ABSTRACT
Coevolution arises from the reciprocal genetic change between species and represents a major evolutionary force that contributes to the generation and maintenance of biodiversity. The tempo and mode of coevolution are affected by environmental conditions that modify species interactions. For example, the scarcity of essential elements influences the nutrition and productivity of host populations, which should not only regulate parasite dynamics, but also drive the evolution of defense and virulence traits. To explore the effects of nutrient availability on antagonistic coevolution, we conducted a long-term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. Our manipulation of nutrient stoichiometry influenced the stability of host-parasite interactions, but also affected the underlying mode of coevolution. By assessing infectivity with more than 18,000 pairwise challenges using time-shift and network analyses, we documented directional selection for increased phage resistance, a pattern that is consistent with coevolutionary arms-race dynamics. In contrast, phage infectivity fluctuated through time, as expected when coevolution is determined by negative frequency-dependent selection, but was 70 % higher on naive hosts that evolved under N-limitation versus P-limitation. Furthermore, infection networks were 25 % more modular under P-limitation than N-limitation reflecting host-range contraction and an asymmetric coevolutionary trajectory. Together, our results demonstrate that nutrient stoichiometry creates eco-evolutionary feedbacks that may alter the dynamics and functioning of environmental and host-associated microbial communities.
SIGNIFICANCE STATEMENT As obligate parasites, phage represent a significant source of mortality for marine cyanobacteria, which are photosynthetic microorganisms that play a central role in the regulation of biogeochemical processes, including energy flow, carbon sequestration, and the cycling of nitrogen (N) and phosphorus (P). Phage also act as agents of evolutionary change by selecting for resistant cyanobacteria, which can give rise to counter-resistant phage. This coevolutionary process was differentially affected by the availability of N and P in ways that could impact the ecology and evolution of one of the most abundant and functionally important groups of microorganisms on Earth.