Wild Host Populations Research Articles

Infection thresholds for two interacting pathogens in a wild animal population

We present a model for the dynamics of two interacting pathogen variants in a wild animal host population. Using the next-generation matrix approach we define the invasion threshold for one pathogen variant when the other is already established and at steady state. We then provide explicit criteria for the special cases where: i) the two pathogen variants exclude each other; ii) one variant excludes the other; iii) the population dynamics of hosts infected with both variants are independent of the order of infection; iv) there is no interaction between the variants; and v) one variant enhances transmission of the other.

When does a parasite become a disease? eDNA unravels complex host-pathogen dynamics across environmental stress gradients in wild salmonid populations

Infectious diseases stem from disrupted interactions among hosts, parasites, and the environment. Both abiotic and biotic factors can influence infection outcomes by shaping the abundance of a parasite's infective stages, as well as the host's ability to fight infection. However, disentangling these mechanisms within natural ecosystems remains challenging. Here, combining environmental DNA analysis and niche modelling at a regional scale, we uncovered the biotic and abiotic drivers of an infectious disease of salmonid fish, triggered by the parasite Tetracapsuloides bryosalmonae. We found that the occurrence and abundance of the parasite in the water—i.e., the propagule pressure— were mainly correlated to the abundances of its two primary hosts, the bryozoan Fredericella sultana and the fish Salmo trutta, but poorly to local abiotic environmental stressors. In contrast, the occurrence and abundance of parasites within fish hosts—i.e., proxies for disease emergence—were closely linked to environmental stressors (water temperature, agricultural activities, dams), and to a lesser extent to parasite propagule pressure. These results suggest that pathogen distribution alone cannot predict the risk of disease in wildlife, and that local anthropogenic stressors may play a pivotal role in disease emergence among wild host populations, likely by modulating the hosts' immune response. Our study sheds light on the intricate interplay between biotic and abiotic factors in shaping pathogen distribution and raises concerns about the effects of global change on pathogen emergence.

Endogenous virophages are active and mitigate giant virus infection in the marine protist Cafeteria burkhardae

Endogenous viral elements (EVEs) are common genetic passengers in various protists. Some EVEs represent viral fossils, whereas others are still active. The marine heterotrophic flagellate Cafeteria burkhardae contains several EVE types related to the virophage mavirus, a small DNA virus that parasitizes the lytic giant virus CroV. We hypothesized that endogenous virophages may act as an antiviral defense system in protists, but no protective effect of virophages in wild host populations has been shown so far. Here, we tested the activity of virophage EVEs and studied their impact on giant virus replication. We found that endogenous mavirus-like elements (EMALEs) from globally distributed Cafeteria populations produced infectious virus particles specifically in response to CroV infection. However, reactivation was stochastic, often inefficient, and poorly reproducible. Interestingly, only one of eight EMALE types responded to CroV infection, implying that other EMALEs may be linked to different giant viruses. We isolated and cloned several reactivated virophages and characterized their particles, genomes, and infection dynamics. All tested virophages inhibited the production of CroV during coinfection, thereby preventing lysis of the host cultures in a dose-dependent manner. Comparative genomics of different C. burkhardae strains revealed that inducible EMALEs are common and are not linked to specific geographic locations. We demonstrate that naturally occurring virophage EVEs reactivate upon giant virus infection, thus providing a striking example that eukaryotic EVEs can become active under specific conditions. Moreover, our results support the hypothesis that virophages can act as an adaptive antiviral defense system in protists.

Co-parasitism in the face of predation: Effects of natural enemies on a neotropical mockingbird.

Co-parasitism is ubiquitous and has important consequences for the ecology and evolution of wild host populations. Studies of parasite co-infections remain limited in scope, with few experimental tests of the fitness consequences of multiple parasites, especially in natural populations. We measured the separate and combined effects of Philornis seguyi nest flies and shiny cowbirds Molothrus bonariensis on the fitness of a shared host, the chalk-browed mockingbird (Mimus saturninus) in Argentina. Using a two-factor experimental approach, we manipulated the presence of nest flies and cowbirds in mockingbird nests and assessed their effects on mockingbird haemoglobin levels, begging and provisioning rates, body size, and fledging success. We also monitored rates of nest predation in relation to parasitism by flies and cowbirds. Nest flies reduced the haemoglobin concentration, body size, and fledging success of mockingbirds, likely because mockingbirds did not compensate for parasitism by begging more or feeding their nestlings more. Cowbirds also reduced the fledging success of mockingbirds, even though they had no detectable effect on haemoglobin or body size. Nests with cowbirds, which beg more than mockingbirds, attracted more nest predators. There was no significant interaction between the effects of flies and cowbirds on any component of mockingbird fitness. The combined effects of nest flies and cowbirds were strictly additive. In summary, we show that nest flies and cowbirds both reduce host fitness, but do not have interactive effects in co-parasitized nests. Our results further suggest that predators exacerbate the effects of nest flies and cowbirds on their hosts. Our study shows that the fitness consequences of co-parasitism are complex, especially in the context of community-level interactions.

Ectoparasites population dynamics are affected by host body size but not host density or water temperature in a 32‐year long time series

Host density, host body size and ambient temperature have all been positively associated with increases in parasite infection. However, the relative importance of these factors in shaping long‐term parasite population dynamics in wild host populations is unknown due to the absence of long‐term studies. Here, we examine long‐term drivers of gill lice (Copepoda) infections in Arctic charr (Salmonidae) over 32 years. We predicted that host density and body size and water temperature would all positively affect parasite population size and population growth rate. Our results show that fish size was the main driver of gill lice infections in Arctic charr. In addition, Arctic charr became infected at smaller sizes and with more parasites in years of higher brown trout population size. Negative intraguild interactions between brown trout and Arctic charr appear to drive smaller Arctic charr to seek refuge in deeper areas of the lake, thus increasing infection risk. There was no effect of host density on the force of infection, and the relationship between Arctic charr density and parasite mean abundance was negative, possibly due to an encounter‐dilution effect. The population densities of host and parasite fluctuated independently of one another. Water temperature had negligible effects on the temporal dynamics of the gill lice population. Understanding long‐term drivers of parasite population dynamics is key for research and management. In fish farms, artificially high densities of hosts lead to vast increases in the transmission of parasitic copepods. However, in wild fish populations fluctuating at natural densities, the surface area available for copepodid attachment might be more important than the density of available hosts.

Spatially structured eco-evolutionary dynamics in a host-pathogen interaction render isolated populations vulnerable to disease

While the negative effects that pathogens have on their hosts are well-documented in humans and agricultural systems, direct evidence of pathogen-driven impacts in wild host populations is scarce and mixed. Here, to determine how the strength of pathogen-imposed selection depends on spatial structure, we analyze growth rates across approximately 4000 host populations of a perennial plant through time coupled with data on pathogen presence-absence. We find that infection decreases growth more in the isolated than well-connected host populations. Our inoculation study reveals isolated populations to be highly susceptible to disease while connected host populations support the highest levels of resistance diversity, regardless of their disease history. A spatial eco-evolutionary model predicts that non-linearity in the costs to resistance may be critical in determining this pattern. Overall, evolutionary feedbacks define the ecological impacts of disease in spatially structured systems with host gene flow being more important than disease history in determining the outcome.

Generalist nematodes dominate the nemabiome of roe deer in sympatry with sheep at a regional level

The growth of livestock farming and the recent expansion of wild ungulate populations in Europe favor opportunities for direct and/or indirect cross-transmission of pathogens. Comparatively few studies have investigated the epidemiology of gastro-intestinal nematode parasites, an ubiquitous and important community of parasites of ungulates, at the wildlife/livestock interface. In this study, we aimed to assess the influence of livestock proximity on the gastrointestinal nematode community of roe deer in a rural landscape located in southern France. Using ITS-2 rDNA nemabiome metabarcoding on fecal larvae, we analysed the gastrointestinal nematode communities of roe deer and sheep. In addition, we investigated Haemonchus contortus nad4 mtDNA diversity to specifically test parasite circulation among domestic and wild host populations. The dominant gastrointestinal nematode species found in both the roe deer and sheep were generalist species commonly found in small ruminant livestock (e.g. H. contortus), whereas the more specialised wild cervid nematode species (e.g. Ostertagia leptospicularis) were only present at low frequencies. This is in marked contrast with previous studies that found the nemabiomes of wild cervid populations to be dominated by cervid specialist nematode species. In addition, the lack of genetic structure of the nad4 mtDNA of H. contortus populations between host species suggests circulation of gastrointestinal nematodes between roe deer and sheep. The risk of contact with livestock only has a small influence on the nemabiome of roe deer, suggesting the parasite population of roe deer has been displaced by generalist livestock parasites due to many decades of sheep farming, not only for deer grazing close to pastures, but also at a larger regional scale. We also observed some seasonal variation in the nemabiome composition of roe deer. Overall, our results demonstrate significant exchange of gastrointestinal nematodes between domestic and wild ungulates, with generalist species spilling over from domestic ungulates dominating wild cervid parasite communities.

Implications of environmentally shaped microbial communities for insecticide resistance in Sitobion miscanthi

Insect-associated bacteria play an important role in the resistance to pesticides, yet bacterial community compositions in wild insect host populations and the environmental factors that shape them are mostly elusive. In this study, Sitobion miscanthi (Takahashi) populations were collected from major wheat growing regions in China. Following high-throughput sequencing of 16S rRNA gene fragments, association analyses were performed within the bacterial community associated with S. miscanthi, as well as with population resistance levels to four commonly used pesticides and different environmental factors. We found that bacterial community structures differed in various regions, and that the abundances of dominant bacteria such as Buchnera, Candidatus Regiella, Candidatus Hamiltonella showed high variations. The resistance of S. miscanthi to avermectin and bifenthrin was shown to decline with increasing bacterial diversity. Meanwhile, with the increase of bacterial network modularity, the resistance of S. miscanthi populations to imidacloprid, avermectin and bifenthrin also increased correspondingly. In addition, correlation analysis indicated that altitude and air pressure had the strongest impact on bacterial community diversity and relative abundance, followed by humidity, rainfall and temperature. Overall, insights into such complex interactions between bacteria and their insect hosts offer new directions for biological pest control.

Seroprevalence and incidence of Puumala orthohantavirus in its bank vole (Myodes glareolus) host population in northeastern France: Between-site and seasonal variability

Given the difficulty of measuring pathogen transmission in wildlife, epidemiological studies frequently rely on cross-sectional seroprevalence. However, seropositivity indicates only exposure to a pathogen at an unknown time. By allowing to obtain repeated test results from individuals sampled multiple times over an extended period, longitudinal data help reduce this uncertainty. We used capture-mark-recapture data on bank vole (Myodes glareolus) individuals collected at four sites over ten years in northeastern France to investigate the impact of environmental variables on seroprevalence and incidence of Puumala orthohantavirus (PUUV). PUUV causes a chronic infection without apparent symptoms, that may however impair survival of its rodent host in the wild. Viral transmission between rodents may occur through direct contact or via the environment. Principal component analysis was used to deal with multicollinearity among environmental variables. Incidence and seroprevalence were investigated with either generalized estimating equations or Poisson regression models depending on the number of observations for each season. In spring, only the factor site was found to be significant for seroprevalence, while a principal component including meteorological conditions of the previous winter and the normalized difference vegetation index (NDVI) of both the previous winter and spring had a significant effect on incidence. In autumn, only the factor site was significant for incidence, while two principal components, including either the meteorological conditions of the autumn and previous spring or NDVI of the autumn significantly affected seroprevalence. We discuss these results in light of the particular demography of small mammals. We encourage other researchers to investigate the relationships between demographic parameters of wild host populations and the environment, by using both incidence and seroprevalence.

Honey bees and climate explain viral prevalence in wild bee communities on a continental scale

Viruses are omnipresent, yet the knowledge on drivers of viral prevalence in wild host populations is often limited. Biotic factors, such as sympatric managed host species, as well as abiotic factors, such as climatic variables, are likely to impact viral prevalence. Managed and wild bees, which harbor several multi-host viruses with a mostly fecal–oral between-species transmission route, provide an excellent system with which to test for the impact of biotic and abiotic factors on viral prevalence in wild host populations. Here we show on a continental scale that the prevalence of three broad host viruses: the AKI-complex (Acute bee paralysis virus, Kashmir bee virus and Israeli acute paralysis virus), Deformed wing virus, and Slow bee paralysis virus in wild bee populations (bumble bees and solitary bees) is positively related to viral prevalence of sympatric honey bees as well as being impacted by climatic variables. The former highlights the need for good beekeeping practices, including Varroa destructor management to reduce honey bee viral infection and hive placement. Furthermore, we found that viral prevalence in wild bees is at its lowest at the extreme ends of both temperature and precipitation ranges. Under predicted climate change, the frequency of extremes in precipitation and temperature will continue to increase and may hence impact viral prevalence in wild bee communities.

Host, Microbiome, and Complex Space: Applying Population and Landscape Genetic Approaches to Gut Microbiome Research in Wild Populations.

In recent years, emerging sequencing technologies and computational tools have driven a tidal wave of research on host-associated microbiomes, particularly the gut microbiome. These studies demonstrate numerous connections between the gut microbiome and vital host functions, primarily in humans, model organisms, and domestic animals. As the adaptive importance of the gut microbiome becomes clearer, interest in studying the gut microbiomes of wild populations has increased, in part due to the potential for discovering conservation applications. The study of wildlife gut microbiomes holds many new challenges and opportunities due to the complex genetic, spatial, and environmental structure of wild host populations, and the potential for these factors to interact with the microbiome. The emerging picture of adaptive coevolution in host-microbiome relationships highlights the importance of understanding microbiome variation in the context of host population genetics and landscape heterogeneity across a wide range of host populations. We propose a conceptual framework for understanding wildlife gut microbiomes in relation to landscape variables and host population genetics, including the potential of approaches derived from landscape genetics. We use this framework to review current research, synthesize important trends, highlight implications for conservation, and recommend future directions for research. Specifically, we focus on how spatial structure and environmental variation interact with host population genetics and microbiome variation in natural populations, and what we can learn from how these patterns of covariation differ depending on host ecological and evolutionary traits.

Development of a PCR-RFLP method for differential identification of Microcotyle sebastis and Microcotyle caudata isolated from cultured rockfish in Korea.

Microcotylid monogeneans can cause considerable health problems in cultured fish, and several Microcotyle species are reported from scorpaenid fish, an economically important aquaculture target species in Korea. We developed a PCR-RFLP assay targeting the mitochondrial cox1 gene, for discriminating Microcotyle sebastis and M.caudata from cultured Korean rockfish Sebastes schlegelii and dark-banded rockfish S.inermis. AseI enzyme treatment of the PCR products showed that M.sebastis sequence was cleaved while M.caudata was not. A total of 95.2% (118/124) of monogeneans from S.schlegelii were identified as M.sebastis, and 96.2% (126/131) of monogeneans from S.inermis were identified as M.caudata by PCR-RFLP. However, the remaining parasites from each host showed the opposite digestion pattern. Additional analyses of these specimens by targeting the ITS region by PCR-RFLP showed the same results, suggesting that cross-species infection by the parasites may have occurred. In Korea, S.inermis net cages are commonly located nearby S.schlegelii net cages, and this encaged proximity might have provided the opportunity for cross-infection to occur. Further examination of wild host populations and experimental cross-infection will be necessary to explain this phenomenon. The PCR-RFLP method in this study will help investigate the epidemiology and infection dynamics of Microcotyle species in S.inermis.

Virus Prevalence and Genetic Diversity Across a Wild Bumblebee Community.

Viruses are key population regulators, but we have limited knowledge of the diversity and ecology of viruses. This is even the case in wild host populations that provide ecosystem services, where small fitness effects may have major ecological impacts in aggregate. One such group of hosts are the bumblebees, which have a major role in the pollination of food crops and have suffered population declines and range contractions in recent decades. In this study, we investigate the diversity of four recently discovered bumblebee viruses (Mayfield virus 1, Mayfield virus 2, River Liunaeg virus, and Loch Morlich virus), and two previously known viruses that infect both wild bumblebees and managed honeybees (Acute bee paralysis virus and Slow bee paralysis virus) from isolates in Scotland. We investigate the ecological and environmental factors that determine viral presence and absence. We show that the recently discovered bumblebee viruses were more genetically diverse than the viruses shared with honeybees. Coinfection is potentially important in shaping prevalence: we found a strong positive association between River Liunaeg virus and Loch Morlich virus presence after controlling for host species, location and other relevant ecological variables. We tested for a relationship between environmental variables (temperature, UV radiation, wind speed, and prevalence), but as we had few sampling sites, and thus low power for site-level analyses, we could not conclude anything regarding these variables. We also describe the relationship between the bumblebee communities at our sampling sites. This study represents a first step in the description of predictors of bumblebee infection in the wild.

Variation in Angiostrongylus cantonensis infection in definitive and intermediate hosts in Hawaii, a global hotspot of rat lungworm disease.

Angiostrongylus cantonensis (rat lungworm) is a tropical and subtropical parasitic nematode, with infections in humans causing angiostrongyliasis (rat lungworm disease), characterized by eosinophilic meningitis. Hawaii has been identified as a global hotspot of infection, with recent reports of high infection rates in humans, as well as rat definitive and snail intermediate hosts. This study investigated variation in A. cantonensis infection, both prevalence and intensity, in wild populations of two species of rats (Rattus exulans and R. rattus) and one species of snail (Parmarion martensi). An overall infection prevalence of 86.2% was observed in P. martensi and 63.8% in rats, with R. exulans (77.4%) greater than R. rattus (47.6%). We found infections to vary with environmental and host-related factors. Body mass was a strong predictor of infection in all three species, with different patterns seen between sexes and species of rats. Infection prevalence and intensity for R. exulans were high in May 2018 and again in February 2019, but generally lower and more variable during the intervening months. Information on sources of variability of infection in wild host populations will be a crucial component in predicting the effectiveness of future disease surveillance or targeted management strategies.

Population- and age-specific patterns of haemosporidian assemblages and infection levels in European bee-eaters (Merops apiaster)

Amongst other factors, host behaviour critically determines the patterns with which blood parasites occur in wild host populations. In particular, migratory hosts that sequentially occupy distant sites within and across years are expected to show distinct patterns of blood parasitism depending on their population-specific schedules and whereabouts. Here, we monitored haemosporidian parasitism in two populations of European bee-eaters (Merops apiaster), breeding in Portugal and Germany, with fundamentally different spatiotemporal migration patterns and colonisation histories. We describe and compare the composition of their parasite fauna as well as host population-, age- and sex-specific patterns in the frequency and intensity of infections. We found haemosporidian prevalence to be higher in Portugal compared with Germany and the prevalence generally increased with host age in both populations. Bee-eaters breeding in Portugal and wintering in western Africa mostly hosted parasites of the genus Haemoproteus, while Plasmodium lineages prevailed in birds breeding in Germany and wintering in central Africa. We found 18 genetic lineages, of which nine uniquely occurred in Germany, three uniquely in Portugal and six occurred in both breeding populations. The infection intensities (= % infected per inspected erythrocytes) ranged from 0.002% up to maximally 2.5% in Portugal and 9.6% in Germany. The intensity was higher in Germany compared with Portugal, vastly varied between the parasite genera (Haemoproteus > Plasmodium), but also differed between lineages of the same genus. Our results suggest that populations from different parts of a host’s breeding range differ in prevalence and the composition of their haemosporidian assemblages, rather than in the intensity of their infections. Whether these patterns are mainly caused by differential habitat use throughout the annual cycle and/or the population-specific co-evolutionary backgrounds of a host species in range expansion remains to be elucidated.

Beak and feather disease virus (BFDV) prevalence, load and excretion in seven species of wild caught common Australian parrots.

Pathogens pose a major risk to wild host populations, especially in the face of ongoing biodiversity declines. Beak and feather disease virus (BFDV) can affect most if not all members of one of the largest and most threatened bird orders world-wide, the Psittaciformes. Signs of disease can be severe and mortality rates high. Its broad host range makes it a risk to threatened species in particular, because infection can occur via spill-over from abundant hosts. Despite these risks, surveillance of BFDV in locally abundant wild host species has been lacking. We used qPCR and haemagglutination assays to investigate BFDV prevalence, load and shedding in seven abundant host species in the wild in south-east Australia: Crimson Rosellas (Platycercus elegans), Eastern Rosellas (Platycercus eximius), Galahs (Eolophus roseicapillus), Sulphur-crested Cockatoos (Cacatua galerita), Blue-winged Parrots (Neophema chrysostoma), Rainbow Lorikeets (Trichoglossus moluccanus) and Red-rumped Parrots (Psephotus haematonotus). We found BFDV infection in clinically normal birds in six of the seven species sampled. We focused our analysis on the four most commonly caught species, namely Crimson Rosellas (BFDV prevalence in blood samples: 41.8%), Sulphur-crested Cockatoos (20.0%), Blue-winged Parrots (11.8%) and Galahs (8.8%). Species, but not sex, was a significant predictor for BFDV prevalence and load. 56.1% of BFDV positive individuals were excreting BFDV antigen into their feathers, indicative of active viral replication with shedding. Being BFDV positive in blood samples predicted shedding in Crimson Rosellas. Our study confirms that BFDV is endemic in our study region, and can inform targeted disease management by providing comparative data on interspecies variation in virus prevalence, load and shedding.

Using wild mice to interrogate immunological mechanisms of asymptomatic malaria

Abstract Malaria is a significant world health problem, with billions of people at risk and over 200 million clinical cases per year that result in over 200,000 deaths. However, the majority of the population in malaria endemic areas (>60%) is asymptomatic (without overt symptoms), even in high transmission areas. Although identified by Plasmodium-infected red blood cells in the circulation, the term asymptomatic malaria is a misnomer with individuals experiencing mild anemia, vascular activation and increased susceptibility to co-morbidities such as non-typhoidal Salmonella infections. The immunological mechanisms governing the development and maintenance of asymptomatic malaria are poorly understood and the influence of host genetics in endemic populations is unknown. Currently, no immunologically intact animal model is available to understand how host genetics influence the asymptomatic nature of Plasmodium infection. Here, we use wild-derived Mus musculus to show that the genetic diversity seen in the wild host population leads to increased variation in anemia upon infection with Plasmodium yoelii XNL with a subpopulation of mice experiencing asymptomatic malaria with mild anemia. Plasma TNF-a was positively correlated with the level of anemia, as might be expected from studies showing a positive correlation of TNF-a with anemia in children. Also, there was a negative correlation between monocyte populations and anemia experienced by the mice, which has also been observed in asymptomatic children in eastern Uganda. These results show that the wild derived mice can model asymptomatic malaria and allow us to interrogate the different immune profiles that lead to the range of phenotypes to malarial disease.

Long-term retrospective assessment of a transmission hotspot for human alveolar echinococcosis in mid-west China

BackgroundHuman alveolar echinococcosis caused by infection with Echinococcus multilocularis is one of the most potentially pathogenic helminthic zoonoses. Transmission occurs involving wildlife cycles typically between fox and small mammal intermediate hosts. In the late 1980s/early 1990s a large focus of human AE was identified in poor upland agricultural communities in south Gansu Province, China. More detailed investigations in 1994–97 expanded community screening and identified key risk factors of dog ownership and landscape type around villages that could support susceptible rodent populations. A crash of the dog population (susceptible domestic definitive host) in the early 1990s appeared to stop transmission.Methodology/FindingsWe subsequently undertook follow-up eco-epidemiological studies based on human population screening and dog survey, in 2005/6 and in 2014/15. Our observations show a decrease in human AE prevalence, especially marked in the 11–30 year old age category. In 2015, although the dog population had recovered and in addition, forest protection and the reforestation of some areas may have favoured red fox (wild definitive host) population growth, there was no evidence of infection in owned dogs.Conclusions/SignificanceThose observations suggest that over decades socio-ecological changes resulted in a cascade of factors that exacerbated and then interrupted parasite emergence, with probable elimination of peri-domestic transmission of E. multilocularis in this area, despite the relative proximity of large active transmission foci on the eastern Tibetan Plateau. This study case exemplifies how anthropogenic land use and behavioural changes can modify emergence events and the transmission of endemic zoonotic parasite infections, and subsequently the importance of considering processes over the long-term in a systems approach in order to understand pathogen and disease distribution.

Population Genetic Divergence and Environment Influence the Gut Microbiome in Oregon Threespine Stickleback.

Much of animal-associated microbiome research has been conducted in species for which little is known of their natural ecology and evolution. Microbiome studies that combine population genetic, environment, and geographic data for wild organisms can be very informative, especially in situations where host genetic variation and the environment both influence microbiome variation. The few studies that have related population genetic and microbiome variation in wild populations have been constrained by observation-based kinship data or incomplete genomic information. Here we integrate population genomic and microbiome analyses in wild threespine stickleback fish distributed throughout western Oregon, USA. We found that gut microbiome diversity and composition partitioned more among than within wild host populations and was better explained by host population genetic divergence than by environment and geography. We also identified gut microbial taxa that were most differentially abundant across environments and across genetically divergent populations. Our findings highlight the benefits of studies that investigate host-associated microbiomes in wild organisms.

Context-dependent costs and benefits of tuberculosis resistance traits in a wild mammalian host.

Disease acts as a powerful driver of evolution in natural host populations, yet individuals in a population often vary in their susceptibility to infection. Energetic trade‐offs between immune and reproductive investment lead to the evolution of distinct life history strategies, driven by the relative fitness costs and benefits of resisting infection. However, examples quantifying the cost of resistance outside of the laboratory are rare. Here, we observe two distinct forms of resistance to bovine tuberculosis (bTB), an important zoonotic pathogen, in a free‐ranging African buffalo (Syncerus caffer) population. We characterize these phenotypes as “infection resistance,” in which hosts delay or prevent infection, and “proliferation resistance,” in which the host limits the spread of lesions caused by the pathogen after infection has occurred. We found weak evidence that infection resistance to bTB may be heritable in this buffalo population (h 2 = 0.10) and comes at the cost of reduced body condition and marginally reduced survival once infected, but also associates with an overall higher reproductive rate. Infection‐resistant animals thus appear to follow a “fast” pace‐of‐life syndrome, in that they reproduce more quickly but die upon infection. In contrast, proliferation resistance had no apparent costs and was associated with measures of positive host health—such as having a higher body condition and reproductive rate. This study quantifies striking phenotypic variation in pathogen resistance and provides evidence for a link between life history variation and a disease resistance trait in a wild mammalian host population.