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David James Páez

Publications and source records attributed to David James Páez.

13 recordsLinked to original sources

Disease-associated mortality drives reduction in Yukon River Chinook salmon escapement: A novel method for quantifying the negative impacts of ‘misfit’ parasites to improve fisheries management

Parasites can suppress host populations through parasite-induced mortality. However, the negative effects of parasites are difficult to measure in wild populations and we have few tools for quantifying the magnitude of parasite-induced mortality. This is especially true for many ‘misfit’ parasites that do not fit into standard classifications (e.g. fungal-like parasites and myxozoans). As such, we are limited in our ability to include the effects of parasites in fish and wildlife management strategies. Chinook salmon ( Oncorhynchus tshawytscha ) are a species of immense cultural and ecological significance but populations are declining across much of their range. In the Yukon River, Alaska, USA, episodic outbreaks of the ichthyosporean parasite Ichthyophonus have been linked to declines, but population-level effects of Ichthyophonus on Yukon Chinook salmon remain largely unknown. We developed a novel model that leverages changes in parasite intensity distributions to quantify the magnitude of disease-induced mortality occurring in host populations. We used it to address two questions to inform management of Yukon Chinook salmon: (i) Is parasite-induced mortality occurring in Chinook salmon and at what magnitude? (ii) What are the drivers of spatio-temporal variability in parasite-induced mortality? Using 3 years of surveys, we quantified the evidence for the presence, magnitude, and variability in Ichthyophonus -induced mortality in Chinook salmon. Our model predicted that Ichthyophonus was responsible for between 8% and 15% mortality of the migrating Chinook salmon population prior to reaching the Canadian border and could describe nearly 35% of unaccounted for mortality at the border. The model predicted that variability in mortality among years could largely be explained by differences in parasite acquisition in the marine environment rather than differences in infection dynamics in the river. Synthesis and applications . Alaska Department of Fish and Game is implementing an annual monitoring program at the mouth of the Yukon River where our model will estimate the proportion of fish at risk from parasite-induced mortality to inform annual management. Moreover, the model is broadly applicable to other fungal-like and myxozoan parasites of conservation concern, where improved estimates of parasite-induced mortality could be used to predict parasite suppression of wild and managed host populations.

Alaska

From understanding to action: Integrating new and old methodologies to manage marine infectious disease

Marine diseases can have far-reaching effects on population, community and ecosystem health; however, our ability to track, predict and manage these diseases has, historically, been poor. As a result, the fields of disease ecology and epidemiology have developed at a slower pace for marine than terrestrial systems [ 1 ]. New methodologies, including genomic tools for diagnostics [ 2 , 3 ], transcriptomic tools for measuring host and pathogen responses to infection (e.g. [ 4 , 5 ]), regional oceanic modelling systems that estimate environmental conditions influencing pathogen dispersal and disease progression [ 6 ], artificial intelligence methods for quantifying pathology from images (e.g. [ 7 ]) and advanced disease modelling techniques [ 8 , 9 ] are precipitating a rapid increase in our understanding of marine pathosystems. In 2016, these efforts led to the first special issue of Philosophical Transactions of the Royal Society B ( Marine diseases, volume 371, issue 1689) focused entirely on marine disease ecology and evolution, and in 2020, the first book, Marine disease ecology, was devoted to this topic [ 10 ]. This special issue, focused on marine disease management , is being published a decade after the first Philosophical Transactions special issue on marine diseases. The shift to a management focus reflects an urgent need for management strategies to address high-impact diseases and the rapid methodological advances that have resulted. The papers included in this issue demonstrate the value of combining classical approaches (e.g. routine disease surveillance, reductionistic pathogen challenge trials, rapid throughput diagnostics) with cutting-edge technologies (e.g. high-resolution oceanographic models, Bayesian models, replicated transcriptomic studies) to identify drivers of disease, quantify impacts and suggest management strategies.

Philosophical Transactions of the Royal Society, S

Region-specific understanding of virus transmission to support salmonid health at hatcheries in three regions of the Pacific Northwest, North America

Juvenile salmonid mortality due to infectious haematopoietic necrosis virus (IHNV) can be a major burden on fish hatcheries. We consider possible IHNV transmission routes and specialist–generalist patterns across three regions in the Pacific Northwest of North America: Coastal Washington and Oregon (CWO), Lower Columbia River Basin (LCRB) and Snake River Basin (SRB) to obtain multi-region inference about IHNV transmission and specialization. While individual regions have been studied previously, our consideration of three regions to identify consistent trends or localized patterns is novel. The most consistent patterns we found were that most exposure to IHNV was from migrating adult salmonids and that the IHNV lineage MD specialized in steelhead and rainbow trout. Our results were consistent with LCRB being a source of IHNV and the SRB and CWO being sinks. Results specific to particular regions include the role of local geography on exposure and influence of hatchery complexes on transmission, which highlights the need to understand local hatchery operations before disease ecology can be understood and suitable hatchery management can be planned. Results demonstrate the need for spatially and temporally explicit quantitative approaches to understand disease dynamics and inform management.

Oregon, Washington

Stochastic within-host dynamics and climate-sensitive traits generate predictable patterns of variation in disease outcomes

Understanding how climatic variables impact host-pathogen relationships in temperature-sensitive ectothermic host organisms is crucial under global change. Few studies have explored how temperature gradients generate inter-individual variation in epidemiological traits like host susceptibility or pathogen replication. Here, we develop a mathematical model to explore a novel hypothesis: stochastic within-host dynamics and simulated thermal mismatches between host and pathogen traits generate predictable variation in infection outcomes among hosts and across thermal gradients. Our model demonstrates that varying trait thermal optima in host immunity and pathogen replication, and stochastic within-host processes produced variation in infection outcomes. Variability was low when temperatures strongly favored host or pathogen traits, but high and diverse when their performance was similar across a broad thermal range. In contrast, when trait performance was equal across all temperatures (no mismatch) variability remained low at all temperatures. Further, the magnitude of variation, quantified by entropy, exhibited predictable patterns depending on host-pathogen thermal mismatches. We conclude that interactions between trait thermal mismatches and within-host stochasticity provide a theoretical framework to improve ectotherm disease models under climate change, providing a valuable tool for exploring the impacts of environmental change on epizootic or epidemic dynamics, particularly in vulnerable marine ecosystems.

Philosophical Transactions of the Royal Society, S

The impacts of co-circulating pathogens in Pacific herring depend on interactions between viral life-cycle traits and transmission parameters, highlighting interdependencies between pathogen epizootics

The average host susceptibility decreases as the epizootic progresses because easily infected hosts are first removed from the population. While host susceptibility is pathogen-specific, it is likely that host susceptibility is correlated between different pathogens, so that co-circulating pathogens may have reciprocal impacts on their epidemics. However, despite well-documented examples of concomitant infections in marine hosts, reciprocal epizootic effects have not been documented in wild marine organisms. We quantify reciprocal impacts between viral haemorrhagic septicaemia and viral erythrocytic necrosis in Pacific herring ( Clupea pallasii ) using field and laboratory work. We show that the causative viruses for both diseases circulate through herring populations and that infection with one pathogen has negative impacts on the epizootic and infection characteristics of the other pathogen, suggesting positive correlations in the susceptibility to infection between pathogens. We then use simulations of a two-strain pathogen model to show that the impact of the correlation is modulated by transmission parameters, such as the incubation period and the initial transmission rate. Our work shows that co-occurring epizootics pose a management challenge because single-pathogen management actions may amplify the epizootics of the non-targeted pathogen. This study provides a framework to evaluate the consequences of reciprocal epizootic impacts through field, experimental and modelling work.

Washington

Distributions of host heterogeneity in susceptibility show signatures of pathogen geographic structure in an insect baculovirus

Segregated variation between populations is a fundamental evolutionary process leading to parasite specialization, yet the resulting impacts on infection heterogeneity within populations are theoretically and empirically understudied. We asked whether the distribution of host susceptibility to infection within populations carries the signatures of geographic structure from pathogen local adaptation, maladaptation, or generalism in a nuclear polyhedrosis virus that infects the Gulf Fritillary butterfly Dione vanillae . For this virus, there is genetic support for two geographically distinct groups within San Diego County, based on whole genome sequencing of 16 virus isolates. Reciprocal laboratory infections showed evidence of two contrasting viral life history strategies: a ‘generalist’ phenotype that consistently infected variable hosts and a ‘specialist’ that performed slightly better in its local host population. As predicted by our theoretical model, the more consistent infection displayed by the generalist across populations corresponded to lower heterogeneity in susceptibility within populations, modeled as gamma distribution. Furthermore, the generalist phenotype was collected over a wider geographic range despite having a tenfold-lower mean infection rate than the specialist, suggesting that a strategy of more consistent infection provides key fitness advantages across diverse host populations. Intriguingly, when there is variation in host susceptibility, interpretations of pathogen local adaptation are dose-dependent. Measuring infectivity across multiple doses enables estimation of the whole distribution of susceptibility, which provides more reliable identification of pathogen specialization to its local host. Our work demonstrates how trait distributions and not only their mean values can carry quantifiable signatures of eco-evolutionary processes in interspecific interactions.

BioRxiv

Prince William Sound Herring Program, fiscal year 2024

Pacific herring ( Clupea pallasii ) were collected from three sites in Prince William Sound (PWS), Alaska (Table 1) during the spring pre-spawn period from March 29 – April 1, 2024, to test for viral hemorrhagic septicemia virus (VHSV), viral erythrocytic necrosis (VEN), and Ichthyophonus prevalence (Table 1). Ichthyophonus was detected in 33% (59/180) of heart cultures from all sites combined. An inverted pattern of decreasing Ichthyophonus infection prevalence with size started around 2019 and continued through 2024 (Fig. 1). VHSV was isolated from one fish collected in Canoe Pass. The isolation was at a very low titer and was detectable only after blind passage. Neutralizing antibodies to VHSV were detected in 4.4% (14/318) of PWS herring in 2024 (Fig. 2). Erythrocytic inclusions indicative of VEN were not detected in any PWS herring (n =180) from 2024, but bacterial rods were noted in the blood films from three fish.

Alaska

Systematic shifts in the variation among host individuals must be considered in climate-disease theory

To make more informed predictions of host–pathogen interactions under climate change, studies have incorporated the thermal performance of host, vector and pathogen traits into disease models to quantify effects on average transmission rates. However, this body of work has omitted the fact that variation in susceptibility among individual hosts affects disease spread and long-term patterns of host population dynamics. Furthermore, and especially for ectothermic host species, variation in susceptibility is likely to be plastic, influenced by variables such as environmental temperature. For example, as host individuals respond idiosyncratically to temperature, this could affect the population-level variation in susceptibility, such that there may be predictable functional relationships between variation in susceptibility and temperature. Quantifying the relationship between temperature and among-host trait variation will therefore be critical for predicting how climate change and disease will interact to influence host–pathogen population dynamics. Here, we use a model to demonstrate how short-term effects of temperature on the distribution of host susceptibility can drive epidemic characteristics, fluctuations in host population sizes and probabilities of host extinction. Our results emphasize that more research is needed in disease ecology and climate biology to understand the mechanisms that shape individual trait variation, not just trait averages.

Proceedings of the Royal Society B: Biological Sci

Local and systemic replicative fitness for viruses in specialist, generalist, and non-specialist interactions with salmonid hosts

Host tissues represent diverse resources or barriers for pathogen replicative fitness. We tested whether viruses in specialist, generalist, and non-specialist interactions replicate differently in local entry tissue (fin), and systemic target tissue (kidney) using infectious hematopoietic necrosis virus (IHNV) and three salmonid fish hosts. Virus tissue replication was host specific, but one feature was shared by specialists and the generalist which was uncommon in the non-specialist interactions: high host entry and replication capacity in the local tissue after contact. Moreover, specialists showed increased replication in systemic target tissues early after host contact. By comparing ancestral and derived IHNV viruses, we also characterized replication tradeoffs associated with specialist and generalist evolution. Compared with the ancestral virus, a derived specialist gained early local replicative fitness in the new host but lost replicative fitness in the ancestral host. By contrast, a derived generalist showed small replication losses relative to the ancestral virus in the ancestral host but increased early replication in the local tissue of novel hosts. This study shows that the mechanisms of specialism and generalism are host specific and that local and systemic replication can contribute differently to overall within host replicative fitness for specialist and generalist viruses.

Journal of General Virology

Coproduction and modeling spatial contact networks prevent bias about infectious hematopoietic necrosis virus transmission for Snake River Basin salmonids

Much remains unknown about variation in pathogen transmission across the geographic range of a free-ranging fish or animal species and about the influence of movement (associated with husbandry practices or animal behavior) on pathogen transmission. Salmonid hatcheries are an ideal system in which to study these processes. Salmonid hatcheries are managed for endangered species recovery, supplementation of threatened or at-risk fish stocks, support of fisheries, and ecosystem stability. Infectious hematopoietic necrosis virus (IHNV) is a rhabdovirus of significant concern to salmon aquaculture. Landscape IHNV transmission dynamics previously had been estimated only for salmonid hatcheries in the Lower Columbia River Basin (LCRB). The objectives of this study were to estimate IHNV transmission dynamics in a unique geographic region, the Snake River Basin (SRB), and to quantitatively estimate the effect of model coproduction on inference because previous assessments of coproduction have been qualitative. In contrast to the LCRB, the SRB has hatchery complexes consisting of a main hatchery and ≥1 satellite facility. Knowledge about hatchery complexes was held by a subset of project researchers but would not have been available to project modelers without coproduction. Project modelers generated and tested multiple versions of Bayesian susceptible-exposedinfected models to realistically represent the SRB and estimate the effect of coproduction. Models estimated the frequency of transmission routes, route-specific infection probabilities, and infection probabilities for combinations of salmonid hosts and IHNV lineages. Model results indicated that in the SRB, avoiding exposure to IHNV-positive adult salmonids is the most important action to prevent juvenile infections. Migrating adult salmonids exposed juvenile cohort-sites most frequently, and the infection probability was greatest following exposure to migrating adults. Without coproduction, the frequency of exposure by migrating adults would have been overestimated by 70 cohort-sites, and the infection probability following exposure to migrating adults would have been underestimated by∼0.09. The coproduced model had less uncertainty in the infection probability if no transmission route could be identified (Bayesian credible interval (BCI) width = 0.12) compared to the model without coproduction (BCI width = 0.34). Evidence for virus lineage MD specialization on steelhead and rainbow trout (both Oncorhynchus mykiss) was apparent without model coproduction. In the SRB, we found a greater probability of virus lineage UC infection in Chinook salmon (Oncorhynchus tshawytscha) compared to in O. mykiss, whereas in the LCRB, UC more clearly exhibited a generalist approach. Coproduction influenced estimates that depended on transmission routes, which operated differently at main hatcheries and satellite sites within hatchery complexes. Hatchery complexes are found outside of the SRB and are not specific to salmonid hatcheries alone. There is great potential for coproduction and modeling spatial contact networks to advance understanding about infectious disease transmission in complex production systems and surrounding free-ranging animal populations.

Idaho, Oregon, Washington

Characteristics of a sea louse (Caligus clemensi) epizootic in wild Pacific herring (Clupea pallasii)

We characterized a natural sea louse epizootic of Caligus clemensi and the effects of parasitism on Pacific herring Clupea pallasii in Port Angeles Harbor, WA, USA. Infestation prevalence on newly metamorphosed age 0 Pacific herring reached 100% prevalence by mid-August. At this time, the mean louse intensity was 4.6 lice/fish, and a positive correlation occurred between louse intensity and herring body length. The epizootic then waned, with infestation prevalence decreasing to less than 25% and the mean parasite intensity falling below 1 louse. While skin injuries were not detected, motile lice preferentially aggregated around head and anterior dorsal areas. However, louse tropism became evenly distributed over the body as the parasite intensity increased. Louse-induced mortality in herring was negligible in controlled experiments. These results indicate that Caligus clemensi epizootics reach high prevalence, but also fade from mid-summer to early fall. Due to the predominant presence of motile copepod stages, we suggest that the epizootic fades because lice complete their life cycle and dislodge from the host; however, multiple explanations for epidemic fading are possible.

Washington

Variation in within-host replication kinetics among virus genotypes provides evidence of specialist and generalist infection strategies across three salmonid host species

Theory of the evolution of pathogen specialization suggests that a specialist pathogen gains high fitness in one host, but this comes with fitness loss in other hosts. By contrast, a generalist pathogen does not achieve high fitness in any host, but gains ecological fitness by exploiting different hosts, and has higher fitness than specialists in nonspecialized hosts. As a result, specialist pathogens are predicted to have greater variation in fitness across hosts, and generalists would have lower fitness variation across hosts. We test these hypotheses by measuring pathogen replicative fitness as within-host viral loads from the onset of infection to the beginning of virus clearance, using the rhabdovirus infectious hematopoietic necrosis virus (IHNV) in salmonid fish. Based on field prevalence and virulence studies, the IHNV subgroups UP, MD, and L are specialists, causing infection and mortality in sockeye salmon, steelhead, and Chinook salmon juveniles, respectively. The UC subgroup evolved naturally from a UP ancestor and is a generalist infecting all three host species but without causing severe disease. We show that the specialist subgroups had the highest peak and mean viral loads in the hosts in which they are specialized, and they had low viral loads in nonspecialized hosts, resulting in large variation in viral load across hosts. Viral kinetics show that the mechanisms of specialization involve the ability to both maximize early virus replication and avoid clearance at later times, with different mechanisms of specialization evident in different host–virus combinations. Additional nuances in the data included different fitness levels for nonspecialist interactions, reflecting different trade-offs for specialist viruses in other hosts. The generalist UC subgroup reached intermediate viral loads in all hosts and showed the smallest variation in fitness across hosts. The evolution of the UC generalist from an ancestral UP sockeye specialist was associated with fitness increases in steelhead and Chinook salmon, but only slight decreases in fitness in sockeye salmon, consistent with low- or no-cost generalism. Our results support major elements of the specialist–generalist theory, providing evidence of a specialist–generalist continuum in a vertebrate pathogen. These results also quantify within-host replicative fitness trade-offs resulting from the natural evolution of specialist and generalist virus lineages in multi-host ecosystems

Virus Evolution