Heritable intraspecific variation among prey in size and movement interact to shape predation risk and potential natural selection

Abstract

Species' traits affect consumer-resource interactions with consequences for population dynamics, food webs, and energy flows through ecosystems. Yet, our expectations for how the strengths of consumer-resource interactions scale with species' traits largely come from interspecific comparisons. It remains unclear whether these interspecific associations hold for intraspecific trait variation among individuals that is subject to natural selection. Few studies have evaluated the heritability of prey traits related to predation risk and their potential genetic correlations to evaluate how selection might operate on intraspecific variation underlying predator-prey interactions. We used outcrossed and then clonally propagated lines of the ciliate Paramecium caudatum to examine variation in morphology and movement behavior, the extent to which this variation was heritable, and how intraspecific differences among lines altered Paramecium susceptibility to predation by the copepod Macrocyclops albidus. We found that the Paramecium lines exhibited heritable variation in body size and movement traits. In contrast to interspecific allometric relationships, body size and movement speed did not covary among clonal lines. The proportion of Paramecium consumed by copepods was positively associated with Paramecium body size and velocity as one might expect from interspecific relationships . However, we also found evidence of an interaction such that greater velocities led to greater predation risk for large body-sized paramecia but did not alter predation risk for smaller body-sized paramecia. The proportion of paramecia consumed was not related to copepod body size. These patterns of predation risk and heritable trait variation in paramecia suggest that copepod predation may act as a selective force that could operate independently on movement speed and body size with the strongest selection against large, high-velocity paramecia. Overall, our results indicate that conclusions drawn from relationships among species in traits and the strengths of consumer-resource interactions need not hold within species. Furthermore, patterns of genetic variation and covariation in traits coupled with their relationships to predation risk can lead to patterns of potential natural selection that would be hard to infer from interspecific patterns alone.