Predicting optimal transmission investment in malaria parasites

Greischar, Megan A.; Mideo, Nicole; Read, Andrew F.; Bjørnstad, Ottar N.

doi:10.1111/evo.12969

Cited by 36 publications

(92 citation statements)

References 72 publications

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“…Such threshold-dependent regulation may explain why sexual commitment rates in P. falciparum are generally confined to upper limits (i.e., below 50%). While commitment rates can be elevated beyond these limits in response to genetic modifications introduced under in vitro conditions 11, 15 , limiting them in response to environmental triggers will ensure sufficient levels of asexual growth within the human host as a prerequisite for transmission success 9, 33 .…”

Section: Discussionmentioning

confidence: 99%

Probing Plasmodium falciparum sexual commitment at the single-cell level

Brancucci¹,

Niz²,

Straub³

et al. 2018

Wellcome Open Res

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Background: Malaria parasites go through major transitions during their complex life cycle, yet the underlying differentiation pathways remain obscure. Here we apply single cell transcriptomics to unravel the program inducing sexual differentiation in Plasmodium falciparum. Parasites have to make this essential life-cycle decision in preparation for human-to-mosquito transmission. Methods: By combining transcriptional profiling with quantitative imaging and genetics, we defined a transcriptional signature in sexually committed cells. Results: We found this transcriptional signature to be distinct from general changes in parasite metabolism that can be observed in response to commitment-inducing conditions. Conclusions: This proof-of-concept study provides a template to capture transcriptional diversity in parasite populations containing complex mixtures of different life-cycle stages and developmental programs, with important implications for our understanding of parasite biology and the ongoing malaria elimination campaign.

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Section: Discussionmentioning

confidence: 99%

Probing Plasmodium falciparum sexual commitment at the single-cell level

Brancucci¹,

Niz²,

Straub³

et al. 2018

Wellcome Open Res

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“…The impact of immunity on transmission investment has been explored elsewhere (Koella and Antia ; McKenzie and Bossert ; Mideo and Day ; Greischar et al. ).…”

Section: Methodsmentioning

confidence: 99%

“…Allocation to transmission (“transmission investment”) represents a trait that is both readily evolvable (Bousema and Drakeley ) and thought to carry substantial fitness consequences for parasites (Koella and Antia ; McKenzie and Bossert ; Mideo and Day ; Greischar et al. ; Birget et al. ).…”

mentioning

confidence: 99%

“…However, it is not obvious how transmission investment influences these measures: even if investment is constant over an infection, the abundance of proliferative forms and gametocytes, and hence the probability of onward transmission, will vary due to the dynamics of red blood cell availability and immune responses (Greischar et al. ). Therefore, models that explicitly track transmission investment—and its impact on within‐host dynamics over the course of infection—are useful for understanding how that trait will evolve in response to ecology at multiple scales.…”

mentioning

confidence: 99%

“…Theory specific to malaria demonstrates that ecology within the host—most dramatically, the presence of a competing strain—can impose intense selection for proliferation at the expense of transmission (McKenzie and Bossert ; Mideo and Day ; Greischar et al. ; Birget et al. ).…”

mentioning

confidence: 99%

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Partitioning the influence of ecology across scales on parasite evolution

2019

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Vector‐borne parasites must succeed at three scales to persist: they must proliferate within a host, establish in vectors, and transmit back to hosts. Ecology outside the host undergoes dramatic seasonal and human‐induced changes, but predicting parasite evolutionary responses requires integrating their success across scales. We develop a novel, data‐driven model to titrate the evolutionary impact of ecology at multiple scales on human malaria parasites. We investigate how parasites invest in transmission versus proliferation, a life‐history trait that influences disease severity and spread. We find that transmission investment controls the pattern of host infectiousness over the course of infection: a trade‐off emerges between early and late infectiousness, and the optimal resolution of that trade‐off depends on ecology outside the host. An expanding epidemic favors rapid proliferation, and can overwhelm the evolutionary influence of host recovery rates and mosquito population dynamics. If transmission investment and recovery rate are positively correlated, then ecology outside the host imposes potent selection for aggressive parasite proliferation at the expense of transmission. Any association between transmission investment and recovery represents a key unknown, one that is likely to influence whether the evolutionary consequences of interventions are beneficial or costly for human health.

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Timing malaria transmission with mosquito fluctuations

et al. 2018

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Temporal variations in the activity of arthropod vectors can dramatically affect the epidemiology and evolution of vector‐borne pathogens. Here, we explore the “Hawking hypothesis”, which states that these pathogens may evolve the ability to time investment in transmission to match the activity of their vectors. First, we use a theoretical model to identify the conditions promoting the evolution of time‐varying transmission strategies in pathogens. Second, we experimentally test the “Hawking hypothesis” by monitoring the within‐host dynamics of Plasmodium relictum throughout the acute and the chronic phases of the bird infection. We detect a periodic increase of parasitemia and mosquito infection in the late afternoon that coincides with an increase in the biting activity of its natural vector. We also detect a positive effect of mosquito bites on Plasmodium replication in the birds both in the acute and in the chronic phases of the infection. This study highlights that Plasmodium parasites use two different strategies to increase the match between transmission potential and vector availability. We discuss the adaptive nature of these unconditional and plastic transmission strategies with respect to the time scale and the predictability of the fluctuations in the activity of the vector.

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Predicting optimal transmission investment in malaria parasites

Cited by 36 publications

References 72 publications

Probing Plasmodium falciparum sexual commitment at the single-cell level

Probing Plasmodium falciparum sexual commitment at the single-cell level

Partitioning the influence of ecology across scales on parasite evolution

Timing malaria transmission with mosquito fluctuations

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