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.

The variable colours of the fiddler crab Uca vomeris and their relation to background and predation

Colour changes in fiddler crabs have long been noted, but a functional interpretation is still lacking. Here we report that neighbouring populations of Uca vomeris in Australia exhibit different degrees of carapace colours, which range from dull mottled to brilliant blue and white. We determined the spectral characteristics of the mud substratum and of the carapace colours of U. vomeris and found that the mottled colours of crabs are cryptic against this background, while display colours provide strong colour contrast for both birds and crabs, but luminance contrast only for a crab visual system. We tested whether crab populations may become cryptic under the influence of bird predation by counting birds overflying or feeding on differently coloured colonies. Colonies with cryptically coloured crabs indeed experience a much higher level of bird presence, compared to colourful colonies. We show in addition that colourful crab individuals subjected to dummy bird predation do change their body colouration over a matter of days. The crabs thus appear to modify their social signalling system depending on their assessment of predation risk.

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.

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.

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.

The expression of pre- and postcopulatory sexually selected traits reflects levels of dietary stress in guppies

Environmental and ecological conditions can shape the evolution of life history traits in many animals. Among such factors, food or nutrition availability can play an important evolutionary role in moderating an animal's life history traits, particularly sexually selected traits. Here, we test whether diet quantity and/or composition in the form of omega-3 long chain polyunsaturated fatty acids (here termed 'n3LC') influence the expression of pre- and postcopulatory traits in the guppy (Poecilia reticulata), a livebearing poeciliid fish. We assigned males haphazardly to one of two experimental diets supplemented with n3LC, and each of these diet treatments was further divided into two diet 'quantity' treatments. Our experimental design therefore explored the main and interacting effects of two factors (n3LC content and diet quantity) on the expression of precopulatory (sexual behaviour and sexual ornamentation, including the size, number and spectral properties of colour spots) and postcopulatory (the velocity, viability, number and length of sperm) sexually selected traits. Our study revealed that diet quantity had significant effects on most of the pre- and postcopulatory traits, while n3LC manipulation had a significant effect on sperm traits and in particular on sperm viability. Our analyses also revealed interacting effects of diet quantity and n3LC levels on courtship displays, and the area of orange and iridescent colour spots in the males' colour patterns. We also confirmed that our dietary manipulations of n3LC resulted in the differential uptake of n3LC in body and testes tissues in the different n3LC groups. This study reveals the effects of diet quantity and n3LC on behavioural, ornamental and ejaculate traits in P. reticulata and underscores the likely role that diet plays in maintaining the high variability in these condition-dependent sexual traits.

Grass-dominated stream sites exhibit low fish species diversity and dominance by guppies: an assessment of two tropical pasture river basins

Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)

Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams.

Evolution has been shown to be a critical determinant of ecological processes in some systems, but its importance relative to traditional ecological effects is not well known. In addition, almost nothing is known about the role of coevolution in shaping ecosystem function. Here, we experimentally evaluated the relative effects of species invasion (a traditional ecological effect), evolution and coevolution on ecosystem processes in Trinidadian streams. We manipulated the presence and population-of-origin of two common fish species, the guppy (Poecilia reticulata) and the killifish (Rivulus hartii). We measured epilithic algal biomass and accrual, aquatic invertebrate biomass, and detrital decomposition. Our results show that, for some ecosystem responses, the effects of evolution and coevolution were larger than the effects of species invasion. Guppy evolution in response to alternative predation regimes significantly influenced algal biomass and accrual rates. Guppies from a high-predation site caused an increase in algae relative to guppies from a low-predation site; algae effects were probably shaped by observed divergence in rates of nutrient excretion and algae consumption. Rivulus-guppy coevolution significantly influenced the biomass of aquatic invertebrates. Locally coevolved populations reduced invertebrate biomass relative to non-coevolved populations. These results challenge the general assumption that intraspecific diversity is a less critical determinant of ecosystem function than is interspecific diversity. Given existing evidence for contemporary evolution in these fish species, our findings suggest considerable potential for eco-evolutionary feedbacks to operate as populations adapt to natural or anthropogenic perturbations.