by Avril Wang, Megan Ann Greischar, Nicole Mideo The timing of investment into reproduction is a key determinant of lifetime reproductive success (fitness). Many organisms exhibit plastic, i.e., environmentally-responsive, investment strategies, raising the questions of what environmental cues trigger responses and why organisms have evolved to respond to those particular cues. For #malaria #parasites (Plasmodium spp.), investment into the production of specialized transmission stages (versus stages that replicate asexually within the host) is synonymous with reproductive investment and also plastic, responding to host- and #parasite-derived factors. Previous theory has identified optimal plastic transmission investment strategies for the rodent #malaria #parasite, Plasmodium chabaudi, as a function of the time since infection, implicitly assuming that #parasites have perfect information about the within-host environment and how it is changing. We extend that theory to ask which cue(s) should #parasites use? Put another way, which cue(s) maximize #parasite fitness, quantified as host infectiousness during acute infection? Our results show that sensing a #parasite-associated cue, e.g., the abundance of infected red blood cells or transmission stages, allows #parasites to achieve fitness approaching that of the optimal time-varying strategy, but only when #parasites perceive the cue non-linearly, responding more sensitively to changes at low densities. However, no single cue can recreate the best time-varying strategy or allow #parasites to adopt terminal investment as the infection ends, a classic expectation for reproductive investment. Sensing two cues—log-transformed infected and uninfected red blood cell abundance—enables #parasites to accurately track the progression of the infection, permits terminal investment, and recovers the fitness of the optimal time-varying investment strategy. Importantly, #parasites that detect two cues more efficiently exploit hosts, resulting in higher virulence compared with those sensing only one cue. However, #parasites sensing two cues also experience larger fitness declines in the face of environmental and developmental fluctuations. Collectively, our results suggest that sensing non-redundant cues enables more optimal transmission investment but trades off against robustness in the face of environmental and developmental noise.

Vacancy at Department of Biology - Microbiology, Aarhus University