A sterol-mediated gleaner-opportunist trade-off underlies the evolution of grazer resistance to cyanobacteria

Abstract

The human-caused proliferation of cyanobacteria severely impacts consumers in freshwater ecosystems. Toxicity is often singled out as the sole trait to which consumers can adapt, even though cyanobacteria are not necessarily toxic and the lack of nutritionally critical sterols in cyanobacteria is known to impair consumers. We studied the relative significance of toxicity and dietary sterol deficiency in driving the evolution of grazer resistance to cyanobacteria in a large lake with a well-documented history of eutrophication and oligotrophication. Resurrecting decades-old Daphnia genotypes from the sediment allowed us to show that the evolution and subsequent loss of grazer resistance to cyanobacteria involved an adaptation to changes in both toxicity and dietary sterol availability. The adaptation of Daphnia to changes in cyanobacteria abundance revealed a sterol-mediated gleaner-opportunist trade-off. Genotypes from peak-eutrophic periods showed a higher affinity for dietary sterols at the cost of a lower maximum growth rate, whereas genotypes from more oligotrophic periods showed a lower affinity for dietary sterols in favor of a higher maximum growth rate. Our data corroborate the significance of sterols as limiting nutrients in aquatic food webs and highlight the applicability of the gleaner-opportunist trade-off for reconstructing eco-evolutionary processes. The human-caused proliferation of cyanobacteria severely impacts consumers in freshwater ecosystems. Toxicity is often singled out as the sole trait to which consumers can adapt, even though cyanobacteria are not necessarily toxic and the lack of nutritionally critical sterols in cyanobacteria is known to impair consumers. We studied the relative significance of toxicity and dietary sterol deficiency in driving the evolution of grazer resistance to cyanobacteria in a large lake with a well-documented history of eutrophication and oligotrophication. Resurrecting decades-old Daphnia genotypes from the sediment allowed us to show that the evolution and subsequent loss of grazer resistance to cyanobacteria involved an adaptation to changes in both toxicity and dietary sterol availability. The adaptation of Daphnia to changes in cyanobacteria abundance revealed a sterol-mediated gleaner-opportunist trade-off. Genotypes from peak-eutrophic periods showed a higher affinity for dietary sterols at the cost of a lower maximum growth rate, whereas genotypes from more oligotrophic periods showed a lower affinity for dietary sterols in favor of a higher maximum growth rate. Our data corroborate the significance of sterols as limiting nutrients in aquatic food webs and highlight the applicability of the gleaner-opportunist trade-off for reconstructing eco-evolutionary processes.