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.

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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 (δ15N) and carbon source (δ13C) 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.