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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 δ 15 N and δ 13 C 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.

Diverse microbial consortia profoundly influence animal biology, necessitating an understanding of microbiome variation in studies of animal adaptation. Yet, little is known about such variability among fish, in spite of their importance in aquatic ecosystems. The Trinidadian guppy, Poecilia reticulata, is an intriguing candidate to test microbiome-related hypotheses on the drivers and consequences of animal adaptation, given the recent parallel origins of a similar ecotype across streams. To assess the relationships between the microbiome and host adaptation, we used 16S rRNA amplicon sequencing to characterize gut bacteria of two guppy ecotypes with known divergence in diet, life history, physiology and morphology collected from low-predation (LP) and high-predation (HP) habitats in four Trinidadian streams. Guts were populated by several recurring, core bacteria that are related to other fish associates and rarely detected in the environment. Although gut communities of lab-reared guppies differed from those in the wild, microbiome divergence between ecotypes from the same stream was evident under identical rearing conditions, suggesting host genetic divergence can affect associations with gut bacteria. In the field, gut communities varied over time, across streams and between ecotypes in a stream-specific manner. This latter finding, along with PICRUSt predictions of metagenome function, argues against strong parallelism of the gut microbiome in association with LP ecotype evolution. Thus, bacteria cannot be invoked in facilitating the heightened reliance of LP guppies on lower-quality diets. We argue that the macroevolutionary microbiome convergence seen across animals with similar diets may be a signature of secondary microbial shifts arising some time after host-driven adaptation.

A trophic niche shift can occur as an adaptive response to environmental change such as altered resource quality, abundance or composition. Alterations in digestive traits such as gut morphology and physiology may enable these niche shifts and affect the persistence of populations and species. Relatively few studies, however, have assessed how niche shifts influence suites of digestive traits through phenotypic plasticity and evolutionary mechanisms, and how these trait changes can subsequently alter the nutrition, fitness and life history of organisms. We investigated how population divergence and plasticity alter the gut physiology of wild Trinidadian guppies (Poecilia reticulata), assessing whether variation in digestive traits correspond with enhanced nutrient assimilation under a pronounced dietary shift. We examined gut enzyme activity, and gut size and mass of wild guppies from both high-predation (HP) and low-predation (LP) habitats when reared in the laboratory and fed on high- or low-quality diets designed to reflect their dietary differences previously found in nature. After 10 weeks on the experimental diets, HP guppies maintained shorter and lighter guts than LP guppies on either diet. Guppies also differed in their digestive enzymatic profiles, more often reflecting nutrient balancing so that increased enzyme expression tended to correspond with more deficient nutrients in the diet. LP guppies had increased somatic phosphorus at the end of the experiment, possibly related to the higher alkaline phosphatase activity in their guts. Our results suggest that differences in gut physiology exist among populations of Trinidadian guppies that may reflect local adaptation to their disparate environments.

Consumer-driven nutrient recycling, the release of chemicals as byproducts and excesses of consumer physiology, can alter ecosystems by changing the availability of limiting nutrients at the base of the food web. The mere presence of predators can alter consumer physiology by restricting food intake and inducing stress. Predation risk, then, can influence ecosystem function by modifying the role of prey as nutrient recyclers, yet there are few empirical tests of how predation risk alters nutrient recycling by prey. Here, we present the results of a test for the effects of predation risk on the C and N budgets of Trinidadian guppies (Poecilia reticulata). We reared female guppies for 7 weeks on diets of varying quality, and we compared control individuals to those exposed continuously to chemical cues emitted by a guppy predator, Crenicichla alta. We measured food consumption, growth rate, tissue elemental stoichiometry and N excretion by guppies on all treatments. Guppies strongly reduced food intake in the presence of predator cues; however, cue-exposed guppies assimilated nutrients more efficiently than controls. Specifically, cue-exposed guppies strongly increased N retention efficiency while only moderately increasing C efficiency. Consequently, guppies reared with predator cues excreted 39% less N than control guppies. We suggest that reduced foraging, enhanced nutrient efficiency, and decreased N excretion are adaptive responses to the extrinsic mortality threat posed by guppy predators. The resulting substantial reduction in N excretion by guppies may influence ecosystem function in natural streams by reducing the supply of a limiting nutrient.

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.