Evolutionary mismatch of mating preferences and male colour patterns in guppies

Transcription

1 Anim. Behav., 1997, 53, Evolutionary mismatch of mating preferences and male colour patterns in guppies ANNE E. HOUDE & MELISSA A. HANKES Department of Biology, Lake Forest College (Received 31 July 1995; initial acceptance 11 October 1995; final acceptance 4 June 1996; MS. number: A7375R) Abstract. Female mating preferences and the male colour pattern characteristics upon which preferences are based vary both within and between guppy, Poecilia reticulata, populations from Trinidad. A general trend is for the degree of preference for orange coloration to match the degree of expression of orange coloration in each population, resulting in a positive correlation between the means of the two traits across populations. This study documented an exception to this trend. The mating preferences of female guppies from Trinidad s Yarra and Paria Rivers were compared using standard behavioural assays. Because Yarra males show less orange coloration in their colour patterns than do Paria males, results of previous studies led to a prediction in the present study of a corresponding difference in mating preferences between Yarra and Paria females. Both Yarra and Paria females, however, showed a strong preference for more orange individuals when responding to courtship by Paria males. The expression of preference in Yarra females therefore does not match the expression of orange coloration as predicted. Several hypotheses are suggested that may account for this apparent mismatch The Association for the Study of Animal Behaviour Theoretical and empirical work (Lande 1981; Kirkpatrick 1982; Kirkpatrick & Ryan 1991; Houde 1993, 1994; Gilburn & Day 1994; Wilkinson & Reillo 1994) has shown that the mating preferences of females and the traits of males on which preferences are based are likely to evolve in parallel. This parallel evolution can come about for two main reasons. The simplest is that mating preferences can result in sexual selection leading to the evolution of corresponding male traits. Under Fisherian and good genes models, the two characters also become genetically correlated due to non-random mating, when females with a particular preference mate with males with corresponding trait development, and both characters are inherited by offspring. This genetic correlation can then result in evolution of female mating preferences as a correlated response to selection on the preferred male trait. In either case, the evolutionary relationship between the two characters may lead to correlated patterns of variation across species or populations (Houde Correspondence: A. E. Houde, Department of Biology, Lake Forest College, 555 North Sheridan Road, Lake Forest, IL 60045, U.S.A. ( houde@lfc.edu). 1993). The prediction of a correspondence between female preferences and male colour patterns across populations depends on several assumptions. First, correlated evolution of male traits and female preferences within a population can only occur if there is sufficient genetic variation in both traits. Second, male traits and female preferences may correspond well only in populations that have reached evolutionary equilibrium for both characters. Finally, correlated evolution of the two traits requires that females in nature are actually expressing the mating preferences that we measure behaviourally in the laboratory, so that mate choice leads to sexual selection on the male trait. Given that these assumptions might not be met in all populations, it is of interest to continue to examine the predicted correspondence between female preferences and male secondary sexual traits, as we have done here. Studies of sexual selection and mating preferences in guppies have produced evidence that female mating preferences and male colour patterns evolve in parallel (Houde 1988a; Houde & Endler 1990; Houde 1994; Endler & Houde 1995; but see Breden & Hornaday 1994). Female /97/ $25.00/0/ar The Association for the Study of Animal Behaviour 343

2 344 Animal Behaviour, 53, 2 guppies from many natural populations show a preference for males with large amounts of orange coloration (e.g. Kodric-Brown 1985; Houde 1987; Houde & Endler 1990). Some populations, however, do not show the strong preference for orange coloration, and the expression of orange in males from these populations tends to be relatively low (Houde 1988a; Houde & Endler 1990; Endler & Houde 1995). A survey of 11 populations showed a significant association between the expression of orange in male colour patterns and the expression of female mating preferences in laboratory behaviour assays (Houde & Endler 1990; Endler & Houde 1995). These comparative results indicate that the evolution of mating preferences and colour patterns can be interdependent. Further evidence for this interdependence comes from artificial selection experiments in which selection for increased and decreased orange coloration was imposed within a population (Houde 1994; but see Breden & Hornaday 1994). In some selection lines, a strong response in the orange character was accompanied by a corresponding shift in female mating preferences, apparently as a correlated response to artificial selection. This kind of correlated response to selection could explain the correlation between preferences and colour patterns across populations. The correspondence between expression of preferences for orange in females and orange coloration in males is not perfect. Some populations show less expression of orange than would be predicted for their level of preference, and others show an opposite pattern (Figure 3 in Endler & Houde 1995), but previous data were not adequate to determine whether this variation was due to experimental error or to other factors affecting the sexual selection system. Most, although not all, of the guppy populations that show strong preferences and strongly expressed orange coloration come from north-flowing streams (notably the Paria River) in the Northern Range mountains of Trinidad, and most of the populations with weak or no preferences and weakly expressed orange coloration come from south-flowing streams on the other side of the range (Houde & Endler 1990; Endler & Houde 1995). In this study, we attempted an additional test of the hypothesis that the evolution of preferences and colour patterns are correlated by comparing mating preferences between two populations from north-flowing streams that differ in expression of orange coloration and predation regime. We examined the mating preferences of female guppies from a population from the lower Yarra river of Trinidad, which shows the least expression of orange coloration of all populations studied from north-flowing streams in Trinidad (Houde & Endler 1990; Endler & Houde 1995). The reduced expression of orange is probably due to selective predation on brightly coloured males by large fishes present in the lower Yarra river (Endler 1983; Reznick et al. 1996). Lower Yarra guppies also show life-history traits consistent with high levels of predation on adults (Reznick et al. 1996). This population is also the most genetically divergent of all guppy populations examined to date (Magurran et al. 1995). It does not appear to be closely related to other north slope populations or to south slope populations. The Yarra population therefore provides an additional test of the hypothesis that colour patterns and mating preferences are evolutionarily linked. Specifically, given that Yarra males have less orange in their colour patterns compared with Paria males, which show the greatest expression of orange of all studied populations (Houde & Endler 1990; Endler & Houde 1995), we predicted that Yarra females should show a correspondingly weaker preference or no preference for orange coloration compared to Paria females. MATERIALS AND METHODS Experimental Fish Guppies (Poeciliidae) are live-bearing fishes native to streams and rivers of Trinidad and adjacent parts of South America. Males show elaborate colour patterns consisting of variously coloured spots; females are uncoloured. Colour patterns are genetically variable within and between populations, depending in part on the risk of predation by piscivorous fishes in each stream (e.g. Endler 1978, 1983). Female mating preferences also vary within and between populations (Endler & Houde 1995; Godin & Dugatkin 1995). Our experiments were conducted using guppies from stocks descended from individuals captured in the Paria and Yarra rivers of Trinidad approximately four generations previously. All fish were reared and maintained under standard conditions (Houde 1987), with Paria and Yarra

3 Houde & Hankes: Guppy mating preference mismatch 345 stocks randomized throughout the laboratory facility. Given the common garden rearing procedure, any differences in behaviour and colour pattern between the populations can be attributed to genetic differences (Houde 1988a). Virgin females for the experiments were obtained by separating them from males at approximately 6 weeks of age, and thus before sexual maturity. Virgin females were housed in separate sections of aquaria and were visually isolated from males. Experimental groups of males were composed of unrelated individuals that had not been reared together. The variation in orange coloration within the experimental groups was maximized by intentionally including males with both large and small amounts of orange coloration. To ensure normal behaviour, males used in the experiments were allowed to interact with other females for several days prior to experimental tests. All behavioural observations commenced within 1 h of the time when aquarium lights came on each morning. Female Mating Preferences To measure female mating preferences, we observed guppies in groups consisting of six Paria males and six Paria or Yarra females, using a standard behavioural assay in which we recorded the responses of females to each male s sigmoid courtship displays (Houde 1987, 1988a, b; Houde & Endler 1990; Endler & Houde 1995). We observed the responses of both Paria and Yarra females to each of five groups of Paria males in separate observation trials (total N=30 males). Groups of Paria and Yarra males and females were matched for age and size. Each group of males was tested with females from the two populations on successive days, in random order. This yielded a direct comparison of the responses of Paria and Yarra females to each male in the experiment. The responsiveness of females to the test males was measured using focal observations of each male. Individual males were identified by their unique colour patterns. The courtship displays of each male in turn were recorded during 5-min observation sessions. Male displays were recorded only if they were directed towards a particular female and if the display was not interrupted by another male (interruptions were rare, however). The order of observation of the males was randomized. Once all six males had been observed, a second round of 5-min observation sessions was conducted, for a total of 10 min of observation on each male. For each male display, a female sexual response was scored if the female stopped her current activity, oriented towards the male and glided (sensu Liley 1966; see also Houde 1987) unambiguously towards him. A male s attractiveness was then measured by the fraction of his displays that resulted in such a female response. The effect of variation in phenotypic characters such as colour pattern elements on attractiveness can then be analysed to determine the overall pattern of preference of females in a population. Houde (1988b) found that this measure of attractiveness predicts mating success under laboratory conditions. Previous work with this measure of attractiveness (Houde 1987, 1988a) has shown that it is normally distributed and can be statistically analysed without transformation. Our method of assaying female preferences using groups of males and females does not eliminate the possibility of male male interactions, but their effects were minimized by eliminating interrupted displays from the data, by using test males that had not been reared together and by using large test aquaria with 1:1 sex ratios. Although male male interactions can affect mating success under some experimental conditions (Kodric- Brown 1992, 1993), male male interactions and male behaviour in general appear to have little effect on attractiveness and mating success as measured under experimental conditions similar to ours (Houde 1987, 1988b). Male Colour Patterns We measured the extent of orange coloration in the colour patterns of the experimental males by recording both sides of each male on videotape, capturing the images onto computer disk, and using an image analysis program to calculate the relative area of orange spots. Males were anaesthetized using MS-222 (0.04 g tricaine methanesulfonic acid dissolved in 150 ml of water). The relative orange area was calculated as the total area of all orange spots (including those on the tail) divided by the total body area of the fish in side view (excluding fins), averaged between the right and left sides. The tails of the guppies were not always fully extended in the video images, so we did not include them in the body

4 346 Animal Behaviour, 53, 2 area measurements. Because previous studies (e.g. Houde & Endler 1990) included tail area as part of body area, we adjusted the data by multiplying body area by 1.25 (the average ratio of body-plustail area to body area from measurements of Paria guppies), providing a standardized body area for the calculation. We measured the extent of orange in all Paria males involved in the mating preference tests and also in a sample of Yarra males of similar age to document the difference in mean orange area. The orange area of test males ranged from 0.05 (5%) to 0.28 (28%) orange. The most orange and least orange males within a test group differed in orange area by a minimum of 0.12 and a maximum of Data Analysis Based on results of previous studies, (e.g. Houde 1987), we predicted that the responsiveness of Paria females to Paria males would depend strongly on orange area of the males. We further predicted that, in tests with the same males, the sexual responsiveness of Yarra females would depend less strongly on orange or would be independent of orange coloration. Our analysis is similar to that used by Houde (1988a). We examined the effect of extent of orange coloration on male attractiveness by calculating the linear regression slope with fraction responses to displays as the dependent variable and orange area as independent variable. A significant positive slope indicates a preference for orange coloration. The fraction of responses by Paria and Yarra females to each test male can be directly compared. Therefore, we tested the hypothesis that there is a difference in degree of preference between them by calculating the slope of the linear regression with the difference in fraction of responses of Paria versus Yarra females as the dependent variable. This method of evaluating the paired data is analogous to a paired sample t-test for means. We also compared the two independent regression slopes, using an analysis of covariance in which a significant population by orange area interaction term would indicate a difference in slopes and thus a difference in the preferences of Paria and Yarra females. Strictly speaking, the potential for male male interactions (Kodric-Brown 1992, 1993) and female copying (Dugatkin 1992; Dugatkin & Godin 1992) in our experimental tests may violate the assumption of independence necessary for the linear regression analyses we performed. The effects of male male interactions were probably minimal, however, as argued above, and previous studies have demonstrated the robustness of regression analyses for similar data (Houde 1987, 1988a; Houde & Endler 1990; Endler & Houde 1995). RESULTS Yarra males showed significantly less orange in their colour patterns than did Paria males (Yarra orange area: X SD= , N=30; Paria orange area: , N=30; significant difference: t 58 =4.9, P<0.001). In addition to the difference in area of orange coloration, the orange spots of Yarra males appear paler and yellower than those of Paria males. These differences are comparable to the differences between Paria and Aripo guppies in a previous study in which differences in preference were documented (Houde 1988a). The test males (all from the Paria population) displayed somewhat less frequently to Yarra females than to Paria females (Fig. 1a; paired t 29 =2.25, P=0.032). The mean fraction of male displays eliciting a response was similar for Yarra and Paria females, however (Fig. 1b; paired t 29 =0.70, P=0.49). There was a significant negative correlation between display rate and orange area when males were displaying to Paria females (r= 0.43, P=0.02, N=30), but not when males were displaying to Yarra females (r=0.10, P=0.61, N=30). Both Yarra and Paria females showed a significant preference for more orange males (Fig. 2; Paria: F 1,28 =16.55, P<0.001, R 2 =0.37; Yarra: F 1,28 =9.20, P=0.005, R 2 =0.25). The slopes of the regressions of fraction female response against male orange area were similar in magnitude for Paria and Yarra females (non-significant interaction of population and orange area in analysis of covariance: F 1,56 =0.14, P=0.70). Moreover, there was no significant relationship between the difference in Paria and Yarra females fraction responses to the same males and male orange area (linear regression: F 1,28 =0.11, P=0.74). Overall, these results indicate that there was no difference in the degree of preference for more orange males by Paria and Yarra females.

5 Houde & Hankes: Guppy mating preference mismatch (a) 1.00 (a) Male display rate Fraction female responses (b) Paria Paria Females DISCUSSION Yarra Yarra Figure 1. (a) Mean SE male display rates of Paria males courting Paria and Yarra females (displays per 10 min). (b) Mean fraction of male displays eliciting a female response in observations with Paria and Yarra females (displays per 10 min). Our results showed a mismatch between the expression of female preferences and the expression of orange coloration in Yarra guppies. Our initial prediction was that difference in the expression of orange coloration between the Paria and Yarra guppy populations should be matched by a corresponding difference in the mating preferences of females. Instead, we found that both Paria and Yarra females showed significant, but similar, preferences for more orange males. The sample sizes used should have been adequate to detect differences in preferences similar to those documented in other studies (e.g. Houde 1988a). In addition to showing similar preferences for individual males based on orange coloration, Paria and Yarra females were similar in overall responsiveness to male displays. Nevertheless, the males courted the Paria females slightly more Paria female preference Yarra female preference (b) Male orange area Figure 2. Effect of relative area of orange coloration on the fraction of male displays eliciting sexual responses from (a) Paria females and (b) Yarra females. Leastsquares regression lines: Y= X (Paria), and Y= X (Yarra). frequently than they did the Yarra females. This difference in courtship rate might represent reluctance of Paria males to court females from a different population, or it could reflect differences in behaviour of the females. Yarra guppies are notably more responsive to attempts to capture them and generally seem more skittish than Paria guppies. A greater rate of movement by Yarra females might reduce the frequency of opportunities for display by males. Males with greater orange area did not owe their attractiveness to a higher rate of courtship relative to males with a smaller orange area. Indeed, orange area was negatively correlated with courtship rate when

6 348 Animal Behaviour, 53, 2 males were courting Paria females, but was uncorrelated with courtship rate with Yarra females. The negative correlation is consistent with a previous observation (Houde 1988b) that attractive males have lower rates of courtship, which may also reflect an influence of female behaviour on male courtship behaviour. It is not clear why the relationship of orange area and male courtship rate differed for Paria and Yarra females, but again, subtle differences in the behaviour of Yarra females may have contributed. Despite the differences in male behaviour when courting Paria and Yarra females, the similar pattern of mating preferences in the two populations is clear. Our initial prediction of parallel variation between female preferences and male colour patterns was based on theoretical expectations (e.g. Lande 1981) and on empirical findings from other guppy populations (Houde 1988a; Houde & Endler 1990; Endler & Houde 1995). Theory predicts that colour patterns should evolve to match levels of preference in populations and also that preferences may undergo correlated responses to selection on colour patterns. Both of these arguments are based on the assumption that females mate non-randomly, with males having phenotypes corresponding to their preference. If genetic variation is present in both colour patterns and female preferences, then this non-random mating can result in evolutionary change in the male trait and also in establishment of genetic correlation of male colour patterns with female mating preferences. Empirically, our prediction of a correspondence between female preferences and male coloration seemed warranted, because colour patterns and mating preferences seemed to vary in parallel in other populations of guppies (Houde 1988a; Houde & Endler 1990; Endler & Houde 1995), and because artificial selection experiments provided some evidence for a genetic correlation between the two traits (Houde 1994). On the other hand, a mismatch similar to that documented here has been found in other studies. Females show a preference for the chuck component of the male call in the frogs Physalaemus pustulosus and P. coloradorum, but the chuck is produced only by P. pustulosus males (Ryan et al. 1990; Ryan & Keddy-Hector 1992). Females from both platyfish, Xiphophorus maculatus, and swordtail, X. helleri, species show a preference for male tails with swords, but the sword is present only in swordtails (Basolo 1990a, b). Basolo (1995) has documented a similar female preference for a sword in Priapella, the sister genus of Xiphophorus, in which swords are not expressed. As in the guppies, Physalaemus frogs and Priapella and Xiphophorus fishes all show a mismatch between female mating preferences and male secondary sexual traits, suggesting that the evolution of these two traits does not always proceed in parallel. The Physalaemus, Xiphophorus and Priapella cases provide evidence that female mating preferences may have their origins in pre-existing sensory biases that predate the evolution of the preferred male traits. This inference is based on detailed phylogenetic information about the taxa involved. For example, Basolo s (1995) results imply that a preference for swords may have originated as a sensory bias in a common ancestor of swordtails, platyfishes and Priapella, and that the sword trait itself evolved as a later response to this preference in some but not all species of this clade. Our data do not permit us to make a similar argument for the evolution of mate preferences in guppies, however, because not enough is known about the phylogeny of guppy populations. Although a preference for orange coloration could have been present in a common ancestor of the Paria and Yarra populations, data from allozyme studies (Magurran et al. 1995) indicate that the Paria population is more closely related to populations in which the orange preference is not expressed than it is to the Yarra population. The evolutionary history of mating preferences in guppies is therefore likely to be more complicated than the relatively straightforward pattern seen in Physalaemus and Xiphophorus Priapella. Further details of the phylogeography of guppy populations in conjunction with data on expression of female mating preferences and male coloration are needed to determine the evolutionary history of sexual selection in guppies. Nevertheless, our major conclusion from the present study remains that not all guppy populations show a correspondence between female mating preferences and male coloration, despite a general tendency for these characters to vary in parallel in this species. The theoretical basis for our initial prediction that mating preferences should match the expression of male colour patterns is compelling, and appears to have some validity in a number of guppy populations. How, then, can we explain the observed mismatches seen in guppies and other species? As noted above, our prediction was based

7 Houde & Hankes: Guppy mating preference mismatch 349 on at least three major assumptions, each of which might not be met under certain conditions. First, the colour pattern of Yarra males may not have responded to sexual selection for increased orange imposed by female mating preferences because of a lack of heritable variation in colour patterns. Given the extremely high levels of heritable variation for colour patterns seen in some guppy populations (Houde 1988b, 1992), it would be very surprising to find that heritability of orange area in the Yarra population was low enough to constrain evolutionary response to sexual selection. Considerable phenotypic variation in colour pattern is present in this population (see Results), and heritability of orange area is currently under investigation. Second, the Yarra and Paria populations may not have been diverging for as long as indicated by allozyme comparisons (Magurran et al. 1995), and the mismatch could reflect a non-equilibrium situation in the Yarra population. Magurran et al. (1995) noted that divergence time could be overestimated if a founder effect contributed to the genetic differentiation between Yarra and other populations. For example, the Yarra population might have been founded relatively recently by immigrants from a low-predation population. Direct selection by predators in the Yarra river could have produced a relatively rapid evolutionary response in male colour patterns with a slower correlated response (Fisher 1930; Lande 1981) to selection in female mating preferences. Therefore, the correlated evolution of mating preferences may have lagged behind and may not yet match the expression of colour patterns. Additional population genetic and quantitative genetic data from the Yarra population would be needed to assess this possibility. Finally, Yarra females in the wild may not be mating with males corresponding to the preferences shown in the laboratory. When females are not able to mate with preferred males, there are two evolutionary consequences. First, sexual selection will not lead to evolution of male traits that correspond to the female preference. Second, a genetic correlation between the preference and the male trait will not be established, and correlated shifts in female preferences and male secondary sexual traits will not occur as predicted by models (e.g. Fisher 1930; Lande 1981). We suggest, therefore, that there may be a behavioural difference between the Paria and Yarra populations that affects the ability of Yarra females to mate with preferred males. What might constrain the ability of females to exercise mate choice? One possibility is that there is plasticity in the expression of mating preferences, so that the behavioural preferences shown by females under laboratory conditions are not always expressed under field conditions. The presence of large predators in the Yarra river, for example, might reduce the discrimination of females there. Godin & Briggs (1996) and Gong & Gibson (1996) have documented reductions in female selectivity in the presence of a predator. Another possibility is that social interactions within and between the sexes may affect the ability of female guppies to choose mates, and that the nature of social interactions may differ between populations, in particular, in response to differences in predation regime. Populations under different predation regimes differ in the rate of sneak copulation attempts by males (Magurran & Novack 1991; Magurran & Seghers 1994; Godin 1995), and in the tendency of males to harass females and of females to avoid the attentions of males (Magurran & Novack 1991; Magurran & Seghers 1994). All of these behaviour patterns could affect the ability of females to exercise choice. Courting males are sometimes interrupted by other males, and copulations are sometimes even stolen by an intruding male (A. E. Houde & M. A. Hankes, personal observations). These kinds of male male interactions are rare in the laboratory, but might be more common under some natural conditions. Differences in density of fish, sex ratio or visibility of courting pairs to other individuals could all affect the rate of interference in courtship, which in turn could affect the likelihood of females mating with their preferred mates. More generally, the relative importance of male male interactions and female choice to the ability of males to obtain copulations could differ between populations (Houde 1988b; Kodric-Brown 1992, 1993). Finally, the tendency of females to copy the mate choice of other females (Dugatkin 1992; Dugatkin & Godin 1992) could affect the expression of mating preferences and patterns of male mating success. Any of these patterns of social interaction could differ between populations as a consequence of variation in predation regime or for other reasons. Such differences could account for an evolutionary mismatch in which female mating preferences

8 350 Animal Behaviour, 53, 2 have not led to the evolution of corresponding secondary sexual traits in males, as we have documented here. The potential ways in which female choice might be constrained and their effects on male mating success need to be investigated. Theoretical and empirical studies have made it clear that mating preferences can have predictable effects on the evolution of male secondary sexual traits. Our finding that the expression of male traits does not always match female mating preferences, and similar results from other studies, indicate that the relationship of mating preferences to the expression of male traits is not always a simple matter of cause and effect. ACKNOWLEDGMENTS We thank Rebecca Bordeau, Kirsten Findlay, Leslie Malmgren and Jonathan Weiland for assistance and discussion, and Joe Benz, Jean-Guy Godin, Michael McManus and an anonymous referee for comments on the manuscript. This study was supported by the Keck Foundation, a faculty research stipend from Lake Forest College, and NSF grant IBN to A.E.H. REFERENCES Basolo, A. 1990a. Female preference for male sword length in the green swordtail, Xiphophorus helleri (Pisces: Poeciliidae). Anim. Behav., 40, Basolo, A. 1990b. Female preference predates the evolution of the sword in swordtail fish. Science, 250, Basolo, A Phylogenetic evidence for the role of a pre-existing bias in sexual selection. Proc. R. Soc. Lond. Ser. B, 259, Breden, F. & Hornaday, K Test of indirect models of selection in the Trinidad guppy. Heredity, 73, Dugatkin, L. A Sexual selection and imitation: females copy the mate choice of others. Am. Nat., 139, Dugatkin, L. A. & Godin, J.-G. J Reversal of female mate choice by copying in the guppy. Proc. R. Soc. Lond. Ser. B, 249, Endler, J. A A predator s view of animal color patterns. Evol. Biol., 11, Endler, J. A Natural and sexual selection on color patterns in poeciliid fishes. Environ. Biol. Fishes, 9, Endler, J. A. & Houde, A. E Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution, 49, Fisher, R. A The Genetical Theory of Natural Selection. Oxford: Clarendon Press. Gilburn, A. & Day, T Evolution of female choice in seaweed flies: Fisherian and good genes mechanisms operate in different populations. Proc. R. Soc. Lond. Ser. B, 225, Godin, J.-G. J Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). Oecologia (Berl.), 103, Godin, J.-G. J. & Briggs, S. E Female mate choice under predation risk in the guppy. Anim. Behav., 51, Godin, J.-G. J. & Dugatkin, L. A Variability and repeatability of mating preference in the guppy. Anim. Behav., 49, Gong, A. & Gibson, R. M Reversal of a female preferences after visual exposure to a predator in the guppy, Poecilia reticulata. Anim. Behav., 52, Houde, A. E Mate choice based upon naturally occurring color pattern variation in a guppy population. Evolution, 41, Houde, A. E. 1988a. Genetic difference in female choice between two guppy populations. Anim. Behav., 36, Houde, A. E. 1988b. The effects of female choice and male male competition on the mating success of male guppies. Anim. Behav., 36, Houde, A. E Sex-linked heritability of a sexually selected character in a natural population of Poecilia reticulata (Pisces: Poeciliidae) (guppies). Heredity, 69, Houde, A. E Evolution by sexual selection: what can population comparisons tell us? Am. Nat., 141, Houde, A. E Effect of artificial selection on male colour patterns on mating preference of female guppies. Proc. R. Soc. Lond. Ser. B, 256, Houde, A. E. & Endler, J. A Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata. Science, 248, Kirkpatrick, M Sexual selection and the evolution of female choice. Evolution, 36, Kirkpatrick, M. & Ryan, M. J The evolution of mating preferences and the paradox of the lek. Nature, Lond., 350, Kodric-Brown, A Female preference and sexual selection for male coloration in the guppy. Behav. Ecol. Sociobiol., 17, Kodric-Brown, A Male dominance can enhance mating success in guppies. Anim. Behav., 44, Kodric-Brown, A Female choice of multiple male criteria in guppies: interacting effects of dominance, coloration and courtship. Behav. Ecol. Sociobiol., 32, Lande, R Models of speciation by sexual selection on polygenic characters. Proc. natn. Acad. Sci. U.S.A., 78, Liley, N. R Ethological isolating mechanisms in four species of poeciliid fishes. Behaviour Suppl., 13, Magurran, A. E. & Novack, M. A Another battle of the sexes: the consequences of sexual asymmetry in

9 Houde & Hankes: Guppy mating preference mismatch 351 mating cost and predation risk in the guppy, Poecilia reticulata. Proc. R. Soc. Lond. Ser. B, 246, Magurran, A. E. & Seghers, B. H Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour, 128, Magurran, A., Seghers, B., Shaw, P. & Carvalho, G Evolutionary basis of the behavioural diversity of the guppy, Poecilia reticulata, populations in Trinidad. Adv. Study. Behav., 24, Reznick, D. N., Rodd, F. H. & Cardenas, M Life history evolution in guppies (Poecilia reticulata: Poeciliidae). IV. Parallelism in life-history phenotypes. Am. Nat., 147, Ryan, M. J. & Keddy-Hector, A Directional patterns of female mate choice and the role of sensory biases. Am. Nat., 139, S4 S35. Ryan, M. J., Fox, J. H., Wilczynski, W. & Rand, A. S Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature, Lond., 343, Wilkinson, G. & Reillo, P Female choice response to artificial selection on an exaggerated male trait in a stalk eyed fly. Proc. R. Soc. Lond. Ser. B, 255, 1 6.

10 352 Animal Behaviour, 53, 2