Numerical data related to Fig 6.

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.

繁殖投入的时机是终生繁殖成功率，即适合度（fitness）的关键决定因素。诸多生物均展现出可塑性（即环境响应型）的投资策略，由此引出两个核心科学问题：哪些环境线索可触发此类响应？以及生物为何会演化出对这些特定线索做出响应的能力？对于疟原虫（Plasmodium spp.）而言，投入资源生产特化传播阶段（相较于宿主内进行无性繁殖的阶段），等同于繁殖投入，且该过程同样具有可塑性，会响应宿主与寄生虫来源的各类因子。既往理论已针对啮齿类疟原虫查氏疟原虫（Plasmodium chabaudi）确定了最优可塑性传播投入策略，该策略以感染后的时长作为函数变量，且默认寄生虫可完整获知宿主内环境及其变化情况。我们对该理论进行拓展，旨在解答如下问题：寄生虫应当利用何种线索？换而言之，哪些线索可最大化寄生虫的适合度——此处适合度以急性感染期宿主的感染性进行量化？我们的研究结果显示，感知与寄生虫相关的线索（例如受感染红细胞或传播阶段的丰度），可使寄生虫达成接近最优时变策略的适合度，但该结果仅当寄生虫以非线性方式感知该线索、对低密度下的浓度变化更为敏感时方可实现。然而，并无单一线索可复刻最优时变策略，亦无法让寄生虫在感染末期采取终端投资——这是繁殖投入领域的经典预期。同时感知两类线索——经对数转换的受感染与未受感染红细胞丰度——可使寄生虫精准追踪感染进程，允许其开展终端投资，并恢复最优时变投资策略的适合度。值得注意的是，相较于仅感知单一线索的寄生虫，可高效探测两类线索的寄生虫能更充分地利用宿主，进而引发更高的毒力。但与此同时，面对环境与发育波动时，感知两类线索的寄生虫也会面临更大的适合度损失。综上，我们的研究结果表明，感知非冗余线索可实现更优的传播投入，但会在面对环境与发育噪声时，以鲁棒性（robustness）为代价。