Trinidadian Guppies Research Articles

Multiple environmental stressors affect predation pressure in a tropical freshwater system

Environmental change can alter predator-prey dynamics. However, studying predators in the context of co-occurring environmental stressors remains rare, especially under field conditions. Using in situ filming, we examined how multiple stressors, including temperature and turbidity, impact the distribution and behaviour of wild fish predators of Trinidadian guppies (Poecilia reticulata). The measured environmental variables accounted for 17.6% of variance in predator species composition. While predator species differed in their associations with environmental variables, the overall prevalence of predators was greatest in slow flowing, deeper, warmer and less turbid habitats. Moreover, these warmer and less turbid habitats were associated with earlier visits to the prey stimulus by predators, and more frequent predator visits and attacks. Our findings highlight the need to consider ecological complexity, such as co-occurring stressors, to better understand how environmental change affects predator-prey interactions.

Parasite load, rather than parasite presence, decreases upstream movement in Trinidadian guppies Poecilia reticulata.

Several factors influence whether an organism remains in its local habitat. Parasites can, for example, influence host movement by impacting their behavior, physiology, and morphology. In rivers, fish that swim efficiently against the current are able to maintain their position without being displaced downstream, a behavior referred to as positive rheotaxis. We hypothesized that both the presence and number of ectoparasites on a host would affect the ability of fish to avoid downstream displacement and thus prevent them from remaining in their habitat. We used the guppy-Gyrodactylus host-ectoparasite model to test whether parasite presence and parasite load had an effect on fish rheotaxis. We quantified rheotaxis of sham-infected and parasite-infected fish in a circular flow tank in the laboratory prior to infection and 5-6 days postinfection. Both parasite-infected and sham-infected individuals expressed similar levels of positive rheotaxis prior to infection and after infection. However, with increasing parasite numbers, guppies covered less distance in the upstream direction and spent more time in slower flow zones. These results suggest that higher numbers of Gyrodactylus ectoparasites negatively influence rheotactic movements. Further research is needed to understand the ecological and evolutionary implications of this ectoparasite on fish movement.

Evolutionary divergence of plasticity in brain morphology between ecologically divergent habitats of Trinidadian guppies.

Phenotypic plasticity is critical for organismal performance and can evolve in response to natural selection. Brain morphology is often developmentally plastic, affecting animal performance in a variety of contexts. However, the degree to which the plasticity of brain morphology evolves has rarely been explored. Here, we use Trinidadian guppies (Poecilia reticulata), which are known for their repeated adaptation to high-predation (HP) and low-predation (LP) environments, to examine the evolution and plasticity of brain morphology. We exposed second-generation offspring of individuals from HP and LP sites to 2 different treatments: predation cues and conspecific social environment. Results show that LP guppies had greater plasticity in brain morphology compared to their ancestral HP population, suggesting that plasticity can evolve in response to environmentally divergent habitats. We also show sexual dimorphism in the plasticity of brain morphology, highlighting the importance of considering sex-specific variation in adaptive diversification. Overall, these results may suggest the evolution of brain morphology plasticity as an important mechanism that allows for ecological diversification and adaptation to divergent habitats.

Disentangling genetic, plastic and social learning drivers of sex-specific foraging behaviour in Trinidadian guppies (Poecilia reticulata).

Evolutionary biologists have long been interested in parsing out the roles of genetics, plasticity and their interaction on adaptive trait divergence. Since males and females often have different ecological and reproductive roles, separating how their traits are shaped by interactions between their genes and environment is necessary and important. Here, we disentangle the sex-specific effects of genetic divergence, developmental plasticity, social learning and contextual plasticity on foraging behaviour in Trinidadian guppies (Poecilia reticulata) adapted to high- or low-predation habitats. We reared second-generation siblings from both predation regimes with or without predator chemical cues, and with adult conspecifics from either high- or low-predation habitats. We then quantified their foraging behaviour in water with and without predator chemical cues. We found that high-predation guppies forage more efficiently than low-predation guppies, but this behavioural difference is context-dependent and shaped by different mechanisms in males and females. Higher foraging efficiency in high-predation females is largely genetically determined, and to a smaller extent socially learned from conspecifics. However, in high-predation males, higher foraging efficiency is plastically induced by predator cues during development. Our study demonstrates sex-specific differences in genetic versus plastic responses in foraging behaviour, a trait of significance in organismal fitness and ecosystem dynamics.

Insights into adaptive behavioural plasticity from the guppy model system.

Behavioural plasticity allows organisms to respond to environmental challenges on short time scales. But what are the ecological and evolutionary processes that underlie behavioural plasticity? The answer to this question is complex and requires experimental dissection of the physiological, neural and molecular mechanisms contributing to behavioural plasticity as well as an understanding of the ecological and evolutionary contexts under which behavioural plasticity is adaptive. Here, we discuss key insights that research with Trinidadian guppies has provided on the underpinnings of adaptive behavioural plasticity. First, we present evidence that guppies exhibit contextual, developmental and transgenerational behavioural plasticity. Next, we review work on behavioural plasticity in guppies spanning three ecological contexts (predation, parasitism and turbidity) and three underlying mechanisms (endocrinological, neurobiological and genetic). Finally, we provide three outstanding questions that could leverage guppies further as a study system and give suggestions for how this research could be done. Research on behavioural plasticity in guppies has provided, and will continue to provide, a valuable opportunity to improve understanding of the ecological and evolutionary causes and consequences of behavioural plasticity.

Trophic niche drives the evolution of craniofacial shape in Trinidadian guppies.

Diverse clades of fishes adapted to feeding on the benthos repeatedly converge on steep craniofacial profiles and shorter, wider heads. But in an incipient radiation, to what extent is this morphological evolution measurable and can we distinguish the relative genetic vs. plastic effects? We use the Trinidadian guppy (Poecilia reticulata) to test the repeatability of adaptation and the alignment of genetic and environmental effects shaping poecilid craniofacial morphology. We compare wild-caught and common garden lab-reared fish to quantify the genetic and plastic components of craniofacial morphology across 4 populations from 2 river drainage systems (n = 56 total). We first use micro-computed tomography to capture 3D morphology, then place both landmarks and semilandmarks to perform size-corrected 3D morphometrics and quantify shape space. We find a measurable, significant, and repeatable divergence in craniofacial shape between high-predation invertivore and low-predation detritivore populations. As predicted from previous examples of piscine adaptive trophic divergence, we find increases in head slope and craniofacial compression among the benthic detritivore foragers. Furthermore, the effects of environmental plasticity among benthic detritivores produce exaggerated craniofacial morphological change along a parallel axis to genetic morphological adaptation from invertivore ancestors. Overall, many of the major patterns of benthic-limnetic craniofacial evolution appear convergent among disparate groups of teleost fishes.

Effects of short‐ and long‐term enrichment on brain and behavior in Trinidadian guppies

AbstractEnvironmental enrichment (EE) often increases positive behavioral and physiological effects on captive animals. Fish are commercially and scientifically important taxa that have been shown to benefit from EE. Here we examined the effects of both short‐ and long‐term EE in Trinidadian guppies (Poecilia reticulata). In the short‐term exposure to EE, female guppies were raised in standard conditions, and after reaching adulthood were moved to either an enriched or a deprived environment for 2 weeks. Long‐term exposure guppies were reared from birth for 12 weeks (until sexual maturity) in either an enriched or deprived environment. We then assessed growth, brain size, and neophobic and exploratory behaviors in standard assays. Guppies given EE were bolder, regardless of timescale, although females showed a more pronounced change in behaviors than males. We further found that guppies reared with EE were smaller yet had larger relative brain sizes than guppies reared under deprived conditions. Here we highlight that EE had influenced growth, brain size, neophobic, and exploratory behaviors in guppies, and behavioral changes were observed after only 2 weeks. Our results highlight the need for assessing the influences of EE in captivity, in particular for researchers studying cognition and behavior.

Evolutionary divergence of developmental plasticity and learning of mating tactics in Trinidadian guppies.

Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve. In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high- or low-predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity. High-predation males learned their mating tactic from conspecific adults as juveniles, while low-predation males did not. High-predation males increased courtship when exposed to chemical predator cues during development; low-predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development. Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not. We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats.

Sexually attractive traits predict predation-threat sensitivity of male alternative mating tactics

Abstract Although visual sexual signals, such as ornamental colors and courtship displays, and large body size in males are attractive to females in numerous species, they may also inadvertently attract the attention of eavesdropping predators and thus may be costly in terms of increasing individual risk of mortality to predation. Theoretically, more color ornamented and larger males should be more predation threat sensitive and suppress their sexual signaling and(or) mating effort relatively more than their less color ornamented and smaller counterparts when under predation hazard. Here, we experimentally tested this hypothesis by quantifying concurrently the rates of alternative mating tactics (courtship displays, sneak mating attempts) expressed by male Trinidadian guppies (Poecilia reticulata) varying in color ornamentation and body size under a staged immediate threat of predation. Males suppressed their overall mating effort in response to the perceived predation threat, decreasing the frequency of their (presumably more conspicuous) courtship displays significantly more on average than the frequency of their sneak mating behavior. Statistically controlling for body length, more color-ornamented males were more threat sensitive in their courtship displays, but not sneak mating attempts, under predation hazard than drabber males. Controlling for body coloration, larger males exhibited lower courtship and sneak mating efforts than smaller males in both predation treatments, but body length only influenced threat sensitivity in sneak mating behavior. These results are consistent with both the threat sensitive hypothesis and asset protection principle and highlight the phenotype dependency and adaptive plasticity of alternative mating tactics in male guppies under varying predation risk.

Aggregation of symbionts on hosts depends on interaction type and host traits

Symbionts tend to be aggregated on their hosts, such that few hosts harbor the majority of symbionts. This ubiquitous pattern can result from stochastic processes, but aggregation patterns may also depend on the type of host–symbiont interaction, along with traits that affect host exposure and susceptibility to symbionts. Untangling how aggregation patterns both within and among populations depend on stochastic processes, interaction type and host traits remains an outstanding challenge. Here, we address this challenge by using null models to compare aggregation patterns in a neutral system of Balanomorpha barnacles attached to patellid limpets and a host–parasite system of Gyrodactylus spp. monogeneans and their Trinidadian guppy Poecilia reticulata hosts. We first used a model to predict patterns of symbiont–host aggregation due to random partitioning of symbionts to hosts. This null model accurately predicted the aggregation of barnacles on limpets, but the degree of aggregation varied across 303 quadrats. Quadrats with larger limpets had less aggregated barnacles, whereas aggregation increased with variation in limpet size. Across 84 guppy populations, Gyrodactylus spp. parasites were significantly less aggregated than predicted by the null model. As in the neutral limpet–barnacle system, aggregation decreased with mean host size. Parasites were significantly less aggregated on males than females because male guppies tended to have higher prevalence and lower parasite burdens than predicted by the null model. Together, these results suggest stochastic processes can explain aggregation patterns in neutral but not parasitic systems, though in both systems host traits affect aggregation patterns. Because the distribution of symbionts on hosts can affect symbiont evolution via intraspecific interactions, and host behavior and evolution via host–symbiont interactions, identifying the drivers of aggregation enriches our understanding of host–symbiont interactions.

Microhabitat conditions drive uncertainty of risk and shape neophobic responses in Trinidadian guppies, Poecilia reticulata.

In response to uncertain risks, prey may rely on neophobic phenotypes to reduce the costs associated with the lack of information regarding local conditions. Neophobia has been shown to be driven by information reliability, ambient risk and predator diversity, all of which shape uncertainty of risk. We similarly expect environmental conditions to shape uncertainty by interfering with information availability. In order to test how environmental variables might shape neophobic responses in Trinidadian guppies (Poecilia reticulata), we conducted an in situ field experiment of two high-predation risk guppy populations designed to determine how the 'average' and 'variance' of several environmental factors might influence the neophobic response to novel predator models and/or novel foraging patches. Our results suggest neophobia is shaped by water velocity, microhabitat complexity, pool width and depth, as well as substrate diversity and heterogeneity. Moreover, we found differential effects of the 'average' and 'variance' environmental variables on food- and predator-related neophobia. Our study highlights that assessment of neophobic drivers should consider predation risk, various microhabitat conditions and neophobia being tested. Neophobic phenotypes are expected to increase the probability of prey survival and reproductive success (i.e. fitness), and are therefore likely linked to population health and species survival. Understanding the drivers and consequences of uncertainty of risk is an increasingly pressing issue, as ecological uncertainty increases with the combined effects of climate change, anthropogenic disturbances and invasive species.

Sex and background risk influence responses to acute predation risk in Trinidadian guppies

AbstractIntraspecific sex differences in morphology, physiology, and behavior are widespread among taxa. However, despite their fundamental importance, they have been relatively understudied in the context of risk assessment. For instance, with Trinidadian guppies (Poecilia reticulata), there has been a bias toward the exclusive use of females, as males are thought to be less responsive to acute predation threats. However, there is little empirical evidence supporting this assumption. Moreover, the antipredator behavior of male guppies has been unexplored, perhaps resulting in the over-generalization of female behavior to both sexes in previous studies. Here, we conducted laboratory experiments involving wild-caught and laboratory-reared guppies. In Experiment 1, shoals of either male or female guppies from a high-predation population were tested for their response to alarm cues, novel odor, or a water control. We found that while female shoals exhibited strong antipredator responses to alarm cues and neophobic responses to novel odor, male shoals exhibited only a weak response to alarm cues and no evidence of neophobia. In Experiment 2, we exposed male and female guppies to high- or low-predation risk and then tested individuals for their responses to alarm cues, novel odor, or water control. Regardless of background risk, males did not respond to any stimulus. In contrast, low-risk females exhibited antipredator responses toward alarm cues and those from high background risk displayed neophobia. Our results suggest that females are more cautious when encountering an acute predation risk, highlighting the importance of accounting for both sexes in studies on predation.

The quest for good genes: Epigamic traits, fitness, MHC and multilocus heterozygosity in the guppy.

The 'good genes' hypothesis for the evolution of male secondary sexual traits poses that female preferences for such traits are driven by indirect genetic benefits. However, support for the hypothesis remains ambiguous, and, in particular, the genetic basis for the benefits has rarely been investigated. Here, we use seminatural populations of Trinidadian guppies to investigate whether sexually selected traits (orange, black and iridescent colouration, gonopodium length and body size) predict fitness measured as the number of grandoffspring, a metric that integrates across fitness components and sexes. Furthermore, we tested whether two potential sources of genetic benefits-major histocompatibility complex (MHC) genotypes and multilocus heterozygosity (MLH)-are significant predictors of fitness and of the size of sexually selected traits. We found a significant, nonlinear effect of the area of black pigmentation and male body size on the number of grandoffspring, suggesting stabilizing selection on black area, and nonlinear selection favouring small body size. MLH was heritable (h2 = 0.14) and significantly predicted the number of grandoffspring, indicating the potential for genetic benefits based on heterozygosity. We also found support for local heterozygosity effects, which may reflect a noneven distribution of genetic load across the genome. MHC genotype was not significantly associated with any tested fitness component, or with the load of Gyrodactylus parasites. Neither MHC nor MLH was significant predictor of sexually selected traits. Overall, our results highlight the role of heterozygosity in determining fitness, but do not provide support for male sexually selected traits being indicators of genetic quality.

Temperature and turbidity interact synergistically to alter anti-predator behaviour in the Trinidadian guppy.

Due to climate change, freshwater habitats are facing increasing temperatures and more extreme weather that disrupts water flow. Together with eutrophication and sedimentation from farming, quarrying and urbanization, freshwaters are becoming more turbid as well as warmer. Predators and prey need to be able to respond to one another adaptively, yet how changes in temperature and turbidity interact to affect predator-prey behaviour remains unexplored. Using a fully factorial design, we tested the combined effects of increased temperature and turbidity on the behaviour of guppy shoals (Poecilia reticulata) in the presence of one of their natural cichlid predators, the blue acara (Andinoacara pulcher). Our results demonstrate that the prey and predator were in closest proximity in warmer, turbid water, with an interaction between these stressors showing a greater than additive effect. There was also an interaction between the stressors in the inter-individual distances between the prey, where shoal cohesion increased with temperature in clear water, but decreased when temperature increased in turbid water. The closer proximity to predators and reduction in shoaling in turbid, warmer water may increase the risk of predation for the guppy, suggesting that the combined effects of elevated temperature and turbidity may favour predators rather than prey.

How to generate and test hypotheses about colour: insights from half a century of guppy research.

Coloration facilitates evolutionary investigations in nature because the interaction between genotype, phenotype and environment is relatively accessible. In a landmark set of studies, Endler addressed this complexity by demonstrating that the evolution of male Trinidadian guppy coloration is shaped by the local balance between selection for mate attractiveness versus crypsis. This became a textbook paradigm for how antagonistic selective pressures may determine evolutionary trajectories in nature. However, recent studies have challenged the generality of this paradigm. Here, we respond to these challenges by reviewing five important yet underappreciated factors that contribute to colour pattern evolution: (i) among-population variation in female preference and correlated variation in male coloration, (ii) differences in how predators versus conspecifics view males, (iii) biased assessment of pigmentary versus structural coloration, (iv) the importance of accounting for multi-species predator communities, and (v) the importance of considering the multivariate genetic architecture and multivariate context of selection and how sexual selection encourages polymorphic divergence. We elaborate these issues using two challenging papers. Our purpose is not to criticize but to point out the potential pitfalls in colour research and to emphasize the depth of consideration necessary for testing evolutionary hypotheses using complex multi-trait phenotypes such as guppy colour patterns.

Males show their best side revisited – Effects of predation pressure on laterality in wild guppies

AbstractThe ability to detect and avoid predators has been suggested as one of the main drivers for behavioral lateralization. This is supported by studies reporting that animals from high‐predation environments are more lateralized than those from low‐predation environments. Some studies, however, have shown no effect of predator regime on lateralization. Lateralized behavior can also be driven by phenotypic asymmetry, where the more attractive side of the body is preferentially displayed during male–female interaction and courtship. The importance of fluctuating asymmetry for mate choice has been highly debated for a number of reasons. Here, we revisited the concepts of predator‐induced behavioral lateralization and phenotypic asymmetry using wild Trinidadian guppies Poecilia reticulata from three different stream systems. Using fish collected from both high‐ and low‐predation environments, we quantified behavioral lateralization in terms of directional turning bias, measured right–left body color asymmetry, and investigated whether a male side‐showing preference was present in male–female interaction trials. We found that guppies were, at best, moderately lateralized on average (across all populations), without any general effect of predator regime. There were some slight stream‐dependent side biases in color asymmetry, but this did not translate into a side‐showing preference in any of the populations in the interaction trials. Some significant observed effects align with previously published results, but these were dependent on stream‐origin and were not repeated across different experiments, complicating interpretation. We conclude that when investigating the effects of predation regime in general, and such effects on behavioral lateralization or fluctuating asymmetry in particular, attention must be focused toward several factors such as experimental assay used and population origin, and broad generalizations from results stemming from experiments including only one population should be avoided.

Female preference for rare males is maintained by indirect selection in Trinidadian guppies

When females prefer mates with rare phenotypes, sexual selection can maintain rather than deplete genetic variation. However, there is no consensus on why this widespread and frequently observed preference might evolve and persist. We examine the fitness consequences of female preference for rare male color patterns in a natural population of Trinidadian guppies, using a pedigree that spans 10 generations. We demonstrate (i) a rare male reproductive advantage, (ii) that females that mate with rare males gain an indirect fitness advantage through the mating success of their sons, and (iii) the fitness benefit that females accrue through their "sexy sons" evaporates for their grandsons as their phenotype becomes common. Counter to prevailing theory, we show that female preference can be maintained through indirect selection.

Female foraging strategy co-evolves with sexual harassment intensity in the Trinidadian guppy

Abstract Sexual harassment is a widespread evolutionary outcome of sexual conflict over mating rates. Male harassment can impose costs on females, and females often change their behaviors to avoid unwanted attention. In Trinidadian guppies (Poecilia reticulata), males use either sneak mating behavior or courtship displays as reproductive tactics. Both behaviors can be sources of sexual harassment, but sneak behavior is likely more harmful. Males adapted to low-predation habitats use more courtship and fewer sneak tactics than their high-predation ancestors. Here, we tested whether female foraging strategy co-evolves with less severe male harassment as guppies colonize low-predation environments. We set up outdoor stream mesocosms with common-garden-reared males and females from either a high- or a low-predation population in a 2 × 2 design, and tested whether populations diverge in female response to male harassment. We found that both sneak behavior and courtship display reduced female foraging, but the effect of sneak behavior was more extensive. Furthermore, the negative effect of sneak behavior was more pronounced on high-predation females. Our results suggest that female foraging strategy coevolved with divergence in male mating strategy: females under more severe sexual harassment evolved a foraging strategy that is more sensitive to varying harassment levels.

Does the Evolution of Ontogenetic Niche Shifts Favor Species Coexistence? An empirical test in Trinidadian streams.

A major question in ecology is how often competing species evolve to reduce competitive interactions and facilitate coexistence. One untested route for a reduction in competitive interactions is through ontogenetic changes in the trophic niche of one or more of the interacting species. In such cases, theory predicts that two species can coexist if the weaker competitor changes its resource niche to a greater degree with increased body size than the superior competitor. We tested this prediction using stable isotopes that yield information about the trophic position (δ15 N) and carbon source (δ13 C) of two coexisting fish species: Trinidadian guppies (Poecilia reticulata) and killifish (Rivulus hartii). We examined fish from locations representing three natural community types: 1) where killifish and guppies live with predators; 2) where killifish and guppies live without predators; and 3) where killifish are the only fish species. We also examined killifish from communities in which we had introduced guppies, providing a temporal sequence of the community changes following the transition from a killifish only to a killifish-guppy community. We found that killifish, which are the weaker competitor, had a much larger ontogenetic niche shift in trophic position than guppies in the community where competition is most intense (killifish-guppy only). This result is consistent with theory for size-structured populations, which predicts that these results should lead to stable coexistence of the two species. Comparisons with other communities containing guppies, killifish and predators and ones where killifish live by themselves revealed that these results are caused primarily by a loss of ontogenetic niche changes in guppies, even though they are the stronger competitor. Comparisons of these natural communities with communities in which guppies were translocated into sites containing only killifish showed that the experimental communities were intermediate between the natural killifish-guppy community and the killifish-guppy-predator community, suggesting contemporary evolution in these ontogenetic trophic differences. These results provide comparative evidence for ontogenetic niche shifts in contributing to species coexistence and comparative and experimental evidence for evolutionary or plastic changes in ontogenetic niche shifts following the formation of new communities.

Exploring the effects of anthropogenic disturbance on predator inspection activity in Trinidadian guppies.

Exploring the effects of anthropogenic disturbance on predator inspection activity in Trinidadian guppies.