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.

Dynamic social networks in guppies (Poecilia reticulata)

One of the main challenges in the study of social networks in vertebrates is to close the gap between group patterns and dynamics. Usually scan samples or transect data are recorded to provide information about social patterns of animals, but these techniques themselves do not shed much light on the underlying dynamics of such groups. Here we show an approach which captures the fission-fusion dynamics of a fish population in the wild and demonstrates how the gap between pattern and dynamics may be closed. Our analysis revealed that guppies have complex association patterns that are characterised by close strong connections between individuals of similar behavioural type. Intriguingly, the preference for particular social partners is not expressed in the length of associations but in their frequency. Finally, we show that the observed association preferences could have important consequences for transmission processes in animal social networks, thus moving the emphasis of network research from descriptive mechanistic studies to functional and predictive ones.

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.

The effects of familiarity and group size on mating preferences in the guppy, Poecilia reticulata

In recent years, it has become evident that frequency dependence in the attractiveness of a particular phenotype to mates can contribute to the maintenance of polymorphism. However, these preferences for rare and unfamiliar male phenotypes have only been demonstrated in small, controlled experiments. Here, we tested the preference for unfamiliar mates in groups of six to 96 individuals over 13 days, in the guppy (Poecilia reticulata). We observed individual behaviour in situ to test whether fish discriminate two unfamiliar individuals among many familiar ones. We found that unfamiliar males and females were preferred over the familiar fishes in all groups and that this effect decayed over time. Increasing group sizes and levels of sexual activity did not hamper the preference for unfamiliar mates, providing further support for the role of frequency dependent mate choice in the maintenance of trait polymorphism in natural populations.

Testing the interactive effects of carotenoids and polyunsaturated fatty acids on ejaculate traits in the guppy Poecilia reticulata (Pisces: Poeciliidae)

Using the polyandrous livebearing guppy Poecilia reticulata, this study revealed no main effects of carotenoids in the diet on ejaculate traits, but significant main effects of polyunsaturated fatty acids (PUFAs) on sperm viability and weak but significant interacting effects of both nutrients on sperm length. Collectively, these findings not only add evidence that PUFAs are critical determinants of sperm quality, but also provide tentative evidence that for some traits these effects may be moderated by carotenoid intake.

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.

Experimental reduction in dietary omega-3 polyunsaturated fatty acids depresses sperm competitiveness

 The health benefits of diets containing rich sources of long-chain omega-3 polyunsaturated fatty acids (n-3 LC-PUFA) are well documented and include reductions in the risk of several diseases typical of Western societies. The dietary intake of n-3 LC-PUFA has also been linked to fertility, and there is abundant evidence that a range of ejaculate traits linked to fertility in humans, livestock and other animals depend on an adequate intake of n-3 LC-PUFA from dietary sources. However, relatively few studies have explored how n-3 LC-PUFA influence reproductive fitness, particularly in the context of sexual selection. Here, we show that experimental reduction in the level of n-3 LC-PUFA in the diet of guppies (Poecilia reticulata) depresses a male’s share of paternity when sperm compete for fertilization, confirming that the currently observed trend for reduced n-3 LC-PUFA in western diets has important implications for individual reproductive fitness.

Variable environmental effects on a multicomponent sexually selected trait

Multicomponent signals are made up of interacting elements that generate a functional signaling unit. The interactions between signal components and their effects on individual fitness are not well understood, and the effect of environment is even less so. It is usually assumed that color patterns appear the same in all light environments and that the effects of each color are additive. Using guppies, Poecilia reticulata, we investigated the effect of water color on the interactions between components of sexually selected male coloration. Through behavioral mate choice trials in four different water colors, we estimated the attractiveness of male color patterns, using multivariate fitness estimates and overall signal contrast. Our results show that females exhibit preferences that favor groups of colors rather than individual colors independently and that each environment favors different color combinations. We found that these effects are consistent with female guppies selecting entire color patterns on the basis of overall visual contrast. This suggests that both individuals and populations inhabiting different light environments will be subject to divergent, multivariate selection. Although the appearance of color patterns changes with light environment, achromatic components change little, suggesting that these could function in species recognition or other aspects of communication that must work across environments. Consequently, we predict different phylogenetic patterns between chromatic and achromatic signals within the same clades.

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.

Towards powerful experimental and statistical approaches to study intraindividual variability in labile traits

There is a long-standing interest in behavioural ecology, exploring the causes and correlates of consistent individual differences in mean behavioural traits ('personality') and the response to the environment ('plasticity'). Recently, it has been observed that individuals also consistently differ in their residual intraindividual variability (rIIV). This variation will probably have broad biological and methodological implications to the study of trait variation in labile traits, such as behaviour and physiology, though we currently need studies to quantify variation in rIIV, using more standardized and powerful methodology. Focusing on activity rates in guppies (Poecilia reticulata), we provide a model example, from sampling design to data analysis, in how to quantify rIIV in labile traits. Building on the doubly hierarchical generalized linear model recently used to quantify individual differences in rIIV, we extend the model to evaluate the covariance between individual mean values and their rIIV. After accounting for time-related change in behaviour, our guppies substantially differed in rIIV, and it was the active individuals that tended to be more consistent (lower rIIV). We provide annotated data analysis code to implement these complex models, and discuss how to further generalize the model to evaluate covariances with other aspects of phenotypic variation.

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.

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.

Inbreeding level does not induce female discrimination between sibs and unrelated males in guppies

Significant empirical evidence has demonstrated the importance of discriminative mate choice as a mechanism to avoid inbreeding. Incestuous mating can be avoided by recognition of kin. The guppy, Poecilia reticulata, is a livebearer with a polygamous mating system and active female choice. Despite potential inbreeding costs in the guppy, Viken et al. (Ethology 112:716–723, 2006) and Pitcher et al. (Genetica 134:137–146, 2008) have found that females do not discriminate between sibs and unrelated males. However, populations experiencing different inbreeding histories can have different levels of inbreeding avoidance, and it is possible that the lack of inbreeding avoidance observed in guppies is a consequence of using outbred fish only. Here we tested the preference of female guppies with different inbreeding coefficients, for olfactory cues of males that were either unrelated but had the same inbreeding coefficient, or were related (i.e. brother) with the same inbreeding coefficient. We found no evidence that female guppies preferred unrelated males with the same inbreeding coefficient. Moreover, inbreeding level did not influence female preference for unrelated males, suggesting that inbreeding history in a population has no influence on female discrimination of unrelated males in guppies.