Do male guppies distinguish virgin females from recently mated ones?

In some mating systems males should benefit from mating with virgin females because of their higher reproductive value. We determined experimentally whether and how males distinguish between virgin and recently mated females in the guppy, Poecilia reticulata, a promiscuous livebearer. In a free-swimming experiment, males showed flexible mating behaviour by adjusting their tactics according to the mating status of the female they encountered, virgin or mated. Males followed, nipped and copulated with virgins more than with mated females, but they performed more sneaky copulations with mated females, possibly because the latter were more reluctant to mate than virgin females. When, in another set of experiments, males received only the visual cues of both virgins and mated females they showed no preference for either, but when they were exposed only to the female olfactory cues, they associated considerably more with the smell of virgin females. These results suggest that male guppies assess female behavioural and olfactory cues to determine female virginity and then use different mating tactics depending on the female's status. It is possible that the changes in male mating behaviour increase male reproductive success.

Mating effort and female receptivity : how do male guppies decide when to invest in sex?

Males vary in the degree to which they invest in mating. Several factors can explain this variation, including differences in males’ individual condition and the fact that males allocate their energy depending on the context they face in each mating attempt. Particularly, female quality affects male reproductive success. Here, we studied whether male guppies (Poecilia reticulata) strategically allocated more mating effort, in terms of mating behaviour and male–male competition, when they were matched with a receptive (R) female than a non-receptive one. In accordance with our prediction, we found that males increased their mating behaviour when they were with a receptive female. Even though male guppies can inseminate non-receptive females, we only found high levels of courtship between males that were with a receptive female rather than a non-receptive one. Although there was little affect of female receptivity on male–male competition, we found that males chased and interrupted courtships more with receptive females than with non-receptive females regardless of odour. Finally, we also studied whether the sexual pheromone produced by receptive female guppies is a cue that males use in order to increase their mating effort. We found that males were more attracted to a female when they perceived the sexual pheromone, but only increased their mating and aggressive behaviours when females showed receptive behaviour. This strategic increase in mating effort could result in higher male reproductive success because mating attempts towards receptive females are likely to be less costly and males could have a greater probability of fertilisation.

Male mate-searching strategies and female cues: how do male guppies find receptive females?

Locating potential mates is critical to mating. We studied males’ association with females and mate-searching patterns in the guppy, Poecilia reticulata, a promiscuous live-bearer. In the field, we examined whether male guppies respond differently to a shoal of conspecific fish based on the members of the shoal. We found that more males were attracted to shoals that contained receptive females than to shoals of nonreceptive females or males. We also conducted laboratory experiments to investigate how males use olfactory cues of nonreceptive and receptive females to search for and associate with females. We gave males the option to associate with nonreceptive females when olfactory cues of receptive or nonreceptive females were present and absent, and when olfactory cues were presented alone. Males associated with females most strongly when both cues were presented simultaneously, but when cues were presented separately males’ association with females differed with respect to the olfactory cues that were added. Males associated with females equally with visual and olfactory cues presented separately when the odour cues were from receptive females. However, when the odour cues were from nonreceptive females, males associated with females less with olfactory than visual cues. Searching activity increased when males had access only to olfactory cues. Taken together these results suggest that olfactory cues influence males’ association with females and searching behaviour, and these changes in behaviour are likely to maximize a male’s opportunity to encounter receptive females.

Stress-induced peak (but not resting) metabolism correlates with mating display intensity in male guppies

Recent empirical and conceptual papers have highlighted the potential for metabolism to act as a proximate mechanism for behavior that could explain animal personality (consistency over time). Under this hypothesis, individuals with consistently high levels of behavioral activity should also have high resting metabolic rate (RMR) as it can reflect capacity to process food and generate energy. We tested for the predicted positive covariance between RMR and three behaviors that differ in energy demands in 30 male guppies, using multivariate mixed models; we repeatedly measured their activity (10 times each), courtship displays (nine times), voracity (10 times), and metabolism (four-times). Resting metabolic rate (measured overnight in respirometry trials) did not consistently differ among males, whereas initial peak metabolism measured during those same trials (R = 0.42), and all behaviors were repeatable (R = 0.33–0.51). RMR declined over time suggesting habituation to the protocol, whereas peak metabolism did not. Initial peak metabolism was negatively correlated with courtship display intensity, and voracity was positively correlated with activity, but all other among-individual correlations were not significant. We conclude that RMR does not provide a proximate explanation for consistent individual differences in behavior in male guppies, and therefore the potential for independent evolution of these physiological and behavioral traits seems possible. Finally, we identify peak metabolism as a potential measure of the stress response to confinement, which highlights the value of considering various aspects of metabolic rates recording during respirometry trials.

Male courtship decisions are influenced by light environment and female receptivity.

The appearance of animal colour signals depends jointly upon the ambient light spectrum and the signal's reflectance spectra. Light environment heterogeneity might, therefore, allow individuals to enhance their signal by signalling in an environment that increases signal efficacy. We tested this hypothesis by providing male guppies (Poecilia reticulata), a choice of three light environments in which to display their colour signal to females: green, lilac, and clear. We paired males with both receptive and non-receptive females to test whether female response might affect male behavioural decisions. Males preferred the clear environment in all trials and this environment also resulted in males having the highest average visual contrast. Sexual behaviour was influenced by complex interactions between female receptivity, light environment, and male colour pattern contrast. Males spent significantly more time in the environment in which their colour signal had the highest contrast, but only when paired with receptive females. Significant interactions between light environment and individual male colour components were also seen only in receptive trials. Our results suggest that males use light environment to enhance their colour pattern, but only in the presence of receptive females.

Ultraviolet vision and mate choice in the guppy (Poecilia reticulata)

Ultraviolet (UV) vision is well documented for many species of vertebrates. UV cues are known to be used in foraging, navigation and in mate choice. We conducted a series of behavioral experiments to investigate the role of UV perception in mate choice in both female and male guppies (Poecilia reticulata). In our experiments the visual appearance of potential mates was manipulated using either UV transmitting (UV+) or UV blocking (UV-) filters. Female guppies significantly preferred UV+ males. Male guppies tended to prefer UV- females, but their preferences were marginally nonsignificant. Further experiments investigating the role of luminance, indicate that UV wavelengths are probably being used for color discrimination rather than for detecting differences in brightness. These experiments raise the possibility that UV is used in mate assessment in different ways by male and female guppies. This may reflect the different strategies that the two sexes have in order to maximize reproductive success. To our knowledge, these are the first data showing that UV is used by any fish species in mate selection.

Geographic variation in allometry in the guppy (Poecilia reticulata)

Variation in static allometry, the power relationship between character size and body size among individuals at similar developmental stages, remains poorly understood. We tested whether predation or other ecological factors could affect static allometry by comparing the allometry between the caudal fin length and the body length in adult male guppies (Poecilia reticulata) among populations from different geographical areas, exposed to different predation pressures. Neither the allometric slopes nor the allometric elevations (intercept at constant slope) changed with predation pressure. However, populations from the Northern Range in Trinidad showed allometry with similar slopes but lower intercepts than populations from the Caroni and the Oropouche drainages. Because most of these populations are exposed to predation by the prawn Macrobrachium crenulatum, we speculated that the specific selection pressures exerted by this predator generated this change in relative caudal fin size, although effects of other environmental factors could not be ruled out. This study further suggests that the allometric elevation is more variable than the allometric slope.

Sex-dependent selection differentially shapes genetic variation on and off the guppy Y chromosome

Because selection is often sex-dependent, alleles can have positive effects on fitness in one sex and negative effects in the other, resulting in intralocus sexual conflict. Evolutionary theory predicts that intralocus sexual conflict can drive the evolution of sex limitation, sex-linkage, and sex chromosome differentiation. However, evidence that sex-dependent selection results in sex-linkage is limited. Here, we formally partition the contribution of Y-linked and non-Y-linked quantitative genetic variation in coloration, tail, and body size of male guppies (Poecilia reticulata)—traits previously implicated as sexually antagonistic. We show that these traits are strongly genetically correlated, both on and off the Y chromosome, but that these correlations differ in sign and magnitude between both parts of the genome. As predicted, variation in attractiveness was found to be associated with the Y-linked, rather than with the non-Y-linked component of genetic variation in male ornamentation. These findings show how the evolution of Y-linkage may be able to resolve sexual conflict. More generally, they provide unique insight into how sex-specific selection has the potential to differentially shape the genetic architecture of fitness traits across different parts of the genome.

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within-population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.

Environmental variation and the maintenance of polymorphism : the effect of ambient light spectrum on mating behaviour and sexual selection in guppies

The intensity of sexual selection is influenced by environmental conditions because these conditions influence signal propagation and the risks of the signal being exploited by predators and parasites. We explore the possibility that spatial or temporal heterogeneity in environmental signalling conditions (in this case light spectrum) may induce fluctuating sexual selection on male behaviour and ornamentation in guppies. We used shade cloth and filters to experimentally manipulate light spectrum, mimicking conditions found naturally: early morning/late afternoon light (SC treatment), midday forest shade (F89 filter treatment) and midday woodland shade (F55 filter treatment). Females were more responsive to male courtship and males were less likely to attempt sneak copulations under F55 light than the other two treatments. By contrast, male display rate was not influenced by treatment. Females tended to prefer the same males under SC and F55 light, but attractiveness in these treatments was unrelated to attractiveness under F89 light. There were similarities among treatments in the traits that females preferred: females preferred males with larger areas of orange in all three treatments. There were, however, also some differences, including preference for larger males under F89 light and for smaller males under the other treatments. Overall, the influence of ambient light spectrum on the relative importance of mate choice and male sneak copulation may have important implications for the mode and strength of sexual selection in different environments. The findings on attractiveness and preference functions, however, suggest that light spectrum only weakly affects the direction of sexual selection by female choice.

Predicting the direction of ornament evolution in Trinidadian guppies (Poecilia reticulata)

Sexual selection is thought to be opposed by natural selection such that ornamental traits express a balance between these two antagonistic influences. Phenotypic variation among populations may indicate local shifts in this balance, or that different stable ‘solutions’ are possible, but testing these alternatives presents a major challenge. In the guppy (Poecilia reticulata), a small freshwater fish with male-limited ornamental coloration, these issues can be addressed by transplanting fish among sites of varying predation pressure, thus effectively manipulating the strength and nature of natural selection. Here, we contrast the evolutionary outcome of two such introductions conducted in the Trinidadian El Cedro and Aripo Rivers. We use sophisticated colour appraisal methods that account for full spectrum colour variation and which incorporate the very latest visual sensitivity data for guppies and their predators. Our data indicate that ornamentation evolved along different trajectories: whereas Aripo males evolved more numerous and/or larger orange, black and iridescent markings, El Cedro males only evolved more extensive and brighter iridescence. Examination of the El Cedro experiment also revealed little or no ornamental evolution at the control site over 29 years, which contrasts markedly with the rapid (approx. 2–3 years) changes reported for introduction populations. Finally, whole colour-pattern analysis suggested that the greatest visual difference between El Cedro introduction and control fish would be perceived by the two most salient viewers: guppies and the putatively dangerous predator Crenicichla alta. We discuss whether and how these evolutionary trajectories may result from founder effects, population-specific mate preferences and/or sensory drive.

Genetic architecture of sexually selected traits - lessons from guppies

I discuss a number of experiments designed to explore the genetic basis of sexual ornamentation and associated life history traits in guppies. This system is unusual because of the large Y-linked contribution to ornamentation and male fitness, and because the Y-chromosome is implicated in inbreeding depression. I discuss the implications of intralocus sexual conflict for the evolution of sex-linkage in guppies and the potential for such a process to drive the evolutionary erosion of Y-chromosomes.