F. Helen Rodd

A possible non-sexual origin of mate preference: are male guppies mimicking fruit?

In most animals, the origins of mating preferences are not clear. The ‘sensory–bias’ hypothesis proposes that biases in female sensory or neural systems are important in triggering sexual selection and in determining which male traits will become elaborated into sexual ornaments. Subsequently, other mechanisms can evolve for discriminating between high–and low–quality mates. Female guppies (Poecilia reticulata) generally show a preference for males with larger, more chromatic orange spots. It has been proposed that this preference originated because it enabled females to obtain high–quality mates. We present evidence for an alternative hypothesis, that the origin of the preference is a pleiotropic effect of a sensory bias for the colour orange, which might have arisen in the context of food detection. In field and laboratory experiments, adult guppies of both sexes were more responsive to orange–coloured objects than to objects of other colours, even outside a mating context. Across populations, variation in attraction to orange objects explained 94% of the inter–population variation in female mate preference for orange coloration on males. This is one of the first studies to show both an association between a potential trigger of a mate–choice preference and a sexually selected trait, and also that an innate attraction to a coloured inanimate object explains almost all of the observed variation in female mate choice. These results support the ‘sensory–bias’ hypothesis for the evolution of mating preferences.

Multiple mating and sequential mate choice in guppies: females trade up.

The trade–up hypothesis outlines a behavioural strategy that females could use to maximize the genetic benefits to their offspring. The hypothesis proposes that females should be more willing to accept a mate when the new male encountered is a superior genetic source to previous mates. We provide a direct test of the trade–up hypothesis using guppies (Poecilia reticulata), and evaluate both behavioural and paternity data. Virgin female guppies were presented sequentially with two males of varying attractiveness, and their responsiveness to each male was quantified. Male attractiveness (ornamentation) was scored as the amount of orange coloration on their body. Females were generally less responsive to second–encountered males, yet responsiveness to second males was an increasing function of male ornamentation. These attractive second males also sired a greater proportion of the offspring. There was an overall tendency for last–male advantage in paternity, and this advantage was most exaggerated when the second male was more ornamented than the first. Finally, we found that our estimate of relative sperm number did not account for any significant variation in paternity. Our results suggest that female guppies may use pre–copulatory mechanisms to maximize the genetic quality of their offspring.

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.

VARIATION IN THE DEMOGRAPHY OF GUPPY POPULATIONS: THE IMPORTANCE OF PREDATION AND LIFE HISTORIES

We compare the demography of natural populations of guppies (Poecilia reticulata) coexisting with two different communities of predators. In some populations, guppies co-occur with Rivulus hartii, a small, gape-limited predator; in others, guppies co-occur with larger species of fish that also prey on guppies. We found an association between the demography of the resident guppy population and the species of predator(s) present at a site. Populations of guppies that co-occurred with Rivulus had fewer small, immature guppies and more mid- and large-sized, mature guppies than populations of guppies that lived in the community of larger predators. The sex ratio of adult guppies did not differ between predator localities but it was significantly more variable among sites with the small predator. Ninety percent of all samples had a female-biased sex ratio. Season (wet vs. dry season) did not have a statistically significant influence on sex ratio or on stage or size distributions. The observed variation in guppy demography could be simply a result of differences in the prey size preferences of the predators. However, guppies from the two types of localities show considerable differences in life history traits, including age at maturity and fecundity. This variation in traits could be contributing to the differences in demography. Indeed, results from an individual-based computer model suggest that fecundity, offspring size, and individual growth rates were most influential in producing interlocality differences in size distributions and the proportions of the populations that were immature. Mortality rates and individual growth rates seem to make the greatest contribution to variation in adult sex ratio. Therefore, the observed patterns in the demography of these populations appear to result from complex interactions between the mortality schedules and life history traits of their constituents.

Life-History Evolution in Guppies (Poecilia reticulata: Poeciliidae). IV. Parallelism in Life-History Phenotypes

In earlier publications, we reported an association between the life-history patterns of guppies and the types of predators with which they co-occur. We contrasted guppies from high-predation sites (Crenicichla localities) with those from low-predation sites (Rivulus localities) found on the south slope of the Northern Range Mountains of Trinidad. Guppies from high-predation localities attain maturity at an earlier age and smaller size, produce more and smaller offspring per litter, and have higher reproductive allotments than their counterparts from low-predation sites. Here we present a parallel series of analyses for guppies from a new series of localities on the north slope of the Northern Range. These fish are also found in what appear to be high- and low-predation communities, but, with one exception, the species of predators are entirely different from those on the south slope. The larger predators are derived from marine families (gobies and mullets) that have invaded freshwater rivers; the south slope fauna is derived from families typical of mainland South America. If predator-induced mortality selects for life-history evolution, then guppies from high- and low-predation sites on the north slope should have life histories similar to their counterparts on the south slope. We compare the life-history phenotypes of guppies from the north slope communities and find that the high- and low-predation contrasts are remarkably similar to those reported earlier for the south slope communities. We reinforce this comparison with multivariate analyses that use discriminant functions derived for the south slope collections to classify north slope samples. Finally, we exploit recent molecular genetic data and the geographical distribution of high- and low-predation communities to argue for the independent origin of these life-history patterns in each drainage.

Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task

The ability to return to, or avoid, specific locations is often critical to fitness-related activities. We tested for differences in spatial memory of guppies, Poecilia reticulata, from low- and high-predation populations in a maze task. We also measured the time each fish took to make a decision in the maze, because individuals can show a trade-off between the speed and the accuracy of their decisions during this kind of task. Because brain size can affect cognitive performance, we also measured brain size. There were no differences in the number of errors made or time to find the reward between predation regimes. However, high-predation guppies tended to take longer to make the decision about which maze chamber to enter than low-predation guppies; thus, low-predation guppies were more willing to make quick and potentially inaccurate decisions, a strategy we have termed ‘hastiness’. Individuals within populations also varied in hastiness and we found that hasty guppies tended to have smaller telencephalons, the brain region most responsible for spatial memory. There was no difference in brain size in relation to predation regime, although lab-reared fish had smaller brains than wild-caught fish. This study shows that the careful observation of an animals strategy for solving spatial problems may reveal subtle differences that are associated with ecology and brain size.

Pigments, Patterns, and Fish Behavior

Color patterns in fish are often multicomponent signals, composed of pigment-based and structural color patches that can be used to communicate within species, in both inter- and intrasexual interactions, and between species. In this review, we discuss some of the roles played by pigment-based elements of color pattern. We begin by discussing general forms of coloration, classifying them by appearance (e.g., cryptic vs. conspicuous) and apparent function (e.g., conspicuous coloration and mating displays, stripes and cooperation, and bars and aggression). We then briefly discuss the roles pigments play in the perception of these color patterns via their presence in the eye. In the last section, we look at the relative importance of carotenoid versus melanic coloration in situations where honest signals to potential rivals and potential mates might be required. In this survey, we have highlighted some recent research, especially studies that consider both the physiological and behavioral processes underlying the evolution and expression of pigment-based color patterns in fish. The nature of pigmented color patterns depends not just on the dynamics of pattern development and physiological regulation, but also on the behavioral roles played by these patterns, both now and in the past. As such, advances in particular fields of study on pigment patterns (physiology, developmental biology, behavioral ecology, evolutionary biology, etc.) will increasingly depend on insights from other fields.

Sequencing and characterization of the guppy ( Poecilia reticulata ) transcriptome

BackgroundNext-generation sequencing is providing researchers with a relatively fast and affordable option for developing genomic resources for organisms that are not among the traditional genetic models. Here we present a de novo assembly of the guppy (Poecilia reticulata) transcriptome using 454 sequence reads, and we evaluate potential uses of this transcriptome, including detection of sex-specific transcripts and deployment as a reference for gene expression analysis in guppies and a related species. Guppies have been model organisms in ecology, evolutionary biology, and animal behaviour for over 100 years. An annotated transcriptome and other genomic tools will facilitate understanding the genetic and molecular bases of adaptation and variation in a vertebrate species with a uniquely well known natural history.ResultsWe generated approximately 336 Mbp of mRNA sequence data from male brain, male body, female brain, and female body. The resulting 1,162,670 reads assembled into 54,921 contigs, creating a reference transcriptome for the guppy with an average read depth of 28×. We annotated nearly 40% of this reference transcriptome by searching protein and gene ontology databases. Using this annotated transcriptome database, we identified candidate genes of interest to the guppy research community, putative single nucleotide polymorphisms (SNPs), and male-specific expressed genes. We also showed that our reference transcriptome can be used for RNA-sequencing-based analysis of differential gene expression. We identified transcripts that, in juveniles, are regulated differently in the presence and absence of an important predator, Rivulus hartii, including two genes implicated in stress response. For each sample in the RNA-seq study, >50% of high-quality reads mapped to unique sequences in the reference database with high confidence. In addition, we evaluated the use of the guppy reference transcriptome for gene expression analyses in a congeneric species, the sailfin molly (Poecilia latipinna). Over 40% of reads from the sailfin molly sample aligned to the guppy transcriptome.ConclusionsWe show that next-generation sequencing provided a reliable and broad reference transcriptome. This resource allowed us to identify candidate gene variants, SNPs in coding regions, and sex-specific gene expression, and permitted quantitative analysis of differential gene expression.

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.

Perceptual processes and the maintenance of polymorphism through frequency-dependent predation

One of the key challenges of both ecology and evolutionary biology is to understand the mechanisms that maintain diversity. Negative frequency-dependent selection is a powerful mechanism for maintaining variation in the population as well as species diversity in the community. There are a number of studies showing that this type of selection, where individuals of a rare type (i.e. a rare morph or a rare species) experience higher survival than those of more common type(s). However, it is still not clear how frequency-dependent selection operates. Search image formation has been invoked as a possible, proximate explanation. Although the conceptual link between search image and frequency-dependent predation is often assumed in ecological and evolutionary studies, a review of the literature reveals a paucity of evidence demonstrating the occurrence of both in a natural predator-prey system. Advances in the field of psychology strongly support the existence of search image, yet these findings are not fully recognized in the realm of ecology and evolutionary biology, in part, we feel because of confusion and inconsistencies in terminology. Here we try to simplify the language, clarify the advances in the study of frequency-dependent predation and search image, and suggest avenues for future research. We feel that the investigations of both proximate (perceptual mechanisms) and ultimate (pattern of predation) processes are necessary to fully understand the importance of individual behavioural processes for mediating evolutionary and ecological diversity.