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

Seasonal abundance and occurrence of the Asian isopod Synidotea laevidorsalis in

Abstract In 1999 the marine isopod Synidotea laevidorsalis (Miers 1881), indigenous to the northwest Pacific, was first documented in Delaware Bay, USA. We monitored weekly recruitment of this isopod and several other motile species in the Maurice River, a tributary of Delaware Bay. A spatial survey was also conducted. Abundance of S. laevidorsalis varied seasonally but overwhelmingly dominated other co-occurring species by an order of magnitude or more throughout most of the year. Isopod abundance increased through the summer of 2004 and peaked in September, coincident with the passing of Hurricane Ivan. Field observations documented large populations, frequently associated with pilings and buoy lines, throughout Delaware Bay in salinities of 4 through 22 ppt. The dramatic abundance of this isopod indicates that there is considerable potential for altering community structure. This isopod has yet to be observed along the Atlantic Coast of New Jersey or in Chesapeake Bay, but it has been reported near Charleston, SC

Effective population sizes of eastern oyster Crassostrea virginica (Gmelin) populations in Delaware Bay, USA

Effective population size (Ne) is an important concept in population genetics as it dictates the rate of genetic change caused by drift. Ne estimates for many marine populations are small relative to the census population size. Small Ne in a large population may indicate high reproductive variance or sweepstakes reproductive success (SRS). The eastern oyster (Crassostrea virginica) may be prone to SRS due to its high fecundity and high larval mortality. To examine if SRS occurs in the eastern oyster, we studied Ne and genetic variation of oyster populations in Delaware Bay. Adult and spat oysters were collected from five locations in different years and genotyped with seven microsatellite markers. Slight genetic differences were revealed by Fst statistics between the adult populations and spat recruits, while the adult populations are spatially homogeneous and temporally stable. Comparisons of genetic diversity and relatedness among adult and spat samples failed to provide convincing evidence for strong SRS. Ne estimates obtained with five different methods were variable, small and often without upper confidence limits. For single sample collections, Ne estimates for spat (140–440) were consistently smaller than that for adults (589–2,779). Analysis of pooled adult samples across all sites suggests that Ne for the whole bay may be very large, as indicated by the large point estimates and the lack of upper confidence limits. These results suggest that Ne may be small for a given spat fall, but the entire adult population may have large Ne and is temporally stable as it is the accumulation of many spat falls per year over many year

An Investigation into the Scallop Parasite Outbreak on the Mid-Atlantic Shelf: Transmission Pathways, Spatio-Temporal Variation of Infection and Consequences to Marketability : Final Report

A disease epizootic has developed that threatens one of the most valuable fisheries in the US. The U.S. sea scallop (Placopecten magellanicus) fishery landed $512 million worth of scallop meats in 2017 (NMFS, 2018). This fishery is based on landings of scallop adductor muscles only, with the remainder of the scallop discarded at sea (NEFSC, 2018). During the spring of 2015 both industry and scientific assessment crews noted unprecedented numbers of a parasitic nematode in the adductor muscle of captured scallops (Figure 1). The presence of the parasite in the adductor muscle is expressed through macroscopic lesions, or cysts. These lesions are rust-brown to orange/brown in color with a typically elongated shape, ranging from 2 -12 mm in length and 1 - 4 mm in width. Nearly all lesions were observed along the exterior edge of the adductor muscle between the mantle velar folds of both valves opposite the catch muscle (sweet-meat). This location on the adductor muscle is anatomically adjacent to the kidney-adductor muscle attachment site and opposite of scallop intestine and anus. Infected scallops were observed in the southern portion of the stock and corresponded with the re-opening of three spatial management areas in this region. The wide distribution of the observed parasite is of concern from a product marketability standpoint and may represent the early stages of an expansion of parasite prevalence and intensity. Preliminary investigations suggest that the nematode observed is Sulcasaris sulcata (Rudders and Roman, 2018a)

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

Intensive oyster aquaculture can reduce disease impacts on sympatric wild oysters

Risks associated with disease spread from fish and shellfish farming have plagued the growth and public perception of aquaculture worldwide. However, by processing nutrients and organic material from the water column, the culture of many suspension-feeding bivalves has been proposed as a novel solution toward mitigating problems facing coastal water quality, including the removal of disease-causing parasites. Here we developed and simulated an epidemiological model describing sympatric oyster Crassostrea virginica populations in aquaculture and the wild impacted by the protozoan parasite Perkinsus marinus. Our model captured the indirect interaction between wild and cultured populations that occurs through sharing water-borne P. marinus transmission stages, and we hypothesized that oyster aquaculture can enhance wild oyster populations through reduced parasitism as long as cultured oysters are harvested prior to spreading disease. We found that the density of oysters in aquaculture, which is commonly thought to lead to the spread of disease through farms and out to nearby populations in the wild, has only indirect effects on P. marinus transmission through its interaction with the rate of aquaculture harvests. Sufficient aquaculture harvest, which varies with the susceptibility of farmed oysters to P. marinus infection and their lifespan once infected, reduces disease by diluting parasites in the environment. Our modeling results offer new insights toward the broader epidemiological implications of oyster aquaculture and effective disease management

Circulation and Water Properties and Their Relationship to the Oyster Disease MSX in Delaware Bay

We apply a high-resolution hydro-dynamical model to investigate the role of physical factors influencing infection prevalence of Haplosporidium nelsoni, causative agent of MSX disease in the eastern oyster (Crassostrea virginica), in Delaware Bay, USA. Validation studies conducted for the years 2000 and 2010-2011 confirm that the model, based upon the Regional Ocean Modeling System, has significant skill in the recovery of observed water level, temperature, salinity, and velocity. Multi-year simulations are performed for periods representing temporal and spatial variations in H. nelsoni infection prevalence (1974-76, 1979-81, 1984-86, 1990-92, and 2006-09) to assess the degree to which the variations in water properties and transport are temporally and spatially correlated with infection prevalence variations. Results show statistically significant correlations between the observed prevalence of MSX and multiple physical factors including river flow and salinity (themselves highly correlated), as well as the co-occurrence of elevated temperature and salinity values. Observed occurrences of high H. nelsoni infection prevalence at upbay locations correspond to periods of enhanced cross-bay and upbay transport together with hospitable temperature and salinity conditions

Understanding How Disease and Environment Combine to Structure Resistance in Estuarine Bivalve Populations

Delaware Bay oyster (Crassostrea virginica) populations are influenced by two lethal parasites that cause Dermo and MSX diseases. As part of the US National Science Foundation Ecology of Infectious Diseases initiative, a program developed for Delaware Bay focuses on understanding how oyster population genetics and population dynamics interact with the environment and these parasites to structure he host populations, and how these interactions might modified by climate change. Laboratory and field studies undertaken during this program include identifying genes related to MSX and Dermo disease resistance, potential regions for refugia and the mechanisms that allow them to exist, phenotypic and genotypic differences in oysters from putative refugia and high-disease areas, and spatial and temporal variability in the effective size of the spawning populations. Resulting data provide inputs to oyster genetics, population dynamics, and larval growth models that interface with a three-dimensional circulation model developed for Delaware Bay. Reconstruction of Lagrangian particle tracks is used to infer transport pathways of oyster larvae and MSX and Dermo disease pathogens. Results emerging from laboratory, field, and modeling studies are providing an understanding of long-term changes in Delaware Bay oyster populations that occur as the oyster population responds to climate, environmental, and biological variability