Vanessa O. Ezenwa

Avian diversity and West Nile virus: testing associations between biodiversity and infectious disease risk

The emergence of several high profile infectious diseases in recent years has focused attention on our need to understand the ecological factors contributing to the spread of infectious diseases. West Nile virus (WNV) is a mosquito-borne zoonotic disease that was first detected in the United States in 1999. The factors accounting for variation in the prevalence of WNV are poorly understood, but recent ideas suggesting links between high biodiversity and reduced vector-borne disease risk may help account for distribution patterns of this disease. Since wild birds are the primary reservoir hosts for WNV, we tested associations between passerine (Passeriform) bird diversity, non-passerine (all other orders) bird diversity and virus infection rates in mosquitoes and humans to examine the extent to which bird diversity is associated with WNV infection risk. We found that non-passerine species richness (number of non-passerine species) was significantly negatively correlated with both mosquito and human infection rates, whereas there was no significant association between passerine species richness and any measure of infection risk. Our findings suggest that non-passerine diversity may play a role in dampening WNV amplification rates in mosquitoes, minimizing human disease risk.

Animal Behavior and the Microbiome

Feedbacks between microbiomes and their hosts affect a range of animal behaviors. Human bodies house trillions of symbiotic microorganisms. The genes in this human microbiome outnumber human genes by 100 to 1, and their study is providing profound insights into human health. But humans are not the only animals with microbiomes, and microbiomes do not just impact health. Recent research is revealing surprising roles for microbiomes in shaping behaviors across many animal taxa—shedding light on how behaviors from diet to social interactions affect the composition of host-associated microbial communities (1, 2), and how microbes in turn influence host behavior in dramatic ways (2–6).

Infecting epidemiology with genetics: a new frontier in disease ecology

Disease ecologists strive to understand the causes and consequences of parasite infection, including the emergence, spread, persistence and evolution of infectious disease. These processes can be illuminated by parasite genetic markers, which can be used to track parasite spread and infer population history. Recently, a growing number of studies have used molecular tools to examine questions on the ecology of infectious diseases. We review this burgeoning area of research by focusing on three topics where genetic tools will increasingly make major contributions: inferring parasite transmission, reconstructing epidemiological history and identifying physical and environmental drivers of disease spread. We also discuss areas for future research and highlight the promise of multidisciplinary collaborations among geneticists, ecologists and epidemiologists.

Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo

Epidemiological studies typically focus on single-parasite systems, although most hosts harbor multiple parasite species; thus, the potential impacts of co-infection on disease dynamics are only beginning to be recognized. Interactions between macroparasites, such as gastrointestinal nematodes, and microparasites causing diseases like TB, AIDS, and malaria are particularly interesting because co-infection may favor transmission and progression of these important diseases. Here we present evidence for strong interactions between gastrointestinal worms and bovine tuberculosis (TB) in free-ranging African buffalo (Syncerus caffer). TB and worms are negatively associated at the population, among-herd, and within-herd scales, and this association is not solely the result of demographic heterogeneities in infection. Combining data from 1362 buffalo with simple mechanistic models, we find that both accelerated mortality of co-infected individuals and TB transmission heterogeneity caused by trade-offs in immunity to the two types of parasites likely contribute to observed infection patterns. This study is one of the first to examine the relevance of within-host immunological trade-offs for understanding parasite distribution patterns in natural populations.

Hidden Consequences of Living in a Wormy World : Nematode-Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co‐occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T‐helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune‐mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown. We used cross‐sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free‐ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode‐induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild.

From Host Immunity to Pathogen Invasion: The Effects of Helminth Coinfection on the Dynamics of Microparasites

Concurrent infections with multiple parasites are ubiquitous in nature. Coinfecting parasites can interact with one another in a variety of ways, including through the hosts immune system via mechanisms such as immune trade-offs and immunosuppression. These within-host immune processes mediating interactions among parasites have been described in detail, but how they scale up to determine disease dynamic patterns at the population level is only beginning to be explored. In this review, we use helminth-microparasite coinfection as a model for examining how within-host immunological effects may influence the ecological outcome of microparasitic diseases, with a specific focus on disease invasion. The current literature on coinfection between helminths and major microparasitic diseases includes many studies documenting the effects of helminths on individual host responses to microparasites. In many cases, the observed host responses map directly onto parameters relevant for quantifying disease dynamics; however, there have been few attempts at integrating data on individual-level effects into theoretical models to extrapolate from the individual to the population level. Moreover, there is considerable variability in the particular combination of disease parameters affected by helminths across different microparasite systems. We develop a conceptual framework identifying some potential sources of such variability: Pathogen persistence and severity, and resource availability to hosts. We also generate testable hypotheses regarding diseases and the environmental contexts when the effects of helminths on microparasite dynamics should be most pronounced. Finally, we use a case study of helminth and mycobacterial coinfection in the African buffalo to illustrate both progress and challenges in understanding the population-level consequences of within-host immunological interactions, and conclude with suggestions for future research that will help improve our understanding of the effects of coinfection on dynamics of infectious diseases.

Habitat overlap and gastrointestinal parasitism in sympatric African bovids

Gastrointestinal parasite infections are widespread among wild ungulates. Because many of these parasites infect multiple host species, inter-specific interactions among hosts potentially play an important role in parasite transmission dynamics in ungulate communities. In this study, the effects of inter-specific contact on parasitism rates in 11 sympatric African bovids was examined using habitat overlap among species as a measure of cross-species contact rates. Across individual hosts, strongyle nematode abundance increased with increasing numbers of bovid species occupying a habitat. Furthermore, comparative analyses show a positive association between strongyle prevalence and level of habitat overlap across taxa. These findings suggest that among sympatric bovids, contact between species contributes significantly to the transmission of generalist nematode parasites. For a more host-specific parasite group, coccidia, parasite abundance and individual probability of infection declined in hosts living in bovid rich habitats. This pattern may reflect enhanced interspecific competition among parasites in these areas. Finally, similar to strongyle abundance, individual parasite richness also increased among hosts occupying habitats with higher numbers of bovid species. No association between habitat overlap and parasite richness was detected at higher taxonomic scales, however, which suggests that contact between host species may not contribute to parasite colonization of new host taxa.

Effects of Vulture Declines on Facultative Scavengers and Potential Implications for Mammalian Disease Transmission

Vultures (Accipitridae and Cathartidae) are the only known obligate scavengers. They feed on rotting carcasses and are the most threatened avian functional group in the world. Possible effects of vulture declines include longer persistence of carcasses and increasing abundance of and contact between facultative scavengers at these carcasses. These changes could increase rates of transmission of infectious diseases, with carcasses serving as hubs of infection. To evaluate these possibilities, we conducted a series of observations and experimental tests of the effects of vulture extirpation on decomposition rates of livestock carcasses and mammalian scavengers in Kenya. We examined whether the absence of vultures changed carcass decomposition time, number of mammalian scavengers visiting carcasses, time spent by mammals at carcasses, and potential for disease transmission at carcasses (measured by changes in intraspecific contact rates). In the absence of vultures, mean carcass decomposition rates nearly tripled. Furthermore, the mean number of mammals at carcasses increased 3-fold (from 1.5 to 4.4 individuals/carcass), and the average time spent by mammals at carcasses increased almost 3-fold (from 55 min to 143 min). There was a nearly 3-fold increase in the mean number of contacts between mammalian scavengers at carcasses without vultures. These results highlight the role of vultures in carcass decomposition and level of contact among mammalian scavengers. In combination, our findings lead us to hypothesize that changes in vulture abundance may affect patterns of disease transmission among mammalian carnivores.

Candidate gene microsatellite variation is associated with parasitism in wild bighorn sheep

The loss of genetic variation in host populations is thought to increase host susceptibility to parasites. However, few data exist to test this hypothesis in natural populations. Bighorn sheep (Ovis canadensis) populations occasionally suffer disease-induced population declines, allowing us to test for the associations between reduced genetic variation and parasitism in this species. Here, we show that individual mean heterozygosity for 15 microsatellite loci is associated with lungworm abundance (Protostrongylus spp.) in a small, recently bottlenecked population of bighorn sheep (linear regression, r2=0.339, p=0.007). This association remains significant for seven microsatellites located in genes (p=0.010), but not for eight neutral microsatellites (p=0.306). Furthermore, heterozygotes at three of four microsatellites located within disease-related genes had lower lungworm burdens. This study corroborates theoretical findings that increased parasitism and disease may be a consequence of reduced heterozygosity in wild populations, and that certain individual loci influence parasite resistance. The results illustrate the usefulness of using genomic information, strong candidate genes and non-invasive sampling for monitoring both genetic variation and fitness-related traits, such as parasite resistance, in natural populations.

Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales

Co-infection complicates treatment Infections rarely occur in isolation, and treating one pathogen may have unpredictable effects on another. Ezenwa and Jolles, working on wild African buffaloes, expected that because deworming relieves immune suppression, such treatment would lead to a drop in tuberculosis because the animals would clear the second infection without further intervention. Not so. Deworming did improve the lot of parasite-infested individuals, but it also increased the spread of tuberculosis among the population. What apparently happened is that the worm-free buffalo lived longer but stayed infected with tuberculosis and had longer to spread the infection among the herd. Science, this issue p. 175 Targeting one pathogen reduces infection by it, but allows a second pathogen to propagate in an African buffalo population. Parasitic worms modulate host immune responses in ways that affect microbial co-infections. For this reason, anthelmintic therapy may be a potent tool for indirectly controlling microbial pathogens. However, the population-level consequences of this type of intervention on co-infecting microbes are unknown. We evaluated the effects of anthelmintic treatment on bovine tuberculosis (BTB) acquisition, mortality after infection, and pathogen fitness in free-ranging African buffalo. We found that treatment had no effect on the probability of BTB infection, but buffalo survival after infection was ninefold higher among treated individuals. These contrasting effects translated into an approximately eightfold increase in the reproductive number of BTB for anthelmintic-treated compared with untreated buffalo. Our results indicate that anthelmintic treatment can enhance the spread of microbial pathogens in some real-world situations.