Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies

Natural enemies such as predators and parasites are known to shape intraspecific variability of behaviour and personality in natural populations, yet several key questions remain: (i) What is the relative importance of predation vs. parasitism in shaping intraspecific variation of behaviour across generations? (ii) What are the contributions of genetic and plastic effects to this behavioural divergence? (iii) And to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (i) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites for (ii) both wild‐caught F0 and laboratory‐reared F2 individuals and coming from (iii) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory‐reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild‐caught F0 individuals. Third, the two lineages showed a mixture of parallel and nonparallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay‐offs in alternative predation/parasitism environments and that parasitism has more transient effects in shaping intraspecific variation of behaviour than does predation.     

Pace of life,predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance

A common evolutionary response to predation pressure is increased investment in reproduction, ultimately resulting in a fast life history. Theory and comparative studies suggest that short-lived organisms invest less in defence against parasites than those that are longer lived (the pace of life hypothesis). Combining these tenets of evolutionary theory leads to the specific, untested prediction that within species, populations experiencing higher predation pressure invest less in defence against parasites. The Trinidadian guppy, Poecilia reticulata, presents an excellent opportunity to test this prediction: guppy populations in lower courses of rivers experience higher predation pressure, and as a consequence have evolved faster life histories, than those in upper courses. Data from a large-scale field survey showed that fish infected with Gyrodactylus parasites were of a lower body condition (quantified using the scaled mass index) than uninfected fish, but only in lower course populations. Although the evidence we present is correlational, it suggests that upper course guppies sustain lower fitness costs of infection, i.e. are more tolerant, than lower course guppies. The data are therefore consistent with the pace of life hypothesis of parasite defence allocation, and suggest that life-history traits mediate the indirect effect of predators on the parasites of their prey.     

Are host-parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels

Natural populations often face multiple mortality sources. Adaptive responses to one mortality source might also be beneficial with respect to other sources of mortality, resulting in "reinforcing adaptations"; or they might be detrimental with respect to other sources of mortality, resulting in "conflicting adaptations". We explored these possibilities by testing experimentally if the responses of guppies (Poecilia reticulata) to the monogenean ectoparasitic worm Gyrodactylus differed between populations adapted to different predation regimes. In experimental stream channels designed to replicate the natural environment, we exposed eight guppy populations (high-predation and low-predation populations from each of four separate rivers) either to their local Gyrodactylus parasites (infection treatment) or to the absence of those parasites (control). We found that infection dynamics varied dramatically among populations in a repeatable fashion, but that this variation was not related to the predation regime of origin. Consistent with previous work, high-predation guppy females gained more mass, had lower reproductive investment, and had more but smaller embryos than did low-predation females. Relative to control (no parasite) channels, guppies from treatment (infected) channels gained less mass but produced similar numbers and sizes of embryos-and thus had a higher reproductive effort. However, no interaction was evident between infection treatment and predation regime. We conclude that parasitism by Gyrodactylus and predation are both likely selective forces for guppies, but that adaptation to predation does not have an obvious deterministic effect on host-parasite dynamics or on life-history traits of female guppies.     

How might Gyrodactylus parasitism modify trade-offs between female preference and susceptibility of males to predation in Trinidadian guppies?

A number of examples exist of trade-offs between mating success and survival; that is, success in one fitness component comes at the cost of success in the other fitness component. However, these expected trade-offs are – perhaps even more commonly – not observed. One explanation for this apparent paradox of missing trade-offs could be that the other factors generating fitness variation across individuals confound or obscure the expected trade-off. These confounding effects could arise in two general ways: (i) the additional source of variation could positively (or negatively) influence both fitness components (“shared confounder” hypothesis), or (ii) the additional source of variation could influence only one fitness component (“non-shared confounder” hypothesis). We tested whether parasitism by Gyrodactylus spp. could be a confounder of trade-offs between female preference and susceptibility to predation for male Trinidadian guppies (Poecilia reticulata). As in previous work, we did not find the expected trade-off; that is, the males preferred by females were not more likely to be eaten by predators. Because half of the experimental males were infected by Gyrodactylus in a paired design, we were able to show that females discriminated against infected males, but that infected males were not more susceptible to predation. Our results thus provide support for the non-shared confounder hypothesis. That is, by negatively affecting one fitness component (female choice) but not the other (susceptibility to predation), parasitism by Gyrodactylus could obscure the expected trade-off between female preference and susceptibility to predation.     

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.     

Predation is associated with variation in colour pattern, but not body shape or colour reflectance, in a rainbowfish (Melanotaenia australis)

1. In freshwater fishes, inter-population variation in male phenotype is often associated with differences in predation intensity, but these effects can be difficult to disentangle from environmental influences. 2. The western rainbowfish Melanotaenia australis exhibits marked sexual dimorphism - females are plain with a slender body, while males have striking coloration and are deeper in the body. Male traits differ in expression among populations, but this has not been described or explored in the literature. 3. This paper describes a study designed to test for geographic structuring of male phenotype in M. australis and to determine whether between-population variation in male phenotype is attributable to variation in predation regime, after accounting for environment. 4. We collected data describing habitat, and the size, activity and abundance of predators at sites containing M. australis populations. We then used photography, spectrometry and geometric morphometrics to describe colour pattern, spectral reflectance and body shape in males from these populations. Finally, we used permutation-based multivariate statistics to partition variance in these traits according to environment and predation regime. 5. Downstream environments posed higher predation risk to M. australis. Furthermore, males from these sites consistently exhibited larger cheek spots and fewer coloured lateral stripes than those from upstream sites. Variation in predation regime accounted for a significant proportion of the total variance in these traits (30·9%), after controlling for the effects of environment. 6. Variation in predation regime did not explain variation in reflectance or shape. Environmental variation, however, explained a significant portion of the total variance in reflectance (74·9%), and there was a strong trend towards it explaining a portion of the total variance in body shape (34·9%). 7. We conclude that natural selection by predators may be an important determinant of the evolution of colour pattern variation in M. australis, but not of that of body shape or colour reflectance. 8. Further study of M. australis will complement existing models, which show complex relationships between predation regime, environment and phenotype. Understanding these relationships is prerequisite to predicting the evolution of phenotypic variation in natural systems.     

Do replicates of independent guppy lineages evolve similarly in a predator‐free laboratory environment?

The Trinidadian guppy is emblematic of parallel and convergent evolution, with repeated demonstrations that predation regime is a driver of adaptive trait evolution. A classic and foundational experiment in this system was conducted by John Endler 40 years ago, where male guppies placed into low‐predation environments in the laboratory evolved increased color in a few generations. However, Endler's experiment did not employ the now typical design for a parallel/convergent evolution study, which would employ replicates of different ancestral lineages. We therefore implemented an experiment that seeded replicate mesocosms with small founding populations of guppies originating from high‐predation populations of two very different lineages. The different mesocosms were maintained identically, and male guppy color was quantified every four months. After one year, we tested whether male color had increased, whether replicates within a lineage had parallel phenotypic trajectories, and whether the different lineages converged on a common phenotype. Results showed that male guppy color generally increased through time, primarily due to changes in melanic color, whereas the other colors showed inconsistent and highly variable trajectories. Most of the nonparallelism in phenotypic trajectories was among mesocosms containing different lineages. In addition to this mixture of parallelism and nonparallelism, convergence was not evident in that the variance in color among the mesocosms actually increased through time. We suggest that our results reflect the potential importance of high variation in female preference and stochastic processes such as drift and founder effects, both of which could be important in nature.     

Predation and the relative importance of larval colour polymorphisms and colour polyphenism in a damselfly

Intraspecific body colour variation is common in many animal species. Predation could be a key selective agent giving rise to variation in body colour, and such variation could be due to genetics (polymorphisms) or phenotypic plasticity (polyphenisms). In this study we examined the degree of colour polymorphism and polyphenism in background colour matching in larvae of the damselfly Coenagrion armatum. In addition, we tested if predation risk is reduced when larvae are exposed to a matching compared to a non-matching background. By raising families of larvae at three different background colours we showed that polymorphism explained about 20 % of the total variation and polyphenism about 35 %. In a predation experiment with fish, we showed that larvae with a body colour matching the background had a higher survival success compared to larvae with a non-matching background colour. We suggest that the background matching is adaptive in terms of survival from predation and that colour diversity is maintained because of spatial and temporal variation in the background experienced by damselfly larvae under field conditions.     

Low Predictability of Colour Polymorphism in Introduced Guppy (Poecilia reticulata) Populations in Panama

Colour polymorphism is a recurrent feature of natural populations, and its maintenance has been studied in a range of taxa in their native ranges. However, less is known about whether (and how) colour polymorphism is maintained when populations are removed from their native environments, as in the case of introduced species. We here address this issue by analyzing variation in colour patterns in recently-discovered introduced populations of the guppy (Poecilia reticulata) in Panama. Specifically, we use classic colour analysis to estimate variation in the number and the relative area of different colour spots across low predation sites in the introduced Panamanian range of the species. We then compare this variation to that found in the native range of the species under low- and high predation regimes. We found aspects of the colour pattern that were both consistent and inconsistent with the classical paradigm of colour evolution in guppies. On one hand, the same colours that dominated in native populations (orange, iridescent and black) were also the most dominant in the introduced populations in Panama. On the other, there were no clear differences between either introduced-low and native low- and high predation populations. Our results are therefore only partially consistent with the traditional role of female preference in the absence of predators, and suggest that additional factors could influence colour patterns when populations are removed from their native environments. Future research on the interaction between female preference and environmental variability (e.g. multifarious selection), could help understand adaptive variation in this widely-introduced species, and the contexts under which variation in adaptive traits parallels (or not) variation in the native range.     

Phenotypic convergence along a gradient of predation risk

A long-standing question in ecology is whether phenotypic plasticity, rather than selection per se, is responsible for phenotypic variation among populations. Plasticity can increase or decrease variation, but most previous studies have been limited to single populations, single traits and a small number of environments assessed using univariate reaction norms. Here, examining two genetically distinct populations of Daphnia pulex with different predation histories, we quantified predator-induced plasticity among 11 traits along a fine-scale gradient of predation risk by a predator (Chaoborus) common to both populations. We test the hypothesis that plasticity can be responsible for convergence in phenotypes among different populations by experimentally characterizing multivariate reaction norms with phenotypic trajectory analysis (PTA). Univariate analyses showed that all genotypes increased age and size at maturity, and invested in defensive spikes (neckteeth), but failed to quantitatively describe whole-organism response. In contrast, PTA quantified and qualified the phenotypic strategy the organism mobilized against the selection pressure. We demonstrate, at the whole-organism level, that the two populations occupy different areas of phenotypic space in the absence of predation but converge in phenotypic space as predation threat increases.     

Are pollinators the agents of selection on flower colour and size in irises?

Plant–pollinator interactions are believed to play a major role in the evolution of floral traits. Flower colour and flower size are important for attracting pollinators, directly influencing reproduction, and thus expected to be under pollinator‐mediated selection. Pollinator‐mediated selection is also proposed to play a role in maintaining flower colour polymorphism within populations. However, pigment concentrations, and thus flower colour, are also under selective pressures independent of pollinators. We quantified phenotypic pollinator‐mediated selection on flower colour and size in two colour polymorphic Iris species. Using female fitness, we estimated phenotypic selection on flower colour and size, and tested for pollinator‐mediated selection by comparing selection gradients between flowers open to natural pollination and supplementary pollinated flowers. In both species, we found evidence for pollen limitation, which set the base for pollinator‐mediated selection. In the colour dimorphic Iris lutescens, while pigment concentration and flower size were found to be under selection, this was independent of pollinators. For the polymorphic Iris pumila, pigment concentration is under selective pressure by pollinators, but only for one colour morph. Our results suggest that pollinators are not the main agents of selection on floral traits in these irises, as opposed to the accepted paradigm on floral evolution. This study provides an opposing example to the largely‐accepted theory that pollinators are the major agent of selection on floral traits.     

Hybridization and transgressive exploration of colour pattern and wing morphology in Heliconius butterflies

Hybridization can generate novel phenotypes distinct from those of parental lineages, a phenomenon known as transgressive trait variation. Transgressive phenotypes might negatively or positively affect hybrid fitness, and increase available variation. Closely related species of Heliconius butterflies regularly produce hybrids in nature, and hybridization is thought to play a role in the diversification of novel wing colour patterns despite strong stabilizing selection due to interspecific mimicry. Here, we studied wing phenotypes in first‐ and second‐generation hybrids produced by controlled crosses between either two co‐mimetic species of Heliconius or between two nonmimetic species. We quantified wing size, shape and colour pattern variation and asked whether hybrids displayed transgressive wing phenotypes. Discrete traits underlain by major‐effect loci, such as the presence or absence of colour patches, generate novel phenotypes. For quantitative traits, such as wing shape or subtle colour pattern characters, hybrids only exceed the parental range in specific dimensions of the morphological space. Overall, our study addresses some of the challenges in defining and measuring phenotypic transgression for multivariate traits and our data suggest that the extent to which transgressive trait variation in hybrids contributes to phenotypic diversity depends on the complexity and the genetic architecture of the traits.     

Variable colour patterns indicate multidimensional,intraspecific trait variation and ecological generalization in moths

Animal colour patterns long have provided information about key processes that drive the ecological and evolutionary dynamics of biological diversity. Theory and empirical evidence indicate that variation in colour patterns and other traits among individuals generally improves the performance of populations and species, for example by reducing predation risk, increasing establishment success, improving resilience to environmental change, and decreasing risk of extinction. However, little is known about whether and how variation in colour pattern among species is associated with variation in other phenotypic dimensions. To address this issue, we analysed associations of colour pattern with morphological, behavioural and life-history traits on the basis of data for nearly 400 species of noctuid moths. We found that moths with more variable colour patterns had longer flight activity periods, more diverse habitats and a greater number of host plant species than species with less variable colour patterns. Variable coloration in adult noctuid moths therefore can be considered as indicative of broader niches and generalist diets. Colour pattern variability was not significantly associated with overwintering stage or body size (wing span), and it was independent of whether the colour pattern of the larvae was non-variable, variable or highly variable. Colour pattern variation during the larval stage tended to increase as the duration of the flight activity period increased, but was independent of the length of the larval period, diet breadth and habitat use. The realization that information on colour pattern variation in adult moths, and possibly other organisms, offers a proxy for niche breadth and dietary generalization can inform management and conservation biology.     

Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids

Parasite diversity and abundance (parasite load) vary greatly among host species. However, the influence of host traits on variation in parasitism remains poorly understood. Comparative studies of parasite load have largely examined measures of parasite species richness and are predominantly based on records obtained from published data. Consequently, little is known about the relationships between host traits and other aspects of parasite load, such as parasite abundance, prevalence and aggregation. Meanwhile, understanding of parasite species richness may be clouded by limitations associated with data collation from multiple independent sources. We conducted a field study of Lake Tanganyika cichlid fishes and their helminth parasites. Using a Bayesian phylogenetic comparative framework, we tested evolutionary associations between five key host traits (body size, gut length, diet breadth, habitat complexity and number of sympatric hosts) predicted to influence parasitism, together with multiple measures of parasite load. We find that the number of host species that a particular host may encounter due to its habitat preferences emerges as a factor of general importance for parasite diversity, abundance and prevalence, but not parasite aggregation. In contrast, body size and gut size are positively related to aspects of parasite load within, but not between species. The influence of host phylogeny varies considerably among measures of parasite load, with the greatest influence exerted on parasite diversity. These results reveal that both host morphology and biotic interactions are key determinants of host–parasite associations and that consideration of multiple aspects of parasite load is required to fully understand patterns in parasitism.     

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.     

When and how can <Emphasis Type="Italic">Daphnia</Emphasis> prepare their offspring for the threat of predation?

The life history of Daphnia exposed to fish kairomone at different developmental stages was examined in a laboratory experiment. The strongest life history response to the applied predation threat was observed in females exposed during the 4th instar. Compared to Daphnia experiencing the presence of fish at earlier or later instars, these individuals reached maturity at a smaller size and released fewer neonates. Moreover, their offspring also demonstrated the strongest reaction to predation threat, exhibiting the broadest phenotypic plasticity in the life history response to predation. The breadth of their reaction norm was, on average, two times larger comparing with individuals from other treatments. Broader phenotypic plasticity may offer clear selective advantages under the unpredictable predation regime. This finding highlights the adaptive role of maternal effect in shaping life history of cladocerans.     

Contemporary Parallel Diversification,Antipredator Adaptations and Phenotypic Integration in an Aquatic Isopod

It is increasingly being recognized that predation can be a strong diversifying agent promoting ecological divergence. Adaptations against different predatory regimes can emerge over short periods of time and include many different traits. We studied antipredator adaptations in two ecotypes of an isopod (Asellus aquaticus) that have, diverged in parallel in two Swedish lakes over the last two decades. We quantified differences in escape speed, morphology and behavior for isopods from different ecotypes present in these lakes. Isopods from the source habitat (reed) coexist with mainly invertebrate predators. They are more stream-profiled and have higher escape speeds than isopods in the newly colonized stonewort habitat, which has higher density of fish predators. Stonewort isopods also show more cautious behaviors and had higher levels of phenotypic integration between coloration and morphological traits than the reed isopods. Colonization of a novel habitat with a different predation regime has thus strengthened the correlations between pigmentation and morphology and weakened escape performance. The strong signature of parallelism for these phenotypic traits indicates that divergence is likely to be adaptive and is likely to have been driven by differences in predatory regimes. Furthermore, our results indicate that physical performance, behavior and morphology can change rapidly and in concert as new habitats are colonized.     

Do Males Form Social Associations Based on Sexual Attractiveness in a Fission-Fusion Fish Society?

Recent theory predicts that males should choose social environments that maximize their relative attractiveness to females by preferentially associating with less attractive rivals, so as to enhance their mating success. Using the Trinidadian guppy (Poecilia reticulata), a highly social species, we tested for non-random social associations among males in mixed-sex groups based on two phenotypic traits (body length and coloration) that predict relative sexual attractiveness to females and sexual (sperm) competitiveness. Based on a well-replicated laboratory dichotomous-choice test of social group preference, we could not reject the null hypothesis that focal males chose randomly between a mixed-sex group that comprised a female and a rival male that was less sexually attractive than themselves and another mixed-sex group containing a sexually more attractive male. The same conclusion was reached when females were absent from the two groups. As might be expected from these laboratory findings, free-ranging males in the field were not assorted by either body length or colour in mixed-sex shoals. The apparent lack of an evolved and expressed preference in wild male guppies from our study population to form social associations with other males based on their relative sexual attractiveness and competitiveness might be due to the fission-fusion dynamics of guppy shoals in nature. Such social dynamics likely places constraints on the formation of stable phenotype-based social associations among males. This possibility is supported by a simulation model which assumes group departure rules based on relative body size and coloration in males.     

The effect of skin reflectance on thermal traits in a small heliothermic ectotherm

Variation in colour patterning is prevalent among and within species. A number of theories have been proposed in explaining its evolution. Because solar radiation interacts with the pigmentation of the integument causing light to either be reflected or absorbed into the body, thermoregulation has been considered to be a primary selective agent, particularly among ectotherms. Accordingly, the colour-mediated thermoregulatory hypothesis states that darker individuals will heat faster and reach higher thermal equilibria while paler individuals will have the opposite traits. It was further predicted that dark colouration would promote slower cooling rates and higher thermal performance temperatures. To test these hypotheses we quantified the reflectance, selected body temperatures, performance optima, as well as heating and cooling rates of an ectothermic vertebrate, Lampropholis delicata. Our results indicated that colour had no influence on thermal physiology, as all thermal traits were uncorrelated with reflectance. We suggest that crypsis may instead be the stronger selective agent as it may have a more direct impact on fitness. Our study has improved our knowledge of the functional differences among individuals with different colour patterns, and the evolutionary significance of morphological variation within species.     

Floral trait differentiation in Anacamptis coriophora: Phenotypic selection on scents,but not on colour

Current divergent selection may promote floral trait differentiation among conspecific populations in flowering plants. However, whether this applies to complex traits such as colour or scents has been little studied, even though these traits often vary within species. In this study, we compared floral colour and odour as well as selective pressures imposed upon these traits among seven populations belonging to three subspecies of the widespread, generalist orchid Anacamptis coriophora. Colour was characterized using calibrated photographs, and scents were sampled using dynamic headspace extraction and analysed using gas chromatography–mass spectrometry. We then quantified phenotypic selection exerted on these traits by regressing fruit set values on floral trait values. We showed that the three studied subspecies were characterized by different floral colour and odour, with one of the two predominant floral volatiles emitted by each subspecies being taxon‐specific. Plant size was positively correlated with fruit set in most populations, whereas we found no apparent link between floral colour and female reproductive success. We detected positive selection on several taxon‐specific compounds in A. coriophora subsp. fragrans, whereas no selection was found on floral volatiles of A. coriophora subsp. coriophora and A. coriophora subsp. martrinii. This study is one of the first to document variation in phenotypic selection exerted on floral scents among conspecific populations. Our results suggest that selection could contribute to ongoing chemical divergence among A. coriophora subspecies.