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1. Identifying individual and spatial drivers of heterogeneous transmission and virulence of malaria in Caribbean anoles

   https://doi.org/10.1002/ecs2.4297  

   Toohey, John M.; Otero, Luisa; Flores Siaca, Ian G.; Acevedo, Miguel A. (December 2022, Ecosphere)

   Abstract Heterogeneous distributions are a fundamental principle of ecology, manifesting as natural variability within ecological levels of organization from individuals to ecosystems. In disease ecology, variability in biotic and abiotic factors can result in heterogeneous patterns of transmission and virulence—broadly defined here as the negative consequences of infection. Still, our classic theoretical understanding of disease dynamics comes from models that assume homogeneous transmission and virulence. Here, we test this assumption by assessing the contribution of various sources of individual and spatial heterogeneity to patterns of transmission and sublethal measurements of virulence in two lizard–malaria systems: a three‐parasite assemblage (Plasmodium floridense,Plasmodium leukocytica, andPlasmodium azurophilum) infecting the lizardAnolis gundlachiin the rainforest of Puerto Rico and a single‐parasite system (P. floridense–Anolis sagrei) in Florida. Using a Bayesian model selection framework, we evaluated whether individual host differences (i.e., body size and sex) or spatial variability (i.e., habitat type and local‐scale host spatial structure) drive heterogeneity in the probability of infection or its associated health costs (i.e., body condition, blood chemistry). We found that the probability of infection increases with increasing lizard body size in both systems. However, in Florida, we found the relationship to be subdued in deforested habitats compared to the adjacent urban hydric forests. Furthermore, infection was spatially clustered within sampling sites, with “hot” and “cold” spots across the landscape. Nevertheless, we found no clear evidence of costs of infection on lizard health in any of the measures assessed and hence no grounds for inference regarding heterogeneous virulence. Ultimately, the consistency of our results across systems suggests prominent roles of individual and spatial heterogeneities as driving factors of transmission of vector‐borne diseases. 

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2. Temperature impacts the environmental suitability for malaria transmission by Anopheles gambiae and Anopheles stephensi

   https://doi.org/10.1002/ecy.3685  

   Villena, Oswaldo C.; Ryan, Sadie J.; Murdock, Courtney C.; Johnson, Leah R. (June 2022, Ecology)

   Abstract Extrinsic environmental factors influence the spatiotemporal dynamics of many organisms, including insects that transmit the pathogens responsible for vector‐borne diseases (VBDs). Temperature is an especially important constraint on the fitness of a wide variety of ectothermic insects. A mechanistic understanding of how temperature impacts traits of ectotherms, and thus the distribution of ectotherms and vector‐borne infections, is key to predicting the consequences of climate change on transmission of VBDs like malaria. However, the response of transmission to temperature and other drivers is complex, as thermal traits of ectotherms are typically nonlinear, and they interact to determine transmission constraints. In this study, we assess and compare the effect of temperature on the transmission of two malaria parasites,Plasmodium falciparumandPlasmodium vivax, by two malaria vector species,Anopheles gambiaeandAnopheles stephensi. We model the nonlinear responses of temperature dependent mosquito and parasite traits (mosquito development rate, bite rate, fecundity, proportion of eggs surviving to adulthood, vector competence, mortality rate, and parasite development rate) and incorporate these traits into a suitability metric based on a model for the basic reproductive number across temperatures. Our model predicts that the optimum temperature for transmission suitability is similar for the four mosquito–parasite combinations assessed in this study, but may differ at the thermal limits. More specifically, we found significant differences in the upper thermal limit between parasites spread by the same mosquito (A. stephensi) and between mosquitoes carryingP. falciparum. In contrast, at the lower thermal limit the significant differences were primarily between the mosquito species that both carried the same pathogen (e.g.,A. stephensiandA. gambiaeboth withP. falciparum). Using prevalence data, we show that the transmission suitability metric calculated from our mechanistic model is consistent with observedP. falciparumprevalence in Africa and Asia but is equivocal forP. vivaxprevalence in Asia, and inconsistent withP. vivaxprevalence in Africa. We mapped risk to illustrate the number of months various areas in Africa and Asia predicted to be suitable for malaria transmission based on this suitability metric. This mapping provides spatially explicit predictions for suitability and transmission risk. 

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3. Transcriptome assembly and differential gene expression of the invasive avian malaria parasite Plasmodium relictum in Hawaiʻi

   https://doi.org/10.1002/ece3.7401  

   Videvall, Elin; Paxton, Kristina L.; Campana, Michael G.; Cassin‐Sackett, Loren; Atkinson, Carter T.; Fleischer, Robert C. (March 2021, Ecology and Evolution)

   Abstract The malaria parasitePlasmodium relictum(lineage GRW4) was introduced less than a century ago to the native avifauna of Hawaiʻi, where it has since caused major declines of endemic bird populations. One of the native bird species that is frequently infected with GRW4 is the Hawaiʻi ʻamakihi (Chlorodrepanis virens). To achieve a better understanding of the transcriptional activities of this virulent parasite, we performed a controlled challenge experiment of 15 ʻamakihi that were infected with GRW4. Blood samples containing malaria parasites were collected at two time points (intermediate and peak infection stages) from host individuals that were either experimentally infected by mosquitoes or inoculated with infected blood. We then used RNA sequencing to assemble a high‐quality blood transcriptome ofP. relictumGRW4, allowing us to quantify parasite expression levels inside individual birds. We found few significant differences (one to two transcripts) in GRW4 expression levels between host infection stages and between inoculation methods. However, 36 transcripts showed differential expression levels among all host individuals, indicating a potential presence of host‐specific gene regulation across hosts. To reduce the extinction risk of the remaining native bird species in Hawaiʻi, genetic resources of the localPlasmodiumlineage are needed to enable further molecular characterization of this parasite. Our newly built Hawaiian GRW4 transcriptome assembly, together with analyses of the parasite's transcriptional activities inside the blood of Hawaiʻi ʻamakihi, can provide us with important knowledge on how to combat this deadly avian disease in the future. 

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4. An intrinsic oscillator drives the blood stage cycle of the malaria parasite Plasmodium falciparum

   https://doi.org/10.1126/science.aba4357  

   Smith, Lauren M.; Motta, Francis C.; Chopra, Garima; Moch, J. Kathleen; Nerem, Robert R.; Cummins, Bree; Roche, Kimberly E.; Kelliher, Christina M.; Leman, Adam R.; Harer, John; et al (May 2020, Science)

   The blood stage of the infection of the malaria parasite Plasmodium falciparum exhibits a 48-hour developmental cycle that culminates in the synchronous release of parasites from red blood cells, which triggers 48-hour fever cycles in the host. This cycle could be driven extrinsically by host circadian processes or by a parasite-intrinsic oscillator. To distinguish between these hypotheses, we examine the P. falciparum cycle in an in vitro culture system and show that the parasite has molecular signatures associated with circadian and cell cycle oscillators. Each of the four strains examined has a different period, which indicates strain-intrinsic period control. Finally, we demonstrate that parasites have low cell-to-cell variance in cycle period, on par with a circadian oscillator. We conclude that an intrinsic oscillator maintains Plasmodium ’s rhythmic life cycle. 

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5. Global drivers of avian haemosporidian infections vary across zoogeographical regions

   https://doi.org/10.1111/geb.13390  

   Fecchio, Alan; Clark, Nicholas J.; Bell, Jeffrey A.; Skeen, Heather R.; Lutz, Holly L.; De La Torre, Gabriel M.; Vaughan, Jefferson A.; Tkach, Vasyl V.; Schunck, Fabio; Ferreira, Francisco C.; et al (September 2021, Global Ecology and Biogeography)

   Abstract AimMacroecological analyses provide valuable insights into factors that influence how parasites are distributed across space and among hosts. Amid large uncertainties that arise when generalizing from local and regional findings, hierarchical approaches applied to global datasets are required to determine whether drivers of parasite infection patterns vary across scales. We assessed global patterns of haemosporidian infections across a broad diversity of avian host clades and zoogeographical realms to depict hotspots of prevalence and to identify possible underlying drivers. LocationGlobal. Time period1994–2019. Major taxa studiedAvian haemosporidian parasites (generaPlasmodium,Haemoproteus,LeucocytozoonandParahaemoproteus). MethodsWe amalgamated infection data from 53,669 individual birds representing 2,445 species world‐wide. Spatio‐phylogenetic hierarchical Bayesian models were built to disentangle potential landscape, climatic and biotic drivers of infection probability while accounting for spatial context and avian host phylogenetic relationships. ResultsIdiosyncratic responses of the three most common haemosporidian genera to climate, habitat, host relatedness and host ecological traits indicated marked variation in host infection rates from local to global scales. Notably, host ecological drivers, such as migration distance forPlasmodiumandParahaemoproteus, exhibited predominantly varying or even opposite effects on infection rates across regions, whereas climatic effects on infection rates were more consistent across realms. Moreover, infections in some low‐prevalence realms were disproportionately concentrated in a few local hotspots, suggesting that regional‐scale variation in habitat and microclimate might influence transmission, in addition to global drivers. Main conclusionsOur hierarchical global analysis supports regional‐scale findings showing the synergistic effects of landscape, climate and host ecological traits on parasite transmission for a cosmopolitan and diverse group of avian parasites. Our results underscore the need to account for such interactions, in addition to possible variation in drivers across regions, to produce the robust inference required to predict changes in infection risk under future scenarios. 

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