Dangerous nutrients: evolution of phytoplankton resource uptake subject to virus attack.

Phytoplankton need multiple resources to grow and reproduce (such as nitrogen, phosphorus, and iron), but the receptors through which they acquire resources are, in many cases, the same channels through which viruses attack. Therefore, phytoplankton can face a bottom-up vs. top-down tradeoff in receptor allocation: Optimize resource uptake or minimize virus attack? We investigate this top-down vs. bottom-up tradeoff using an evolutionary ecology model of multiple essential resources, specialist viruses that attack through the resource receptors, and a phytoplankton population that can evolve to alter the fraction of receptors used for each resource/virus type. Without viruses present the singular continuously stable strategy is to allocate receptors such that resources are co-limiting, which also minimizes the equilibrium concentrations of both resources. Only one virus type can be present at equilibrium (because phytoplankton, in this model, are a single resource for viruses), and when a virus type is present, it controls the equilibrium phytoplankton population size. Despite this top-down control on equilibrium densities, bottom-up control determines the evolutionary outcome. Regardless of which virus type is present, the allocation strategy that yields co-limitation between the two resources is continuously stable. This is true even when the virus type attacking through the limiting resource channel is present, even though selection for co-limitation in this case decreases the equilibrium phytoplankton population and does not decrease the equilibrium concentration of the limiting resource. Therefore, although moving toward co-limitation and decreasing the equilibrium concentration of the limiting resource often co-occur in models, it is co-limitation, and not necessarily the lowest equilibrium concentration of the limiting resource, that is the result of selection. This result adds to the growing body of literature suggesting that co-limitation at equilibrium is a winning strategy.