Publications by authors named "Mercedes Pascual"

106 Publications

The impact of indoor residual spraying on Plasmodium falciparum microsatellite variation in an area of high seasonal malaria transmission in Ghana, West Africa.

Mol Ecol 2021 Jun 18. Epub 2021 Jun 18.

School of BioSciences, Bio21 Institute, The University of Melbourne, Melbourne, Vic., Australia.

Here, we report the first population genetic study to examine the impact of indoor residual spraying (IRS) on Plasmodium falciparum in humans. This study was conducted in an area of high seasonal malaria transmission in Bongo District, Ghana. IRS was implemented during the dry season (November-May) in three consecutive years between 2013 and 2015 to reduce transmission and attempt to bottleneck the parasite population in humans towards lower diversity with greater linkage disequilibrium. The study was done against a background of widespread use of long-lasting insecticidal nets, typical for contemporary malaria control in West Africa. Microsatellite genotyping with 10 loci was used to construct 392 P. falciparum multilocus infection haplotypes collected from two age-stratified cross-sectional surveys at the end of the wet seasons pre- and post-IRS. Three-rounds of IRS, under operational conditions, led to a >90% reduction in transmission intensity and a 35.7% reduction in the P. falciparum prevalence (p < .001). Despite these declines, population genetic analysis of the infection haplotypes revealed no dramatic changes with only a slight, but significant increase in genetic diversity (H : pre-IRS = 0.79 vs. post-IRS = 0.81, p = .048). Reduced relatedness of the parasite population (p < .001) was observed post-IRS, probably due to decreased opportunities for outcrossing. Spatiotemporal genetic differentiation between the pre- and post-IRS surveys (D = 0.0329 [95% CI: 0.0209 - 0.0473], p = .034) was identified. These data provide a genetic explanation for the resilience of P. falciparum to short-term IRS programmes in high-transmission settings in sub-Saharan Africa.
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http://dx.doi.org/10.1111/mec.16029DOI Listing
June 2021

What happens when forests fall?

Elife 2021 04 6;10. Epub 2021 Apr 6.

Department of Ecology and Evolution, University of Chicago, Chicago, United States.

Combining spatial and temporal data is helping researchers to understand how deforestation influences the risk of malaria.
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http://dx.doi.org/10.7554/eLife.67863DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8024005PMC
April 2021

Malaria trends in Ethiopian highlands track the 2000 'slowdown' in global warming.

Nat Commun 2021 03 10;12(1):1555. Epub 2021 Mar 10.

Department of Ecology and Evolution, University of Chicago, Chicago, IL, USA.

A counterargument to the importance of climate change for malaria transmission has been that regions where an effect of warmer temperatures is expected, have experienced a marked decrease in seasonal epidemic size since the turn of the new century. This decline has been observed in the densely populated highlands of East Africa at the center of the earlier debate on causes of the pronounced increase in epidemic size from the 1970s to the 1990s. The turnaround of the incidence trend around 2000 is documented here with an extensive temporal record for malaria cases for both Plasmodium falciparum and Plasmodium vivax in an Ethiopian highland. With statistical analyses and a process-based transmission model, we show that this decline was driven by the transient slowdown in global warming and associated changes in climate variability, especially ENSO. Decadal changes in temperature and concurrent climate variability facilitated rather than opposed the effect of interventions.
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http://dx.doi.org/10.1038/s41467-021-21815-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7946882PMC
March 2021

An antigenic diversification threshold for falciparum malaria transmission at high endemicity.

PLoS Comput Biol 2021 02 19;17(2):e1008729. Epub 2021 Feb 19.

Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, United States of America.

In malaria and several other important infectious diseases, high prevalence occurs concomitantly with incomplete immunity. This apparent paradox poses major challenges to malaria elimination in highly endemic regions, where asymptomatic Plasmodium falciparum infections are present across all age classes creating a large reservoir that maintains transmission. This reservoir is in turn enabled by extreme antigenic diversity of the parasite and turnover of new variants. We present here the concept of a threshold in local pathogen diversification that defines a sharp transition in transmission intensity below which new antigen-encoding genes generated by either recombination or migration cannot establish. Transmission still occurs below this threshold, but diversity of these genes can neither accumulate nor recover from interventions that further reduce it. An analytical expectation for this threshold is derived and compared to numerical results from a stochastic individual-based model of malaria transmission that incorporates the major antigen-encoding multigene family known as var. This threshold corresponds to an "innovation" number we call Rdiv; it is different from, and complementary to, the one defined by the classic basic reproductive number of infectious diseases, R0, which does not readily is better apply under large and dynamic strain diversity. This new threshold concept can be exploited for effective malaria control and applied more broadly to other pathogens with large multilocus antigenic diversity.
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http://dx.doi.org/10.1371/journal.pcbi.1008729DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7928509PMC
February 2021

Quantifying asymptomatic infection and transmission of COVID-19 in New York City using observed cases, serology, and testing capacity.

Proc Natl Acad Sci U S A 2021 03;118(9)

Department of Ecology and Evolution, Biological Sciences Division, University of Chicago, Chicago, IL 60637;

The contributions of asymptomatic infections to herd immunity and community transmission are key to the resurgence and control of COVID-19, but are difficult to estimate using current models that ignore changes in testing capacity. Using a model that incorporates daily testing information fit to the case and serology data from New York City, we show that the proportion of symptomatic cases is low, ranging from 13 to 18%, and that the reproductive number may be larger than often assumed. Asymptomatic infections contribute substantially to herd immunity, and to community transmission together with presymptomatic ones. If asymptomatic infections transmit at similar rates as symptomatic ones, the overall reproductive number across all classes is larger than often assumed, with estimates ranging from 3.2 to 4.4. If they transmit poorly, then symptomatic cases have a larger reproductive number ranging from 3.9 to 8.1. Even in this regime, presymptomatic and asymptomatic cases together comprise at least 50% of the force of infection at the outbreak peak. We find no regimes in which all infection subpopulations have reproductive numbers lower than three. These findings elucidate the uncertainty that current case and serology data cannot resolve, despite consideration of different model structures. They also emphasize how temporal data on testing can reduce and better define this uncertainty, as we move forward through longer surveillance and second epidemic waves. Complementary information is required to determine the transmissibility of asymptomatic cases, which we discuss. Regardless, current assumptions about the basic reproductive number of severe acute respiratory syndrome coronavirus 2 (SARS-Cov-2) should be reconsidered.
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http://dx.doi.org/10.1073/pnas.2019716118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7936345PMC
March 2021

COVID-Clarity demands unification of health and environmental policy.

Glob Chang Biol 2021 04 28;27(7):1319-1321. Epub 2021 Jan 28.

Department of Ecology and Evolution, University of Chicago, Chicago, IL, USA.

Spillover of novel pathogens from wildlife to people, such as the virus responsible for the COVID-19 pandemic, is increasing and this trend is most strongly associated with tropical deforestation driven by agricultural expansion. This same process is eroding natural capital, reducing forest-associated health co-benefits, and accelerating climate change. Protecting and promoting tropical forests is one of the most immediate steps we can take to simultaneously mitigate climate change while reducing the risk of future pandemics; however, success in this undertaking will require greater connectivity of policy initiatives from local to global, as well as unification of health and environmental policy.
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http://dx.doi.org/10.1111/gcb.15508DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8014021PMC
April 2021

Emerging arboviruses in the urbanized Amazon rainforest.

BMJ 2020 11 13;371:m4385. Epub 2020 Nov 13.

Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, USA

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http://dx.doi.org/10.1136/bmj.m4385DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7664915PMC
November 2020

The network structure and eco-evolutionary dynamics of CRISPR-induced immune diversification.

Nat Ecol Evol 2020 12 19;4(12):1650-1660. Epub 2020 Oct 19.

Department of Ecology and Evolution, University of Chicago, Chicago, IL, USA.

As a heritable sequence-specific adaptive immune system, CRISPR-Cas is a powerful force shaping strain diversity in host-virus systems. While the diversity of CRISPR alleles has been explored, the associated structure and dynamics of host-virus interactions have not. We explore the role of CRISPR in mediating the interplay between host-virus interaction structure and eco-evolutionary dynamics in a computational model and compare the results with three empirical datasets from natural systems. We show that the structure of the networks describing who infects whom and the degree to which strains are immune, are respectively modular (containing groups of hosts and viruses that interact strongly) and weighted-nested (specialist hosts are more susceptible to subsets of viruses that in turn also infect the more generalist hosts with many spacers matching many viruses). The dynamic interplay between these networks influences transitions between dynamical regimes of virus diversification and host control. The three empirical systems exhibit weighted-nested immunity networks, a pattern our theory shows is indicative of hosts able to suppress virus diversification. Previously missing from studies of microbial host-pathogen systems, the immunity network plays a key role in the coevolutionary dynamics.
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http://dx.doi.org/10.1038/s41559-020-01312-zDOI Listing
December 2020

Predicting re-emergence times of dengue epidemics at low reproductive numbers: DENV1 in Rio de Janeiro, 1986-1990.

J R Soc Interface 2020 06 24;17(167):20200273. Epub 2020 Jun 24.

Department of Ecology and Evolution, and, University of Chicago, Chicago, IL, USA.

Predicting arbovirus re-emergence remains challenging in regions with limited off-season transmission and intermittent epidemics. Current mathematical models treat the depletion and replenishment of susceptible (non-immune) hosts as the principal drivers of re-emergence, based on established understanding of highly transmissible childhood diseases with frequent epidemics. We extend an analytical approach to determine the number of 'skip' years preceding re-emergence for diseases with continuous seasonal transmission, population growth and under-reporting. Re-emergence times are shown to be highly sensitive to small changes in low (secondary cases produced from a primary infection in a fully susceptible population). We then fit a stochastic Susceptible-Infected-Recovered (SIR) model to observed case data for the emergence of dengue serotype DENV1 in Rio de Janeiro. This aggregated city-level model substantially over-estimates observed re-emergence times either in terms of skips or outbreak probability under forward simulation. The inability of susceptible depletion and replenishment to explain re-emergence under 'well-mixed' conditions at a city-wide scale demonstrates a key limitation of SIR aggregated models, including those applied to other arboviruses. The predictive uncertainty and high skip sensitivity to epidemiological parameters suggest a need to investigate the relevant spatial scales of susceptible depletion and the scaling of microscale transmission dynamics to formulate simpler models that apply at coarse resolutions.
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http://dx.doi.org/10.1098/rsif.2020.0273DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7328382PMC
June 2020

Tube Well Use as Protection Against Rotavirus Infection During the Monsoons in an Urban Setting.

J Infect Dis 2020 01;221(2):238-242

Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA.

Rotavirus, a diarrheal pathogen spread via fecal-oral transmission, is typically characterized by a winter incidence peak in most countries. Unlike for cholera and other waterborne infections, the role of sanitation and socioeconomic factors on the spatial variation of rotavirus seasonality remains unclear. In the current study, we analyzed their association with rotavirus seasonality, specifically the odds of monsoon cases, across 46 locations from 2001 to 2012 in Dhaka. Drinking water from tube wells, compared to other sources, has a clear protective effect against cases during the monsoon, when flooding and water contamination are more likely. This finding supports a significant environmental component of transmission.
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http://dx.doi.org/10.1093/infdis/jiz436DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6936003PMC
January 2020

Development, environmental degradation, and disease spread in the Brazilian Amazon.

PLoS Biol 2019 11 15;17(11):e3000526. Epub 2019 Nov 15.

Departamento de Ingeniería Biomédica, Grupo de Investigación en Biología Matemática y Computacional BIOMAC, Universidad de los Andes, Bogotá, Colombia.

The Amazon is Brazil's greatest natural resource and invaluable to the rest of the world as a buffer against climate change. The recent election of Brazil's president brought disputes over development plans for the region back into the spotlight. Historically, the development model for the Amazon has focused on exploitation of natural resources, resulting in environmental degradation, particularly deforestation. Although considerable attention has focused on the long-term global cost of "losing the Amazon," too little attention has focused on the emergence and reemergence of vector-borne diseases that directly impact the local population, with spillover effects to other neighboring areas. We discuss the impact of Amazon development models on human health, with a focus on vector-borne disease risk. We outline policy actions that could mitigate these negative impacts while creating opportunities for environmentally sensitive economic activities.
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http://dx.doi.org/10.1371/journal.pbio.3000526DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6881077PMC
November 2019

Let's Train More Theoretical Ecologists - Here Is Why.

Trends Ecol Evol 2019 09 11;34(9):759-762. Epub 2019 Jul 11.

ELTE-MTA Theoretical Biology and Evolutionary Ecology Research Group, Budapest, Hungary; Department of Biological Physics, Eötvös Loránd University, Budapest, Hungary.

A tangled web of vicious circles, driven by cultural issues, has prevented ecology from growing strong theoretical roots. Now this hinders development of effective conservation policies. To overcome these barriers in view of urgent societal needs, we propose a global network of postgraduate theoretical training programs.
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http://dx.doi.org/10.1016/j.tree.2019.06.004DOI Listing
September 2019

Competition for hosts modulates vast antigenic diversity to generate persistent strain structure in Plasmodium falciparum.

PLoS Biol 2019 06 24;17(6):e3000336. Epub 2019 Jun 24.

Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, United States of America.

In their competition for hosts, parasites with antigens that are novel to the host immune system will be at a competitive advantage. The resulting frequency-dependent selection can structure parasite populations into strains of limited genetic overlap. For the causative agent of malaria, Plasmodium falciparum, the high recombination rates and associated vast diversity of its highly antigenic and multicopy var genes preclude such clear clustering in endemic regions. This undermines the definition of strains as specific, temporally persisting gene variant combinations. We use temporal multilayer networks to analyze the genetic similarity of parasites in both simulated data and in an extensively and longitudinally sampled population in Ghana. When viewed over time, populations are structured into modules (i.e., groups) of parasite genomes whose var gene combinations are more similar within than between the modules and whose persistence is much longer than that of the individual genomes that compose them. Comparison to neutral models that retain parasite population dynamics but lack competition reveals that the selection imposed by host immunity promotes the persistence of these modules. The modular structure is, in turn, associated with a slower acquisition of immunity by individual hosts. Modules thus represent dynamically generated niches in host immune space, which can be interpreted as strains. Negative frequency-dependent selection therefore shapes the organization of the var diversity into parasite genomes, leaving a persistence signature over ecological time scales. Multilayer networks extend the scope of phylodynamics analyses by allowing quantification of temporal genetic structure in organisms that generate variation via recombination or other non-bifurcating processes. A strain structure similar to the one described here should apply to other pathogens with large antigenic spaces that evolve via recombination. For malaria, the temporal modular structure should enable the formulation of tractable epidemiological models that account for parasite antigenic diversity and its influence on intervention outcomes.
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http://dx.doi.org/10.1371/journal.pbio.3000336DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6611651PMC
June 2019

Critical transitions in malaria transmission models are consistently generated by superinfection.

Philos Trans R Soc Lond B Biol Sci 2019 06;374(1775):20180275

3 Santa Fe Institute , Hyde Park Road, Santa Fe, NM , USA.

The history of modelling vector-borne infections essentially begins with the papers by Ross on malaria. His models assume that the dynamics of malaria can most simply be characterized by two equations that describe the prevalence of malaria in the human and mosquito hosts. This structure has formed the central core of models for malaria and most other vector-borne diseases for the past century, with additions acknowledging important aetiological details. We partially add to this tradition by describing a malaria model that provides for vital dynamics in the vector and the possibility of super-infection in the human host: reinfection of asymptomatic hosts before they have cleared a prior infection. These key features of malaria aetiology create the potential for break points in the prevalence of infected hosts, sudden transitions that seem to characterize malaria's response to control in different locations. We show that this potential for critical transitions is a general and underappreciated feature of any model for vector-borne diseases with incomplete immunity, including the canonical Ross-McDonald model. Ignoring these details of the host's immune response to infection can potentially lead to serious misunderstanding in the interpretation of malaria distribution patterns and the design of control schemes for other vector-borne diseases. This article is part of the theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: approaches and important themes'. This issue is linked with the subsequent theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: epidemic forecasting and control'.
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http://dx.doi.org/10.1098/rstb.2018.0275DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6553601PMC
June 2019

Mosquito-borne transmission in urban landscapes: the missing link between vector abundance and human density.

Proc Biol Sci 2018 08 15;285(1884). Epub 2018 Aug 15.

Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA

With escalating urbanization, the environmental, demographic, and socio-economic heterogeneity of urban landscapes poses a challenge to mathematical models for the transmission of vector-borne infections. Classical coupled vector-human models typically assume that mosquito abundance is either independent from, or proportional to, human population density, implying a decreasing force of infection, or infection rate with host number. We question these assumptions by introducing an explicit dependence between host and vector densities through different recruitment functions, whose dynamical consequences we examine in a modified model formulation. Contrasting patterns in the force of infection are demonstrated, including in particular increasing trends when recruitment grows sufficiently fast with human density. Interaction of these patterns with seasonality in temperature can give rise to pronounced differences in timing, relative peak sizes, and duration of epidemics. These proposed dependencies explain empirical dengue risk patterns observed in the city of Delhi where socio-economic status has an impact on both human and mosquito densities. These observed risk trends with host density are inconsistent with current standard models. A better understanding of the connection between vector recruitment and host density is needed to address the population dynamics of mosquito-transmitted infections in urban landscapes.
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http://dx.doi.org/10.1098/rspb.2018.0826DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6111166PMC
August 2018

Identifying functional groups among the diverse, recombining antigenic var genes of the malaria parasite Plasmodium falciparum from a local community in Ghana.

PLoS Comput Biol 2018 06 13;14(6):e1006174. Epub 2018 Jun 13.

Department of Ecology and Evolution, University of Chicago, Chicago, IL, United States of America.

A challenge in studying diverse multi-copy gene families is deciphering distinct functional types within immense sequence variation. Functional changes can in some cases be tracked through the evolutionary history of a gene family; however phylogenetic approaches are not possible in cases where gene families diversify primarily by recombination. We take a network theoretical approach to functionally classify the highly recombining var antigenic gene family of the malaria parasite Plasmodium falciparum. We sample var DBLα sequence types from a local population in Ghana, and classify 9,276 of these variants into just 48 functional types. Our approach is to first decompose each sequence type into its constituent, recombining parts; we then use a stochastic block model to identify functional groups among the parts; finally, we classify the sequence types based on which functional groups they contain. This method for functional classification does not rely on an inferred phylogenetic history, nor does it rely on inferring function based on conserved sequence features. Instead, it infers functional similarity among recombining parts based on the sharing of similar co-occurrence interactions with other parts. This method can therefore group sequences that have undetectable sequence homology or even distinct origination. Describing these 48 var functional types allows us to simplify the antigenic diversity within our dataset by over two orders of magnitude. We consider how the var functional types are distributed in isolates, and find a nonrandom pattern reflecting that common var functional types are non-randomly distinct from one another in terms of their functional composition. The coarse-graining of var gene diversity into biologically meaningful functional groups has important implications for understanding the disease ecology and evolution of this system, as well as for designing effective epidemiological monitoring and intervention.
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http://dx.doi.org/10.1371/journal.pcbi.1006174DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6016947PMC
June 2018

Networks of genetic similarity reveal non-neutral processes shape strain structure in Plasmodium falciparum.

Nat Commun 2018 05 8;9(1):1817. Epub 2018 May 8.

Department of Ecology and Evolution, University of Chicago, 1101 E 57th Street, Chicago, IL, 60637, USA.

Pathogens compete for hosts through patterns of cross-protection conferred by immune responses to antigens. In Plasmodium falciparum malaria, the var multigene family encoding for the major blood-stage antigen PfEMP1 has evolved enormous genetic diversity through ectopic recombination and mutation. With 50-60 var genes per genome, it is unclear whether immune selection can act as a dominant force in structuring var repertoires of local populations. The combinatorial complexity of the var system remains beyond the reach of existing strain theory and previous evidence for non-random structure cannot demonstrate immune selection without comparison with neutral models. We develop two neutral models that encompass malaria epidemiology but exclude competitive interactions between parasites. These models, combined with networks of genetic similarity, reveal non-neutral strain structure in both simulated systems and an extensively sampled population in Ghana. The unique population structure we identify underlies the large transmission reservoir characteristic of highly endemic regions in Africa.
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http://dx.doi.org/10.1038/s41467-018-04219-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5940794PMC
May 2018

Signatures of competition and strain structure within the major blood-stage antigen of in a local community in Ghana.

Ecol Evol 2018 Apr 1;8(7):3574-3588. Epub 2018 Mar 1.

Department of Ecology and Evolution University of Chicago Chicago IL USA.

The concept of niche partitioning has received considerable theoretical attention at the interface of ecology and evolution of infectious diseases. Strain theory postulates that pathogen populations can be structured into distinct nonoverlapping strains by frequency-dependent selection in response to intraspecific competition for host immune space. The malaria parasite presents an opportunity to investigate this phenomenon in nature, under conditions of high recombination rate and extensive antigenic diversity. The parasite's major blood-stage antigen, EMP1, is encoded by the hyperdiverse genes. With a dataset that includes thousands of DBLα sequence types sampled from asymptomatic cases within an area of high endemicity in Ghana, we address how diversity is distributed within isolates and compare this to the distribution of microsatellite allelic diversity within isolates to test whether antigenic and neutral regions of the genome are structured differently. With respect to DBLα sequence types, we find that on average isolates exhibit significantly lower overlap than expected randomly, but that there also exists frequent pairs of isolates that are highly related. Furthermore, the linkage network of DBLα sequence types reveals a pattern of nonrandom modularity unique to these antigenic genes, and we find that modules of highly linked DBLα types are not explainable by neutral forces related to recombination constraints, microsatellite diversity, sampling location, host age, or multiplicity of infection. These findings of reduced overlap and modularity among the antigenic genes are consistent with a role for immune selection as proposed by strain theory. Identifying the evolutionary and ecological dynamics that are responsible for the nonrandom structure in antigenic diversity is important for designing effective intervention in endemic areas.
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http://dx.doi.org/10.1002/ece3.3803DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5901166PMC
April 2018

Incidence Prediction for the 2017-2018 Influenza Season in the United States with an Evolution-informed Model.

PLoS Curr 2018 Jan 17;10. Epub 2018 Jan 17.

Ecology and Evolution, University of Chicago, Chicago, Illinois, USA.

Introduction: Seasonal influenza is responsible for a high disease burden in the United States and worldwide. Predicting outbreak size in advance can contribute to the timely control of seasonal influenza by informing health care and vaccination planning.

Methods: Recently, a process-based model was developed for forecasting incidence dynamics ahead of the season, with the approach validated by several statistical criteria, including an accurate real-time prediction for the past 2016-2017 influenza season before it started.

Results: Based on this model and data up to June 2017, a forecast for the upcoming 2017-2018 influenza season is presented here, indicating an above-average, moderately severe, outbreak dominated by the H3N2 subtype.

Discussion: The prediction is consistent with surveillance data so far, which already indicate the predominance of H3N2. The forecast for the upcoming 2017-2018 influenza season reinforces the importance of the on-going vaccination campaign.
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http://dx.doi.org/10.1371/currents.outbreaks.6f03b36587ae74b11353c1127cbe7d0eDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5843489PMC
January 2018

Understanding the role of parasites in food webs using the group model.

J Anim Ecol 2018 05 18;87(3):790-800. Epub 2017 Dec 18.

Department of Ecology & Evolution, University of Chicago, Chicago, IL, USA.

Parasites are ubiquitous and have been shown to influence macroscopic measures of ecological network structure, such as connectance and robustness, as well as local structure, such as subgraph frequencies. Nevertheless, they are often under-represented in ecological studies due to their small size and often complex life cycles. We consider whether or not parasites play structurally unique roles in ecological networks; that is, can we distinguish parasites from other species using network structure alone? We partition the species in a community statistically using the group model, and we test whether or not parasites tend to cluster in their own groups, using a measure of "imbalance." We find that parasites form highly imbalanced groups, and that concomitant predation, in which a predator consumes a prey and its parasites, but not the number of interactions, improves the group model's ability to distinguish parasites from non-parasites. This work demonstrates that parasites and non-parasites interact in networks in statistically distinct ways, and that these differences are partly, but not entirely, due to the existence of concomitant predation.
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http://dx.doi.org/10.1111/1365-2656.12782DOI Listing
May 2018

Climate-driven endemic cholera is modulated by human mobility in a megacity.

Adv Water Resour 2017 Oct 27;108:367-376. Epub 2016 Nov 27.

Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA.

Although a differential sensitivity of cholera dynamics to climate variability has been reported in the spatially heterogeneous megacity of Dhaka, Bangladesh, the specific patterns of spread of the resulting risk within the city remain unclear. We build on an established probabilistic spatial model to investigate the importance and role of human mobility in modulating spatial cholera transmission. Mobility fluxes were inferred using a straightforward and generalizable methodology that relies on mapping population density based on a high resolution urban footprint product, and a parameter-free human mobility model. In accordance with previous findings, we highlight the higher sensitivity to the El Niño Southern Oscillation (ENSO) in the highly populated urban center than in the more rural periphery. More significantly, our results show that cholera risk is largely transmitted from the climate-sensitive core to the periphery of the city, with implications for the planning of control efforts. In addition, including human mobility improves the outbreak prediction performance of the model with an 11 month lead. The interplay between climatic and human mobility factors in cholera transmission is discussed from the perspective of the rapid growth of megacities across the developing world.
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http://dx.doi.org/10.1016/j.advwatres.2016.11.013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5654324PMC
October 2017

Evolution-informed forecasting of seasonal influenza A (H3N2).

Sci Transl Med 2017 Oct;9(413)

Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA.

Interpandemic or seasonal influenza A, currently subtypes H3N2 and H1N1, exacts an enormous annual burden both in terms of human health and economic impact. Incidence prediction ahead of season remains a challenge largely because of the virus' antigenic evolution. We propose a forecasting approach that incorporates evolutionary change into a mechanistic epidemiological model. The proposed models are simple enough that their parameters can be estimated from retrospective surveillance data. These models link amino acid sequences of hemagglutinin epitopes with a transmission model for seasonal H3N2 influenza, also informed by H1N1 levels. With a monthly time series of H3N2 incidence in the United States for more than 10 years, we demonstrate the feasibility of skillful prediction for total cases ahead of season, with a tendency to underpredict monthly peak epidemic size, and an accurate real-time forecast for the 2016/2017 influenza season.
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http://dx.doi.org/10.1126/scitranslmed.aan5325DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5805486PMC
October 2017

General ecological models for human subsistence, health and poverty.

Nat Ecol Evol 2017 Aug 3;1(8):1153-1159. Epub 2017 Jul 3.

Department of Global Health and Social Medicine, Harvard Medical School, Boston, MA, 02115, USA.

The world's rural poor rely heavily on their immediate natural environment for subsistence and suffer high rates of morbidity and mortality from infectious diseases. We present a general framework for modelling subsistence and health of the rural poor by coupling simple dynamic models of population ecology with those for economic growth. The models show that feedbacks between the biological and economic systems can lead to a state of persistent poverty. Analyses of a wide range of specific systems under alternative assumptions show the existence of three possible regimes corresponding to a globally stable development equilibrium, a globally stable poverty equilibrium and bistability. Bistability consistently emerges as a property of generalized disease-economic systems for about a fifth of the feasible parameter space. The overall proportion of parameters leading to poverty is larger than that resulting in healthy/wealthy development. All the systems are found to be most sensitive to human disease parameters. The framework highlights feedbacks, processes and parameters that are important to measure in studies of rural poverty to identify effective pathways towards sustainable development.
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http://dx.doi.org/10.1038/s41559-017-0221-8DOI Listing
August 2017

The rise and fall of malaria under land-use change in frontier regions.

Nat Ecol Evol 2017 Mar 20;1(5):108. Epub 2017 Mar 20.

Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA.

Land-use change is the main force behind ecological and social change in many countries around the globe; it is primarily driven by resource needs and external economic incentives. Concomitantly, transformations of the land are the main drivers for the emergence and re-emergence of malaria. An understanding of malaria population dynamics in transforming landscapes is lacking, despite its relevance for developmental and public health policies. We develop a mathematical model that couples malaria epidemiology with the socio-economic and demographic processes that occur in a landscape undergoing land-use change. This allows us to identify different types of malaria dynamics that can arise in early stages of this transformation. In particular, we show that an increase in transmission followed by either a decline, or a further enhancement, of risk is a common outcome. This increase results from the asymmetry between the relatively fast ecological changes in transformed landscapes, and the slower pace of investment in malaria protection. These results underscore the importance of reducing ecological risk, while providing services and economic opportunities to early migrants for longer periods. Consideration of these socio-ecological processes and, more importantly, the temporal scale on which they act, is critical to avoid potential bifurcations that lead to long-lasting endemic malaria.
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http://dx.doi.org/10.1038/s41559-017-0108DOI Listing
March 2017

The multilayer nature of ecological networks.

Nat Ecol Evol 2017 Mar 23;1(4):101. Epub 2017 Mar 23.

Institut des Sciences de l'Evolution, BioDICée team, UMR 5554, Université de Montpellier, CNRS, IRD, EPHE, CC 065, Place Eugéne Bataillon, 34095 Montpellier Cedex 05, France.

Although networks provide a powerful approach to study a large variety of ecological systems, their formulation does not typically account for multiple interaction types, interactions that vary in space and time, and interconnected systems such as networks of networks. The emergent field of 'multilayer networks' provides a natural framework for extending analyses of ecological systems to include such multiple layers of complexity, as it specifically allows one to differentiate and model 'intralayer' and 'interlayer' connectivity. The framework provides a set of concepts and tools that can be adapted and applied to ecology, facilitating research on high-dimensional, heterogeneous systems in nature. Here, we formally define ecological multilayer networks based on a review of previous, related approaches; illustrate their application and potential with analyses of existing data; and discuss limitations, challenges, and future applications. The integration of multilayer network theory into ecology offers largely untapped potential to investigate ecological complexity and provide new theoretical and empirical insights into the architecture and dynamics of ecological systems.
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http://dx.doi.org/10.1038/s41559-017-0101DOI Listing
March 2017

Seasonal Variation in the Epidemiology of Asymptomatic Infections across Two Catchment Areas in Bongo District, Ghana.

Am J Trop Med Hyg 2017 Jul;97(1):199-212

Department of Microbiology, New York University, New York, New York.

Understanding the epidemiology of asymptomatic infections is critical for countries to move toward malaria elimination. Using different methods for parasite detection, we evaluated how seasonality, spatial location, and other factors affect the age-specific epidemiology of asymptomatic malaria in Bongo District, Ghana. Asymptomatic prevalence by microscopy decreased significantly from 42.5% at the end of the wet to 27.5% at the end of the dry season ( < 0.001). Using the polymerase chain reactions (PCRs), all microscopy-negative samples were screened and prevalence of submicroscopic infections also decreased significantly from the wet (55.4%) to the dry (20.7%) season ( < 0.001). Combining detection methods, 74.4% and 42.5% of the population in the wet and dry seasons, respectively, had evidence of a . infection. Interestingly in those > 20 years of age, we found evidence of infection in 64.3% of the population in the wet and 27.0% in the dry season. Using both microscopy and PCR, the asymptomatic . reservoir peaks at the end of the wet season and infections in all age groups constitute the reservoir of malaria infection. At the end of the wet season, spatial heterogeneity in the prevalence and density of . infections was observed between the two catchment areas surveyed in Bongo District. These results indicate that if elimination is to succeed, interventions will need to target not just . infections in children but also in adults, and be implemented toward the end of the dry season in this area of West Africa.
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http://dx.doi.org/10.4269/ajtmh.16-0959DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5508908PMC
July 2017

Evidence of strain structure in gene repertoires in children from Gabon, West Africa.

Proc Natl Acad Sci U S A 2017 05 1;114(20):E4103-E4111. Epub 2017 May 1.

Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637.

Existing theory on competition for hosts between pathogen strains has proposed that immune selection can lead to the maintenance of strain structure consisting of discrete, weakly overlapping antigenic repertoires. This prediction of strain theory has conceptual overlap with fundamental ideas in ecology on niche partitioning and limiting similarity between coexisting species in an ecosystem, which oppose the hypothesis of neutral coexistence. For , strain theory has been specifically proposed in relation to the major surface antigen of the blood stage, known as EMP1 and encoded by the multicopy multigene family known as the genes. Deep sampling of the DBLα domain of genes in the local population of Bakoumba, West Africa, was completed to define whether patterns of repertoire overlap support a role of immune selection under the opposing force of high outcrossing, a characteristic of areas of intense malaria transmission. Using a 454 high-throughput sequencing protocol, we report extremely high diversity of the DBLα domain and a large parasite population with DBLα repertoires structured into nonrandom patterns of overlap. Such population structure, significant for the high diversity of genes that compose it at a local level, supports the existence of "strains" characterized by distinct gene repertoires. Nonneutral, frequency-dependent competition would be at play and could underlie these patterns. With a computational experiment that simulates an intervention similar to mass drug administration, we argue that the observed repertoire structure matters for the antigenic diversity of the parasite population remaining after intervention.
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http://dx.doi.org/10.1073/pnas.1613018114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5441825PMC
May 2017

Cholera forecast for Dhaka, Bangladesh, with the 2015-2016 El Niño: Lessons learned.

PLoS One 2017 2;12(3):e0172355. Epub 2017 Mar 2.

Department of Ecology and Evolution, University of Chicago, Chicago, Illinois, United States of America.

A substantial body of work supports a teleconnection between the El Niño-Southern Oscillation (ENSO) and cholera incidence in Bangladesh. In particular, high positive anomalies during the winter (Dec-Feb) in sea surface temperatures (SST) in the tropical Pacific have been shown to exacerbate the seasonal outbreak of cholera following the monsoons from August to November. Climate studies have indicated a role of regional precipitation over Bangladesh in mediating this long-distance effect. Motivated by this previous evidence, we took advantage of the strong 2015-2016 El Niño event to evaluate the predictability of cholera dynamics for the city in recent times based on two transmission models that incorporate SST anomalies and are fitted to the earlier surveillance records starting in 1995. We implemented a mechanistic temporal model that incorporates both epidemiological processes and the effect of ENSO, as well as a previously published statistical model that resolves space at the level of districts (thanas). Prediction accuracy was evaluated with "out-of-fit" data from the same surveillance efforts (post 2008 and 2010 for the two models respectively), by comparing the total number of cholera cases observed for the season to those predicted by model simulations eight to twelve months ahead, starting in January each year. Although forecasts were accurate for the low cholera risk observed for the years preceding the 2015-2016 El Niño, the models also predicted a high probability of observing a large outbreak in fall 2016. Observed cholera cases up to Oct 2016 did not show evidence of an anomalous season. We discuss these predictions in the context of regional and local climate conditions, which show that despite positive regional rainfall anomalies, rainfall and inundation in Dhaka remained low. Possible explanations for these patterns are given together with future implications for cholera dynamics and directions to improve their prediction for the city.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0172355PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5333828PMC
August 2017

Population Density, Climate Variables and Poverty Synergistically Structure Spatial Risk in Urban Malaria in India.

PLoS Negl Trop Dis 2016 12 1;10(12):e0005155. Epub 2016 Dec 1.

Department of Ecology and Evolution, University of Chicago, Chicago, United States of America.

Background: The world is rapidly becoming urban with the global population living in cities projected to double by 2050. This increase in urbanization poses new challenges for the spread and control of communicable diseases such as malaria. In particular, urban environments create highly heterogeneous socio-economic and environmental conditions that can affect the transmission of vector-borne diseases dependent on human water storage and waste water management. Interestingly India, as opposed to Africa, harbors a mosquito vector, Anopheles stephensi, which thrives in the man-made environments of cities and acts as the vector for both Plasmodium vivax and Plasmodium falciparum, making the malaria problem a truly urban phenomenon. Here we address the role and determinants of within-city spatial heterogeneity in the incidence patterns of vivax malaria, and then draw comparisons with results for falciparum malaria.

Methodology/principal Findings: Statistical analyses and a phenomenological transmission model are applied to an extensive spatio-temporal dataset on cases of Plasmodium vivax in the city of Ahmedabad (Gujarat, India) that spans 12 years monthly at the level of wards. A spatial pattern in malaria incidence is described that is largely stationary in time for this parasite. Malaria risk is then shown to be associated with socioeconomic indicators and environmental parameters, temperature and humidity. In a more dynamical perspective, an Inhomogeneous Markov Chain Model is used to predict vivax malaria risk. Models that account for climate factors, socioeconomic level and population size show the highest predictive skill. A comparison to the transmission dynamics of falciparum malaria reinforces the conclusion that the spatio-temporal patterns of risk are strongly driven by extrinsic factors.

Conclusion/significance: Climate forcing and socio-economic heterogeneity act synergistically at local scales on the population dynamics of urban malaria in this city. The stationarity of malaria risk patterns provides a basis for more targeted intervention, such as vector control, based on transmission 'hotspots'. This is especially relevant for P. vivax, a more resilient parasite than P. falciparum, due to its ability to relapse and the operational shortcomings of delivering a "radical cure".
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http://dx.doi.org/10.1371/journal.pntd.0005155DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5131912PMC
December 2016

Climate forcing and infectious disease transmission in urban landscapes: integrating demographic and socioeconomic heterogeneity.

Ann N Y Acad Sci 2016 10 28;1382(1):44-55. Epub 2016 Sep 28.

Ecology and Evolution Department, University of Chicago, Chicago, Illinois.

Urbanization and climate change are the two major environmental challenges of the 21st century. The dramatic expansion of cities around the world creates new conditions for the spread, surveillance, and control of infectious diseases. In particular, urban growth generates pronounced spatial heterogeneity within cities, which can modulate the effect of climate factors at local spatial scales in large urban environments. Importantly, the interaction between environmental forcing and socioeconomic heterogeneity at local scales remains an open area in infectious disease dynamics, especially for urban landscapes of the developing world. A quantitative and conceptual framework on urban health with a focus on infectious diseases would benefit from integrating aspects of climate forcing, population density, and level of wealth. In this paper, we review what is known about these drivers acting independently and jointly on urban infectious diseases; we then outline elements that are missing and would contribute to building such a framework.
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http://dx.doi.org/10.1111/nyas.13229DOI Listing
October 2016
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