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Kelly R. Zamudio

Publications and source records attributed to Kelly R. Zamudio.

6 recordsLinked to original sources

Similar population dynamics before and after a chytridiomycosis outbreak in a tropical riparian amphibian species

Emerging infectious diseases can cause rapid, widespread host mortality, and the lack of demographic data before and after pathogen emergence complicates understanding mechanisms of host persistence. This challenge is further compounded by environmental conditions that influence host behavior, while driving pathogen growth and virulence. These interactions create complex disease outcomes that hinder predictions of when and how hosts endure pathogen outbreaks. Here, we analyzed 10 years of capture-mark-recapture data (2000–2014) spanning wet and dry seasons for male Espadarana prosoblepon in El Copé, Panama, encompassing a period before (2000–2004) and after (2010–2014) a Batrachochytrium dendrobatidis ( Bd ) outbreak using Jolly-Seber models. We found that post- Bd male E. prosoblepon population size (range in mean population size among primary periods = 136–225 individuals) was similar to pre- Bd population size (range in mean population size among primary periods = 201–242 individuals). Pre- Bd , average monthly survival probability in the wet season was 0.93 (95% credible interval [CI] = 0.90–0.96). Post- Bd , uninfected individuals had survival probability higher in the wet season (mean = 0.97; [95% CI = 0.95–0.98]) than the dry season (mean = 0.90 [95% CI = 0.84–0.94]), while survival probability for infected individuals decreased as a function of Bd infection intensity. Pre- Bd , mean monthly per-capita entry probability was 0.07 (95% CI = 0.05–0.10), and post- Bd , mean monthly per-capita entry probability was 0.06 (95% CI = 0.00–0.10). Lastly, infection probability during the wet season was lower (mean = 0.04 [95% CI = 0.03–0.05]) than the dry season (mean = 0.10 [95% CI = 0.05–0.15]), and recovery probability during the wet season was lower (mean = 0.19 [95% CI = 0.11–0.28]) than the dry season (mean = 0.54 [95% CI = 0.20–0.88]). Our findings suggest that survival probabilities of uninfected individuals, as well as per-capita entry probabilities, are similar pre- and post- Bd , leading to a stable and similar sized pre- Bd population. These results contribute to understanding disease dynamics and tropical amphibian ecology.

Ecosphere

Eco‐evolutionary rescue promotes host–pathogen coexistence

Emerging infectious pathogens are responsible for some of the most severe host mass mortality events in wild populations. Yet, effective pathogen control strategies are notoriously difficult to identify, in part because quantifying and forecasting pathogen spread and disease dynamics is challenging. Following an outbreak, hosts must cope with the presence of the pathogen, leading to host–pathogen coexistence or extirpation. Despite decades of research, little is known about host–pathogen coexistence post‐outbreak when low host abundances and cryptic species make these interactions difficult to study. Using a novel disease‐structured N‐mixture model, we evaluate empirical support for three host–pathogen coexistence hypotheses (source–sink, eco‐evolutionary rescue, and spatial variation in pathogen transmission) in a Neotropical amphibian community decimated by Batrachochytrium dendrobatidis ( Bd ) in 2004. During 2010–2014, we surveyed amphibians in Parque Nacional G. D. Omar Torríjos Herrera, Coclé Province, El Copé, Panama. We found that the primary driver of host–pathogen coexistence was eco‐evolutionary rescue, as evidenced by similar amphibian survival and recruitment rates between infected and uninfected hosts. Average apparent monthly survival rates of uninfected and infected hosts were both close to 96%, and the expected number of uninfected and infected hosts recruited (via immigration/reproduction) was less than one host per disease state per 20‐m site. The secondary driver of host–pathogen coexistence was spatial variation in pathogen transmission as we found that transmission was highest in areas of low abundance but there was no support for the source–sink hypothesis. Our results indicate that changes in the host community (i.e., through genetic or species composition) can reduce the impacts of emerging infectious disease post‐outbreak. Our disease‐structured N‐mixture model represents a valuable advancement for conservation managers trying to understand underlying host–pathogen interactions and provides new opportunities to study disease dynamics in remnant host populations decimated by virulent pathogens.

Ecological Applications

Imperfect pathogen detection from non-invasive skin swabs biases disease inference

1. Conservation managers rely on accurate estimates of disease parameters, such as pathogen prevalence and infection intensity, to assess disease status of a host population. However, these disease metrics may be biased if low-level infection intensities are missed by sampling methods or laboratory diagnostic tests. These false negatives underestimate pathogen prevalence and overestimate mean infection intensity of infected individuals. 2. Our objectives were two-fold. First, we quantified false negative error rates of Batrachochytrium dendrobatidis on non-invasive skin swabs collected from an amphibian community in El Copé, Panama. We swabbed amphibians twice in sequence, and we used a recently developed hierarchical Bayesian estimator to assess disease status of the population. Second, we developed a novel hierarchical Bayesian model to simultaneously account for imperfect pathogen detection from field sampling and laboratory diagnostic testing. We evaluated the performance of the model using simulations and varying sampling design to quantify the magnitude of bias in estimates of pathogen prevalence and infection intensity. 3. We show that Bd detection probability from skin swabs was related to host infection intensity, where Bd infections < 10 zoospores have < 95% probability of being detected. If imperfect Bd detection was not considered, then Bd prevalence was underestimated by as much as 16%. In the Bd-amphibian system, this indicates a need to correct for imperfect pathogen detection caused by skin swabs in persisting host communities with low-level infections. More generally, our results have implications for study designs in other disease systems, particularly those with similar objectives, biology, and sampling decisions. 4. Uncertainty in pathogen detection is an inherent property of most sampling protocols and diagnostic tests, where the magnitude of bias depends on the study system, type of infection, and false negative error rates. Given that it may be difficult to know this information in advance, we advocate that the most cautious approach is to assume all errors are possible and to accommodate them by adjusting sampling designs. The modeling framework presented here improves the accuracy in estimating pathogen prevalence and infection intensity.

Methods in Ecology and Evolution

Selection, trans-species polymorphism, and locus identification of major histocompatibility complex class IIβ alleles of New World ranid frogs

Genes encoded by the major histocompatibility complex (MHC) play key roles in the vertebrate immune system. However, our understanding of the evolutionary processes and underlying genetic mechanisms shaping these genes is limited in many taxa, including amphibians, a group currently impacted by emerging infectious diseases. To further elucidate the evolution of the MHC in frogs (anurans) and develop tools for population genetics, we surveyed allelic diversity of the MHC class II ??1 domain in both genomic and complementary DNA of seven New World species in the genus Rana (Lithobates). To assign locus affiliation to our alleles, we used a "gene walking" technique to obtain intron 2 sequences that flanked MHC class II?? exon 2. Two distinct intron sequences were recovered, suggesting the presence of at least two class II?? loci in Rana. We designed a primer pair that successfully amplified an orthologous locus from all seven Rana species. In total, we recovered 13 alleles and documented trans-species polymorphism for four of the alleles. We also found quantitative evidence of selection acting on amino acid residues that are putatively involved in peptide binding and structural stability of the ??1 domain of anurans. Our results indicated that primer mismatch can result in polymerase chain reaction (PCR) bias, which influences the number of alleles that are recovered. Using a single locus may minimize PCR bias caused by primer mismatch, and the gene walking technique was an effective approach for generating single-copy orthologous markers necessary for future studies of MHC allelic variation in natural amphibian populations. ?? 2010 Springer-Verlag.

Immunogenetics

Toward immunogenetic studies of amphibian chytridiomycosis: Linking innate and acquired immunity

Recent declines in amphibian diversity and abundance have contributed significantly to the global loss of biodiversity. The fungal disease chytridiomycosis is widely considered to be a primary cause of these declines, yet the critical question of why amphibian species differ in susceptibility remains unanswered. Considerable evidence links environmental conditions and interspecific variability of the innate immune system to differential infection responses, but other sources of individual, population, or species-typical variation may also be important. In this article we review the preliminary evidence supporting a role for acquired immune defenses against chytridiomycosis, and advocate for targeted investigation of genes controlling acquired responses, as well as those that functionally bridge the innate and acquired immune systems. Immunogenetic data promise to answer key questions about chytridiomycosis susceptibility and host-pathogen coevolution, and will draw much needed attention to the importance of considering evolutionary processes in amphibian conservation management and practice. ?? 2009 by American Institute of Biological Sciences.

BioScience

Delayed genetic effects of habitat fragmentation on the ecologically specialized Florida sand skink ( Plestiodon reynoldsi )

Populations rarely show immediate genetic responses to habitat fragmentation, even in taxa that possess suites of traits known to increase their vulnerability to extinction. Thus conservation geneticists must consider the time scale over which contemporary evolutionary processes operate to accurately portray the effects of habitat isolation. Here, we examine the genetic impacts of fragmentation on the Florida sand skink Plestiodon reynoldsi , a sand swimming lizard that is highly adapted to the upland scrub habitat of central Florida. We studied fragments located on the southern Lake Wales Ridge, where human activity in the latter half of the 20th century has modified the natural patchiness of the landscape. Based on a relaxed molecular clock method, we estimate that sand skinks have persisted in this region for approximately 1.5 million years and that the time frame of human disturbance is equivalent to fewer than 30 skink generations. Using genotypes from eight microsatellite loci, we screened for molecular signatures of this disturbance by assessing congruence between population structure, as inferred from spatially-informed Bayesian assignment tests, and the current geography of scrub fragments. We also tested for potential intrapopulation genetic effects of inbreeding in isolated populations by comparing the average pairwise relatedness of individuals within fragments of different areas and isolation. Our results indicate that although some patches show a higher degree of relatedness than expected under random mating, the genetic effects of recent isolation are not evident in this part of the species’ range. We argue that this result is an artefact of a time-lag in the response to disturbance, and that species-typical demographic features may explain the genetic inertia observed in these populations.

Conservation Genetics