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

Predator and prey traits are important determinants of the outcomes of trophic interactions. In turn, the outcomes of trophic interactions shape predator and prey trait evolution. How species' traits respond to selection from trophic interactions depends crucially on whether and how heritable species' traits are and their genetic correlations. Of the many traits influencing the outcomes of trophic interactions, body size and movement traits have emerged as key traits. Yet, how these traits shape and are shaped by trophic interactions is unclear, as few studies have simultaneously measured the impacts of these traits on the outcomes of trophic interactions, their heritability, and their correlations within the same system. We used outcrossed lines of the ciliate protist Paramecium caudatum from natural populations to examine variation in morphology and movement behaviour, the heritability of that variation, and its effects on 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 expectations from allometric relationships, body size and movement speed showed little covariance among clonal lines. The proportion of Paramecium consumed by copepods was positively associated with Paramecium body size and velocity but with an interaction such that greater velocities led to greater predation risk for large body‐sized paramecia but did not alter predation risk for smaller 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 operating independently on movement and body size and generating the strongest selection against large, high‐velocity paramecia. Our results illustrate how ecology and genetics can shape potential natural selection on prey traits through the outcomes of trophic interactions. Further simultaneous measures of predation outcomes, traits, and their quantitative genetics will provide insights into the evolutionary ecology of species interactions and their eco‐evolutionary consequences. Read the free Plain Language Summary for this article on the Journal blog.