals within a given environment. Finally, this experimental approach allows us to fo- cus on variation in a single trait of interest (and thereby control for indirect selection on correlated traits) because models can be made otherwise identical. Here, we use plasticine models of mice, which differ in only color phenotype, to test for and quantify the selective advantage of camouflaging color in realistic models by exposing them to natural predators in the wild. Materials and Methods The most extreme case of color adaptation in Peromyscus occurs among subspecies of Peromyscus polionotus —the dark-brown dorsal coats of inland subspecies occupying abandoned agricul- tural fields (oldfields) contrast strikingly with the pale-colored beach mice that inhabit Florida’s coastal sand dunes and barrier is- lands (Sumner 1929a,b). Using nonhardening plasticine, we con- structed 250 models of P. polionotus , half of which were painted to mimic the coat color and pattern of the dark oldfield mouse ( Peromyscus polionotus subgriseus ) and half the light Santa Rosa Island beach mouse ( P. p. leucocephalus ). We then deployed these models in both light and dark habitat, recorded predation events, and estimated the selective advantage of camouflage. MOUSE MODEL CONSTRUCTION To produce the most realistic models, we created silicone molds of P. polionotus specimens preserved in a crouched position and poured fully liquefied Van Aken Plastilina into these molds. When cooled, we removed models and painted them using Rustoleum (Rust-Oleum, Vernon Hills, IL) textured spray paint. All models were first spray-coated with white, the dark models received an additional coat of gray then tan paint, and both types were finalized with hand painting of eyes and dorsal pelage in either brown (dark models) or tan (light models). MODEL DEPLOYMENT Models were simultaneously deployed in eight linear transects, four set in beach habitat, at Topsail Hill Preserve State Park (N30 21 0 50.831 00 W86 17 0 18.368 00 ) and four in inland fields, 29.2 kilometers northeast at Lafayette Creek Wildlife Manage- ment Area in Florida (N30 32 0 22.999 00 W86 3 0 26.568 00 ; Fig. 1A). At both locations, we had recently captured live P. polionotus . Over the course of the experiment, we moved each of the eight transects four times, for a total of 32 transects, each left in place for 72 h. Within each habitat (beach or inland), simultaneous transects were set a minimum of 100 m apart or end to end, and consecutive sets of transects were set a minimum of 500 m apart. Transects consisted of 14 light and 14 dark models set out in a random order, spaced 10 m apart, and placed in the most open soil patch available. Models were checked every 24 h, and attacked models were replaced with an identical type to maintain light:dark ratios. This design resulted in a total of 2688 “model-nights.” PREDATION SCORES Predation events were identified as models that had been obvi- ously attacked (based on the presence of tooth marks, bill marks or other imprints) or clearly picked up and carried in the presence of predator tracks. We were unable to find 12 models, which we identified as missing. These data were not included in selection estimates, but could be included in survival analyses for which they were considered “censored data.” Five models had imprints that we could not assign to a predator class (i.e., mammalian or avian); however, the results of the analyses did not differ when these data were omitted, so they were included (and labeled “am- biguous”). We also excluded five models that showed evidence of nonpredatory rodent gnawing. MODEL AND SOIL BRIGHTNESS We collected soil samples from around each deployed model and measured soil brightness. Brightness was measured similarly for models and four representative museum specimens of each subspecies (Fig. S1). Specifically, we measured reflectance across the light spectrum visible to most predators (300–700 nm; Bennett and Cuthill 1994), using a USB2000 spectrophotometer (Ocean Optics, Dunedin, FL). We calculated overall brightness as the average reflectance across these wavelengths (following Mullen and Hoekstra 2008). Because the models were exposed to a natural community of predators, we did not take into account the visual sensitivity of any particular receiver, which can provide a more accurate measure of camouflage (see Stevens 2007). To account for heterogeneity within a sample, we averaged across multiple independent measurements; 10 for soil and 22 for mouse models and specimens (14 from the shoulder to the rump laterally on the left [1–7] and right [8–14], and 8 dorsally from the forehead to the base of the tail [15–22]). The average brightness for each soil and model sample was used in subsequent analyses. The measurements obtained for real mice fall within the range of those obtained for model mice (Fig. S2). 2 EVOLUTION 2010
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