Anne E. Houde

Geographic variation in female preferences for male traits in Poecilia reticulata

We examined the preferences of female guppies (Poecilia reticulata) from 11 localities in Trinidad with respect to male color‐pattern elements, body shape and size, and overall color and brightness contrast. Females are on average more attracted to males from their own population than from alien populations, and populations appear to vary in the criteria used in female choice. Multiple‐regression analysis suggests that mate‐preference criteria vary among localities in intensity, sign, and the number of traits used. Although preference estimators and color‐pattern parameters are unique to each population, only orange, black, and color contrast showed a correlation between degree of male trait and degree of preference for that trait. There is a clear effect of water color and a possible effect of predation intensity. The results are discussed in light of various models of sexual selection and the early stages of speciation.

Correlated Evolution of Female Mating Preferences and Male Color Patterns in the Guppy Poecilia reticulata.

Sexual selection may explain why secondary sexual traits of males are so strongly developed in some species that they seem maladaptive. Female mate choice appears to favor the evolution of conspicuous color patterns in male guppies (Poecilia reticulata) from Trinidad, but color patterns vary strikingly among populations. According to most theory, correlated evolution of female mating preferences and preferred male traits within populations could promote this kind of divergence between populations. But mating preferences could also constrain the evolution of male traits. In some guppy populations, females discriminate among males based on variation in the extent of orange pigment in male color patterns, and populations differ significantly in the degree offemale preferences for orange area. In a comparison ofseven populations, the degree offemale preference based on orange is correlated with the population average orange area. Thus male traits and female preferences appear to be evolving in parallel.

Frequency-dependent survival in natural guppy populations

The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology. Of the processes capable of maintaining variation, negative frequency-dependent selection (where rare types are favoured by selection) is the most powerful, at least in theory; however, few experimental studies have confirmed that this process operates in nature. One of the most extreme, unexplained genetic polymorphisms is seen in the colour patterns of male guppies (Poecilia reticulata). Here we manipulated the frequencies of males with different colour patterns in three natural populations to estimate survival rates, and found that rare phenotypes had a highly significant survival advantage compared to common phenotypes. Evidence from humans and other species implicates frequency-dependent survival in the maintenance of molecular, morphological and health-related polymorphisms. As a controlled manipulation in nature, this study provides unequivocal support for frequency-dependent survival—an evolutionary process capable of maintaining extreme polymorphism.

Sex-linked heritability of a sexually selected character in a natural population of Poecilia reticulata (Pisces: Poeciliidae) (guppies)

The relative extent of orange-pigmented spots in the colour patterns of male guppies, Poecilia reticulata, has previously been shown to be a basis for female choice. Parent–offspring and half-sib breeding experiments and selection experiments were conducted to determine if heritability of this character is maintained in the face of apparent sexual selection. The results demonstrate strong heritability of orange area. High father–son regression slopes, strong response to selection and a relatively small dam component of variance indicate that this character has Y-linked inheritance. This result for a quantitative character is in agreement with earlier work showing Y-linked inheritance of particular colour pattern elements in guppies. The high heritability of orange area suggests that this trait is probably not an indicator of fitness variation as postulated by some ‘good genes’ models for the evolution of female mate choice but that it does have the potential for further evolutionary change and elaboration.

Possible role of female discrimination against 'redundant' males in the evolution of colour pattern polymorphism in guppies

Multiple paternity of offspring can result from active preferences on the part of females or sexual harassment by males. We examined sexual responses of female guppies to a previous mate versus a novel male (experiment 1) or to a male with a colour pattern similar to that of the previous mate versus a novel male (experiment 2). Females showed significantly more sexual responses to courtship by novel males than to previous mates in experiment 1 or to males that resembled previous mates in experiment 2. These results suggest that females discriminate actively against previous mates, and extend this discrimination to males with similar colour patterns to previous mates. This could lead to negative frequency–dependent sexual selection against common colour patterns (a ‘redundant male effect’), which could contribute to the maintenance of the extraordinarily high levels of genetic polymorphism in guppy colour patterns.

Genetic difference in female choice between two guppy populations

Abstract The pattern of mating preferences of female guppies, Poecilia reticulata, differs genetically between two Trinidadian populations. Males from the Aripo and Paria rivers of Trinidad differ in the extent and intensity of orange pigment in their colour patterns. The relative area of orange in Paria colour patterns was nearly twice that in Aripo colour patterns. To test the hypothesis that a difference in female mating preferences could have contributed to the difference in colour patterns, patterns of female choice between laboratory-reared Paria and Aripo females were compared. The frequency of sexual responses to male courtship displays was used to measure the average preference of females for individual males. Paria females discriminated significantly between Paria males based upon differences in the extent of orange in the colour pattern. Aripo females showed no evidence of discrimination between Paria males, and thus differed significantly from Paria females in choice behaviour. Neither group of females discriminated between Aripo males. These results are evidence that female choice behaviour can vary genetically within a species and suggest that differences in preferences may have contributed to divergence in colour patterns among guppy populations.

The effects of female choice and male-male competition on the mating success of male guppies

Abstract This study examined the effects of female choice and male-male competition on male mating success in the guppy, Poecilia reticulata. The fraction of a males displays that elicited a sexual response from a female was used as a measure of relative female preference for that male. Male mating success was measured by scoring paternity of sons, using colour pattern as a genetic marker. Female preference had a significant effect on male mating success. Male-male competition was relatively uncommon, and did not involve direct threats or combat. Data on male-male competition did not significantly predict mating success. Males from different experimental groups with the same colour pattern had similar mating success. This suggests that female choice could have been based on colour pattern. However, there was no obvious relationship of particular colour pattern elements to mating success or female preference. The males with the same colour pattern were related and most were reared together, so other genetic or environmental factors could have led to similar mating success.

Effect of Artificial Selection on Male Colour Patterns on Mating Preference of Female Guppies

Theoretical models predict that the evolution of female mating preference may depend on a genetic correlation with the male traits on which preference depends. This correlation has been the subject of controversy, and has been demonstrated to exist in only a few cases. The relative extent of orange coloration exhibited by male guppies (Poecilia reticulata) contributes to the mating preference of female guppies in certain populations. If the predicted genetic correlation between preference and male traits exists, then artificial selection for increased and decreased amounts of orange in colour patterns of male guppies should result in corresponding shifts in female mating preference. Four separate selection experiments produced an immediate divergence in male colour patterns between high and low selection lines. Analysis of mate choice of females from the selection experiments provides some evidence for correlated divergence in preference as predicted by theory. Females from lines in which males were selected for increased orange tended to show stronger preference for orange than did females from lines selected for decreased orange. This kind of correlated change in preference could contribute to the correlated pattern of variation in colour pattern and female preference across guppy populations.

Mating advantage for rare males in wild guppy populations

To understand the processes that maintain genetic diversity is a long-standing challenge in evolutionary biology, with implications for predicting disease resistance, response to environmental change, and population persistence. Simple population genetic models are not sufficient to explain the high levels of genetic diversity sometimes observed in ecologically important traits. In guppies (Poecilia reticulata), male colour pattern is both diverse and heritable, and is arguably one of the most extreme examples of morphological polymorphism known. Negative frequency-dependent selection (NFDS), a form of selection in which genotypes are favoured when they are rare, can potentially maintain such extensive polymorphism, but few experimental studies have confirmed its operation in nature. Here we use highly replicated experimental manipulations of natural populations to show that males with rare colour patterns have higher reproductive fitness, demonstrating NFDS mediated by sexual selection. Rare males acquired more mates and sired more offspring compared to common males and, as previously reported, had higher rates of survival. Orange colour, implicated in other studies of sexual selection in guppies, did predict male reproductive success, but only in one of three populations. These data support the hypothesis that NFDS maintains diversity in the colour patterns of male guppies through two selective agents, mates and predators. Similar field-based manipulations of genotype frequencies could provide a powerful approach to reveal the underlying ecological and behavioural mechanisms that maintain genetic and phenotypic diversity.

Evolution of frequency-dependent mate choice: keeping up with fashion trends

The diversity of sexual traits favoured by females is enormous and, curiously, includes preferences for males with rare or novel phenotypes. We modelled the evolution of a preference for rarity that yielded two surprising results. First, a Fisherian ‘sexy son’ effect can boost female preferences to a frequency well above that predicted by mutation–selection balance, even if there are significant mortality costs for females. Preferences do not reach fixation, however, as they are subject to frequency-dependent selection: if choosy females are too common, then rare genotypes in one generation become common, and thus unattractive, in the offspring generation. Nevertheless, even at relatively low frequency, preferences maintain polymorphism in male traits. The second unexpected result is that the preferences can evolve to much higher frequencies if choice is hindered, such that females cannot always express their preferences. Our results emphasize the need to consider feedback where preferences determine the dynamics of male genotypes and vice versa. They also highlight the similarity between the arbitrariness of behavioural norms in models of social evolution with punishment (the so-called ‘folk theorem’) and the diversity of sexual traits that can be preferred simply because deviating from the norm produces unattractive offspring and is, in this sense, ‘punished’.