Anna E. Jolles

Impacts of biodiversity on the emergence and transmission of infectious diseases

Current unprecedented declines in biodiversity reduce the ability of ecological communities to provide many fundamental ecosystem services. Here we evaluate evidence that reduced biodiversity affects the transmission of infectious diseases of humans, other animals and plants. In principle, loss of biodiversity could either increase or decrease disease transmission. However, mounting evidence indicates that biodiversity loss frequently increases disease transmission. In contrast, areas of naturally high biodiversity may serve as a source pool for new pathogens. Overall, despite many remaining questions, current evidence indicates that preserving intact ecosystems and their endemic biodiversity should generally reduce the prevalence of infectious diseases.

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.

Hidden Effects of Chronic Tuberculosis in African Buffalo

Infectious diseases can bring about population declines and local host extinctions, contributing significantly to the global biodiversity crisis. Nonetheless, studies measuring population-level effects of pathogens in wild host populations are rare, and taxonomically biased toward avian hosts and macroparasitic infections. We investigated the effects of bovine tuberculosis (bTB), caused by the bacterial pathogen Mycobacterium bovis, on African buffalo (Syncerus caffer) at Hluhluwe-iMfolozi Park, South Africa. We tested 1180 buffalo for bTB infection between May 2000 and November 2001. Most infections were mild, confirming the chronic nature of the disease in buffalo. However, our data indicate that bTB affects both adult survival and fecundity. Using an age-structured population model, we demonstrate that the pathogen can reduce population growth rate drastically; yet its effects appear difficult to detect at the population level: bTB causes no conspicuous mass mortalities or fast population declines, nor...

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.

DISEASE TRANSMISSION OF ASPERGILLOSIS IN SEA FANS: INFERRING PROCESS FROM SPATIAL PATTERN

Despite recent high impacts of disease in the ocean, quantitative studies of diseases in natural marine populations lag far behind terrestrial systems. Transmission processes are poorly known in relatively open marine systems. We studied infection of sea fans Gorgonia ventalina by the fungus Aspergillus sydowii. To assess detectability and mechanisms of secondary transmission of the fungus, we analyzed the spatial distribution of disease among the fans, using Ripleys K as a measure of disease aggregation. Coral populations and disease were mapped at three reefs in the Florida Keys. Where disease prevalence was low, the disease was distributed randomly among sea fans. This is consistent with disease transmission by input of infectious fungal material from terrestrial sources only. However, where disease prevalence was high, the disease was significantly aggregated among sea fans at the 2-8 m scale, consistent with secondary disease trans- mission. Such transmission could take place by physical contact between neighboring fans, or infected fans might shed fungal material into the water column, and other fans become infected by these fomites. Our results suggest that water-borne transmission occurs, but secondary transmission by physical contact is also likely. We cannot falsify the hypothesis that small-scale local environmental conditions also contribute to disease aggregation.

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.

Life History and Demographic Drivers of Reservoir Competence for Three Tick-Borne Zoonotic Pathogens

Animal and plant species differ dramatically in their quality as hosts for multi-host pathogens, but the causes of this variation are poorly understood. A group of small mammals, including small rodents and shrews, are among the most competent natural reservoirs for three tick-borne zoonotic pathogens, Borrelia burgdorferi, Babesia microti, and Anaplasma phagocytophilum, in eastern North America. For a group of nine commonly-infected mammals spanning >2 orders of magnitude in body mass, we asked whether life history features or surrogates for (unknown) encounter rates with ticks, predicted reservoir competence for each pathogen. Life history features associated with a fast pace of life generally were positively correlated with reservoir competence. However, a model comparison approach revealed that host population density, as a proxy for encounter rates between hosts and pathogens, generally received more support than did life history features. The specific life history features and the importance of host population density differed somewhat between the different pathogens. We interpret these results as supporting two alternative but non-exclusive hypotheses for why ecologically widespread, synanthropic species are often the most competent reservoirs for multi-host pathogens. First, multi-host pathogens might adapt to those hosts they are most likely to experience, which are likely to be the most abundant and/or frequently bitten by tick vectors. Second, species with fast life histories might allocate less to certain immune defenses, which could increase their reservoir competence. Results suggest that of the host species that might potentially be exposed, those with comparatively high population densities, small bodies, and fast pace of life will often be keystone reservoirs that should be targeted for surveillance or management.

Non-random biodiversity loss underlies predictable increases in viral disease prevalence

Disease dilution (reduced disease prevalence with increasing biodiversity) has been described for many different pathogens. Although the mechanisms causing this phenomenon remain unclear, the disassembly of communities to predictable subsets of species, which can be caused by changing climate, land use or invasive species, underlies one important hypothesis. In this case, infection prevalence could reflect the competence of the remaining hosts. To test this hypothesis, we measured local host species abundance and prevalence of four generalist aphid-vectored pathogens (barley and cereal yellow dwarf viruses) in a ubiquitous annual grass host at 10 sites spanning 2000 km along the North American West Coast. In laboratory and field trials, we measured viral infection as well as aphid fecundity and feeding preference on several host species. Virus prevalence increased as local host richness declined. Community disassembly was non-random: ubiquitous hosts dominating species-poor assemblages were among the most competent for vector production and virus transmission. This suggests that non-random biodiversity loss led to increased virus prevalence. Because diversity loss is occurring globally in response to anthropogenic changes, such work can inform medical, agricultural and veterinary disease research by providing insights into the dynamics of pathogens nested within a complex web of environmental forces.

Horns honestly advertise parasite infection in male and female African buffalo

The evolution and maintenance of elaborate secondary sexual characters in males have been the subject of intense interest since Darwins time. Parasite-mediated sexual selection (PMSS) suggests that elaborate ornaments serve as honest indicators of male health and parasite resistance. Studies testing this key prediction of PMSS have largely focused on ornaments, with the role parasites might play in the maintenance of elaborate weapons being relatively understudied. Here, we tested whether weapon (horn) size was an indicator of health status in male and female African buffalo, Syncerus caffer. We examined whether individuals with larger horns were less likely to be infected with parasites, and had lower parasite loads and stronger immune systems. In males, horn size was significantly negatively correlated with the number of different parasites infecting an individual (parasite richness), the likelihood of infection with strongyle nematodes and coccidia, and strongyle intensity. In females, horn size was significantly negatively correlated with parasite richness, occurrence of coccidia infection, coccidia intensity and white blood cell count. These findings were robust when the effects of body condition, age and season were controlled for, consistent with the idea that horns function as honest indicators of health in both sexes. Our study provides new insight into the evolution and maintenance of elaborate weapons in mammals, suggesting a role for PMSS in both males and females.