Michael C. Marshall

Local adaptation in Trinidadian guppies alters ecosystem processes

Theory suggests evolutionary change can significantly influence and act in tandem with ecological forces via ecological-evolutionary feedbacks. This theory assumes that significant evolutionary change occurs over ecologically relevant timescales and that phenotypes have differential effects on the environment. Here we test the hypothesis that local adaptation causes ecosystem structure and function to diverge. We demonstrate that populations of Trinidadian guppies (Poecilia reticulata), characterized by differences in phenotypic and population-level traits, differ in their impact on ecosystem properties. We report results from a replicated, common garden mesocosm experiment and show that differences between guppy phenotypes result in the divergence of ecosystem structure (algal, invertebrate, and detrital standing stocks) and function (gross primary productivity, leaf decomposition rates, and nutrient flux). These phenotypic effects are further modified by effects of guppy density. We evaluated the generality of these effects by replicating the experiment using guppies derived from two independent origins of the phenotype. Finally, we tested the ability of multiple guppy traits to explain observed differences in the mesocosms. Our findings demonstrate that evolution can significantly affect both ecosystem structure and function. The ecosystem differences reported here are consistent with patterns observed across natural streams and argue that guppies play a significant role in shaping these ecosystems.

Experimental evaluation of evolution and coevolution as agents of ecosystem change in Trinidadian streams.

Evolution has been shown to be a critical determinant of ecological processes in some systems, but its importance relative to traditional ecological effects is not well known. In addition, almost nothing is known about the role of coevolution in shaping ecosystem function. Here, we experimentally evaluated the relative effects of species invasion (a traditional ecological effect), evolution and coevolution on ecosystem processes in Trinidadian streams. We manipulated the presence and population-of-origin of two common fish species, the guppy (Poecilia reticulata) and the killifish (Rivulus hartii). We measured epilithic algal biomass and accrual, aquatic invertebrate biomass, and detrital decomposition. Our results show that, for some ecosystem responses, the effects of evolution and coevolution were larger than the effects of species invasion. Guppy evolution in response to alternative predation regimes significantly influenced algal biomass and accrual rates. Guppies from a high-predation site caused an increase in algae relative to guppies from a low-predation site; algae effects were probably shaped by observed divergence in rates of nutrient excretion and algae consumption. Rivulus–guppy coevolution significantly influenced the biomass of aquatic invertebrates. Locally coevolved populations reduced invertebrate biomass relative to non-coevolved populations. These results challenge the general assumption that intraspecific diversity is a less critical determinant of ecosystem function than is interspecific diversity. Given existing evidence for contemporary evolution in these fish species, our findings suggest considerable potential for eco-evolutionary feedbacks to operate as populations adapt to natural or anthropogenic perturbations.

Direct and Indirect Ecosystem Effects of Evolutionary Adaptation in the Trinidadian Guppy (Poecilia reticulata)

Ecological and evolutionary processes may interact on the same timescale, but we are just beginning to understand how. Several studies have examined the net effects of adaptive evolution on ecosystem properties. However, we do not know whether these effects are confined to direct interactions or whether they propagate further through indirect ecological pathways. Even less well understood is how the combination of direct and indirect ecological effects of the phenotype promotes or inhibits evolutionary change. We coupled mesocosm experiments and ecosystem modeling to evaluate the ecological effects of local adaptation in Trinidadian guppies (Poecilia reticulata). The experiments show that guppies adapted to life with and without predators alter the ecosystem directly through differences in diet. The ecosystem model reveals that the small total indirect effect of the phenotype observed in the experiments is likely a combination of several large indirect effects that act in opposing directions. The model further suggests that these indirect effects can reverse the direction of selection that direct effects alone exert back on phenotypic variation. We conclude that phenotypic divergence can have major effects deep in the web of indirect ecological interactions and that even small total indirect effects can radically change the dynamics of adaptation.

Flow, nutrients, and light availability influence Neotropical epilithon biomass and stoichiometry

Abstract.  Light, nutrient availability, and flow are strong factors controlling the elemental composition and biomass of epilithon in temperate stream ecosystems. However, comparatively little is known about these relationships in tropical streams. We investigated how gradients of light and nutrient availability, seasonality, and habitat influenced epilithon biomass, chlorophyll a, and nutrient ratios in montane streams of Trinidad, West Indies. We sampled 4 focal tributaries of a single river, 2 of which had canopies experimentally thinned, every other month over a 2-y period to observe temporal dynamics and light effects on epilithon. We also sampled 18 sites across Trinidads Northern Range Mountains once each in a wet and dry season to examine the effects of naturally occurring differences in light and dissolved nutrient availability on epilithic characteristics. We found greater chlorophyll a concentrations in habitats with greater light availability, but the effect of light on epilithon stoichiometry differed between the site-survey and focal-tributary data. In general, epilithic C∶nutrient ratios decreased with increasing dissolved nutrient concentrations, but relationships between nutrient availability and biomass probably were obscured by naturally high dissolved N and P concentrations in many of the streams. Season and habitat type had profound effects on epilithon variables. Biomass and % C generally decreased in riffles and under wet-season conditions. These results suggest multiple controls for the quantity and quality of stream epilithon and have important implications for in-stream consumers.

Environmental and organismal predictors of intraspecific variation in the stoichiometry of a neotropical freshwater fish.

The elemental composition of animals, or their organismal stoichiometry, is thought to constrain their contribution to nutrient recycling, their interactions with other animals, and their demographic rates. Factors that affect organismal stoichiometry are generally poorly understood, but likely reflect elemental investments in morphological features and life history traits, acting in concert with the environmental availability of elements. We assessed the relative contribution of organismal traits and environmental variability to the stoichiometry of an insectivorous Neotropical stream fish, Rivulus hartii. We characterized the influence of body size, life history phenotype, stage of maturity, and environmental variability on organismal stoichiometry in 6 streams that differ in a broad suite of environmental variables. The elemental composition of R. hartii was variable, and overlapped with the wide range of elemental composition documented across freshwater fish taxa. Average %P composition was ∼3.2%(±0.6), average %N∼10.7%(±0.9), and average %C∼41.7%(±3.1). Streams were the strongest predictor of organismal stoichiometry, and explained up to 18% of the overall variance. This effect appeared to be largely explained by variability in quality of basal resources such as epilithon N∶P and benthic organic matter C∶N, along with variability in invertebrate standing stocks, an important food source for R. hartii. Organismal traits were weak predictors of organismal stoichiometry in this species, explaining when combined up to 7% of the overall variance in stoichiometry. Body size was significantly and positively correlated with %P, and negatively with N∶P, and C∶P, and life history phenotype was significantly correlated with %C, %P, C∶P and C∶N. Our study suggests that spatial variability in elemental availability is more strongly correlated with organismal stoichiometry than organismal traits, and suggests that the stoichiometry of carnivores may not be completely buffered from environmental variability. We discuss the relevance of these findings to ecological stoichiometry theory.

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.

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.

Local Adaptation in Trinidadian Guppies Alters Stream Ecosystem Structure at Landscape Scales despite High Environmental Variability

While previous studies have shown that evolutionary divergence alters ecological processes in small-scale experiments, a major challenge is to assess whether such evolutionary effects are important in natural ecosystems at larger spatial scales. At the landscape scale, across eight streams in the Caroni drainage, we found that the presence of locally adapted populations of guppies (Poecilia reticulata) is associated with reduced algal biomass and increased invertebrate biomass, while the opposite trends were true in streams with experimentally introduced populations of non-locally adapted guppies. Exclusion experiments conducted in two separate reaches of a single stream showed that guppies with locally adapted phenotypes significantly reduced algae with no effect on invertebrates, while non-adapted guppies had no effect on algae but significantly reduced invertebrates. These divergent effects of phenotype on stream ecosystems are comparable in strength to the effects of abiotic factors (e.g., light) known to be important drivers of ecosystem condition. They also corroborate the results of previous experiments conducted in artificial streams. Our results demonstrate that local adaptation can produce phenotypes with significantly different effects in natural ecosystems at a landscape scale, within a tropical watershed, despite high variability in abiotic factors: five of the seven physical and chemical parameters measured across the eight study streams varied by more than one order of magnitude. Our findings suggest that ecosystem structure is, in part, an evolutionary product and not simply an ecological pattern.

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.