Population Regulation and Density-Dependent Demography in the Trinidadian Guppy.

AbstractClassic theory for density-dependent selection for delayed maturation requires that a population be regulated through some combination of adult fecundity and/or juvenile survival. We tested whether those demographic conditions were met in four experimental populations of Trinidadian guppies in which delayed maturation of males evolved when the densities of those populations became high. We used monthly mark-recapture data to examine population dynamics and demography in these populations. Three of the four populations displayed clear evidence of regulation. In all four populations, monthly adult survival rates were independent of biomass density or actually increased with increased biomass density. Juvenile recruitment, which is a combination of adult fecundity and juvenile survival, decreased as biomass density increased in all four populations. Demography showed marked seasonality, with greater survival and higher recruitment in the dry season than the wet season. Population regulation via juvenile recruitment supports the hypothesis that density-dependent selection was responsible for the evolution of delayed maturity in males. This body of work represents one of the few complete tests of density-dependent selection theory.

Size-Dependent Intraguild Predation, Cannibalism, and Resource Allocation Determine the Outcome of Species Coexistence.

AbstractIntraguild predation (IGP), a system in which species compete for resources and prey on each other, is more common than existing theory predicts. In theory, an IG predator and its prey can coexist if the IG predator is a weaker competitor for a shared resource and the predator directly benefits from consuming the prey. However, many species that are IG predators also consume members of their own species (cannibalism). Here, we ask whether cannibalism can help resolve the paradox of IGP systems. Our approach differs from previous work on IGP and cannibalism by explicitly considering the size dependence of predatory interactions and how the benefits of predation are allocated to survival, growth, and fecundity of the predator or cannibal. Our results show that cannibalism facilitates coexistence under conditions that are opposite of those predicted by standard IGP theory: species can coexist when the cannibal is a better competitor on the shared resources, directly benefits little from consuming conspecifics, and allocates resources from predation more toward growth and fecundity over survival. Because the effects of IGP and cannibalism are opposite, when an IGP predator is also a cannibal, coexistence between the IGP predator and its prey is not possible and instead depends on the operation of other coexistence mechanisms (e.g., resource partitioning). These results point to the importance of understanding the relative rates of IGP and cannibalism as well as the resource allocation strategy of the IG predator in determining the likelihood of species coexistence.

Experimental evolution of dispersal: Unifying theory, experiments and natural systems.

Dispersal is a central life history trait that affects the ecological and evolutionary dynamics of populations and communities. The recent use of experimental evolution for the study of dispersal is a promising avenue for demonstrating valuable proofs of concept, bringing insight into alternative dispersal strategies and trade-offs, and testing the repeatability of evolutionary outcomes. Practical constraints restrict experimental evolution studies of dispersal to a set of typically small, short-lived organisms reared in artificial laboratory conditions. Here, we argue that despite these restrictions, inferences from these studies can reinforce links between theoretical predictions and empirical observations and advance our understanding of the eco-evolutionary consequences of dispersal. We illustrate how applying an integrative framework of theory, experimental evolution and natural systems can improve our understanding of dispersal evolution under more complex and realistic biological scenarios, such as the role of biotic interactions and complex dispersal syndromes.

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.

Does the evolution of ontogenetic niche shifts favour 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.

Pathways to global-change effects on biodiversity: new opportunities for dynamically forecasting demography and species interactions.

In structured populations, persistence under environmental change may be particularly threatened when abiotic factors simultaneously negatively affect survival and reproduction of several life cycle stages, as opposed to a single stage. Such effects can then be exacerbated when species interactions generate reciprocal feedbacks between the demographic rates of the different species. Despite the importance of such demographic feedbacks, forecasts that account for them are limited as individual-based data on interacting species are perceived to be essential for such mechanistic forecasting-but are rarely available. Here, we first review the current shortcomings in assessing demographic feedbacks in population and community dynamics. We then present an overview of advances in statistical tools that provide an opportunity to leverage population-level data on abundances of multiple species to infer stage-specific demography. Lastly, we showcase a state-of-the-art Bayesian method to infer and project stage-specific survival and reproduction for several interacting species in a Mediterranean shrub community. This case study shows that climate change threatens populations most strongly by changing the interaction effects of conspecific and heterospecific neighbours on both juvenile and adult survival. Thus, the repurposing of multi-species abundance data for mechanistic forecasting can substantially improve our understanding of emerging threats on biodiversity.

The evolution of size-dependent competitive interactions promotes species coexistence.

Theory indicates that competing species coexist in a community when intraspecific competition is stronger than interspecific competition. When body size determines the outcome of competitive interactions between individuals, coexistence depends also on how resource use and the ability to compete for these resources change with body size. Testing coexistence theory in size-structured communities, therefore, requires disentangling the effects of size-dependent competitive abilities and niche shifts. Here, we tested the hypothesis that the evolution of species- and size-dependent competitive asymmetries increased the likelihood of coexistence between interacting species. We experimentally estimated the effects of size-dependent competitive interactions on somatic growth rates of two interacting fish species, Trinidadian guppies Poecilia reticulata and killifish Rivulus hartii. We controlled for the effects of size-dependent changes in the niche at two competitive settings representing the early (allopatric) and late (sympatric) evolutionary stages of a killifish-guppy community. We fitted the growth data to a model that incorporates species- and size-dependent competitive asymmetries to test whether changes in the competitive interactions across sizes increased the likelihood of species coexistence from allopatry to sympatry. We found that guppies are competitively superior to killifish but were less so in sympatric populations. The decrease in the effects of interspecific competition on the fitness of killifish and increase in the interspecific effect on guppies' fitness increased the likelihood that sympatric guppies and killifish will coexist. However, while the competitive asymmetries between the species changed consistently between allopatry and sympatry between drainages, the magnitude of the size-dependent competitive asymmetries varied between drainages. These results demonstrate the importance of integrating evolution and trait-based interactions into the research on how species coexist.

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.

Towards a more precise - and accurate - view of eco-evolution.

Over the past 15 years, the number of papers focused on 'eco-evo dynamics' has increased exponentially (Figure 1). This pattern suggests the rapid growth of a new, integrative discipline. We argue this overstates the case. First, the terms 'eco-evo dynamics' and 'eco-evo interactions' are used too imprecisely. As a result, many studies that claim to describe eco-evo dynamics are actually describing basic ecological or evolutionary processes. Second, these terms are often used as if the study of how ecological and evolutionary processes are intertwined is novel when, in fact, it is not. The result is confusion over what the term 'eco-evolution' and its derivatives describe. We advocate a more precise definition of eco-evolution that is more useful in efforts to understand and characterise the diversity of ecological and evolutionary processes and that focuses attention on the subset of those processes that occur only when ecological and evolutionary timescales are comparable. [Figure: see text].

Environmental Change, If Unaccounted, Prevents Detection of Cryptic Evolution in a Wild Population.

AbstractDetecting contemporary evolution requires demonstrating that genetic change has occurred. Mixed effects models allow estimation of quantitative genetic parameters and are widely used to study evolution in wild populations. However, predictions of evolution based on these parameters frequently fail to match observations. Here, we applied three commonly used quantitative genetic approaches to predict the evolution of size at maturity in a wild population of Trinidadian guppies. Crucially, we tested our predictions against evolutionary change observed in common-garden experiments performed on samples from the same population. We show that standard quantitative genetic models underestimated or failed to detect the cryptic evolution of this trait as demonstrated by the common-garden experiments. The models failed because (1) size at maturity and fitness both decreased with increases in population density, (2) offspring experienced higher population densities than their parents, and (3) selection on size was strongest at high densities. When we accounted for environmental change, predictions better matched observations in the common-garden experiments, although substantial uncertainty remained. Our results demonstrate that predictions of evolution are unreliable if environmental change is not appropriately captured in models.

On the Origin of Coexisting Species.

Speciation is frequently initiated but rarely completed, a phenomenon hypothesized to arise due to the failure of nascent lineages to persist. Although a failure to persist often has ecological causes, key gaps exist between ecological and evolutionary theories that, if filled, would clarify when and why speciation succeeds or fails. Here, we apply ecological coexistence theory to show how the alignment between different forms of niche opportunity and niche use shape the initiation, progression, and completion of speciation. Niche evolution may drive coexistence or competitive exclusion, and an ability to coexist ecologically may help or hinder speciation. Our perspective allows progress towards unifying the origin and maintenance of species diversity across the tree of life.

Novel parasite invasion leads to rapid demographic compensation and recovery in an experimental population of guppies.

The global movement of pathogens is altering populations and communities through a variety of direct and indirect ecological pathways. The direct effect of a pathogen on a host is reduced survival, which can lead to decreased population densities. However, theory also suggests that increased mortality can lead to no change or even increases in the density of the host. This paradoxical result can occur in a regulated population when the pathogen's negative effect on survival is countered by increased reproduction at the lower density. Here, we analyze data from a long-term capture-mark-recapture experiment of Trinidadian guppies (Poecilia reticulata) that were recently infected with a nematode parasite (Camallanus cotti). By comparing the newly infected population with a control population that was not infected, we show that decreases in the density of the infected guppy population were transient. The guppy population compensated for the decreased survival by a density-dependent increase in recruitment of new individuals into the population, without any change in the underlying recruitment function. Increased recruitment was related to an increase in the somatic growth of uninfected fish. Twenty months into the new invasion, the population had fully recovered to preinvasion densities even though the prevalence of infection of fish in the population remained high (72%). These results show that density-mediated indirect effects of novel parasites can be positive, not negative, which makes it difficult to extrapolate to how pathogens will affect species interactions in communities. We discuss possible hypotheses for the rapid recovery.

Individual differences determine the strength of ecological interactions.

Biotic interactions are central to both ecological and evolutionary dynamics. In the vast majority of empirical studies, the strength of intraspecific interactions is estimated by using simple measures of population size. Biologists have long known that these are crude metrics, with experiments and theory suggesting that interactions between individuals should depend on traits, such as body size. Despite this, it has been difficult to estimate the impact of traits on competitive ability from ecological field data, and this explains why the strength of biotic interactions has empirically been treated in a simplistic manner. Using long-term observational data from four different populations, we show that large Trinidadian guppies impose a significantly larger competitive pressure on conspecifics than individuals that are smaller; in other words, competition is asymmetric. When we incorporate this asymmetry into integral projection models, the predicted size structure is much closer to what we see in the field compared with models where competition is independent of body size. This difference in size structure translates into a twofold difference in reproductive output. This demonstrates how the nature of ecological interactions drives the size structure, which, in turn, will have important implications for both the ecological and evolutionary dynamics.

Metabolic Rate Interacts with Resource Availability to Determine Individual Variation in Microhabitat Use in the Wild.

Ecological pressures such as competition can lead individuals within a population to partition resources or habitats, but the underlying intrinsic mechanisms that determine an individual's resource use are not well understood. Here we show that an individual's own energy demand and associated competitive ability influence its resource use, but only when food is more limiting. We tested whether intraspecific variation in metabolic rate leads to microhabitat partitioning among juvenile Atlantic salmon (Salmo salar) in natural streams subjected to manipulated nutrient levels and subsequent per capita food availability. We found that individual salmon from families with a higher baseline (standard) metabolic rate (which is associated with greater competitive ability) tended to occupy faster-flowing water, but only in streams with lower per capita food availability. Faster-flowing microhabitats yield more food, but high metabolic rate fish only benefited from faster growth in streams with high food levels, presumably because in low-food environments the cost of a high metabolism offsets the benefits of acquiring a productive microhabitat. The benefits of a given metabolic rate were thus context dependent. These results demonstrate that intraspecific variation in metabolic rate can interact with resource availability to determine the spatial structuring of wild populations.

Upper thermal limits are repeatable in Trinidadian guppies.

Measurements of thermal tolerance are critical for predicting species vulnerability to climate change. Critical thermal maximum (CTmax) is a measure of an animal's upper thermal tolerance, but there is limited evidence for how repeatable it is within individuals over time. We measured the CTmax of Trinidadian guppies (Poecilia reticulata) across six consecutive trials, each a week apart. The repeatability of CTmax over six trials was 0.43 (0.26-0.62). However, CTmax also changed over time, ranging from 39.0 to 39.6 °C and increasing by 0.6 °C across the first four trials before leveling off. This is most likely the effect of heat hardening, indicating that thermal tolerance can increase after repeated exposure to extreme heat events.

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.

Competitive asymmetry and local adaptation in Trinidadian guppies.

The outcome of competition between individuals often depends on body size. These competitive asymmetries can drive variation in demographic rates, influencing the ecology and evolution of life histories. The magnitude and direction of such asymmetries differ among taxa, yet little is known empirically about how adaptation to resource limitation alters competitive asymmetries. Here, we investigate the relationship between size-dependent competitive ability and adaptation to resource limitation. We examined size-dependent competition in two ecotypes of Trinidadian guppy, adapted to high or low levels of resource competition. Using aquaria-based competition experiments, we describe how the size and ecotype of competitors influence somatic growth rate, whilst controlling for the confounding effect of niche differentiation. We replicated our study across two independent evolutionary origins of the "competitive" ecotype. The two "competitive" ecotypes differed markedly in size-dependent asymmetry, indicating that adaptation to resource limitation alone is insufficient to explain changes in size-dependent competitive asymmetry. For one origin, the ecotype adapted to resource limitation was a superior competitor over a wide range of size pairings. The equivalence of competitors varied over fivefold, dependent on size and ecotype; in three of four populations, larger individuals had a competitive advantage. Our results demonstrate that competitive asymmetry has strong effects on somatic growth. Because somatic growth contributes to demographic parameters, intraspecific trait variation is likely to play a key role in regulating demographic rates. Our findings imply that the evolution of size-dependent asymmetries under conditions of intense competition is likely to be constrained by niche availability, although further research is needed to verify this.

Nutrients from salmon parents alter selection pressures on their offspring.

Organisms can modify their surrounding environment, but whether these changes are large enough to feed back and alter their evolutionary trajectories is not well understood, particularly in wild populations. Here we show that nutrient pulses from decomposing Atlantic salmon (Salmo salar) parents alter selection pressures on their offspring with important consequences for their phenotypic and genetic diversity. We found a strong survival advantage to larger eggs and faster juvenile metabolic rates in streams lacking carcasses but not in streams containing this parental nutrient input. Differences in selection intensities led to significant phenotypic divergence in these two traits among stream types. Stronger selection in streams with low parental nutrient input also decreased the number of surviving families compared to streams with high parental nutrient levels. Observed effects of parent-derived nutrients on selection pressures provide experimental evidence for key components of eco-evolutionary feedbacks in wild populations.

Predicting coexistence in species with continuous ontogenetic niche shifts and competitive asymmetry.

A longstanding problem in ecology is whether structured life cycles impede or facilitate coexistence between species. Theory based on populations with only two discrete stages in the life-cycle indicates that for two species to coexist, at least one must shift its niche between stages and each species must be a better competitor in one of the niches. However, in many cases, niche shifts are associated with changes in an underlying continuous trait like body size and we have few predictions concerning conditions for coexistence for such a widespread form of ontogenetic development. We develop a framework for analyzing species coexistence based on Integral Projection Models (IPMs) that incorporates continuous ontogenetic changes in both the resource niche and competitive ability. We parameterize the model using experimental data from Trinidadian guppies and show how niche shifts and competitive symmetries impact species coexistence. Overall, our results show that the effects of competition on fitness depend upon trait-mediated niche-separation, trait-mediated competitive asymmetry in the part of the niche that is shared across body sizes, and the sensitivity of fitness to body size. Interactions among these processes generate multiple routes to coexistence. We discuss how our modeling framework expands results from two-stage models to mutli-stage or continuous stage models and allows for deriving predictions that can be tested in populations displaying continuous changes in niche use and competitive ability.

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.