Female preference for swords in Xiphophorus helleri reflects a bias for large apparent size (sexual selectionyvisual signalsypreexisting biasyvideo playbackyPoeciliidae)

Swordtail fish (Poeciliidae: genus Xiphophorus) are a paradigmatic case of sexual selection by sensory exploitation. Female preference for males with a conspicuous ‘‘sword’’ ornament is ancestral, suggesting that male morphology has evolved in response to a preexisting bias. The perceptual mechanisms underlying female mate choice have not been identified, complicating efforts to understand the selection pressures acting on ornament design. We consider two alternative models of receiver behavior, each consistent with previous results. Females could respond either to specific characteristics of the sword or to more general cues, such as the apparent size of potential mates. We showed female swordtails a series of computer-altered video sequences depicting a courting male. Footage of an intact male was preferred strongly to otherwise identical sequences in which portions of the sword had been deleted selectively, but a disembodied courting sword was less attractive than an intact male. There was no difference between responses to an isolated sword and to a swordless male of comparable length, or between an isolated sword and a homogenous background. Female preference for a sworded male was abolished by enlarging the image of a swordless male to compensate for the reduction in length caused by removing the ornament. This pattern of results is consistent with mate choice being mediated by a general preference for large males rather than by specific characters. Similar processes may account for the evolution of exaggerated traits in other systems. The evolution of the conspicuous signals used in mate choice is constrained by the perceptual properties of receivers. This constraint is most evident in cases of ‘‘sensory exploitation,’’ in which male signals have evolved to match preexisting female biases (1–5). The resulting ornaments are relatively stereotyped, exhibiting the same distinguishing features within a species. The specific nature of ornaments that have evolved in response to ancestral biases suggests two possible accounts of their origin. Females may exercise a specific, narrowly defined, preference for a particular stimulus. Sexual selection would then substantially constrain the design of the male ornament. Alternatively, females may have a predilection for broad classes of stimuli. If this scenario was true, a wide variety of phenotypes might increase male mating success. The specific form of an ornament would then be constrained by factors other than mate choice, such as intrasexual competition, natural selection, and evolutionary history. Male swordtails (Xiphophorus) were cited by Darwin (6) as an example of extreme sexual ornamentation. The lower rays of the caudal fin are elongated into a conspicuous, usually pigmented, ‘‘sword.’’ Xiphophorus includes the swordtails, in which most species have males with swords, and the platies, in which all of the species lack swords. Males of the sister group Priapella are also swordless. Females from two platy species, X. maculatus (2) and X. variatus (7), and female P. olmecae (1) all prefer conspecific males with artificial swords attached, indicating that a female preference for the ornament predates the appearance of the structure in males. There are at least two distinct ways in which female perceptual processes may have shaped male morphology in this system. It is possible that female swordtails have a narrow preference for swords or sword-like structures. In this case, swords effectively would be acting as a releaser of female mating behavior (8). Alternatively, a more general preference may have interacted with specific factors limiting male expression of conspicuous traits. For example, fin elongations elsewhere on the body may bear a higher hydrodynamic cost or be subject to greater developmental constraint. There also might be simply a lack of genetic variation for all but one or a few traits. A permissive bias could manifest itself in a preference for males of larger total size, which is a widespread trait in poeciliids (1, 9–11) and many other taxa (12). Assessing the specificity of female mate choice criteria requires highly controlled manipulations of male morphology. It has been historically difficult to conduct experimental analyses of the responses evoked by visual signals, but recent studies have used video playback techniques to explore successfully a diverse array of systems (13–18). A major advantage over static models is that video stimuli retain sexual display characteristics. Female green swordtails prefer analog video sequences of a courting male to sequences of the same male engaged in noncourting movements or remaining inactive (17), suggesting that courtship-specific motor patterns are an important part of the visual signal. We used computer-generated animations to analyze the perceptual basis of female response to visual signals in green swordtails. Two sets of experiments were conducted. In the first, we assessed female preferences for different components of the sword by presenting an animation of a normal male engaged in courtship display and two sequences, derived from this, in which portions of the sword had been removed digitally. In the second experiment, we tested between alternative hypotheses concerning the specificity of the female preference by presenting components of the sword in isolation and by manipulating stimulus size. MATERIALS AND METHODS Subjects. Female X. helleri were obtained from the Xiphophorus Genetic Stock Center at Southwest Texas State University (San Marcos, TX). All of the subjects were descendants of individuals collected at various sites in southern Mexico between 1963 and 1980. We maintained the fish in the laboratory on a 14:10 h light:dark cycle, with both natural and © 1998 by The National Academy of Sciences 0027-8424y98y954431-6$2.00y0 PNAS is available online at http:yywww.pnas.org. Abbreviations, SL, standard length; TL, total length. †To whom correspondence should be addressed. e-mail: fishman@ mail.utexas.edu.