Tad Dallas

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Species are not most abundant in the centre of their geographic range or climatic niche

The pervasive idea that species should be most abundant in the centre of their geographic range or centre of their climatic niche is a key assumption in many existing ecological hypotheses and has been declared a general macroecological rule. However, empirical support for decreasing population abundance with increasing distance from geographic range or climatic niche centre (distance-abundance relationships) remains fairly weak. We examine over 1400 bird, mammal, fish and tree species to provide a thorough test of distance-abundance relationships, and their associations with species traits and phylogenetic relationships. We failed to detect consistent distance-abundance relationships, and found no association between distance-abundance slope and species traits or phylogenetic relatedness. Together, our analyses suggest that distance-abundance relationships may be rare, difficult to detect, or are an oversimplification of the complex biogeographical forces that determine species spatial abundance patterns.

Nitrate enrichment alters a Daphnia–microparasite interaction through multiple pathways

Nutrient pollution has the potential to alter many ecological interactions, including host–parasite relationships. One of the largest sources of nutrient pollution comes from anthropogenic alteration of the nitrogen (N) cycle, specifically the increased rate of nitrate (NO3-N) deposition to aquatic environments, potentially altering host–parasite relationships. This study aimed to assess the mechanisms through which nitrate may impact host–pathogen relationships using a fungal pathogen (Metschnikowia bicuspidata) parasitic to crustacean zooplankton (Daphnia dentifera) as a tractable model system. First, the influence of nitrate on host population dynamics was assessed along a gradient of nitrate concentrations. Nitrate decreased host population size and increased infection prevalence. Second, the influence of nitrate on host reproduction, mortality, and infection intensity was assessed at the individual host level by examining the relationship between pathogen dose and infection prevalence at ambient (0.4 mg NO3-N*L−1) and intermediate (12 mg NO3-N*L−1) levels of nitrate. Host fecundity and infection intensity both decreased with increasing pathogen dose, but increased nitrate levels corresponded to greater infection intensities. Nitrate had no effect on host growth rate, suggesting that hosts do not alter feeding behavior in nitrate-treated media compared with ambient conditions. This study suggests that nutrient enrichment may enhance disease through increased transmission and infection intensity, but that high levels of nitrate may result in smaller epidemics through reduced transmission caused by smaller population sizes and increased pathogen mortality.

Parasite biodiversity faces extinction and redistribution in a changing climate

Parasites face range loss and shifts under climate change, with likely parasite extinction rates of up to one in three species. Climate change is a well-documented driver of both wildlife extinction and disease emergence, but the negative impacts of climate change on parasite diversity are undocumented. We compiled the most comprehensive spatially explicit data set available for parasites, projected range shifts in a changing climate, and estimated extinction rates for eight major parasite clades. On the basis of 53,133 occurrences capturing the geographic ranges of 457 parasite species, conservative model projections suggest that 5 to 10% of these species are committed to extinction by 2070 from climate-driven habitat loss alone. We find no evidence that parasites with zoonotic potential have a significantly higher potential to gain range in a changing climate, but we do find that ectoparasites (especially ticks) fare disproportionately worse than endoparasites. Accounting for host-driven coextinctions, models predict that up to 30% of parasitic worms are committed to extinction, driven by a combination of direct and indirect pressures. Despite high local extinction rates, parasite richness could still increase by an order of magnitude in some places, because species successfully tracking climate change invade temperate ecosystems and replace native species with unpredictable ecological consequences.

Data-driven identification of potential Zika virus vectors

Zika is an emerging virus whose rapid spread is of great public health concern. Knowledge about transmission remains incomplete, especially concerning potential transmission in geographic areas in which it has not yet been introduced. To identify unknown vectors of Zika, we developed a data-driven model linking vector species and the Zika virus via vector-virus trait combinations that confer a propensity toward associations in an ecological network connecting flaviviruses and their mosquito vectors. Our model predicts that thirty-five species may be able to transmit the virus, seven of which are found in the continental United States, including Culex quinquefasciatus and Cx. pipiens. We suggest that empirical studies prioritize these species to confirm predictions of vector competence, enabling the correct identification of populations at risk for transmission within the United States. DOI: http://dx.doi.org/10.7554/eLife.22053.001

Relative importance of environmental, geographic, and spatial variables on zooplankton metacommunities

Understanding the factors responsible for structuring ecological communities is a central goal in community ecology. Previous work has focused on determining the relative roles of two classes of variables (e.g., spatial and environmental) on community composition. However, this approach may ignore the disproportionate impact of variables within classes, and is often confounded by spatial autocorrelation leading to collinearity among variables of different classes. Here, we combine pattern-based metacommunity and machine learning analyses to characterize metacommunity structure of zooplankton from lakes in the northeast United States and to identify environmental, spatial, and geographic covariates associated with metacommunity structure. Analyses were performed for the entire metacommunity and for three zooplankton subsets (cladocerans, copepods, and rotifers), as the variables associated with community structure in these groups were hypothesized to differ. Species distributions of all subsets adhered to an environmental, spatial, and/or geographic gradient, but differed in metacommunity pattern, as copepod species distributions responded independently of one another, while the entire zooplankton metacommunity, cladocerans, and rotifers replaced one another in discrete groups. While environmental variables were nearly always the most important to metacommunity structure, the relative importance of variables differed among zooplankton subsets, suggesting that zooplankton subsets differ in their environmental tolerances and dispersal-limitation.

Costs of resistance and infection by a generalist pathogen

Abstract Pathogen infection is typically costly to hosts, resulting in reduced fitness. However, pathogen exposure may also come at a cost even if the host does not become infected. These fitness reductions, referred to as “resistance costs”, are inducible physiological costs expressed as a result of a trade‐off between resistance to a pathogen and aspects of host fitness (e.g., reproduction). Here, we examine resistance and infection costs of a generalist fungal pathogen (Metschnikowia bicuspidata) capable of infecting a number of host species. Costs were quantified as reductions in host lifespan, total reproduction, and mean clutch size as a function of pathogen exposure (resistance cost) or infection (infection cost). We provide empirical support for infection costs and modest support for resistance costs for five Daphnia host species. Specifically, only one host species examined incurred a significant cost of resistance. This species was the least susceptible to infection, suggesting the possibility that host susceptibility to infection is associated with the detectability and size of resistance cost. Host age at the time of pathogen exposure did not influence the magnitude of resistance or infection cost. Lastly, resistant hosts had fitness values intermediate between unexposed control hosts and infected hosts. Although not statistically significant, this could suggest that pathogen exposure does come at some marginal cost. Taken together, our findings suggest that infection is costly, resistance costs may simply be difficult to detect, and the magnitude of resistance cost may vary among host species as a result of host life history or susceptibility.

Predicting cryptic links in host-parasite networks

Networks are a way to represent interactions among one (e.g., social networks) or more (e.g., plant-pollinator networks) classes of nodes. The ability to predict likely, but unobserved, interactions has generated a great deal of interest, and is sometimes referred to as the link prediction problem. However, most studies of link prediction have focused on social networks, and have assumed a completely censused network. In biological networks, it is unlikely that all interactions are censused, and ignoring incomplete detection of interactions may lead to biased or incorrect conclusions. Previous attempts to predict network interactions have relied on known properties of network structure, making the approach sensitive to observation errors. This is an obvious shortcoming, as networks are dynamic, and sometimes not well sampled, leading to incomplete detection of links. Here, we develop an algorithm to predict missing links based on conditional probability estimation and associated, node-level features. We validate this algorithm on simulated data, and then apply it to a desert small mammal host-parasite network. Our approach achieves high accuracy on simulated and observed data, providing a simple method to accurately predict missing links in networks without relying on prior knowledge about network structure.

Competition-mediated feedbacks in experimental multispecies epizootics.

Competition structures ecological communities and alters host-pathogen interactions. In environmentally transmitted pathogens, an infection-resistant competitor may influence infection dynamics in a susceptible species through the negative impacts of competition (e.g., by reducing host density or causing nutritional stress that increases susceptibility to infection) and/or the positive impacts of reducing transmission efficiency (e.g., by removing environmental pathogen stages). Thus, a non-susceptible competitor may enhance, reduce, or have no net effect on susceptible host density and infection prevalence. Here, we couple an epidemiological model with experimental epidemics to test how resource competition with a non-susceptible competitor (Daphnia pulicaria) influences fungal microparasite (Metschnikowia bicuspidata) infection dynamics in a susceptible host species (D. dentifera). Our model and experiments suggest that competitor density can mediate the direction and magnitude of the effect of competition on infection dynamics, with a peak in infection prevalence occurring at intermediate competitor densities. At low densities, the non-susceptible competitor D. pulicaria may reduce infection prevalence in the susceptible host by removing fungal spores from the environment through feeding. However, when competitor density is increased and resources become limiting, D. pulicaria negatively impacts the susceptible host by increasing susceptible host feeding rates, and therefore fungal spore intake, and further by reducing susceptible host population size as it is driven toward competitive exclusion. In conclusion, these results show that a tradeoff between the competitor as a consumer of pathogen, which serves to reduce epidemic size, and as a modifier of susceptible host foraging ecology, which influences infection rates, may alternately enhance or dampen the magnitude of local epidemics.

Chemical attraction of Dermacentor variabilis ticks parasitic to Peromyscus leucopus based on host body mass and sex

Macroparasites are commonly aggregated on a small subset of a host population. Previous explanations for this aggregation relate to differences in immunocompetence or the degree to which hosts encounter parasites. We propose active tick host choice through chemical attraction as a potential mechanism leading to aggregated tick burdens. We test this hypothesis using a Y-maze olfactometer, comparing chemical attraction responses of larval and nymphal Dermacentor variabilis ticks parasitic to the white-footed mouse, Peromyscus leucopus, as a function of host sex and host body mass. We hypothesized that larger hosts and male hosts would be most attractive to searching ticks, as these hosts commonly have higher tick burdens in the field. Chemical attraction trials were run in the presence and absence of a known tick attractant, host-produced carbon dioxide (CO2). Male hosts and larger hosts were preferred by nymphal D. variabilis in the presence and absence of CO2, whereas larvae had no detectable host preference. The current study suggests that host-produced chemical cues may promote aggregated tick burdens among hosts of a single species based on host body mass and sex.