Julie C. Blackwood

Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats

Significance Bats are a frequent source of pathogen spillover to humans and livestock, and a reservoir for emerging infectious diseases. Transmission mechanisms within bat populations remain enigmatic, precluding effective management of zoonotic infections. Vampire bats transmit rabies virus throughout Latin America, causing lethal human rabies and thousands of livestock deaths every year. By selecting among competing transmission models applied to spatially replicated, longitudinal field data, we find that most rabies virus exposures are nonlethal and instead immunize bats, thus facilitating viral persistence. Further, frequent interactions among bats from different colonies are necessary to maintain the chain of transmission. We also evaluate the efficacy of bat culling and demonstrate that it has minimal effects on seroprevalence when spatially coordinated control is absent. Bats are important reservoirs for emerging infectious diseases, yet the mechanisms that allow highly virulent pathogens to persist within bat populations remain obscure. In Latin America, vampire-bat–transmitted rabies virus represents a key example of how such uncertainty can impede efforts to prevent cross-species transmission. Despite decades of agricultural and human health losses, control efforts have had limited success. To establish persistence mechanisms of vampire-bat–transmitted rabies virus in Latin America, we use data from a spatially replicated, longitudinal field study of vampire bats in Peru to parameterize a series of mechanistic transmission models. We find that single-colony persistence cannot occur. Instead, dispersal of bats between colonies, combined with a high frequency of immunizing nonlethal infections, is necessary to maintain rabies virus at levels consistent with field observations. Simulations show that the strong spatial component to transmission dynamics could explain the failure of bat culls to eliminate rabies and suggests that geographic coordination of control efforts might reduce transmission to humans and domestic animals. These findings offer spatial dynamics as a mechanism for rabies persistence in bats that might be important for the understanding and control of other bat-borne pathogens.

The effect of fishing on hysteresis in Caribbean coral reefs

Coral resilience is important for withstanding ecological disturbances as well as anthropogenic changes to the environment. However, the last several decades have demonstrated a decline in resilience that has often resulted in phase shifts to a degraded coral-depleted state with high levels of algal abundance. A major defining issue in current research is to identify when and how it is possible to reverse these phase shifts allowing for the ecosystem to escape coral depletion and maintain coral-based ecosystem services. We extend an analytic model to focus on the effects of over-harvesting of herbivorous reef fish in the Caribbean by explicitly including grazer dynamics which introduces feedbacks between habitat and grazer abundance posing constraints on management options excluded in previous studies. This allows us to develop ecosystem-based management recommendations for two distinct scenarios of coral reef recovery: The first follows significant habitat damage in response to a large disturbance and the second maintains reef structure but has suffered from events such as coral bleaching. We identify critical fishing effort levels to allow for coral recovery and demonstrate that regions exhibiting severe damage to reef structure have little resilience implying that fishing reductions should be coupled with other restoration methods. Regions that are coral-depleted but maintain reef structure allow for recovery given sufficiently small levels of fishing mortality. However, we demonstrate the difference in recovery time in response to varying levels of control efforts on fishing.

Bioeconomic synergy between tactics for insect eradication in the presence of Allee effects.

Preventing the establishment of invading pest species can be beneficial with respect to averting future environmental and economic impacts and also in preventing the accumulation of control costs. Allee effects play an important role in the dynamics of newly established, low-density populations by driving small populations into self-extinction, making Allee effects critical in influencing outcomes of eradication efforts. We consider interactions between management tactics in the presence of Allee effects to determine cost-effective and time-efficient combinations to achieve eradication by developing a model that considers pesticide application, predator augmentation and mating disruption as control tactics, using the gypsy moth as a case study. Our findings indicate that given a range of constant expenditure levels, applying moderate levels of pesticides in conjunction with mating disruption increases the Allee threshold which simultaneously substantially decreases the time to eradication relative to either tactic alone. In contrast, increasing predation in conjunction with other tactics requires larger economic expenditures to achieve similar outcomes for the use of pesticide application or mating disruption alone. These results demonstrate the beneficial synergy that may arise from nonlinearities associated with the simultaneous application of multiple eradication tactics and offer new prospects for preventing the establishment of damaging non-native species.

Deciphering the impacts of vaccination and immunity on pertussis epidemiology in Thailand

Pertussis is a highly infectious respiratory disease that is currently responsible for nearly 300,000 annual deaths worldwide, primarily in infants in developing countries. Despite sustained high vaccine uptake, a resurgence in pertussis incidence has been reported in a number of countries. This resurgence has led to critical questions regarding the transmission impacts of vaccination and pertussis immunology. We analyzed pertussis incidence in Thailand—both age-stratified and longitudinal aggregate reports—over the past 30 y. To dissect the contributions of waning pertussis immunity and repeat infections to pertussis epidemiology in Thailand following a pronounced increase in vaccine uptake, we used likelihood-based statistical inference methods to evaluate the support for multiple competing transmission models. We found that, in contrast to other settings, there is no evidence for pertussis resurgence in Thailand, with each model examined pointing to a substantial rise in herd immunity over the past 30 y. Using a variety of empirical metrics, we verified our findings by documenting signatures of changing herd immunity over the study period. Importantly, this work leads to the conclusion that repeat infections have played little role in shaping pertussis epidemiology in Thailand. Our results are surprisingly emphatic in support of measurable impact of herd immunity given the uncertainty associated with pertussis epidemiology.

Zika virus dynamics: When does sexual transmission matter?

The Zika virus (ZIKV) has captured worldwide attention with the ongoing epidemic in South America and its link to severe birth defects, most notably microcephaly. ZIKV is spread to humans through a combination of vector and sexual transmission, but the relative contribution of these transmission routes to the overall epidemic remains largely unknown. Furthermore, a disparity in the reported number of infections between males and females has been observed. We develop a mathematical model that describes the transmission dynamics of ZIKV to determine the processes driving the observed epidemic patterns. Our model reveals a 4.8% contribution of sexual transmission to the basic reproductive number, R0. This contribution is too minor to independently sustain an outbreak but suggests that vector transmission is the main driver of the ongoing epidemic. We also find a minor, yet statistically significant, difference in the mean number of cases in males and females, both at the peak of the epidemic and at equilibrium. While this suggests an intrinsic disparity between males and females, the differences do not account for the vastly greater number of reported cases for females, indicative of a large reporting bias. In addition, we identify conditions under which sexual transmission may play a key role in sparking an epidemic, including temperate areas where ZIKV mosquito vectors are less prevalent.

The population ecology of infectious diseases: pertussis in Thailand as a case study

Many of the fundamental concepts in studying infectious diseases are rooted in population ecology. We describe the importance of population ecology in exploring central issues in infectious disease research including identifying the drivers and dynamics of host-pathogen interactions and pathogen persistence, and evaluating the success of public health policies. The use of ecological concepts in infectious disease research is demonstrated with simple theoretical examples in addition to an analysis of case notification data of pertussis, a childhood respiratory disease, in Thailand as a case study. We stress that further integration of these fields will have significant impacts in infectious diseases research.

A cascade of destabilizations: Combining Wolbachia and Allee effects to eradicate insect pests

The management of insect pests has long been dominated by the use of chemical insecticides, with the aim of instantaneously killing enough individuals to limit their damage. To minimize unwanted consequences, environmentally friendly approaches have been proposed that utilize biological control and take advantage of intrinsic demographic processes to reduce pest populations. We address the feasibility of a novel pest management strategy based on the release of insects infected with Wolbachia, which causes cytoplasmic incompatibilities in its host population, into a population with a pre-existing Allee effect. We hypothesize that the transient decline in population size caused by a successful invasion of Wolbachia can bring the population below its Allee threshold and, consequently, trigger extinction. We develop a stochastic population model that accounts for Wolbachia-induced cytoplasmic incompatibilities in addition to an Allee effect arising from mating failures at low population densities. Using our model, we identify conditions under which cytoplasmic incompatibilities and Allee effects successfully interact to drive insect pest populations towards extinction. Based on our results, we delineate control strategies based on introductions of Wolbachia-infected insects. We extend this analysis to evaluate control strategies that implement successive introductions of two incompatible Wolbachia strains. Additionally, we consider methods that combine Wolbachia invasion with mating disruption tactics to enhance the pre-existing Allee effect. We demonstrate that Wolbachia-induced cytoplasmic incompatibility and the Allee effect act independently from one another: the Allee effect does not modify the Wolbachia invasion threshold, and cytoplasmic incompatibilities only have a marginal effect on the Allee threshold. However, the interaction of these two processes can drive even large populations to extinction. The success of this method can be amplified by the introduction of multiple Wolbachia cytotypes as well as the addition of mating disruption. Our study extends the existing literature by proposing the use of Wolbachia introductions to capitalize on pre-existing Allee effects and consequently eradicate insect pests. More generally, it highlights the importance of transient dynamics, and the relevance of manipulating a cascade of destabilizatons for pest management.

The role of interconnectivity in control of an Ebola epidemic.

Several West African countries - Liberia, Sierra Leone and Guinea - experienced significant morbidity and mortality during the largest Ebola epidemic to date, from late 2013 through 2015. The extent of the epidemic was fueled by outbreaks in large urban population centers as well as movement of the pathogen between populations. During the epidemic there was no known vaccine or drug, so effective disease control required coordinated efforts that include both standard medical and community practices such as hospitalization, quarantine and safe burials. Due to the high connectivity of the region, control of the epidemic not only depended on internal strategies but also was impacted by neighboring countries. In this paper, we use a deterministic framework to examine the role of movement between two populations in the overall success of practices designed to minimize the extent of Ebola epidemics. We find that it is possible for even small amounts of intermixing between populations to positively impact the control of an epidemic on a more global scale.

Competition and Stragglers as Mediators of Developmental Synchrony in Periodical Cicadas

Periodical cicadas are enigmatic organisms: broods spanning large spatial ranges consist of developmentally synchronized populations of 3–4 sympatric species that emerge as adults every 13 or 17 years. Only one brood typically occupies any single location, with well-defined boundaries separating distinct broods. The cause of such synchronous development remains uncertain, but it is known that synchronous emergence of large numbers of adults in a single year satiates predators, allowing a substantial fraction of emerging adults to survive long enough to reproduce. Competition among nymphs feeding on tree roots almost certainly plays a role in limiting populations. However, due to the difficulty of working with such long-lived subterranean life stages, the mechanisms governing competition in periodical cicadas have not been identified. A second process that may affect synchrony among periodical cicadas is their ability to delay or accelerate their emergence as adults by 1 year and accelerate it by 4 years (stragglers). We develop a nonlinear Leslie matrix–type model that describes cicada dynamics accounting for predation, competition, and stragglers. Using numerical simulations, we identify conditions that generate dynamics in which a single brood occupies a given geographical location. Our results show that while stragglers have the potential for introducing multiple sympatric broods, the interaction of interbrood competition with predation-driven Allee effects creates a system resistant to such invasions, and populations maintain developmental synchrony.

An introduction to compartmental modeling for the budding infectious disease modeler

ABSTRACT Mathematical models are ubiquitous in the study of the transmission dynamics of infectious diseases, In particular, the classic ‘susceptible-infectious-recovered’ (SIR) paradigm provides a modeling framework that can be adapted to describe the core transmission dynamics of a range of human and wildlife diseases. These models provide an important tool for uncovering the mechanisms generating observed disease dynamics, evaluating potential control strategies, and predicting future outbreaks. With ongoing advances in computational tools as well as access to disease incidence data, the use of such models continues to increase. Here, we provide a basic introduction to disease modeling that is primarily intended for individuals who are new to developing SIR-type models. In particular, we highlight several common issues encountered when structuring and analyzing these models.