Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts

Abstract

The host breadth of any particular herbivore reflects a compromise between evolutionary forces that promote specialism and those that promote polyphagy. Because most terrestrial herbivorous insects specialize, explorations of this evolutionary balance have focused largely on specialist than on polyphagous herbivores. Here, we experimentally tested whether fitness-based tradeoffs in utilizing alternative hosts can be detected within a polyphagous marine herbivore. The marine amphipod Ampithoe longimana occurs on multiple seaweeds year-round (especially the genera Sargassum, Ulva and Hypnea), but is particularly abundant on the diterpene-rich genus Dictyota during warmer summer months. If fitness-based tradeoffs in using these alternative hosts are present, A. longimana may experience fluctuating selection across seasons. To test this possibility, we performed a controlled natural-selection experiment in which amphipods were isolated on Dictyota or a mixed seaweed assemblage that did not include Dictyota. Within 15 weeks (less than five overlapping generations), Dictyota-lines had greater feeding tolerance for Dictyota and its secondary metabolites than did mixed-seaweed-lines. Dictyota-line females reproduced more quickly than did mixed-seaweed-line females on Dictyota, but mixed-seaweed-line juveniles had greater growth on Sargassum and Ulva and higher fecundity on all hosts than did Dictyota-line juveniles. While experimental shifts in preference and performance are likely genetically-mediated, our experimental protocol does not preclude a role for phenotypic plasticity. The presence of a fitness cost to evolving greater preference for Dictyota suggests that fluctuating selection may operate on feeding preference across seasons, but our test of this hypothesis was equivocal. We suggest that one reason that polyphagy persists within A. longimana and potentially other marine grazers is because polyphagy broadens resource use across seasons, and this benefit outweighs the fitness-based costs that can favor specialism. Our results also reinforce the notion that timescales of ecological and evolutionary dynamics can overlap.