My research focuses on the ecology of infectious disease. I am interested in how climate, species interactions, and global change drive infectious disease dynamics in humans and natural ecosystems. This research combines mathematical modeling and empirical work.
I finished my PhD in 2012 at the University of California Santa Barbara in Ecology, Evolution, and Marine Biology. I then completed a 2-year NSF postdoctoral research fellowship in the Intersection of Biology and Mathematical and Physical Sciences and Engineering at the University of North Carolina at Chapel Hill and North Carolina State University. I have been at Stanford since January 2015.
Boards, Advisory Committees, Professional Organizations
Faculty Fellow, Center for Innovation in Global Health (2015 - Present)
Member, Jasper Ridge Advisory Committee (2015 - Present)
B.S., University of Georgia, Honors Interdisciplinary Studies in Mathematical Biology (2007)
PhD, University of California Santa Barbara, Ecology, Evolution, and Marine Biology (2012)
Current Research and Scholarly Interests
Our research focuses on the ecology of infectious disease. We are interested in how climate, species interactions, and global change drive infectious disease dynamics in humans and natural ecosystems. This research combines mathematical modeling and empirical work. Our main study systems include vector-borne diseases in humans and fungal pathogens in California grasses.
- Introduction to Ecology
BIO 81 (Aut)
Independent Studies (8)
- Advanced Research Laboratory in Experimental Biology
BIO 199 (Aut, Win, Spr, Sum)
- Directed Reading in Biology
BIO 198 (Aut, Win)
- Directed Reading in Environment and Resources
ENVRES 398 (Win, Spr, Sum)
- Directed Research in Environment and Resources
ENVRES 399 (Aut, Win, Spr, Sum)
- Graduate Research
BIO 300 (Aut, Win, Spr, Sum)
- Out-of-Department Directed Reading
BIO 198X (Aut, Win)
- Out-of-Department Graduate Research
BIO 300X (Aut, Win, Spr, Sum)
- Teaching of Biology
BIO 290 (Win)
- Advanced Research Laboratory in Experimental Biology
Prior Year Courses
BIO 101 (Aut)
- Ecology and Evolution of Infectious Disease in a Changing World
BIO 2N (Spr)
Graduate and Fellowship Programs
Biology (School of Humanities and Sciences) (Phd Program)
Detecting the impact of temperature on transmission of Zika, dengue, and chikungunya using mechanistic models.
PLoS neglected tropical diseases
2017; 11 (4)
Recent epidemics of Zika, dengue, and chikungunya have heightened the need to understand the seasonal and geographic range of transmission by Aedes aegypti and Ae. albopictus mosquitoes. We use mechanistic transmission models to derive predictions for how the probability and magnitude of transmission for Zika, chikungunya, and dengue change with mean temperature, and we show that these predictions are well matched by human case data. Across all three viruses, models and human case data both show that transmission occurs between 18-34°C with maximal transmission occurring in a range from 26-29°C. Controlling for population size and two socioeconomic factors, temperature-dependent transmission based on our mechanistic model is an important predictor of human transmission occurrence and incidence. Risk maps indicate that tropical and subtropical regions are suitable for extended seasonal or year-round transmission, but transmission in temperate areas is limited to at most three months per year even if vectors are present. Such brief transmission windows limit the likelihood of major epidemics following disease introduction in temperate zones.
View details for DOI 10.1371/journal.pntd.0005568
View details for PubMedID 28448507
Environmental and Social Change Drive the Explosive Emergence of Zika Virus in the Americas.
PLoS neglected tropical diseases
2017; 11 (2)
Since Zika virus (ZIKV) was detected in Brazil in 2015, it has spread explosively across the Americas and has been linked to increased incidence of microcephaly and Guillain-Barré syndrome (GBS). In one year, it has infected over 500,000 people (suspected and confirmed cases) in 40 countries and territories in the Americas. Along with recent epidemics of dengue (DENV) and chikungunya virus (CHIKV), which are also transmitted by Aedes aegypti and Ae. albopictus mosquitoes, the emergence of ZIKV suggests an ongoing intensification of environmental and social factors that have given rise to a new regime of arbovirus transmission. Here, we review hypotheses and preliminary evidence for the environmental and social changes that have fueled the ZIKV epidemic. Potential drivers include climate variation, land use change, poverty, and human movement. Beyond the direct impact of microcephaly and GBS, the ZIKV epidemic will likely have social ramifications for women's health and economic consequences for tourism and beyond.
View details for DOI 10.1371/journal.pntd.0005135
View details for PubMedID 28182667
View details for PubMedCentralID PMC5300271
Mathematical models are a powerful method to understand and control the spread of Huanglongbing
Huanglongbing (HLB), or citrus greening, is a global citrus disease occurring in almost all citrus growing regions. It causes substantial economic burdens to individual growers, citrus industries and governments. Successful management strategies to reduce disease burden are desperately needed but with so many possible interventions and combinations thereof it is difficult to know which are worthwhile or cost-effective. We review how mathematical models have yielded useful insights into controlling disease spread for other vector-borne plant diseases, and the small number of mathematical models of HLB. We adapt a malaria model to HLB, by including temperature-dependent psyllid traits, "flushing" of trees, and economic costs, to show how models can be used to highlight the parameters that require more data collection or that should be targeted for intervention. We analyze the most common intervention strategy, insecticide spraying, to determine the most cost-effective spraying strategy. We find that fecundity and feeding rate of the vector require more experimental data collection, for wider temperatures ranges. Also, the best strategy for insecticide intervention is to spray for more days rather than pay extra for a more efficient spray. We conclude that mathematical models are able to provide useful recommendations for managing HLB spread.
View details for DOI 10.7717/peerj.2642
View details for Web of Science ID 000387170800006
View details for PubMedID 27833809
The role of competition - colonization tradeoffs and spatial heterogeneity in promoting trematode coexistence
2016; 97 (6): 1484-1496
Competition - colonization tradeoffs occur in many systems, and theory predicts that they can strongly promote species coexistence. However, there is little empirical evidence that observed competition - colonization tradeoffs are strong enough to maintain diversity in natural systems. This is due in part to a mismatch between theoretical assumptions and biological reality in some systems. We tested whether a competition - colonization tradeoff explains how a diverse trematode guild coexists in California horn snail populations, a system that meets the requisite criteria for the tradeoff to promote coexistence. A field experiment showed that subordinate trematode species tended to have higher colonization rates than dominant species. This tradeoff promoted coexistence in parameterized models but did not fully explain trematode diversity and abundance, suggesting a role of additional diversity maintenance mechanisms. Spatial heterogeneity is an alternative way to promote coexistence if it isolates competing species. We used scale transition theory to expand the competition - colonization tradeoff model to include spatial variation. The parameterized model showed that spatial variation in trematode prevalence did not isolate most species sufficiently to explain the overall high diversity, but could benefit some rare species. Together, the results suggest that several mechanisms combine to maintain diversity, even when a competition - colonization tradeoff occurs.
View details for DOI 10.1890/15-0753.1
View details for Web of Science ID 000377219900012
View details for PubMedID 27459779
The role of drought- and disturbance-mediated competition in shaping community responses to varied environments
2016; 181 (2): 621-632
By altering the strength of intra- and interspecific competition, droughts may reshape plant communities. Furthermore, species may respond differently to drought when other influences, such as herbivory, are considered. To explore this relationship, we conducted a greenhouse experiment measuring responses to inter- and intraspecific competition for two grasses, Schedonorus arundinaceus and Paspalum dilatatum, while varying water availability and simulating herbivory via clipping. We then parameterized population growth models to examine the long-term outcome of competition under these conditions. Under drought, S. arundinaceus was less water stressed than P. dilatatum, which exhibited severe water stress; clipping alleviated this stress, increasing the competitive ability of P. dilatatum relative to S. arundinaceus. Although P. dilatatum competed weakly under drought, clipping reduced water stress in P. dilatatum, thereby enhancing its ability to compete with S. arundinaceus under drought. Supporting these observations, population growth models predicted that P. dilatatum would exclude S. arundinaceus when clipped under drought, while S. arundinaceus would exclude P. dilatatum when unclipped under drought. When the modeled environment varied temporally, environmental variation promoted niche differences that, though insufficient to maintain stable coexistence, prevented unconditional competitive exclusion by promoting priority effects. Our results suggest that it is important to consider how species respond not just to stable, but also to variable, environments. When species differ in their responses to drought, competition, and simulated herbivory, stable environments may promote competitive exclusion, while fluctuating environments may promote coexistence. These interactions are critical to understanding how species will respond to global change.
View details for DOI 10.1007/s00442-016-3582-9
View details for Web of Science ID 000376296000026
View details for PubMedID 26893230
The rise and fall of infectious disease in a warmer world.
Now-outdated estimates proposed that climate change should have increased the number of people at risk of malaria, yet malaria and several other infectious diseases have declined. Although some diseases have increased as the climate has warmed, evidence for widespread climate-driven disease expansion has not materialized, despite increased research attention. Biological responses to warming depend on the non-linear relationships between physiological performance and temperature, called the thermal response curve. This leads performance to rise and fall with temperature. Under climate change, host species and their associated parasites face extinction if they cannot either thermoregulate or adapt by shifting phenology or geographic range. Climate change might also affect disease transmission through increases or decreases in host susceptibility and infective stage (and vector) production, longevity, and pathology. Many other factors drive disease transmission, especially economics, and some change in time along with temperature, making it hard to distinguish whether temperature drives disease or just correlates with disease drivers. Although it is difficult to predict how climate change will affect infectious disease, an ecological approach can help meet the challenge.
View details for DOI 10.12688/f1000research.8766.1
View details for PubMedID 27610227
- Within-Host Niche Differences and Fitness Trade-offs Promote Coexistence of Plant Viruses AMERICAN NATURALIST 2016; 187 (1): E13-E26
- Mapping Physiological Suitability Limits for Malaria in Africa Under Climate Change VECTOR-BORNE AND ZOONOTIC DISEASES 2015; 15 (12): 718-725
- Controls over native perennial grass exclusion and persistence in California grasslands invaded by annuals ECOLOGY 2015; 96 (10): 2643-2652
Differential Impacts of Virus Diversity on Biomass Production of a Native and an Exotic Grass Host
2015; 10 (7)
Pathogens are common and diverse in natural communities and have been implicated in the success of host invasions. Yet few studies have experimentally measured how pathogens impact native versus exotic hosts, particularly when individual hosts are simultaneously coinfected by diverse pathogens. To estimate effects of interactions among multiple pathogens within host individuals on both transmission of pathogens and fitness consequences for hosts, we conducted a greenhouse experiment using California grassland species: the native perennial grass Nassella (Stipa) pulchra, the exotic annual grass Bromus hordeaceus, and three virus species, Barley yellow dwarf virus-PAV, Barley yellow dwarf virus-MAV, and Cereal yellow dwarf virus-RPV. In terms of virus transmission, the native host was less susceptible than the exotic host to MAV. Coinfection of PAV and MAV did not occur in any of the 157 co-inoculated native host plants. In the exotic host, PAV infection most strongly reduced root and shoot biomass, and coinfections that included PAV severely reduced biomass. Infection with single or multiple viruses did not affect biomass in the native host. However, in this species the most potentially pathogenic coinfections (PAV + MAV and PAV + MAV + RPV) did not occur. Together, these results suggest that interactions among multiple pathogens can have important consequences for host health, which may not be predictable from interactions between hosts and individual pathogens. This work addresses a key empirical gap in understanding the impact of multiple generalist pathogens on competing host species, with potential implications for population and community dynamics of native and exotic species. It also demonstrates how pathogens with relatively mild impacts independently can more substantially reduce host performance in coinfection.
View details for DOI 10.1371/journal.pone.0134355
View details for Web of Science ID 000358838400105
View details for PubMedID 26230720
- Pathogen impacts on plant diversity in variable environments OIKOS 2015; 124 (4): 414-420
The community ecology of pathogens: coinfection, coexistence and community composition
2015; 18 (4): 401-415
Disease and community ecology share conceptual and theoretical lineages, and there has been a resurgence of interest in strengthening links between these fields. Building on recent syntheses focused on the effects of host community composition on single pathogen systems, we examine pathogen (microparasite) communities using a stochastic metacommunity model as a starting point to bridge community and disease ecology perspectives. Such models incorporate the effects of core community processes, such as ecological drift, selection and dispersal, but have not been extended to incorporate host-pathogen interactions, such as immunosuppression or synergistic mortality, that are central to disease ecology. We use a two-pathogen susceptible-infected (SI) model to fill these gaps in the metacommunity approach; however, SI models can be intractable for examining species-diverse, spatially structured systems. By placing disease into a framework developed for community ecology, our synthesis highlights areas ripe for progress, including a theoretical framework that incorporates host dynamics, spatial structuring and evolutionary processes, as well as the data needed to test the predictions of such a model. Our synthesis points the way for this framework and demonstrates that a deeper understanding of pathogen community dynamics will emerge from approaches working at the interface of disease and community ecology.
View details for DOI 10.1111/ele.12418
View details for Web of Science ID 000351619500009
View details for PubMedID 25728488
Understanding uncertainty in temperature effects on vector-borne disease: a Bayesian approach
2015; 96 (1): 203-213
Extrinsic environmental factors influence the distribution and population dynamics of many organisms, including insects that are of concern for human health and agriculture. This is particularly true for vector-borne infectious diseases like malaria, which is a major source of morbidity and mortality in humans. Understanding the mechanistic links between environment and population processes for these diseases is key to predicting the consequences of climate change on transmission and for developing effective interventions. An important measure of the intensity of disease transmission is the reproductive number R0. However, understanding the mechanisms linking R0 and temperature, an environmental factor driving disease risk, can be challenging because the data available for parameterization are often poor. To address this, we show how a Bayesian approach can help identify critical uncertainties in components of R0 and how this uncertainty is propagated into the estimate of R0. Most notably, we find that different parameters dominate the uncertainty at different temperature regimes: bite rate from 15 degrees C to 25 degrees C; fecundity across all temperatures, but especially approximately 25-32 degrees C; mortality from 20 degrees C to 30 degrees C; parasite development rate at degrees 15-16 degrees C and again at approximately 33-35 degrees C. Focusing empirical studies on these parameters and corresponding temperature ranges would be the most efficient way to improve estimates of R0. While we focus on malaria, our methods apply to improving process-based models more generally, including epidemiological, physiological niche, and species distribution models.
View details for DOI 10.1890/13-1964.1
View details for Web of Science ID 000349198900023
View details for PubMedID 26236905
Despite spillover, a shared pathogen promotes native plant persistence in a cheatgrass-invaded grassland
2013; 94 (12): 2744-2753
How pathogen spillover influences host community diversity and composition is poorly understood. Spillover occurs when transmission from a reservoir host species drives infection in another host species. In cheatgrass-invaded grasslands in the western United States, a fungal seed pathogen, black fingers of death (Pyrenophora semeniperda), spills over from exotic cheatgrass (Bromus tectorum) to native perennial bunchgrasses such as squirreltail (Elymus elymoides). Previous theoretical work based on this system predicts that pathogens that spill over can favor either host coexistence, the exclusion of either host species, or priority effects, depending on species-specific transmission rates and pathogen tolerance. Here, these model predictions were tested by parameterizing a population growth model with field data from Skull Valley, Utah, USA. The model suggests that, across the observed range of demographic variation, the pathogen is most likely to provide a net benefit to squirreltail and a net cost to cheatgrass, though both effects are relatively weak. Although cheatgrass (the reservoir host) is more tolerant, squirreltail is far less susceptible to infection, and its long-lived adult stage buffers population growth against seed losses to the pathogen. This work shows that, despite pathogen spillover, the shared pathogen promotes native grass persistence by reducing exotic grass competition. Counterintuitively, the reservoir host does not necessarily benefit from the presence of the pathogen, and may even suffer greater costs than the nonreservoir host. Understanding the consequences of shared pathogens for host communities requires weighing species differences in susceptibility, transmission, and tolerance using quantitative models.
View details for DOI 10.1890/13-0086.1
View details for Web of Science ID 000328928300009
View details for PubMedID 24597221
Consequences of Pathogen Spillover for Cheatgrass-Invaded Grasslands: Coexistence, Competitive Exclusion, or Priority Effects
2013; 181 (6): 737-747
With the rise in species invasions and emerging infectious diseases, pathogen spillover from abundant reservoir hosts to their competitors is increasingly common. Although the potential for pathogen spillover is widespread, its consequences for host community composition remain poorly understood. To address this gap, I examine the consequences of fungal seed pathogen spillover from an exotic annual grass (cheatgrass) to a native perennial bunchgrass in the Intermountain West, United States, using a model. Integrating generalist pathogens with broader coexistence theory, the model measures the pathogen's effect on host niche differences and fitness differences, which determine the outcome of competition. The model demonstrates that the consequences of pathogen spillover depend on host differences in species-specific transmission and disease tolerance. Counterintuitively, spillover can lead to coexistence, native grass exclusion, or priority effects, in which either species can exclude the other when initially more dominant. Cheatgrass has higher tolerance for infection, which could lead to competitive dominance or to coexistence if the native grass has a fecundity or survival advantage. In sum, multihost pathogens can affect host communities in a range of ways, depending on the specific mechanism of spillover.
View details for DOI 10.1086/670190
View details for Web of Science ID 000318996500004
View details for PubMedID 23669537
Optimal temperature for malaria transmission is dramatically lower than previously predicted
2013; 16 (1): 22-30
The ecology of mosquito vectors and malaria parasites affect the incidence, seasonal transmission and geographical range of malaria. Most malaria models to date assume constant or linear responses of mosquito and parasite life-history traits to temperature, predicting optimal transmission at 31 °C. These models are at odds with field observations of transmission dating back nearly a century. We build a model with more realistic ecological assumptions about the thermal physiology of insects. Our model, which includes empirically derived nonlinear thermal responses, predicts optimal malaria transmission at 25 °C (6 °C lower than previous models). Moreover, the model predicts that transmission decreases dramatically at temperatures > 28 °C, altering predictions about how climate change will affect malaria. A large data set on malaria transmission risk in Africa validates both the 25 °C optimum and the decline above 28 °C. Using these more accurate nonlinear thermal-response models will aid in understanding the effects of current and future temperature regimes on disease transmission.
View details for DOI 10.1111/ele.12015
View details for Web of Science ID 000312301300003
View details for PubMedID 23050931
Soil Moisture and Fungi Affect Seed Survival in California Grassland Annual Plants
2012; 7 (6)
Survival of seeds in the seed bank is important for the population dynamics of many plant species, yet the environmental factors that control seed survival at a landscape level remain poorly understood. These factors may include soil moisture, vegetation cover, soil type, and soil pathogens. Because many soil fungi respond to moisture and host species, fungi may mediate environmental drivers of seed survival. Here, I measure patterns of seed survival in California annual grassland plants across 15 species in three experiments. First, I surveyed seed survival for eight species at 18 grasslands and coastal sage scrub sites ranging across coastal and inland Santa Barbara County, California. Species differed in seed survival, and soil moisture and geographic location had the strongest influence on survival. Grasslands had higher survival than coastal sage scrub sites for some species. Second, I used a fungicide addition and exotic grass thatch removal experiment in the field to tease apart the relative impact of fungi, thatch, and their interaction in an invaded grassland. Seed survival was lower in the winter (wet season) than in the summer (dry season), but fungicide improved winter survival. Seed survival varied between species but did not depend on thatch. Third, I manipulated water and fungicide in the laboratory to directly examine the relationship between water, fungi, and survival. Seed survival declined from dry to single watered to continuously watered treatments. Fungicide slightly improved seed survival when seeds were watered once but not continually. Together, these experiments demonstrate an important role of soil moisture, potentially mediated by fungal pathogens, in driving seed survival.
View details for DOI 10.1371/journal.pone.0039083
View details for Web of Science ID 000305340000065
View details for PubMedID 22720037
Pathogen impacts on plant communities: unifying theory, concepts, and empirical work
2011; 81 (3): 429-441
View details for Web of Science ID 000293457300003
Competition-defense tradeoffs and the maintenance of plant diversity
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
2010; 107 (40): 17217-17222
Ecologists have long observed that consumers can maintain species diversity in communities of their prey. Many theories of how consumers mediate diversity invoke a tradeoff between species' competitive ability and their ability to withstand predation. Under this constraint, the best competitors are also most susceptible to consumers, preventing them from excluding other species. However, empirical evidence for competition-defense tradeoffs is limited and, as such, the mechanisms by which consumers regulate diversity remain uncertain. We performed a meta-analysis of 36 studies to evaluate the prevalence of the competition-defense tradeoff and its role in maintaining diversity in plant communities. We quantified species' responses to experimental resource addition and consumer removal as estimates of competitive ability and resistance to consumers, respectively. With this analysis, we found mixed empirical evidence for a competition-defense tradeoff; in fact, competitive ability tended to be weakly positively correlated with defense overall. However, when present, negative relationships between competitive ability and defense influenced species diversity in the manner predicted by theory. In the minority of communities for which a tradeoff was detected, species evenness was higher, and resource addition and consumer removal reduced diversity. Our analysis reframes the commonly held notion that consumers structure plant communities through a competition-defense tradeoff. Such a tradeoff can maintain diversity when present, but negative correlations between competitive ability and defense were less common than is often assumed. In this respect, this study supports an emerging theoretical paradigm in which predation interacts with competition to both enhance and reduce species diversity.
View details for DOI 10.1073/pnas.1007745107
View details for Web of Science ID 000282512000032
View details for PubMedID 20855605
- Soil moisture mediated interaction between Polygonatum biflorum and leaf spot disease PLANT ECOLOGY 2010; 209 (1): 1-9
Parasites in food webs: the ultimate missing links
2008; 11 (6): 533-546
Parasitism is the most common consumer strategy among organisms, yet only recently has there been a call for the inclusion of infectious disease agents in food webs. The value of this effort hinges on whether parasites affect food-web properties. Increasing evidence suggests that parasites have the potential to uniquely alter food-web topology in terms of chain length, connectance and robustness. In addition, parasites might affect food-web stability, interaction strength and energy flow. Food-web structure also affects infectious disease dynamics because parasites depend on the ecological networks in which they live. Empirically, incorporating parasites into food webs is straightforward. We may start with existing food webs and add parasites as nodes, or we may try to build food webs around systems for which we already have a good understanding of infectious processes. In the future, perhaps researchers will add parasites while they construct food webs. Less clear is how food-web theory can accommodate parasites. This is a deep and central problem in theoretical biology and applied mathematics. For instance, is representing parasites with complex life cycles as a single node equivalent to representing other species with ontogenetic niche shifts as a single node? Can parasitism fit into fundamental frameworks such as the niche model? Can we integrate infectious disease models into the emerging field of dynamic food-web modelling? Future progress will benefit from interdisciplinary collaborations between ecologists and infectious disease biologists.
View details for DOI 10.1111/j.1461-0248.2008.01174.x
View details for Web of Science ID 000255552100001
View details for PubMedID 18462196