The experimental range extension of guppies (Poecilia reticulata) influences the metabolic activity of tropical streams.

The ecological consequences of biological range extensions reflect the interplay between the functional characteristics of the newly arrived species and their recipient ecosystems. Teasing apart the relative contribution of each component is difficult because most colonization events are studied retrospectively, i.e., after a species became established and its consequences apparent. We conducted a prospective experiment to study the ecosystem consequences of a consumer introduction, using whole-stream metabolism as our integrator of ecosystem activity. In four Trinidadian streams, we extended the range of a native fish, the guppy (Poecilia reticulata), by introducing it over barrier waterfalls that historically excluded it from these upper reaches. To assess the context dependence of these range extensions, we thinned the riparian forest canopy on two of these streams to increase benthic algal biomass and productivity. Guppy's range extension into upper stream reaches significantly impacted stream metabolism but the effects depended upon the specific stream into which they had been introduced. Generally, increases in guppy biomass caused an increase in gross primary production (GPP) and community respiration (CR). The effects guppies had on GPP were similar to those induced by increased light level and were larger in strength than the effects stream stage had on CR. These results, combined with results from prior experiments, contribute to our growing understanding of how consumers impact stream ecosystem function when they expand their range into novel habitats. Further study will reveal whether local adaptation, known to occur rapidly in these guppy populations, modifies the ecological consequences of this species introduction.

Predation risk shapes the degree of placentation in natural populations of live-bearing fish.

The placenta is a complex life-history trait that is ubiquitous across the tree of life. Theory proposes that the placenta evolves in response to high performance-demanding conditions by shifting maternal investment from pre- to post-fertilisation, thereby reducing a female's reproductive burden during pregnancy. We test this hypothesis by studying populations of the fish species Poeciliopsis retropinna in Costa Rica. We found substantial variation in the degree of placentation among natural populations associated with predation risk: females from high predation populations had significantly higher degrees of placentation compared to low predation females, while number, size and quality of offspring at birth remained unaffected. Moreover, a higher degree of placentation correlated with a lower reproductive burden and hence likely an improved swimming performance during pregnancy. Our study advances an adaptive explanation for why the placenta evolves by arguing that an increased degree of placentation offers a selective advantage in high predation environments.

Eco-Evolutionary Feedbacks Predict the Time Course of Rapid Life-History Evolution.

Organisms can change their environment and in doing so change the selection they experience and how they evolve. Population density is one potential mediator of such interactions because high population densities can impact the ecosystem and reduce resource availability. At present, such interactions are best known from theory and laboratory experiments. Here we quantify the importance of such interactions in nature by transplanting guppies from a stream where they co-occur with predators into tributaries that previously lacked both guppies and predators. If guppies evolve solely because of the immediate reduction in mortality rate, the strength of selection and rate of evolution should be greatest at the outset and then decline as the population adapts to its new environment. If indirect effects caused by the increase in guppy population density in the absence of predation prevail, then there should be a lag in guppy evolution because time is required for them to modify their environment. The duration of this lag is predicted to be associated with the environmental modification caused by guppies. We observed a lag in life-history evolution associated with increases in population density and altered ecology. How guppies evolved matched predictions derived from evolutionary theory that incorporates such density effects.

Landscape patterns in top-down control of decomposition: omnivory disrupts a tropical detrital-based trophic cascade.

Detrital-based trophic cascades are often considered weak or absent in tropical stream ecosystems because of the prevalence of omnivorous macroconsumers and the dearth of leaf-shredding insects. In this study, we isolate top-down effects of three macroconsumer species on detrital processing in headwater streams draining Trinidad's northern mountains. We separated effects of different macroconsumers by experimentally manipulating their temporal access to isolated benthic habitat over the diel cycle. We found no evidence that omnivorous macroconsumers, including a freshwater crab (Eudaniela garmani) and guppy (Poecilia reticulata), increased leaf decomposition via consumption. By contrast, above a waterfall excluding guppies, the insectivorous killifish, Anablepsoides hartii, reduced the biomass of the leaf-shredding insect Phylloicus hansoni 4-fold, which consequently reduced leaf decomposition rates 1.6-fold. This detrital cascade did not occur below the barrier waterfall, where omnivorous guppies join the assemblage and reduce killifish densities; here killifish had no significant effects on Phylloicus or decomposition rates. These patterns of detrital processing were also observed in upstream-downstream comparisons in a landscape study across paired reaches of six streams. Above waterfalls, where killifish were present, but guppies absent, leaf decomposition rates and Phylloicus biomass were 2.5- and ~35-fold lower, respectively, compared to measurements below waterfalls. Moreover, the strength of top-down control by killifish is reflected by the 20- and 5-fold reductions in variability (±SE) surrounding mean Phylloicus biomass and leaf decomposition rates in upstream relative to downstream reaches where no top-down control was detected. Findings show a clear, detrital-based trophic cascade among killifish, a leaf-shredding insect, and leaf decomposition rates. Results also show how omnivorous guppies disrupt this cascade by depressing killifish densities, thereby releasing invertebrate shredders from predation, and significantly increasing decomposition rates. Moreover, this combination of direct and indirect trophic interactions drives patterns in decomposition rates in stream networks at a landscape scale, resulting in significantly lower rates of decomposition above vs. below barrier waterfalls. Our findings reveal that omnivory can result in significant indirect effects on a key ecosystem process, illustrating the importance of these hidden trophic pathways in detrital-based systems and suggesting that resource control in tropical systems may be even more complex than previously envisioned.

Predictable adaptive trajectories of sexual coloration in the wild: Evidence from replicate experimental guppy populations.

The question of whether populations evolve predictably and consistently under similar selective regimes is fundamental to understanding how adaptation proceeds in the wild. We address this question with a replicated evolution experiment focused upon male sexual coloration in guppies (Poecilia reticulata). Fish were transplanted from a single high predation population in the Guanapo River to four replicate, guppy-free low predation headwater streams. Two streams had their canopies thinned to adjust the setting under which male coloration is displayed and perceived. We assessed evolutionary divergence using second-generation lab-bred offspring of fish sampled four to six years following translocation. A prior experiment of the same design, performed in an adjacent drainage, resulted in the evolution of more extensive orange, black, and iridescent markings. We however found evidence for expansion only in structural coloration (iridescent blue/green), no change in orange, and a reduction in black. This response amplifies earlier findings for Guanapo fish, revealing that trajectories of color elaboration differ among drainages. We also found that color phenotypes evolved more greatly at the thinned-canopy sites. Our findings support the predictability of sexual trait evolution in the wild, and underscore the importance of signaling conditions and ornamental starting points in shaping adaptive trajectories.

Population variation in the trophic niche of the Trinidadian guppy from different predation regimes.

Population variation in trophic niche is widespread among organisms and is of increasing interest given its role in both speciation and adaptation to changing environments. Trinidadian guppies (Poecilia reticulata) inhabiting stream reaches with different predation regimes have rapidly evolved divergent life history traits. Here, we investigated the effects of both predation and resource availability on guppy trophic niches by evaluating their gut contents, resource standing stocks, and δ15N and δ13C stable isotopes across five streams during the wet season. We found that guppies from low predation (LP) sites had a consistently higher trophic position and proportion of invertebrates in their guts and assimilate less epilithon than guppies from high predation (HP) sites. Higher trophic position was also associated with lower benthic invertebrate availability. Our results suggest that LP guppies could be more efficient invertebrate consumers, possibly as an evolutionary response to greater intraspecific competition for higher quality food. This may be intensified by seasonality, as wet season conditions can alter resource availability, feeding rates, and the intensity of intraspecific competition. Understanding how guppy diets vary among communities is critical to elucidating the role of niche shifts in mediating the link between environmental change and the evolution of life histories.

The evolution of coexistence: Reciprocal adaptation promotes the assembly of a simple community.

Species coexistence may result by chance when co-occurring species do not strongly interact or it may be an evolutionary outcome of strongly interacting species adapting to each other. Although patterns like character displacement indicate that coexistence has often been an evolutionary outcome, it is unclear how often the evolution of coexistence represents adaptation in only one species or reciprocal adaptation among all interacting species. Here, we demonstrate a strong role for evolution in the coexistence of guppies and killifish in Trinidadian streams. We experimentally recreated the temporal stages in the invasion and establishment of guppies into communities that previously contained only killifish. We combined demographic responses of guppies and killifish with a size-based integral projection model to calculate the fitness of the phenotypes of each species in each of the stages of community assembly. We show that guppies from locally adapted populations that are sympatric with killifish have higher fitness when paired with killifish than guppies from allopatric populations. This elevated fitness involves effects traceable to both guppy and killifish evolution. We discuss the implications of our results to the study of species coexistence and how it may be mediated through eco-evolutionary feedbacks.

Fish introductions and light modulate food web fluxes in tropical streams: a whole-ecosystem experimental approach.

Decades of ecological study have demonstrated the importance of top-down and bottom-up controls on food webs, yet few studies within this context have quantified the magnitude of energy and material fluxes at the whole-ecosystem scale. We examined top-down and bottom-up effects on food web fluxes using a field experiment that manipulated the presence of a consumer, the Trinidadian guppy Poecilia reticulata, and the production of basal resources by thinning the riparian forest canopy to increase incident light. To gauge the effects of these reach-scale manipulations on food web fluxes, we used a nitrogen (15 N) stable isotope tracer to compare basal resource treatments (thinned canopy vs. control) and consumer treatments (guppy introduction vs. control). The thinned canopy stream had higher primary production than the natural canopy control, leading to increased N fluxes to invertebrates that feed on benthic biofilms (grazers), fine benthic organic matter (collector-gatherers), and organic particles suspended in the water column (filter feeders). Stream reaches with guppies also had higher primary productivity and higher N fluxes to grazers and filter feeders. In contrast, N fluxes to collector-gatherers were reduced in guppy introduction reaches relative to upstream controls. N fluxes to leaf-shredding invertebrates, predatory invertebrates, and the other fish species present (Hart's killifish, Anablepsoides hartii) did not differ across light or guppy treatments, suggesting that effects on detritus-based linkages and upper trophic levels were not as strong. Effect sizes of guppy and canopy treatments on N flux rates were similar for most taxa, though guppy effects were the strongest for filter feeding invertebrates while canopy effects were the strongest for collector-gatherer invertebrates. Combined, these results extend previous knowledge about top-down and bottom-up controls on ecosystems by providing experimental, reach-scale evidence that both pathways can act simultaneously and have equally strong influence on nutrient fluxes from inorganic pools through primary consumers.

Sex-specific local life-history adaptation in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana).

Cavefishes have long been used as model organisms showcasing adaptive diversification, but does adaptation to caves also facilitate the evolution of reproductive isolation from surface ancestors? We raised offspring of wild-caught surface- and cave-dwelling ecotypes of the neotropical fish Poecilia mexicana to sexual maturity in a 12-month common garden experiment. Fish were raised under one of two food regimes (high vs. low), and this was crossed with differences in lighting conditions (permanent darkness vs. 12:12 h light:dark cycle) in a 2 × 2 factorial design, allowing us to elucidate potential patterns of local adaptation in life histories. Our results reveal a pattern of sex-specific local life-history adaptation: Surface molly females had the highest fitness in the treatment best resembling their habitat of origin (high food and a light:dark cycle), and suffered from almost complete reproductive failure in darkness, while cave molly females were not similarly affected in any treatment. Males of both ecotypes, on the other hand, showed only weak evidence for local adaptation. Nonetheless, local life-history adaptation in females likely contributes to ecological diversification in this system and other cave animals, further supporting the role of local adaptation due to strong divergent selection as a major force in ecological speciation.

Population size-structure-dependent fitness and ecosystem consequences in Trinidadian guppies.

Decades of theory and recent empirical results have shown that evolutionary, population, community and ecosystem properties are the result of feedbacks between ecological and evolutionary processes. The vast majority of theory and empirical research on these eco-evolutionary feedbacks has focused on interactions among population size and mean traits of populations. However, numbers and mean traits represent only a fraction of the possible feedback dimensions. Populations of many organisms consist of different size classes that differ in their impact on the environment and each other. Moreover, rarely do we know the map of ecological pathways through which changes in numbers or size structure cause evolutionary change. The goal of this study was to test the role of size structure in eco-evolutionary feedbacks of Trinidadian guppies and to begin to build an eco-evolutionary map along this unexplored dimension. We used a factorial experiment in mesocosms wherein we crossed high- and low-predation guppy phenotypes with population size structure. We tested the ability of changes in size structure to generate selection on the demographic rates of guppies using an integral projection model (IPM). To understand how fitness differences among high- and low-predation phenotypes may be generated, we measured the response of the biomass of lower trophic levels and nutrient cycling to the different phenotype and size structure treatments. We found a significant interaction between guppy phenotype and the size structure treatments for absolute fitness. Size structure had a very large effect on invertebrate biomass in the mesocosms, but there was little or no effect of the phenotype. The effect of size structure on algal biomass depended on guppy phenotype, with no difference in algal biomass in populations with more, smaller guppies, but a large decrease in algal biomass in mesocosms with phenotypes adapted to low-predation risk. These results indicate an important role for size structure partially driving eco-evolutionary feedbacks in guppies. The changes in the ecosystem suggest that the absence of a steep decline in guppy fitness of the low-predation risk populations is likely due to higher consumption of algae when invertebrates are comparatively rare. Overall, these results demonstrate size structure as a possible dimension through which eco-evolutionary feedbacks may occur in natural populations.

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.

Parallelism isn't perfect: could disease and flooding drive a life-history anomaly in Trinidadian guppies?

Nonparallel evolution, where independent populations occupy similar environments but show phenotypic differences, can uncover previously ignored selective factors. We investigated a nonparallelism in the life-history strategy of a Trinidadian guppy population, a system famous for parallel adaptation to differences in predation risk. We tested the hypothesis that high mortality drives an observed fast life-history pattern (i.e., earlier maturation and more frequent reproductive events) that is atypical for a low-predation environment. Using mark-recapture techniques, we compared neighboring low-predation populations, finding significantly higher mortality rates in the population with atypical life-history traits. Mortality was elevated during the wet season, when flooding was common. Moreover, individuals from the anomalous population were more likely to transition from healthy to infected disease states. Our results stand out against previous patterns observed in this system, indicating that higher mortality caused by disease and flooding may have selected for a faster life history. Thus, we highlight that even in systems famous for parallel adaptation, variation in selective pressures can result in nonparallel phenotypic evolution.

Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies.

In semelparous populations, dormant germ banks (e.g. seeds) have been proposed as important in maintaining genotypes that are adaptive at different times in fluctuating environments. Such hidden storage of genetic diversity need not be exclusive to dormant banks. Genotype diversity may be preserved in many iteroparous animals through sperm-storage mechanisms in females. This allows males to reproduce posthumously and increase the effective sizes of seemingly female-biased populations. Although long-term sperm storage has been demonstrated in many organisms, the understanding of its importance in the wild is very poor. We here show the prevalence of male posthumous reproduction in wild Trinidadian guppies, through the combination of mark-recapture and pedigree analyses of a multigenerational individual-based dataset. A significant proportion of the reproductive population consisted of dead males, who could conceive up to 10 months after death (the maximum allowed by the length of the dataset), which is more than twice the estimated generation time. Demographic analysis shows that the fecundity of dead males can play an important role in population growth and selection.

Predator-induced phenotypic plasticity in metabolism and rate of growth: rapid adaptation to a novel environment.

Novel environments often impose directional selection for a new phenotypic optimum. Novel environments, however, can also change the distribution of phenotypes exposed to selection by inducing phenotypic plasticity. Plasticity can produce phenotypes that either align with or oppose the direction of selection. When plasticity and selection are parallel, plasticity is considered adaptive because it provides a better pairing between the phenotype and the environment. If the plastic response is incomplete and falls short of producing the optimum phenotype, synergistic selection can lead to genetic divergence and bring the phenotype closer to the optimum. In contrast, non-adaptive plasticity should increase the strength of selection, because phenotypes will be further from the local optimum, requiring antagonistic selection to overcome the phenotype-environment mismatch and facilitate adaptive divergence. We test these ideas by documenting predator-induced plasticity for resting metabolic rate and growth rate in populations of the Trinidadian guppy (Poecilia reticulata) adapted to high and low predation. We find reduced metabolic rates and growth rates when cues from a predator are present during development, a pattern suggestive of adaptive and non-adaptive plasticity, respectively. When we compared populations recently transplanted from a high-predation environment into four streams lacking predators, we found evidence for rapid adaptive evolution both in metabolism and growth rate. We discuss the implications for predicting how traits will respond to selection, depending on the type of plasticity they exhibit.

Experimental evidence for density-dependent regulation and selection on Trinidadian guppy life histories.

Recent study of feedbacks between ecological and evolutionary processes has renewed interest in population regulation and density-dependent selection because they represent black-box descriptions of these feedbacks. The roles of population regulation and density-dependent selection in life-history evolution have received a significant amount of theoretical attention, but there are few empirical examples demonstrating their importance. We address this challenge in natural populations of the Trinidadian guppy (Poecilia reticulata) that differ in their predation regimes. First, we tested whether natural populations of guppies are regulated by density dependence and quantified in which phases of the life cycle the effects of density are important. We found that guppies from low-predation (LP) environments are tightly regulated and that the density-dependent responses disproportionately affected some size classes. Second, we tested whether there are differences in density-dependent selection between guppies from LP or high-predation (HP) environments. We found that the fitness of HP guppies is more sensitive to the depressant effects of density than the fitness of LP guppies. Finally, we used an evolutionary invasion analysis to show that, depending on the effect of density on survival of the HP phenotype, this greater sensitivity of the HP phenotype to density can partially explain the evolution of the LP phenotype. We discuss the relevance of these findings to the study of feedbacks between ecology and evolution.

Local adaptation and the evolution of phenotypic plasticity in Trinidadian guppies (Poecilia reticulata).

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator-induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high- and low-predation environments. We reared full-siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high-predation ecotype. However, when reared in the absence of predator cues, guppies from high- and low-predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high- versus low-predation environments. Thus, divergence in plasticity is due to phenotypic differences between high- and low-predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by-product of adaptation to the derived environment.

Effects of consumer interactions on benthic resources and ecosystem processes in a neotropical stream.

The effect of consumers on their resources has been demonstrated in many systems but is often confounded by trophic interactions with other consumers. Consumers may also have behavioral and life history adaptations to each other and to co-occurring predators that may additionally modulate their particular roles in ecosystems. We experimentally excluded large consumers from tile periphyton, leaves and natural benthic substrata using submerged electrified frames in three stream reaches with overlapping consumer assemblages in Trinidad, West Indies. Concurrently, we assessed visits to (non-electrified) control frames by the three most common large consumers-primarily insectivorous killifish (Rivulus hartii), omnivorous guppies (Poecilia reticulata) and omnivorous crabs (Eudaniela garmani). Consumers caused the greatest decrease in final chlorophyll a biomass and accrual rates the most in the downstream reach containing all three focal consumers in the presence of fish predators. Consumers also caused the greatest increase in leaf decay rates in the upstream reach containing only killifish and crabs. In the downstream reach where guppies co-occur with predators, we found significantly lower benthic invertebrate biomass in control relative to exclosure treatments than the midstream reach where guppies occur in the absence of predators. These data suggest that differences in guppy foraging, potentially driven by differences in their life history phenotype, may affect ecosystem structure and processes as much as their presence or absence and that interactions among consumers may further mediate their effects in these stream ecosystems.

Life-history evolution in guppies VIII: the demographics of density regulation in guppies (Poecilia reticulata).

In prior research, we found the way guppy life histories evolve in response to living in environments with a high or low risk of predation is consistent with life-history theory that assumes no density dependence. We later found that guppies from high-predation environments experience higher mortality rates than those from low-predation environments, but the increased risk was evenly distributed across all age/size classes. Life-history theory that assumes density-independent population growth predicts that life histories will not evolve under such circumstances, yet we have shown with field introduction experiments that they do evolve. However, theory that incorporates density regulation predicts this pattern of mortality can result in the patterns of life-history evolution we had observed. Here we report on density manipulation experiments performed in populations of guppies from low-predation environments to ask whether natural populations normally experience density regulation and, if so, to characterize the short-term demographic changes that underlie density regulation. Our experiments reveal that these populations are density regulated. Decreased density resulted in higher juvenile growth, decreased juvenile mortality rates, and increased reproductive investment by adult females. Increased density causes reduced offspring size, decreased fat storage by adult females, and increased adult mortality.

Convergence of life-history phenotypes in a Trinidadian killifish (Rivulus hartii).

Convergent evolution is characterized by the independent evolution of similar phenotypes within similar selective environments. Previous work on Trinidadian killifish, Rivulus hartii, demonstrated repeatable life-history differences across communities that differ in predation intensity. These studies were performed in rivers located on the south slope of Trinidad's Northern Range Mountains. There exists a parallel series of rivers on the north slope of these mountains. As on the south slope, Rivulus is found across a gradient of fish predation. However, the predatory fish species in north-slope rivers are derived from marine families, whereas south-slope rivers contain a predatory fish fauna characteristic of the South American mainland. If predator-induced mortality and the associated indirect effects are the causal factors selecting for life-history patterns in Rivulus, and these are similar in north- and south-slope rivers, then the specific predatory species should be interchangeable and we would expect convergence of life-history phenotypes across slopes. Here, we characterize the life-history phenotypes of Rivulus from north-slope communities by measuring number of eggs, egg weight, reproductive allotment, reproductive tissue weight, and size at maturity. We find similar patterns of life-history divergence across analogous predator communities. Between slopes, minor differences in Rivulus life-history traits exist and one potential cause of these differences is the abundance of Macrobrachium prawns in north-slope rivers.

Experimentally induced life-history evolution in a killifish in response to the introduction of guppies.

Life-history theory predicts that increased predation on juvenile age/size-classes favors delayed maturation and decreased reproductive investment. Although this theory has received correlative support, experimental tests in nature are rare. In 1976 and 1981, guppies (Poecilia reticulata) were transplanted into localities that previously only contained a killifish, Rivulus hartii. This situation presents an opportunity to experimentally test this life-history prediction because guppies prey upon young Rivulus. We evaluated the response to selection in Rivulus by measuring phenotypic and genotypic divergence between introduction and upstream "control" localities that lack guppies. Contrary to expectations, Rivulus from the introduction sites evolved earlier maturation and increased reproductive investment within 25 years. Such evolutionary changes parallel previous investigations on natural communities of Rivulus, but do not comply with predictions of age/size-specific theory. Guppies also caused reduced densities and increased growth rates of Rivulus, which are hypothesized indirect effects of predation. Additional life-history theories show that changes in density and growth can interact with predator-induced mortality to alter the predicted trajectory of evolution. We discuss how these latter frameworks improve the fit between theory and evolution in Rivulus.