Browsing by Author "Cassirer, E. Frances"

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Age-specific infectious period shapes dynamics of pneumonia in bighorn sheep
(2017-09) Plowright, Raina K.; Manlove, Kezia R.; Besser, Thomas E.; Paez, David J.; Andrews, Kimberly R.; Matthews, Patrick E.; Waits, Lisette P.; Hudson, Peter J.; Cassirer, E. Frances
Superspreading, the phenomenon where a small proportion of individuals contribute disproportionately to new infections, has profound effects on disease dynamics. Superspreading can arise through variation in contacts, infectiousness or infectious periods. The latter has received little attention, yet it drives the dynamics of many diseases of critical public health, livestock health and conservation concern. Here, we present rare evidence of variation in infectious periods underlying a superspreading phenomenon in a free-ranging wildlife system. We detected persistent infections of Mycoplasma ovipneumoniae, the primary causative agent of pneumonia in bighorn sheep (Ovis canadensis), in a small number of older individuals that were homozygous at an immunologically relevant genetic locus. Interactions among age-structure, genetic composition and infectious periods may drive feedbacks in disease dynamics that determine the magnitude of population response to infection. Accordingly, variation in initial conditions may explain divergent population responses to infection that range from recovery to catastrophic decline and extirpation.
A bioinformatic pipeline for identifying informative SNP panels for parentage assignment from RADseq data
(2018-06) Andrews, Kimberly R.; Adams, Jennifer R.; Cassirer, E. Frances; Plowright, Raina K.; Gardner, Colby; Dwire, Maggie; Hohenlohe, Paul A.; Waits, Lisette P.
The development of high-throughput sequencing technologies is dramatically increasing the use of single nucleotide polymorphisms (SNPs) across the field of genetics, but most parentage studies of wild populations still rely on microsatellites. We developed a bioinformatic pipeline for identifying SNP panels that are informative for parentage analysis from restriction site-associated DNA sequencing (RADseq) data. This pipeline includes options for analysis with or without a reference genome, and provides methods to maximize genotyping accuracy and select sets of unlinked loci that have high statistical power. We test this pipeline on small populations of Mexican gray wolf and bighorn sheep, for which parentage analyses are expected to be challenging due to low genetic diversity and the presence of many closely related individuals. We compare the results of parentage analysis across SNP panels generated with or without the use of a reference genome, and between SNPs and microsatellites. For Mexican gray wolf, we conducted parentage analyses for 30 pups from a single cohort where samples were available from 64% of possible mothers and 53% of possible fathers, and the accuracy of parentage assignments could be estimated because true identities of parents were known a priori based on field data. For bighorn sheep, we conducted maternity analyses for 39 lambs from five cohorts where 77% of possible mothers were sampled, but true identities of parents were unknown. Analyses with and without a reference genome produced SNP panels with â‰¥95% parentage assignment accuracy for Mexican gray wolf, outperforming microsatellites at 78% accuracy. Maternity assignments were completely consistent across all SNP panels for the bighorn sheep, and were 74.4% consistent with assignments from microsatellites. Accuracy and consistency of parentage analysis were not reduced when using as few as 284 SNPs for Mexican gray wolf and 142 SNPs for bighorn sheep, indicating our pipeline can be used to develop SNP genotyping assays for parentage analysis with relatively small numbers of loci.
Contact and contagion: Probability of transmission given contact varies with demographic state in bighorn sheep
(2017-05) Manlove, Kezia R.; Cassirer, E. Frances; Plowright, Raina K.; Cross, Paul C.; Hudson, Peter J.
Understanding both contact and probability of transmission given contact are key to managing wildlife disease. However, wildlife disease research tends to focus on contact heterogeneity, in part because the probability of transmission given contact is notoriously difficult to measure. Here, we present a first step towards empirically investigating the probability of transmission given contact in free-ranging wildlife. We used measured contact networks to test whether bighorn sheep demographic states vary systematically in infectiousness or susceptibility to Mycoplasma ovipneumoniae, an agent responsible for bighorn sheep pneumonia. We built covariates using contact network metrics, demographic information and infection status, and used logistic regression to relate those covariates to lamb survival. The covariate set contained degree, a classic network metric describing node centrality, but also included covariates breaking the network metrics into subsets that differentiated between contacts with yearlings, ewes with lambs, and ewes without lambs, and animals with and without active infections. Yearlings, ewes with lambs, and ewes without lambs showed similar group membership patterns, but direct interactions involving touch occurred at a rate two orders of magnitude higher between lambs and reproductive ewes than between any classes of adults or yearlings, and one order of magnitude higher than direct interactions between multiple lambs. Although yearlings and non-reproductive bighorn ewes regularly carried M. ovipneumoniae, our models suggest that a contact with an infected reproductive ewe had approximately five times the odds of producing a lamb mortality event of an identical contact with an infected dry ewe or yearling. Consequently, management actions targeting infected animals might lead to unnecessary removal of young animals that carry pathogens but rarely transmit. This analysis demonstrates a simple logistic regression approach for testing a priori hypotheses about variation in the odds of transmission given contact for free-ranging hosts, and may be broadly applicable for investigations in wildlife disease ecology.
Disease introduction is associated with a phase transition in bighorn sheep demographics
(2016-10) Manlove, Kezia R.; Cassirer, E. Frances; Plowright, Raina K.
Ecological theory suggests that pathogens are capable of regulating or limiting host population dynamics, and this relationship has been empirically established in several settings. However, although studies of childhood diseases were integral to the development of disease ecology, few studies show population limitation by a disease affecting juveniles. Here, we present empirical evidence that disease in lambs constrains population growth in bighorn sheep (Ovis canadensis) based on 45years of population-level and 18years of individual-level monitoring across 12 populations. While populations generally increased (=1.11) prior to disease introduction, most of these same populations experienced an abrupt change in trajectory at the time of disease invasion, usually followed by stagnant-to-declining growth rates (=0.98) over the next 20 years. Disease-induced juvenile mortality imposed strong constraints on population growth that were not observed prior to disease introduction, even as adult survival returned to pre-invasion levels. Simulations suggested that models including persistent disease-induced mortality in juveniles qualitatively matched observed population trajectories, whereas models that only incorporated all-age disease events did not. We use these results to argue that pathogen persistence may pose a lasting, but under-recognized, threat to host populations, particularly in cases where clinical disease manifests primarily in juveniles.
Evidence for strain-specific immunity to pneumonia in bighorn sheep
(2017-01) Cassirer, E. Frances; Manlove, Kezia R.; Plowright, Raina K.; Besser, Thomas E.
Transmission of pathogens commonly carried by domestic sheep and goats poses a serious threat to bighorn sheep (Ovis canadensis) populations. All-age pneumonia die-offs usually ensue, followed by asymptomatic carriage of Mycoplasma ovipneumoniae by some of the survivors. Lambs born into these chronically infected populations often succumb to pneumonia, but adults are usually healthy. Surprisingly, we found that introduction of a new genotype (strain) of M. ovipneumoniae into a chronically infected bighorn sheep population in the Hells Canyon region of Washington and Oregon was accompanied by adult morbidity (100%) and pneumonia-induced mortality (33%) similar to that reported in epizootics following exposure of naive bighorn sheep. This suggests an immune mismatch occurred that led to ineffective cross-strain protection. To understand the broader context surrounding this event, we conducted a retrospective analysis of M. ovipneumoniae strains detected in 14 interconnected populations in Hells Canyon over nearly 3 decades. We used multi-locus sequence typing of DNA extracts from 123 upper respiratory tract and fresh, frozen, and formalin-fixed lung samples to identify 5 distinct strains of M. ovipneumoniae associated with all-age disease outbreaks between 1986 and 2014, a pattern consistent with repeated transmission events (spillover) from reservoir hosts. Phylogenetic analysis showed that the strain associated with the outbreak observed in this study was likely of domestic goat origin, whereas strains from other recent disease outbreaks probably originated in domestic sheep. Some strains persisted and spread across populations, whereas others faded out or were replaced. Lack of cross-strain immunity in the face of recurrent spillovers from reservoir hosts may account for a significant proportion of the disease outbreaks in bighorn sheep that continue to happen regularly despite a century of exposure to domestic sheep and goats. Strain-specific immunity could also complicate efforts to develop vaccines. The results of our study support existing management direction to prevent contacts that could lead to pathogen transmission from domestic small ruminants to wild sheep, even if the wild sheep have previously been exposed. Our data also show that under current management, spillover is continuing to occur, suggesting that enhanced efforts are indicated to avoid introducing new strains of M. ovipneumoniae into wild sheep populations. We recommend looking for new management approaches, such as clearing M. ovipneumoniae infection from domestic animal reservoirs in bighorn sheep range, and placing greater emphasis on existing strategies to elicit more active cooperation by the public and to increase vigilance on the part of resource managers.