The complex ecology of genitalia: Gonopodium length and allometry in the Trinidadian guppy

Male genitalia present an extraordinary pattern of rapid divergence in animals with internal fertilization, which is usually attributed to sexual selection. However, the effect of ecological factors on genitalia divergence could also be important, especially so in animals with nonretractable genitalia because of their stronger interaction with the surrounding environment in comparison with animals with retractable genitalia. Here, we examine the potential of a pervasive ecological factor (predation) to influence the length and allometry of the male genitalia in guppies. We sampled guppies from pairs of low‐predation (LP) and high‐predation (HP) populations in seven rivers in Trinidad, and measured their body and gonopodium length. A key finding was that HP adult males do not have consistently longer gonopodia than do LP adult males, as had been described in previous work. However, we did find such divergence for juvenile males: HP juveniles have longer gonopodia than do LP juveniles. We therefore suggest that an evolutionary trend toward the development of longer gonopodia in HP males (as seen in the juveniles) is erased after maturity owing to the higher mortality of mature males with longer gonopodia. Beyond these generalities, gonopodium length and gonopodium allometry were remarkably variable among populations even within a predation regime, thus indicating strong context dependence to their development/evolution. Our findings highlight the complex dynamics of genitalia evolution in Trinidadian guppies.     

Locally adapted traits maintained in the face of high gene flow

Gene flow between phenotypically divergent populations can disrupt local adaptation or, alternatively, may stimulate adaptive evolution by increasing genetic variation. We capitalised on historical Trinidadian guppy transplant experiments to test the phenotypic effects of increased gene flow caused by replicated introductions of adaptively divergent guppies, which were translocated from high‐ to low‐predation environments. We sampled two native populations prior to the onset of gene flow, six historic introduction sites, introduction sources and multiple downstream points in each basin. Extensive gene flow from introductions occurred in all streams, yet adaptive phenotypic divergence across a gradient in predation level was maintained. Descendants of guppies from a high‐predation source site showed high phenotypic similarity with native low‐predation guppies in as few as ~12 generations after gene flow, likely through a combination of adaptive evolution and phenotypic plasticity. Our results demonstrate that locally adapted phenotypes can be maintained despite extensive gene flow from divergent populations.     

Contrasting Population and Diet Influences on Gut Length of an Omnivorous Tropical Fish,the Trinidadian Guppy (Poecilia reticulata)

Phenotypic plasticity is advantageous for organisms that live in variable environments. The digestive system is particularly plastic, responding to changes in diet. Gut length is the result of a trade-off between maximum nutrient absorption and minimum cost for its maintenance and it can be influenced by diet and by evolutionary history. We assessed variation in gut length of Trinidadian guppies (Poecilia reticulata) as a function of diet, season, ontogeny, and local adaptation. Populations of guppies adapted to different predation levels have evolved different life history traits and have different diets. We sampled guppies from sites with low (LP) and high predation (HP) pressure in the Aripo and Guanapo Rivers in Trinidad. We collected fish during both the dry and wet season and assessed their diet and gut length. During the dry season, guppies from HP sites fed mostly on invertebrates, while guppies in the LP sites fed mainly on detritus. During the wet season, the diet of LP and HP populations became very similar. We did not find strong evidence of an ontogenetic diet shift. Gut length was negatively correlated with the proportion of invertebrates in diet across fish from all sites, supporting the hypothesis that guppy digestive systems adapt in length to changes in diet. Population of origin also had an effect on gut length, as HP and LP fish maintained different gut lengths even in the wet season, when their diets were very similar and individuals in both types of populations fed mostly on detritus. Thus, both environment and population of origin influenced guppies gut length, but population of origin seemed to have a stronger effect. Our study also showed that, even in omnivorous fish, gut length adapted to different diets, being more evident when the magnitude of difference between animal and plant material in the diet was very large.     

Phenotypic variation in male guppies from natural inland populations: an additional test of Haskins' sexual selection/predation hypothesis

Synopsis In Venezuela, guppies,Poecilia reticulata, are found in a diversity of aquatic ecosystems fringing the western slope of the eastern Andes. These inland drainages are associated with large between-site variation in both physical and biotic environments. Numbers of potential guppy predators vary greatly between low diversity piedmont streams and high diversity llanos swamps. We analyze geographic variation in several phenotypic traits associated with conspicuousness of male guppies as an independent test of Haskins' (Haskins et al. 1961) hypothesis of natural balance between sexual selection (driving male conspicuousness) and predation (driving crypsis). Four sites were compared: a diverse llanos swamp (high predation), two Andean piedmont streams (intermediate and low predation), and a spring pool located south of Venezuela's Paría Peninsula (no aquatic predators). Because tropical wet and dry seasons are associated with varying degrees of environmental change at these sites, within-site seasonal samples provided an additional test of the role of selective predation on Male phenotypes. Phenotypic traits associated with both size and coloration supported the sexual selection/predation hypothesis. male guppies from the spring were generally more colorful than male guppies from inland drainages. Males from the diverse swamp site were smaller and less colorful than guppies from other sites. Males from the swamp population were smallest and least colorful during the early dry season, when diurnal aquatic piscivores were more diverse and abundant. Dominant spot pigments at each site were generally those that provided greatest contrast with the predominant environmental background color, lending further evidence that coloration patterns in male guppies enhance conspicuousness.     

Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies

Environmental gradients often lead to the parallel evolution of populations and species. To what extent do such gradients also lead to parallel evolution of the sexes? We used guppies (Poecilia reticulata) to examine the parallel and independent (sex‐specific) aspects of population divergence in response to predation and habitat features. Geometric morphometrics was used to analyse size and shape variation for 1335 guppies from 27 to 31 sites sampled in each of 2 years. Body size showed strong parallel population divergence; both sexes were larger at sites with a more open canopy and with higher flow. Body shape showed a mixture of parallel and independent population divergence. The strongest and most consistent effects were (1) high‐predation sites had males with smaller heads and deeper caudal peduncles, (2) open‐canopy sites had females with smaller heads and more distended abdomens and (3) high‐flow sites had males and females with smaller heads and deeper caudal peduncles.     

Carotenoid limitation of sexual coloration along an environmental gradient in guppies

Carotenoids produce most of the brilliant orange and yellow colours seen in animals, but animals cannot synthesize these pigments and must rely on dietary sources. The idea that carotenoids make good signals because they are a scarce limiting resource was proposed two decades ago and has become the leading hypothesis for the role of carotenoids in animal communication. To our knowledge, until now, however, there has been no direct evidence that carotenoids are a limiting resource in nature. We showed that carotenoid availability in the wild limits the expression of sexual coloration in guppies (Poecilia reticulata), a species in which females prefer males with brighter orange carotenoid-containing spots. Further, the degree of carotenoid limitation varies geographically along a replicated environmental gradient (rainforest canopy cover), which opens new avenues for testing signal evolution theory.     

Rapid color evolution in an aposematic species: a phylogenetic analysis of color variation in the strikingly polymorphic strawberry poison-dart frog

Aposematism is one of the great mysteries of evolutionary biology. The evolution of aposematic coloration is poorly understood, but even less understood is the evolution of polymorphism in aposematic signals. Here, we use a phylogeographic approach to investigate the evolution of color polymorphism in Dendrobates pumilio, a well-known poison-dart frog (family Dendrobatidae), which displays perhaps the most striking color variation of any aposematic species. With over a dozen color morphs, ranging from bright red to dull green, D. pumilio provides an ideal opportunity to examine the evolution of color polymorphism and evolutionary shifts to cryptic coloration in an otherwise aposematic species. We constructed a phylogenetic tree for all D. pumilio color morphs from 3051bp of mtDNA sequence data, reconstructed ancestral states using parsimony and Bayesian methods, and tested the recovered tree against constraint trees using parametric bootstrapping to determine the number of changes to each color type. We find strong evidence for nearly maximal numbers of changes in all color traits, including five independent shifts to dull dorsal coloration. Our results indicate that shifts in coloration in aposematic species may occur more regularly than predicted and that convergence in coloration may indicate that similar forces are repeatedly driving these shifts.     

Disentangling the selective factors that act on male colour in wild guppies

The colour pattern of male guppies ( Poecilia reticulata ) is thought to evolve as a compromise between sexual selection (favouring conspicuousness) and natural selection (favouring crypsis). Underpinning this classic explanation is the observation that guppies living with dangerous fish predators are less colourful than guppies living without these predators. However, high fish-predation sites are generally farther downstream than low fish-predation sites, and so may also differ in physical habitat features related to stream size, as well as in the abundance of predatory prawns ( Macrobrachium crenulatum ). The goal of our study was to disentangle the effects of fish predation on colour evolution from the potential effects of physical habitat features and predation by prawns. We collected 20 male guppies from each of 29 sites in two Trinidadian rivers. We then quantified the colour pattern of these fish; each spot was measured for size and assigned to a colour category. For each site, we determined the fish predation regime and quantified stream size, water colour, canopy openness, and prawn abundance. We then used regressions to assess the relative importance of these factors in explaining variation in guppy colour. Supporting previous work, the presence of predatory fishes was the most important explanatory variable for many components of colour pattern. Physical habitat features explained some of the remaining variation, but in inconsistent ways between the two rivers. The abundance of predatory prawns also explained variation in male colour. Our results suggest that predatory fishes impose the strongest selection on the colour pattern of male guppies but that other factors are also important.     

Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for covariation in visual tuning, light environment and mate preferences. Female preference co‐evolves with male coloration, such that guppy females from ‘low‐predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high‐predation’ environments. Here, we show that colour vision also varies across populations, with ‘low’‐predation guppies investing more of their colour vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS‐1 and LWS‐3 (the most abundant LWS opsins) in ‘low‐predation’ populations than ‘high‐predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high‐ and low‐predation populations. Together, this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of female preference variation in this model system.     

Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments

Prior research has demonstrated a strong association between the species of predators that co-occur with guppies and the evolution of guppy life histories. The evolution of these differences in life histories has been attributed to the higher mortality rates experienced by guppies in high-predation environments. Here, we evaluate whether there might be indirect effects of predation on the evolution of life-history patterns and whether there are environmental differences that are correlated with predation. To do so, we quantified features of the physical and chemical environment and the population biology of guppies from seven high- and low-predation localities. We found that high-predation environments tend to be larger streams with higher light levels and higher primary productivity, which should enhance food availability for guppies. We also found that guppy populations from high-predation environments have many more small individuals and fewer large individuals than those from low-predation environments, which is caused by their higher birth rates and death rates. Because of these differences in size distribution, guppies from high-predation environments have only one-fourth of the biomass per unit area, which should also enhance food availability for guppies in these localities. Guppies from high-predation sites allocate more resources to reproduction, grow faster, and attain larger asymptotic sizes, all of which are consistent with higher levels of resource availability. We conclude that guppies from high-predation environments experience higher levels of resource availability in part because of correlated differences in the environment (light levels, primary productivity) and in part as an indirect consequence of predation (death rates and biomass density). These differences in resource availability can, in turn, augment the effect of predator-induced mortality as factors that shape the evolution of guppy life-history patterns. We found no differences in the invertebrate communities from high- and low-predation localities, so we conclude that there do not appear to be multitrophic, indirect effects associated with these differences in predation.     

This is not déjà vu all over again: male guppy colour in a new experimental introduction

We use an experimental introduction in nature to examine factors that influence parallel evolution. In 1996, 200 high-predation guppies (Poecilia reticulata) from the Yarra River were introduced into the Damier River, which previously lacked guppies. Eight years later, we quantified the colour of wild-caught guppies ('phenotypic' divergence) and lab-reared guppies ('genetic' divergence) from low- and high-predation environments in both rivers. Phenotypic and genetic divergence between predation environments within the Yarra was evident for black and for orange. Phenotypic divergence within the Damier was parallel to the Yarra for black but not for orange. Genetic divergence was absent between predation environments within the Damier, but was evident when comparing both Damier populations to their Yarra ancestors. The evolution of male colour thus depends on factors other than the simple contrast between 'high' and 'low' predation. We suggest that the parallel evolution of male signalling traits may sometimes first require the parallel evolution of female preferences.     

Population genomics of natural and experimental populations of guppies (Poecilia reticulata)

Convergent evolution represents one of the best lines of evidence for adaptation, but few cases of phenotypic convergence are understood at the genetic level. Guppies inhabiting the Northern Mountain Range of Trinidad provide a classic example of phenotypic convergent evolution, where adaptation to low or high predation environments has been found for a variety of traits. A major advantage of this system is the possibility of long‐term experimental studies in nature, including transplantation from high to low predation sites. We used genome scans of guppies from three natural high and low predation populations and from two experimentally established populations and their sources to examine whether phenotypic convergent evolution leaves footprints at the genome level. We used population‐genetic modelling approaches to reconstruct the demographic history and migration among sampled populations. Naturally colonized low predation populations had signatures of increased effective population size since colonization, while introduction populations had signatures of decreased effective population size. Only a small number of regions across the genome had signatures of selection in all natural populations. However, the two experimental populations shared many genomic regions under apparent selection, more than expected by chance. This overlap coupled with a population decrease since introduction provides evidence for convergent selection occurring in the two introduced populations. The lack of genetic convergence in the natural populations suggests that convergent evolution is lacking in these populations or that the effects of selection become difficult to detect after a long‐time period.     

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.     

Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait

Although conspicuous visual sexual signals, such as bright colors,in males serve to attract females in numerous species, theymay also attract the attention of potential predators and thusmay be costly in terms of increasing individual risk of mortalityto predation. Most models of the evolution of extravagant malesexual traits and female preferences for them assume that thesexually preferred male trait is costly to produce and maintain.However, there is surprisingly little empirical evidence fordirect fitness costs associated with sexually selected visualtraits that enhance male mating success. In the present study,we report a direct fitness cost for sexually selected, brightbody-color patterns in males in the form of an associated greaterrisk of mortality to predation. By using the guppy (Poeciliareticulata) and the blue acara cichlid fish (Aequidens pulcher)as a model prey–predator system, we demonstrate experimentallythat individual cichlids preferentially and consistently approached,attacked, and captured the more brightly colored of two size-matchedmale guppies presented simultaneously in staged encounters.This resulted in the brightly colored male incurring, on average,a significantly higher risk of mortality given an encounterwith the predator than with the drabber male in matched pairs.Our results constitute strong behavioral evidence for a directviability cost associated with bright coloration in male guppies,and they corroborate the generally accepted paradigm that directionalpredation by visual fish predators against brightly colored,adult male guppies underlies the evolution of the known divergentcolor patterns in natural guppy populations that experiencedifferent intensities of predation. The viability cost associatedwith bright conspicuous coloration in male guppies potentiallyreinforces for females the reliability of this sexually selectedtrait as an indicator trait of male quality.     

Female preference for blue in Japan blue guppies (Poecilia reticulata)

Guppies (Poecilia reticulata) are widely used as a model species in mate choice studies. Although native to South America, guppies have been introduced to natural water bodies in disparate regions of the globe. Here, for the first time, we examine guppies from one such introduced population in Japan where males have evolved a predominantly blue color pattern. Previous studies of wild-type guppies have shown blue to play a relatively minor role in the mate choice decisions of females compared to other traits, such as orange, and the importance of blue is not universally supported by all studies. The Japanese population therefore presents an ideal opportunity to re-examine the potential significance of blue as a mate choice cue in guppies. Mate choice experiments, in which female Japan blue guppies were given a choice between pairs of males that differed in their area of blue coloration but were matched for other traits, revealed that females prefer males with proportionately larger amounts of blue in their color patterns. We discuss possible factors, including sexual and ecological selection, which may have led to the evolution of unusually large areas of blue at the expense of other colors in Japan blue guppies. However, further studies are needed to distinguish between these scenarios.     

Does relaxed predation drive phenotypic divergence among insular populations?

The evolution of striking phenotypes on islands is a well‐known phenomenon, and there has been a long‐standing debate on the patterns of body size evolution on islands. The ecological causes driving divergence in insular populations are, however, poorly understood. Reduced predator fauna is expected to lower escape propensity, increase body size and relax selection for crypsis in small‐bodied, insular prey species. Here, we investigated whether escape behaviour, body size and dorsal coloration have diverged as predicted under predation release in spatially replicated islet and mainland populations of the lizard species Podarcis gaigeae. We show that islet lizards escape approaching observers at shorter distances and are larger than mainland lizards. Additionally, we found evidence for larger between‐population variation in body size among the islet populations than mainland populations. Moreover, islet populations are significantly more divergent in dorsal coloration and match their respective habitats poorer than mainland lizards. These results strongly suggest that predation release on islets has driven population divergence in phenotypic and behavioural traits and that selective release has affected both trait means and variances. Relaxed predation pressure is therefore likely to be one of the major ecological factors driving body size divergence on these islands.     

Evolution of juvenile growth rates in female guppies (Poecilia reticulata): predator regime or resource level?

Recent theoretical and empirical work argues that growth rate can evolve and be optimized, rather than always being maximized. Chronically low resource availability is predicted to favour the evolution of slow growth, whereas attaining a size-refuge from mortality risk is predicted to favour the evolution of rapid growth. Guppies (Poecilia reticulata) evolve differences in behaviour, morphology and life-history traits in response to predation, thus demonstrating that predators are potent agents of selection. Predators in low-predation environments prey preferentially on small guppies, but those in high-predation environments appear to be non-selective. Because guppies can outgrow their main predator in low- but not high-predation localities, we predict that predation will select for higher growth rates in the low-predation environments.However, low-predation localities also tend to have lower productivity than high-predation localities, yield-ing the prediction that guppies from these sites should have slower growth rates. Here we compare the growth rates of the second laboratory-born generation of guppies from paired high- and low-predation localities from four different drainages. In two out of four comparisons, guppies from high-predation sites grew significantly faster than their low-predation counterparts. We also compare laboratory born descendants from a field introduction experiment and show that guppies introduced to a low-predation environment evolved slower growth rates after 13 years, although this was evident only at the high food level. The weight of the evidence suggests that resource availability plays a more important role than predation in shaping the evolution of growth rates.     

Warning signals are seductive: Relative contributions of color and pattern to predator avoidance and mate attraction in Heliconius butterflies

Visual signaling in animals can serve many uses, including predator deterrence and mate attraction. In many cases, signals used to advertise unprofitability to predators are also used for intraspecific communication. Although aposematism and mate choice are significant forces driving the evolution of many animal phenotypes, the interplay between relevant visual signals remains little explored. Here, we address this question in the aposematic passion‐vine butterfly Heliconius erato by using color‐ and pattern‐manipulated models to test the contributions of different visual features to both mate choice and warning coloration. We found that the relative effectiveness of a model at escaping predation was correlated with its effectiveness at inducing mating behavior, and in both cases wing color was more predictive of presumptive fitness benefits than wing pattern. Overall, however, a combination of the natural (local) color and pattern was most successful for both predator deterrence and mate attraction. By exploring the relative contributions of color versus pattern composition in predation and mate preference studies, we have shown how both natural and sexual selection may work in parallel to drive the evolution of specific animal color patterns.     

SPATIOTEMPORAL VARIATION IN LINEAR NATURAL SELECTION ON BODY COLOR IN WILD GUPPIES (POECILIA RETICULATA)

We conducted 10 mark–recapture experiments in natural populations of Trinidadian guppies to test hypotheses concerning the role of viability selection in geographic patterns of male color variation. Previous work has reported that male guppies are more colorful in low‐predation sites than in high‐predation sites. This pattern of phenotypic variation has been theorized to reflect differences in the balance between natural (viability) selection that disfavors bright male color (owing to predation) and sexual selection that favors bright color (owing to female choice). Our results support the prediction that male color is disfavored by viability selection in both predation regimes. However, it does not support the prediction that viability selection against male color is weaker in low‐predation experiments. Instead, some of the most intense bouts of selection against color occurred in low‐predation experiments. Our results illustrate considerable spatiotemporal variation in selection among experiments, but such variation was not generally correlated with local patterns of color diversity. More complex selective interactions, possibly including the indirect effects of predators on variation in mating behavior, as well as other environmental factors, might be required to more fully explain patterns of secondary sexual trait variation in this system.     

Increased juvenile predation is not associated with evolved differences in adult brain size in Trinidadian killifish (Rivulus hartii)

Vertebrates exhibit extensive variation in brain size. The long‐standing assumption is that this variation is driven by ecologically mediated selection. Recent work has shown that an increase in predator‐induced mortality is associated with evolved increases and decreases in brain size. Thus, the manner in which predators induce shifts in brain size remains unclear. Increased predation early in life is a key driver of many adult traits, including life‐history and behavioral traits. Such results foreshadow a connection between age‐specific mortality and selection on adult brain size. Trinidadian killifish, Rivulus hartii, are found in sites with and without guppies, Poecilia reticulata. The densities of Rivulus drop dramatically in sites with guppies because guppies prey upon juvenile Rivulus. Previous work has shown that guppy predation is associated with the evolution of adult life‐history traits in Rivulus. In this study, we compared second‐generation laboratory‐born Rivulus from sites with and without guppies for differences in brain size and associated trade‐offs between brain size and other components of fitness. Despite the large amount of existing research on the importance of early‐life events on the evolution of adult traits, and the role of predation on both behavior and brain size, we did not find an association between the presence of guppies and evolutionary shifts in Rivulus brain size. Such results argue that increased rates of juvenile mortality may not alter selection on adult brain size.