An Introduction to Ecology of Infectious Diseases - Oysters and Estuaries

Infectious diseases are recognized as an important factor regulating marine ecosystems (Harvell et al., 1999, 2002, 2004; Porter et al., 2001; McCallum et al., 2004; Ward and Lafferty, 2004; Stewart et al., 2008; Bienfang et al., 2011). Many of the organisms affected by marine diseases have important ecological roles in estuarine and coastal environments and some are also commercially important. Outbreaks of infectious diseases in these environments, referred to as epizootics, can produce significant population declines and extinctions, both of which threaten biodiversity, food web interactions, and ecosystem productivity (Harvell et al., 2002, 2004)

Development of resistance to an introduced marine pathogen by a native host

In 1957–1959, the introduced protistan parasite, Haplosporidium nelsoni, killed 90–95% of the oysters (Crassostrea virginica) in lower Delaware Bay and about half of those in the upper bay. Shortly thereafter, H. nelsoni-caused mortality in the wild population of the lower bay declined, approximating that of first-generation selectively bred oysters. For nearly three decades thereafter no further change in survival of the wild population was evident, although steady improvement was achieved by continued selective breeding. Survival of the wild population is thought to have plateaued because the great majority of oysters inhabited the upper bay where they were protected from H. nelsoni infection and selective mortality by low salinity. Consequently, they contributed most of the offspring to the bay population. From 1957 through 1987, H. nelsoni prevalence was cyclic, but overall high (annual maxima of 60 to 85%) in the lower bay. Since 1988, however, prevalence in wild oysters has rarely exceeded 30% anywhere in the bay, even though unselected oysters continue to become heavily infected when exposed, and molecular evidence indicates that the parasite remains present throughout the bay. This apparent second step in the development of resistance in the wild oysters occurred after a drought-associated incursion of H. nelsoni into the upper bay in the mid-1980s. Mortalities were widespread, heavy and more extreme than during the 1957–59 epizootic. Resistant survivors of the second epizootic have apparently repopulated the bay. When compared to unselected stocks, common-garden exposure to H. nelsoni of oysters from both upbay and downbay sites indicates that a high degree of resistance to the development of MSX disease has become widespread in the wild oyster population of Delaware Bay after two major selection events separated by nearly 30 years

Spatial and temporal variability of disease refuges in an estuary: Implications for the development of resistance

Although the concept of genetic refuge has long been employed in ecological and paleoecological context, it has only rarely been used to identify regions where organisms are protected from diseases that affect the rest of a population. The refuges harbor individuals that have not been exposed to selective mortality and remain susceptible to the disease. They represent a reservoir of susceptibility alleles that can mix with those from resistant survivors of disease and can retard the development of resistance in the population as a whole. Two water-borne protistan parasites affect oysters along the east coast of the United States: Haplosporidium nelsoni (MSX disease) and Perkinsus marinus (dermo disease). Both are sensitive to low salinity and their prevalence is reduced in the upper reaches of estuaries. We investigated the temporal and spatial structure and extent of putative refuges from these diseases in the upper Delaware Bay, USA and their potential to affect the development of resistance in the oyster population. Our results showed that refuges occurred as a continuum of zones, regions where a pathogen (1) was not present; (2) was present, but did not cause observable infections; and (3) caused infection, but neither disease nor mortality. The zones were transient, driven only partly by short-term climatic conditions, and differed according to parasite: H. nelsoni was often not present in the refuges, as inferred by the absence of polymerase chain reaction (PCR) – positive signals on the gills, and when it was present, it did not always cause lethal, or even histologically detectable, infections. In contrast, P. marinus was present in all upper estuary areas sampled, where it caused detectable, although not necessarily lethal-level, infections. Thus, a significant fraction of the oyster population is protected from selective mortality in these refuges even when the parasites are present. An incursion of H. nelsoni into the upper Bay in the 1980s left most of the surviving population highly resistant to MSX disease, although populations in the upper-most reaches are still susceptible. The lack of selection pressure in the refuges likely helps to retard the development of resistance to dermo disease, and theoretically could cause resistance to MSX disease to regress although there is no evidence to date that this has occurred

Long-term patterns of an estuarine pathogen along a salinity gradient

Parasitic, disease-causing pathogens can exert strong control over marine populations yet few long-term studies exist that describe these relationships. Understanding the connections to long-term large-scale processes relative to local short-term processes should facilitate better planning for disease impacts in the management of marine resources. We describe a 21-yr dataset of dermo disease (Perkinsus marinus) in eastern oysters (Crassostrea virginica) in Delaware Bay, USA. Analyses indicated (1) a strong positive association between disease and mortality that was non-linear and defined by thresholds, (2) a clear spatial gradient of increasing disease and mortality with increasing salinity, (3) an apparent 7-year cycle in which peaks were associated with strong positive anomalies of the North Atlantic Oscillation (NAO), (4) an inverse relationship with freshwater inflow, and (5) no obvious response to natural selection from persistent disease pressure. These data quantify the impact of environmental variables on the disease in a wild population and provide new insight into how disease interacts with host populations by linking disease patterns with larger climate controlling processes. Understanding these connections will facilitate prediction of and response to disease outbreaks

The association of attention deficit hyperactivity disorder with socioeconomic disadvantage: alternative explanations and evidence

addresses: ESRC Centre for Genomics in Society (Egenis) & Institute of Health Research, University of Exeter Medical School, Exeter, UK.OnlineOpen Article. This is a copy of an article published in the Journal of Child Psychology and Psychiatry. This journal is available online at: http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1469-7610Studies throughout Northern Europe, the United States and Australia have found an association between childhood attention deficit hyperactivity disorder (ADHD) and family socioeconomic disadvantage. We report further evidence for the association and review potential causal pathways that might explain the link.ESRC’s Secondary Data Analysis InitiativeNational Institute for Health Research (NIHR) Collaboration for Leadership in Applied Health Research and Care (CLAHRC) for the South West Peninsul

The Potential for Oysters, Crassostrea Virginica, to Develop Resistance to Dermo Disease in the Field: Evaluation Using a Gene-Based Population Dynamics Model

Today, populations of eastern oysters, Crassostrea virginica, are commonly limited by disease mortality. Resistance to MSX disease has developed in a number of cases, but the development of resistance to Dermo disease would appear to be limited, despite the high mortality rates and frequency of epizootics. Can aspects of the host\u27s genetics or population dynamics limit the response to the disease despite the apparent opportunity afforded by alleles conferring disease resistance or tolerance? To answer this question, we use a gene-based population dynamics model, configured for C. virginica, to simulate the development of disease resistance using mortality as the agent of selection. Simulated populations were exposed to 4 levels of mortality covering the range in mortality observed in Delaware Bay in the l990s. In each case, disease resistance increased in the simulated population over time, normally proportional to the increase in mortality rate imposed by the disease. However, simulations show that the population responds even at its most rapid rate on multidecadal to half-century timescales. As the mortality rate declines with increasing disease resistance, the rate of further improvement in disease resistance likewise declines. Thus, disease resistance develops over decadal timescales at a 40%-per-year mortality rate, but, as mortality rate falls to 25% per year, the rate of further development of disease resistance extends to half-century timescales. The discouraging profundity is that a mortality rate of 25% per year, yielding a rate of selection profoundly slow, is still very high. In northern climes, significant decrements in oyster abundance will occur. Evidence from fisheries retrospectives suggests that oysters cannot withstand a constant removal at this scale without compromising population integrity noticeably. So, a mortality rate that grievously limits the development of disease resistance still sorely strains the species\u27 ability to maintain a vibrant population necessary to its long-term survival

Modeling the MSX Parasite in Eastern Oyster (Crassostrea virginica) Populations. III. Regional Application and the Problem of Transmission

A model of transmission for Haplosporidium nelsoni, the disease agent for MSX disease, is developed and applied to sites in Delaware Bay and Chesapeake Bay. The environmental factors that force the oyster population- H. nelsoni model are salinity, temperature, food, and total suspended solids. The simulated development of MSX disease was verified using 3 time series of disease prevalence and intensity: 1960 to 1970 and 1980 to 1990 for Delaware Bay, and 1980 to 1994 for Chesapeake Bay, and for a series of sites covering the salinity gradient in each bay. Additional simulations consider the implications of assumptions made in development of the model for constraining the mode of transmission of H. nelsoni disease in oyster populations. Transmission of H. nelsoni includes non-local factors that exert a paramount influence on the transmission process. Key environmental forcing factors of season, salinity, and winter temperature exert a direct control on the transmission process, either by controlling the availability of infective particles in the water column or by controlling the population dynamics of an alternate host. Salinity\u27s role is a dual one. Salinity acts on the local host population by varying the infectivity of infective particles as they impinge the oyster gill during the filtration process. In addition, salinity exerts a regional influence on the transmission process by controlling, in part and on a bay-wide scale, the concentration of infective particles in the water column (or perhaps the abundance of an alternate host). In addition to the effect of salinity, infective particle concentration also decreases for 1 to 2 years after a cold winter and returns to high levels faster after a warm winter. It is the presence in the H. nelsoni transmission model of these bay-wide influences of environmental change that make this model different: from most other transmission models. Simulations suggest that epizootic cycles are principally the product of enhanced transmission rather than enhanced intensification. These influences of transmission on the course of infection, in many cases, have multiyear implications for prevalence and infection intensity, and the root of much of this multiyear behavior is in the processes that control the concentration of infective particles in the water column

Modeling The MSX Parasite in Eastern Oyster (Crassostrea virginica) Populations. II. Salinity Effects

An oyster population model coupled with a model for Haplosporidium nelsoni, the causative agent of the oyster disease MSX, was used with salinity time-series constructed from Delaware River flow measurements to study environmentally-induced variations in the annual cycle of this disease in Delaware Bay oyster populations. Model simulations for the lower Bay (high salinity) sire reproduced the annual cycle observed in lower Delaware Bay. Simulations at both upper Bay (low salinity) and lower Bay sites produced prevalences and intensities that were consistent with field observations. At all sites, low freshwater discharge resulted in increased disease levels, whereas high freshwater discharge produced decreased levels. At upper Bay sites, simulated changes in runoff produced high variability in disease prevalence; in the lower Bay, they produced a much lesser effect. Changes in salinity within the 10-20 ppt range produced the greatest changes in disease levels and patterns. Simulated shifts in timing of the spring runoff from March to either February or May affected the mid-Bay (13-19 ppt) only. A February runoff reduced the spring prevalence peak and caused a complete loss of systemic infections. In contrast, a May discharge occurred too late to affect parasite proliferation in the spring so that the spring peak was higher than average. Almost 100% of the infections were systemic by June, which resulted in high oyster mortality during July at this site. Model results indicate that parasite infection intensity under changing salinity is more complex than a simple function of salinity as it affects parasite proliferation and death rates within the oyster, and that the rate of infection is most likely reduced at low salinity. The simulated results demonstrate the ability of the model to reproduce field measurements and its usefulness in elucidating the association between the magnitude and timing of Delaware River discharge, its associated salinity variations, and the H. nelsoni annual cycle

Outcomes of Asymmetric Selection Pressure and Larval Dispersal on Evolution of Disease Resistance: A Metapopulation Modeling Study With Oysters

Marine diseases are a strong selective force that can have important economic and ecological consequences. Larval dispersal patterns, selective mortality and individual growth rates can modulate metapopulation responses to disease pressure. Here, we use a modeling framework that includes distinct populations, connected via larval transport, with varying disease selection pressure and connectivity to examine how these dynamics enhance or inhibit the evolution of disease resistance in metapopulations. Our system, oysters and MSX disease, is one in which disease resistance is highly and demonstrably heritable. Simulations show that under conditions of population isolation (i.e. local retention of larvae) and strong disease selection, populations rapidly evolve genetic disease resistance. Varying the patterns of larval dispersal alone doubles the time for evolution of disease resistance. Spatially varying disease in the absence of larval dispersal leaves some populations unable to respond to the disease, whereas adding larval dispersal slows the response of populations under strong selection and speeds the response in populations under low selection when fitness is based on relatively limited genetic structure (‘juvenile fitness’ in our simulations). Under spatially variable disease pressure, larval dispersal generates a fourfold greater variance in fitness outcomes across the dispersal patterns tested. In a metapopulation, populations experiencing lower selection pressure will tend to slow the development of other, more heavily selected populations. This suggests that conservation efforts aimed at improving overall metapopulation resistance in the face of marine diseases should target those populations under modest or high disease pressure, rather than protecting those experiencing low selective pressure

Can Oysters Crassostrea virginica Develop Resistance to Dermo Disease in the Field: The Impediment Posed by Climate Cycles

Populations of eastern oysters, Crassostrea virginica, are commonly limited by mortality from dermo disease. Little development of resistance to Perkinsus marinus, the dermo pathogen, has occurred, despite the high mortality rates and frequency of epizootics. Can the tendency of the parasite to exhibit cyclic epizootics limit the oyster\u27s response to the disease despite the presence of alleles apparently conferring disease resistance? We utilize a gene-based population dynamics model to simulate the development of disease resistance in Crassostrea virginica populations exposed to cyclic mortality encompassing periodicities expected of dermo disease over the geographic range at which epizootics have been observed. Cyclic disease reduces the incremental rate of development of disease resistance profoundly, primarily as a consequence of a reduction in the time-integrated population mortality rate, which will be about half the cycle\u27s apogean rate. Cyclicity enhances host survival for more susceptible genotypes at cycle nadir. Moreover, alleles conferring disease resistance typically are rare in the naive population. Cyclicity permits these rare alleles to drift and most often, that drift is towards lower frequencies because fewer animals carrying these alleles predestines a lower probability of their successful dissemination during sweepstakes reproduction at cycle nadir. Variations in population dynamics, such as differences in abundance, fecundity at size, and in the number of individuals successfully producing recruits varied the outcome little. The large number of loci contributing to disease resistance, the cyclic nature of the exposure relieving the population in predictable time units from selection pressure, and the tendency for conditions that might enhance development of disease resistance such as rapid growth to be counterbalanced by multiple yearly spawnings, hamper the rapid development of disease resistance. Unfortunately, epizootic mortality rates at cycle apogee, twice that observed at cycle nadir or prior to onset of disease, are consequential from the standpoint of population sustainability, but much less consequential for driving selection towards disease resistance. The periodicity of dermo epizootics may doom oyster populations to an extended period of low abundance, during which disease resistance slowly improves; bit by bit limiting the depredations of the disease