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Behavioral Ecology Vol. 10 No. 1: 63–67 The evolution of bill coloration and plumage dimorphism supports the transference hypothesis in dabbling ducks Kevin P. Johnson Bell Museum of Natural History and Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108, USA Bright coloration in male birds is typically thought to be driven by sexual selection (female choice or male–male competition). Bird species often vary in the intensity of bright coloration, but few studies have addressed this cross-species variation. Potentially this variation could result from either variation in female preferences or in the relative costs of male traits. Species of dabbling ducks vary in the presence of bright male plumage and bill coloration. I tested the transference hypothesis for ornament evolution in dabbling ducks using a phylogenetic study of character evolution. The transference hypothesis makes three predictions: (1) a costly male ornamental trait is the ancestral condition, (2) a less costly male ornamental trait is the derived condition, and (3) gains in the less costly trait are associated with losses or absence of the more costly male trait. All three of these predictions were satisfied in this study of the evolution of plumage dimorphism and bright bill coloration in the dabbling ducks, given that bright plumage coloration is more costly than bright bill coloration. Key words: Anas, female choice, ornamentation, sexual selection, waterfowl. [Behav Ecol 10:63–67 (1999)] T heoretical and empirical studies of female mate choice and sexual selection make predictions about why females should prefer ornamental male traits (Andersson, 1994; Fisher, 1930; Grafen, 1990; Iwasa et al., 1991; Lande, 1981; Pomiankowski et al., 1991; Ryan et al., 1990; Zahavi, 1975). However, few workers have examined why male secondary sexual traits take the particular form that they do (Wiley and Richards, 1978; Zahavi, 1987) or why these traits vary among species as they do (Hamilton and Zuk, 1982; Read and Weary, 1992). Because many male secondary sexual traits are assumed to be costly, variation among species might arise due to differences in the cost of these traits (Endler, 1977; Endler and Houde, 1995). One hypothesis to explain evolution and evolutionary variation in male traits is ‘‘transference’’ (Borgia, 1993; Gilliard, 1956, 1963; Kusmierski et al., 1993). According to this hypothesis, if males are able to use less costly traits and still attract females, then these less costly traits should be favored by natural selection and evolve. This hypothesis was developed for bowerbirds because it was noted (Borgia, 1993; Gilliard, 1956, 1963) that bowerbird species with bright male plumage tend to build simple bowers, whereas monomorphic species with dull males tend to build elaborate bowers with many decorations. Ornamentation may be transferred to the bower if it is a less costly trait than male plumage because the male can ‘‘escape’’ the costly ornament if necessary (Gilliard 1956, 1963). Borgia (1993) examined the cost of the bower display in male satin bowerbirds (Ptilonorhynchus violaceus) and found no evidence of a high cost for this display; however, the cost of bright plumage in bowerbird males has not been measured. A phylogenetic test of the transference hypothesis in bowerbirds was partially consistent with the prediction that K. P. Johnson is currently at the Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, UT 84112-0840, USA. E-mail: [email protected]. Received 10 February 1998; revised 16 June 1998; accepted 29 June 1998. q 1999 International Society for Behavioral Ecology bright male plumage and lack of sophisticated bowerbuilding are the ancestral conditions (Kusmierski et al., 1993). The transference hypothesis of male trait evolution, which can be extended to other taxa, makes three major predictions: (1) elaborate (more costly) ornaments should be the ancestral condition, (2) less costly ornaments should be a derived condition, and (3) gains in the less costly ornament should be associated with absence or loss of the more costly ornament. I tested these predictions in dabbling ducks by examining the evolution of bill coloration and dimorphic plumage using a phylogeny derived from mitochondrial DNA sequences ( Johnson, 1997; Johnson and Sorenson, 1998). Dabbling ducks have worldwide distribution, and they exhibit remarkable variation between species in traits that are believed to be under sexual selection. Both bill coloration and plumage characteristics are targets of female choice in dabbling ducks. In mallards (Anas platyrhynchos), Omland (1996a,b) found that females strongly prefer males with brightly colored bills and that females also show a preference for overall plumage condition (Holmberg et al., 1989; Weidmann, 1990). In northern pintails (Anas acuta), Sorenson and Derrickson (1994) found that females have preferences for some plumage ornaments but not others. These results, taken together with the elaborateness of male plumage and bill coloration in dabbling ducks, suggest that these traits are likely to be under the influence of sexual selection in many dabbling duck species. Because bright male plumage often covers most of the male’s body and is often very striking, it is likely that bright plumage is more costly (at least in terms of predator pressure) than a bill spot (which only covers a small portion of the bill). Metz and Ankney (1991) documented increased hunter-caused mortality of male ducks with brightly colored plumage compared to dull individuals. It is currently unknown whether bright bill coloration or bright plumage is more costly to produce, so I assumed differences in predation costs for this analysis. I investigated the evolution and evolutionary correlation of these two traits with respect to the transference hypothesis of female choice with the expectation that gains in carotenoid bill coloration are associated with monomorphic plumage. Behavioral Ecology Vol. 10 No. 1 64 Figure 1 Phylogenetic reconstruction of carotenoid bill-coloration using unordered parsimony. Three alternative reconstructions shown as equivocal branches. A. 5 Anas. METHODS I scored (using colored plates in Madge and Burn, 1988) the presence or absence of male bill coloration and plumage dimorphism as dichotomous characters for 42 species of dabbling ducks. Species were scored as possessing bill coloration if the bill of the male has spots or is completely colored with carotenoid pigmentation. I assumed that red or yellow bills or spots contained carotenoids. For example, the male whitecheeked pintail (Anas bahamensis) possesses a red bill spot, while the bill of the male mallard (Anas platyrhynchos) is entirely yellow. Both of these species were considered to have carotenoid bill coloration. Scoring of plumage dimorphism and bill coloration by two independent observers produced identical coding for both characters. I optimized the dichotomous characters bill coloration and plumage dimorphism over the phylogenetic tree ( Johnson, 1997; Johnson and Sorenson, 1998) using MacClade (Maddison and Maddison, 1992) with unordered parsimony. Given the phylogenetic distribution of these two characters in waterfowl, the unordered assumption seems reasonable (but see Omland, 1997, for an alternative view). I examined all possible reconstructions for each character. I used the concentrated changes test (Maddison, 1990) to test for an association between gains and losses in one character and a particular character state in the other character. I did this for all possible (six in this case) combinations of character reconstructions. Under the transference hypothesis, gains and losses in bill coloration should be associated with monomorphic and dimorphic plumage, respectively, because bill coloration is assumed to be less costly than bright plumage. The concentrated changes test examines, in this case, whether more gains in bright bill coloration (changes from white to black in Figure 1) occur on branches with monomorphic plumage reconstructed (white branches in Figure 2) than expected by chance. However, I also tested for the alternative association; that is, whether the changes in plumage were associated with the state of bill coloration. RESULTS Optimization of plumage dimorphism over the tree resulted in two equally parsimonious reconstructions of plumage dimorphism. In both reconstructions bright male dimorphic plumage was the ancestral condition. Either six losses and five gains of dimorphism or five losses and six gains were reconstructed (Figure 2). This is consistent with the first prediction of the transference hypothesis that the more costly male trait is ancestral. I found three equally parsimonious reconstructions for bill coloration. Between six and eight gains in bill coloration and between three and one losses occur in this character (Figure 1). In all reconstructions, the absence of bill coloration is the ancestral condition, and bill coloration evolves independently at least six times. This is consistent with the second prediction of the transference hypothesis that the less costly male trait is a derived condition. When I examined the association of gains in bill coloration with monomorphic plumage and losses of bill coloration with dimorphic plumage, I found that there was a strong association (concentrated changes test, p , .01 for all six combinations of reconstructions, range 0.005 to , 0.001). That is, the several independent gains in bill coloration were concentrated on branches that had monomorphic plumage reconstructed on them. This is consistent with the final prediction of the transference hypothesis that gains in the less costly ornament should be associated with absence or loss of the more costly ornament. Alternatively, when I examined the association of changes in plumage dimorphism with the presence or absence of bill coloration, there was no association (concentrated changes test, p . .50 for all six combinations of reconstructions). That Johnson • Transference hypothesis in dabbling ducks 65 Figure 2 Phylogenetic reconstruction of plumage dimorphism using unordered parsimony. Two alternative reconstructions shown as equivocal branches. A. 5 Anas. is, changes in the more costly trait are not influenced by the state of the less costly trait, but once the more costly trait is lost, origin of the less costly trait is favored. This result is in accordance with the transference hypothesis, which makes predictions about the origin of the less costly trait (bright bill coloration) but not about the origin of the more costly trait (bright plumage). DISCUSSION The three predictions of the transference hypothesis are supported for bill coloration and plumage dimorphism in dabbling ducks. The more costly male secondary sexual trait (in terms of its potential obviousness to predators), bright male plumage, is the ancestral condition in dabbling ducks, and it has been lost several times. The less costly trait, bill coloration, is derived several times independently within dabbling ducks. Gains in bill coloration are associated with the absence of bright dimorphic plumage. The pattern of changes in these male traits supports the transference hypothesis (Kusmierski et al., 1993). Nearly all species that possess bill coloration have monomorphic plumage. The exception to this pattern is the mallard (A. platyrhynchos). The mallard has dimorphic plumage and a colored bill. Female mate-choice experiments in this species have shown that bill coloration and overall plumage condition are both important predictors of female choice (Holmberg et al., 1989; Omland, 1996a,b; Weidmann, 1990). The mallard group has also radiated recently compared to other dabbling duck groups ( Johnson, 1997; Johnson and Sorenson, 1998), and this may result in an evolutionary time lag in the changes in plumage and bill coloration. Support for the transference hypothesis relies on the assumption that bill coloration is less costly than bright plumage. Although the actual costs of bill coloration and bright plumage in male dabbling ducks have not been measured (but see Metz and Ankney, 1991, who documented hunter preference for bright males), there is indirect evidence that this is the case. Females of species with bright male bill coloration often have colored bills (10 out of 14 species). This could be due to a genetic correlation between males and females which causes bill coloration to be present in females because it is being selected for in males (Fisher, 1930; Lande, 1980; Møller, 1994). Typically, colored bills are duller in females than in males ( Johnson KP, personal observation). In contrast, in species with markedly bright plumage, only the males possess this coloration in the plumage. Females of dimorphic species are typically mottled brown, presumably an adaptation for crypsis to avoid predation while sitting on the nest (Sargeant and Raveling, 1992). This pattern is further evidence suggesting that bill coloration is not as costly as bright plumage; presumably selection for females to lose bill coloration is weak. While changes in these two male secondary sexual traits form a strong pattern, it is unknown how female preferences change in relation to male traits. The transference hypothesis as developed (Kusmierski et al., 1993) suggests that female preferences should also change in association with changes in the male traits. Relatively few mate choice experiments have been performed using dabbling duck species (mallard: Holmberg et al., 1989; Omland, 1996a, b; Weidmann, 1990; northern pintail: Sorenson and Derrickson, 1994). To understand the full nature of the pattern of change in male traits, it will also be important to document how female preferences change. For example, do females of dimorphic species have preferences for bright plumage but lack preference for bill coloration, or do females have a preexisting bias (Basolo, 1990; Ryan et al., 1990) for bill coloration that favors the repeated evolution of this trait in dabbling ducks? Even though bill brightness is clearly associated with monomorphic plumage, it is unclear from this analysis what forces are driving changes in plumage brightness. Although the an- Behavioral Ecology Vol. 10 No. 1 66 cestral condition of dimorphic plumage is consistent with the transference hypothesis, the five to six rederivations of plumage dimorphism are not easily explained. Under the transference hypothesis, it is expected that once female preference has shifted to a less costly male trait, the trait should be stable against further evolution to a more costly trait. Other factors (perhaps ecological or social) influencing the cost and/or benefit of particular male traits might play a role in the evolutionary changes in plumage dimorphism. In addition to plumage and bill coloration, male dabbling ducks also use a wide variety of movement and vocal displays in their courtship (Lorenz, 1941; McKinney, 1975). Large display repertoires are associated with dimorphic plumage ( Johnson, 1997), but few studies have documented female preferences for displays. Mallard males that display more frequently tend to obtain more mates (Bossema and Kruijt, 1982; Holmberg et al., 1989; Klint et al., 1989); however, none of these studies experimentally manipulated display rates, so the actual role of display performance and intensity in female choice is still uncertain. Future experimental and phylogenetic studies integrating male variation in plumage, bill coloration, and movement and vocal display with female choice are needed to fully understand the evolution of secondary sexual traits in dabbling ducks. In conclusion, although the transference hypothesis appears to be supported in bowerbirds (Kusmierski et al., 1993) and dabbling ducks (this study), it is unclear how broadly it will apply to other taxa. The cost of ornaments is assumed by the transference hypothesis, but the transference hypothesis does not make assumptions about the mechanism of sexual selection (e.g., Fisher, 1930; Ryan et al., 1990; Zahavi, 1975). The costliness of ornaments is an underlying theme of all theories of sexual selection by female choice. If ornaments are not costly, then they could be explained by ‘‘ordinary’’ natural selection, and female choice would not need to be invoked (Andersson, 1994). The fact that female choice overrides the negative fitness costs of male ornaments is of primary interest in theories of sexual selection. The transference hypothesis could generally operate under any of the models of female choice. In runaway sexual selection models (Fisher, 1930; Lande, 1981; Pomiankowski et al., 1991), ornaments with a smaller fitness penalty (that females prefer equally to more costly ornaments) should be favored by selection and displace more costly ornaments. Likewise, under handicap models of sexual selection (Grafen, 1990; Iwasa et al., 1991; Zahavi, 1975), if a less costly trait provides just as much information about a male as a more costly trait, it should be favored and displace the more costly trait (Grafen, 1990). Even under the preexisting bias models (Ryan et al., 1990), biases for less costly traits are more likely to prevail in a population than biases of similar magnitude for more costly traits. Variation in costs and kinds of male ornaments should be of considerable interest in explorations of sexual selection. In most taxa, courtship and female choice often involve several traits (and often different types of traits, such as morphology versus vocalizations). Presumably some of these traits are less costly for males to produce than others. If this is the case, then there should be selection for males to use cheaper displays, given that females show equal or compensating preferences for these traits. The evolution of less costly traits from costly traits bears more investigation in other taxa. I thank F. McKinney, D. Clayton, and two anonymous reviewers who reviewed earlier versions of this manuscript and made helpful suggestions. Discussions with K. Omland provided valuable insights into the nature of female choice in dabbling ducks. B. Walther and T. Jones provided independent scoring of the characters used in this study. 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