Genomics reveals historic and contemporary transmission dynamics of a bacterial disease among wildlife and livestock

Whole-genome sequencing has provided fundamental insights into infectious disease epidemiology, but has rarely been used for examining transmission dynamics of a bacterial pathogen in wildlife. In the Greater Yellowstone Ecosystem (GYE), outbreaks of brucellosis have increased in cattle along with rising seroprevalence in elk. Here we use a genomic approach to examine Brucella abortus evolution, cross-species transmission and spatial spread in the GYE. We find that brucellosis was introduced into wildlife in this region at least five times. The diffusion rate varies among Brucella lineages (∼3 to 8 km per year) and over time. We also estimate 12 host transitions from bison to elk, and 5 from elk to bison. Our results support the notion that free-ranging elk are currently a self-sustaining brucellosis reservoir and the source of livestock infections, and that control measures in bison are unlikely to affect the dynamics of unrelated strains circulating in nearby elk populations

Genomics of Brucellosis in Wildlife and Livestock of the Greater Yellowstone Ecosystem

Brucellosis, a disease caused by the bacterium Brucella abortus, has recently been expanding its distribution in the Greater Yellowstone Ecosystem (GYE), with increased outbreaks in cattle and rising seroprevalence in elk (Cervus elaphus) over the past decade. Genetic studies suggest elk are a primary source of recent transmission to cattle. However, these studies are based on Variable Number Tandem Repeat (VNTR) data, which are limited in assessing and quantifying transmission among species. The goal of this study was to (i) investigate the introduction history of B. abortus in the GYE, (ii) identify B. abortus lineages associated with host species and/or geographic localities, and (iii) quantify transmission across wildlife and livestock host species and populations. We sequenced B. abortus whole genomes (n= 207) derived from isolates collected from three host species (bison, elk, cattle) over the past 30 years, throughout the GYE. We identified genetic variation among isolates, and applied a spatial diffusion phylogeographic modeling approach that incorporated temporal information from sampling. Based on these data, our results suggest four divergent Brucella lineages, with a time to most recent common ancestor of ~130 years ago, possibly representing a minimum of four brucellosis introductions into the GYE. Two Brucella lineages were generally clustered by geography. Evidence for cross-species transmission was detected among all species, though most events occur within species and herds. Understanding transmission dynamics is imperative for implementing effective control measures and may assist in identifying source populations responsible for past and future brucellosis infections in wildlife and outbreaks in livestock

Predicting Bison Migration out of Yellowstone National Park Using Bayesian Models

Long distance migrations by ungulate species often surpass the boundaries of preservation areas where conflicts with various publics lead to management actions that can threaten populations. We chose the partially migratory bison (Bison bison) population in Yellowstone National Park as an example of integrating science into management policies to better conserve migratory ungulates. Approximately 60% of these bison have been exposed to bovine brucellosis and thousands of migrants exiting the park boundary have been culled during the past two decades to reduce the risk of disease transmission to cattle. Data were assimilated using models representing competing hypotheses of bison migration during 1990–2009 in a hierarchal Bayesian framework. Migration differed at the scale of herds, but a single unifying logistic model was useful for predicting migrations by both herds. Migration beyond the northern park boundary was affected by herd size, accumulated snow water equivalent, and aboveground dried biomass. Migration beyond the western park boundary was less influenced by these predictors and process model performance suggested an important control on recent migrations was excluded. Simulations of migrations over the next decade suggest that allowing increased numbers of bison beyond park boundaries during severe climate conditions may be the only means of avoiding episodic, large-scale reductions to the Yellowstone bison population in the foreseeable future. This research is an example of how long distance migration dynamics can be incorporated into improved management policies

Data from: Yellowstone bison—should we preserve artificial population substructure or rely on ecological processes?

Halbert et al. (2012) analyzed microsatellite genotypes collected from 661 Yellowstone bison sampled during winters from 1999 through 2003 and identified 2 genetically distinct subpopulations (central, northern) based on genotypic diversity and allelic distributions. Based on these findings, they raised concerns about the management and long-term conservation of Yellowstone bison due to disproportionate culling of the 2 subpopulations in some winters. The data and findings of Halbert et al. (2012) are significant and useful for managers charged with conserving these iconic wildlife. However, their article provides information regarding the behavior and management of Yellowstone bison that does not accurately portray historic or current conditions. This response clarifies those conditions and challenges some of their apparent deductions and recommendations

NPSResponseToHalbert_etal_TableS1_JHered_Apr2012

Breeding season ranges used by radio-collared, female bison in Yellowstone National Park during 2002-201

NPSResponseToHalbert_etal_TableS2_JHered_Apr2012

Estimates of F-statistics and the number of migrants between central and northern breeding herds based on DNA extracted from fecal samples collected from male and female Yellowstone bison in both herds during the breeding seasons of 2006 and 2008 (Gardipee 2007)

Evaluation of fecal samples as a valid source of DNA by comparing paired blood and fecal samples from American bison (Bison bison)

Abstract Background The collection and analysis of fecal DNA is a common practice, especially when dealing with wildlife species that are difficult to track or capture. While fecal DNA is known to be lower quality than traditional sources of DNA, such as blood or other tissues, few investigations have verified fecal samples as a valid source of DNA by directly comparing the results to high quality DNA samples from the same individuals. Our goal was to compare DNA from fecal and blood samples from the same 50 American plains bison (Bison bison) from Yellowstone National Park, analyze 35 short tandem repeat (STR) loci for genotyping efficiency, and compare heterozygosity estimates. Results We discovered that some of the fecal-derived genotypes obtained were significantly different from the blood-derived genotypes from the same bison. We also found that fecal-derived DNA samples often underestimated heterozygosity values, in some cases by over 20%. Conclusions These findings highlight a potential shortcoming inherent in previous wildlife studies that relied solely on a multi-tube approach, using exclusively low quality fecal DNA samples with no quality control to account for false alleles and allelic dropout. Herein, we present a rigorous marker selection protocol that is applicable for a wide range of species and report a set of 15 STR markers for use in future bison studies that yielded consistent results from both fecal and blood-derived DNA

Data from: State-space modeling to support management of brucellosis in the Yellowstone bison population

The Yellowstone bison (Bison bison) exemplifies the challenge of conserving large mammals that migrate across the boundaries of conservation areas. Bison in Yellowstone are infected with brucellosis (Brucella abortus). Their seasonal movements can expose livestock to infection. We developed a Bayesian state-space model to reveal the influence of brucellosis on the dynamics of the Yellowstone bison population and to inform decisions on bison management. A model of frequency dependent transmission was superior to a density dependent model in its ability to predict out-of-sample observations of the probability of horizontal transmission (mean square prediction error frequency model = 0.78, density dependent model = 0.91). Conditional on the frequency dependent model, the median transmission rate of brucellosis was 1.86 year-1 (95% equal-tailed credible interval, BCI = 1.5, 2.2). The median of the posterior distribution of the basic reproductive ratio (R0) was 1.76 (BCI = 1.47, 2.36). Seroprevalence of adult females varied around 60% during the last two decades; however only 13 of 100 adult females were infectious (BCI = 0.1, 0.15). Estimation of population growth rate (_) in the presence of brucellosis reflected the depressing effect of the disease on recruitment; _ for an infected population averaged 1.07 (BCI = 1.03, 1.11) and for a healthy population _ = 1.12 (BCI = 1.07, 1.16). We used forecasting with a five year horizon to evaluate the ability of different actions to meet goals for management relative to a no action alternative. Annually removing 200 seropositive female bison increased the probability of reducing seroprevalence below 40% by 30-fold relative to no action and increased the probability of achieving a 50% reduction in transmission probability by a factor of 110 relative to no action. Annually vaccinating 200 seronegative animals increased the probability of achieving a 50% reduction transmission probability by five fold over no action. Forecasts of the future state of the population became increasingly uncertain with increases in the forecast horizon. Our findings emphasize the necessity of iterative, adaptive management with a relatively short term commitment to action, a commitment that must be reevaluated frequently in response to new data and model forecasts

Mitochondrial Genome Analysis Reveals Historical Lineages in Yellowstone Bison

<div><p>Yellowstone National Park is home to one of the only plains bison populations that have continuously existed on their present landscape since prehistoric times without evidence of domestic cattle introgression. Previous studies characterized the relatively high levels of nuclear genetic diversity in these bison, but little is known about their mitochondrial haplotype diversity. This study assessed mitochondrial genomes from 25 randomly selected Yellowstone bison and found 10 different mitochondrial haplotypes with a haplotype diversity of 0.78 (± 0.06). Spatial analysis of these mitochondrial DNA (mtDNA) haplotypes did not detect geographic population subdivision (F_ST = -0.06, p = 0.76). However, we identified two independent and historically important lineages in Yellowstone bison by combining data from 65 bison (defined by 120 polymorphic sites) from across North America representing a total of 30 different mitochondrial DNA haplotypes. Mitochondrial DNA haplotypes from one of the Yellowstone lineages represent descendants of the 22 indigenous bison remaining in central Yellowstone in 1902. The other mitochondrial DNA lineage represents descendants of the 18 females introduced from northern Montana in 1902 to supplement the indigenous bison population and develop a new breeding herd in the northern region of the park. Comparing modern and historical mitochondrial DNA diversity in Yellowstone bison helps uncover a historical context of park restoration efforts during the early 1900s, provides evidence against a hypothesized mitochondrial disease in bison, and reveals the signature of recent hybridization between American plains bison (<i>Bison bison bison</i>) and Canadian wood bison (<i>B</i>. <i>b</i>. <i>athabascae</i>). Our study demonstrates how mitochondrial DNA can be applied to delineate the history of wildlife species and inform future conservation actions.</p></div

Data from: Manipulating the system: how large herbivores control bottom-up regulation of grasslands

1.Decades of grazing studies have identified a number of key plant and soil processes affected by large herbivores and how those grazer effects vary among different grassland types. However, there remains little mechanistic understanding about how the effects of grazers on plants and soils may be biogeochemically linked in regulating grassland processes. 2.Here we measured monthly plant and soil variables, including soil moisture, soil nitrogen (N) availability, plant biomass, shoot N concentration and plant production, in grazed and ungrazed (fenced) grasslands during the 2012-2014 growing seasons. Measurements were used to assess direct and indirect biogeochemical pathways by which grazers influenced net aboveground plant production (NAP) in dry and mesic grasslands in Yellowstone National Park (YNP). 3.Herbivores only had direct effects on plant variables at the dry grassland compared to direct and indirect effects on both plant and soil variables at the mesic grassland. By enhancing leaf N content at both grasslands, grazers shifted the resource controlling NAP from N in ungrazed grassland to moisture, and potentially phosphorus and/or other soil nutrients, in grazed grassland. 4.Synthesis. These results indicate the mechanistic linkage between top-down (herbivore) and bottom-up (soil resource) control of grassland production. Changing the resources that limit NAP likely has a profound impact on how grazed vs ungrazed YNP grasslands respond to environmental (e.g., climate, atmospheric N deposition) variability. Because grazing enhances leaf N among many types of grasslands, increasing the sensitivity of plant production to the availability of moisture and nutrients other than N may be a general response of grasslands to grazing