Wild chinook salmon survive better than hatchery salmon in a period of poor production

The population dynamics of chinook salmon (Oncorhynchus tshawytscha) from the Cowichan River on Vancouver Island, British Columbia, Canada are used by the Pacific Salmon Commission as an index of the general state of chinook salmon coast wide. In recent years the production declined to very low levels despite the use of a hatchery that was intended to increase production by improving the number of smolts entering the ocean. In 2008, we carried out an extensive study of the early marine survival of the hatchery and wild juvenile chinook salmon. We found that both rearing types mostly remained within the Gulf Islands study area during the period when most of the marine mortality occurred for the hatchery fish. By mid September, approximately 1.3% of all hatchery fish survived, compared to 7.8%–31.5% for wild fish. This six to 24 times difference in survival could negate an estimated increased egg-to-smolt survival of about 13% that is theorized to result through the use of a hatchery. Estimates of the early marine survival are approximate, but sufficient to show a dramatic difference in the response of the two rearing types to the marine nursery area. If the declining trend in production continues for both rearing types, modifications to the hatchery program are needed to improve survival or an emphasis on improving the abundances of wild stocks is necessary, or both. The discovery that the juvenile Cowichan River chinook salmon remain within a relatively confined area of the Gulf Islands within the Strait of Georgia offers an excellent opportunity to research the mechanisms that cause the early marine mortalities and hopefully contribute to a management that improves the production.     

Consequences to fitness‐related traits of hybridization between farmed and wild Atlantic salmon, Salmo salar

Increasing concern has been expressed about the genetic effects of cultured salmonid fishes on natural populations. Avoidance of extreme negative outcomes was one reason for the establishment of a genetic management policy for the State of Alaska. However, domestication within the hatchery may still cause divergence from the wild donor population. This divergence could potentially lead to adverse impacts on wild stocks through straying and introgression. This study examines potential domestication in two Alaskan chinook salmon stocks. The Little Port Walter (LPW) Hatchery Chickamin River stock resulted from a small collection of wild broodstock in 1976. The LPW Unuk stock was founded with a larger number of individuals in 1976 and has had subsequent infusion of wild gametes. These lines have been maintained at LPW through ocean ranching of tagged smolts. Comparisons are made between the hatchery lines, progeny of wild chinook collected from the Chickamin and Unuk Rivers, and hybrids between the hatchery and wild groups. Mature ocean‐ranched female chinook salmon returning to the facility were periodically graded for ripeness and spawned. Body size and meristic measurements were collected from these mature spawners. Maturation timing, fecundity, and individual egg size of these fourth generation hatchery fish are compared with that of offspring of wild fish from the same donor stock. Stock of origin is confirmed for all spawners and offspring using microsatellite DNA analysis.     

Comparison of maturation timing,egg size and fecundity between hatchery lines of chinook salmon and their wild donor stocks

Increasing concern has been expressed about the genetic effects of cultured salmonid fishes on natural populations. Avoidance of extreme negative outcomes was one reason for the establishment of a genetic management policy for the State of Alaska. However, domestication within the hatchery may still cause divergence from the wild donor population. This divergence could potentially lead to adverse impacts on wild stocks through straying and introgression. This study examines potential domestication in two Alaskan chinook salmon stocks. The Little Port Walter (LPW) Hatchery Chickamin River stock resulted from a small collection of wild broodstock in 1976. The LPW Unuk stock was founded with a larger number of individuals in 1976 and has had subsequent infusion of wild gametes. These lines have been maintained at LPW through ocean ranching of tagged smolts. Comparisons are made between the hatchery lines, progeny of wild chinook collected from the Chickamin and Unuk Rivers, and hybrids between the hatchery and wild groups. Mature ocean‐ranched female chinook salmon returning to the facility were periodically graded for ripeness and spawned. Body size and meristic measurements were collected from these mature spawners. Maturation timing, fecundity, and individual egg size of these fourth generation hatchery fish are compared with that of offspring of wild fish from the same donor stock. Stock of origin is confirmed for all spawners and offspring using microsatellite DNA analysis.     

Understanding the adaptive consequences of hatchery-wild interactions in Alaska salmon

About 31% of salmon harvested in Alaska comes from the hatchery production of hundreds of millions of pink and chum salmon and smaller numbers of sockeye, Chinook, and coho salmon. The numbers of hatchery-reared juveniles released in some areas are greater than the numbers of juveniles from wild populations. However, virtually nothing is known about the effects of hatchery fish on wild populations in Alaska. Possible effects of these interactions can be inferred from studies of salmonids in other areas, from studies of other animals, and from theory. Numerous studies show a complex relationship between the genetic architecture of a population and its environment. Adaptive responses to nature and anthropogenic selection can be influenced by variation at a single gene, or more often, by the additive effects of several genes. Studies of salmonids in other areas show that hatchery practices can lead to the loss of genetic diversity, to shifts in adult run timing and earlier maturity, to increases in parasite load, to increases in straying, to altered levels of boldness and dominance, to shifts in juvenile out-migration timing, and to changes in growth. Controlled experiments across generations show, and theory predicts, that the loss of adaptive fitness in hatchery salmon, relative to fitness in wild salmon, can occur on a remarkably short time scale. All of these changes can influence survival and impose selective regimes that influence genetically based adaptive traits. The preservation of adaptive potential in wild populations is an important buffer against diseases and climate variability and, hence, should be considered in planning hatchery production levels and release locations. The protection of wild populations is the foundation for achieving sustained harvests of salmon in Alaska.     

Some consequences of Pacific salmon hatchery production in Kamchatka: changes in age structure and contributions to natural spawning populations

Aggregate hatchery production of Pacific salmon in the Kamchatka region of the Russian Federation is very low (< 0.5% of total harvest, with five hatcheries releasing approximately 41 M juvenile salmon annually), but contributions in certain rivers can be substantial. Enhancement programs in these rivers may strongly influence fitness and production of wild salmon. In this paper we document significant divergence in demographic traits in hatchery salmon populations in the Bolshaya River and we estimate the proportion of hatchery chum salmon in the total run in the Paratunka River to demonstrate the magnitude of enhancement in this system. We observed a reduction in the expression of life history types in hatchery populations (ranging from 1 to 9 types) compared to wild populations (17 types) of sockeye salmon in the Bolshaya River. We found similar trends in Chinook salmon in the same river system. This reduced life history diversity may make these fish less resilient to changes in habitat and climate. We estimate hatchery chum salmon currently contribute 17-45% to the natural spawning population in the Paratunka River. As hatchery fish increase in numbers at natural spawning sites, this hatchery production may affect wild salmon production. It is important to investigate the risk of introgression between hatchery and wild salmon that can lead to reduction in salmon fitness in Kamchatka rivers, as well as the potential of ecological interactions that can have consequences on status of wild salmon and overall salmon production in this region.     

Analysis of gene origin in the first adult returns to the Cultus sockeye salmon captive breeding program

Rigorous evaluation of the utility of captive breeding for the restoration of depleted wild salmonid fish populations has not been undertaken. In particular, little is known about the reproductive success of captively-bred individuals that are released back into an extant population and their capacity to assist in long-term population persistence. For the endangered Cultus Lake sockeye salmon population, we examined the potential genetic contribution of the first juvenile fish released from a captive breeding program upon their maturity in the natural Cultus Lake environment. Genetic analysis of 792 Cultus sockeye salmon that were spawned in captivity in 2004 and their adult progeny of 2007 and 2008 revealed a genetic bottleneck originating from 20 wild sockeye salmon hatchery-spawned at Cultus Lake in the previous generation. Pedigree analysis revealed that six of the 20 sockeye salmon spawned in 2001 (grandparents) gave rise to a majority of the hatchery spawners in 2004 (parents) and provided more than 30% of the genes in the progeny that survived to maturity in the wild. Allele frequencies and genetic diversity of the age three progeny that returned to Cultus Lake from their marine migration in 2007 reflected the bottleneck, but its genetic signature was faint among the more genetically diverse age four fish that returned in 2008. Two-generation analysis of gene origin among fish resulting from 2004 hatchery production indicated that they contained the genetic diversity expected from 36 effective ancestors.     

Overview of salmon stock enhancement in southeast Alaska and compatibility with maintenance of hatchery and wild stocks

Modern salmon hatcheries in Southeast Alaska were established in the 1970s when wild runs were at record low levels. Enhancement programs were designed to help rehabilitate depressed fisheries and to protect wild salmon stocks through detailed planning and permitting processes that included focused policies on genetics, pathology, and management. Hatcheries were located away from significant wild stocks, local sources were used to develop hatchery broodstocks, and juveniles are marked so management can target fisheries on hatchery fish. Initially conceived as a state-run system, the Southeast Alaska (SEAK) program has evolved into a private, non-profit concept centered around regional aquaculture associations run by fishermen and other stakeholders that pay for hatchery operations through landing fees and sale of fish. Today there are 15 production hatcheries and 2 research hatcheries in SEAK that between 2005 and 2009 released from 474 to 580 million (average 517 million) juvenile salmon per year. During this same period commercial harvest of salmon in the region ranged from 28 to 71 million salmon per year (average 49 million). Contributions of hatchery-origin fish to this harvest respectively averaged 2%, 9%, 19%, 20%, and 78% for pink, sockeye, Chinook, coho, and chum salmon. Both hatchery and wild salmon stocks throughout much of Alaska have experienced high marine survivals since the 1980s and 1990s resulting in record harvests over the past two decades. Although some interactions between hatchery salmon and wild salmon are unavoidable including increasing concerns over straying of hatchery fish into wild salmon streams, obvious adverse impacts from hatcheries on production of wild salmon populations in this region are not readily evident.     

Ecological Risk Assessment Paradigm for Salmon: Analyzing Immune Function to Evaluate Risk

Wild Pacific salmon populations are in serious decline, and as a result, a number of salmon stocks are listed as threatened or endangered under the Endangered Species Act. Our research identifies and supports the possibility that certain environmental contaminants can alter salmon survival, and as a result may contribute to these species being at risk. We have shown that juvenile chinook salmon (Oncorhynchus tshawytscha) are exposed to polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) as they migrate through a contaminated urban estuary in Puget Sound WA (the Duwamish Waterway estuary). Immune function was analyzed in these fish by examining the ability of their anterior kidney and splenic leukocytes to produce a primary and secondary in vitro plaque-forming cell (PFC) response to the hapten, trinitrophenyl (TNP), and by determining their susceptibility to a marine pathogen, Vibrio anguillarum. We found that fish outmigrating from the urban estuary produced a significantly lower PFC response to TNP and were more susceptible to the pathogen, compared to juvenile salmon collected from a rural estuary during their outmigration. In the laboratory, we exposed juvenile chinook salmon collected from a hatchery to either a PCB technical mixture or a PAH compound to determine if these contaminants have the potential to alter immune function in salmon. Indeed, we found that salmon exposed in the laboratory to either the PCB mixture or the PAH also produced lower PFC responses and were more susceptible to disease compared to animals treated with the solvent vehicle. In summary, contaminants such as PAHs and PCBs are demonstrated to influence salmon health, and thus have the potential to adversely impact salmon populations.     

Evidence for a carrier state of infectious hematopoietic necrosis virus in chinook salmon Oncorhynchus tshawytscha.

In British Columbia, Canada, infectious hematopoietic necrosis virus (IHNV) is prevalent in wild sockeye salmon Oncorhynchus nerka and has caused disease in seawater net-pen reared Atlantic salmon Salmo salar. In this study, chinook salmon Oncorhynchus tshawytscha experimentally exposed to an isolate of IHNV found in British Columbia became carriers of the virus. When Atlantic salmon were cohabited with these virus-exposed chinook salmon, IHNV was isolated from the Atlantic salmon. Identification of chinook salmon populations that have been exposed to IHNV may be difficult, as virus isolation was successful only in fish that were concurrently infected with either Renibacterium salmoninarum or Piscirickettisia salmonis. Also, IHNV-specific antibodies were detected in only 2 of the 70 fish experimentally exposed to the virus. Two samples collected from chinook salmon exposed to IHNV while at a salt water net-pen site had a seroprevalence of 19 and 22%; however, the inconsistencies between our laboratory and field data suggest that further research is required before we can rely on serological analysis for identifying potential carrier populations. Because of the difficulty in determining the exposure status of populations of chinook salmon, especially if there is no concurrent disease, it may be prudent not to cohabit Atlantic salmon with chinook salmon on a farm if there is any possibility that the latter have been exposed to the virus.     

Innate and enhanced predator recognition in hatchery-reared chinook salmon

We used a laboratory behaviour assay to investigate how innate predator recognition, handling stress, retention time, and number of conditioning events might affect chemically mediated anti-predator conditioning for hatchery-reared chinook salmon, Oncorhynchus tshawytscha. Juvenile chinook salmon with no prior exposure to predatory stimuli exhibited innate fright responses to northern pikeminnow, Ptychocheilis oregonensis, odour, regardless of whether the salmon came from a population that exists in sympatry or allopatry with northern pikeminnows. Juvenile chinook salmon exhibited enhanced predator recognition following a single conditioning event with conspecific extract and northern pikeminnow odour. Handling similar to what hatchery salmon might experience prior to release did not substantially reduce the conditioned response. When we conditioned juvenile chinook salmon in hatchery rearing vessels, fish from tanks treated once exhibited a conditioned response to northern pikeminnow odour in aquaria, but only for one behaviour (feeding response), and fish treated twice did not respond. The results suggest that enhanced recognition of predator stimuli occurs quickly, but may be to some extent context-specific, which may limit conditioned fright responses after release into the natural environment.     

Maladaptation and phenotypic mismatch in cultured Atlantic salmon used for stocking

Compared to wild populations, cultured Atlantic salmon often sustain higher mortality rates and lower adult return rates when stocked as juveniles into natural streams. The ultimate causes for such differences in fitness, however, are not clear. Here we tested if relaxed levels of natural selection and improved survival in the hatchery environment could account for the observed degree of maladaptation among stocked fish. To do this, we assessed the degree of phenotypic mismatch between wild and cultured fish in three populations over five consecutive years. Significant differences were found in several phenotypic traits that are likely to have fitness implications. Thus, if the objective is to mimic wild individuals for restoration purposes, current hatchery practices aimed at maximising juvenile survival and enhancing growth may need to be revised.     

Evidence for competition at sea between Norton Sound chum salmon and Asian hatchery chum salmon

Increasing production of hatchery salmon over the past four decades has led to concerns about possible density-dependent effects on wild Pacific salmon populations in the North Pacific Ocean. The concern arises because salmon from distant regions overlap in the ocean, and wild salmon populations having low productivity may compete for food with abundant hatchery populations. We tested the hypothesis that adult length-at-age, age-at-maturation, productivity, and abundance of a Norton Sound, Alaska, chum salmon population were influenced by Asian hatchery chum salmon, which have become exceptionally abundant and surpassed the abundance of wild chum salmon in the North Pacific beginning in the early 1980s. We found that smaller adult length-at-age, delayed age-at-maturation, and reduced productivity and abundance of the Norton Sound salmon population were associated with greater production of Asian hatchery chum salmon since 1965. Modeling of the density-dependent relationship, while controlling for other influential variables, indicated that an increase in adult hatchery chum salmon abundance from 10 million to 80 million adult fish led to a 72% reduction in the abundance of the wild chum salmon population. These findings indicate that competition with hatchery chum salmon contributed to the low productivity and abundance of Norton Sound chum salmon, which includes several stocks that are classified as Stocks of Concern by the State of Alaska. This study provides new evidence indicating that large-scale hatchery production may influence body size, age-at-maturation, productivity and abundance of a distant wild salmon population.     

Disease interaction between farmed and wild fish populations

This paper reviews the literature on disease interaction between wild and farmed fish and recommends strategies to reduce the disease risks to both populations. Most, if not all, diseases of farmed fish originate in wild populations. The close contact between farmed and wild fish readily leads to pathogens exchange. Aquaculture creates conditions ( e.g. high stocking levels) conducive to pathogen transmission and disease; hence pathogens can overspill back, resulting in high levels of challenge to wild populations. This is exemplified by sea lice infections in farmed Atlantic salmon. Stocking with hatchery reared fish or aquaculture escapees can affect disease dynamics in wild populations. Whirling disease has been spread to many wild rainbow trout populations in the US with the release of hatchery reared stock. The greatest impact of aquaculture on disease in wild populations has resulted from the movement of fish for cultivation. Examples of exotic disease introduction following movement of live fish for aquaculture with serious consequences for wild populations are reviewed. The salmon parasite, Gyrodactylus salaris, has destroyed wild salmon populations in 44 Norwegian rivers. Crayfish plague has wiped out European crayfish over much of Europe. Eels numbers have declined in Europe and infection with the swimbladder nematode Anguillicola crassus has in part been blamed. The impact of disease in farmed fish on wild populations can mitigated. Risk analysis methods need to be refined and applied to live fish movement and new aquacultural developments. Appropriate biosecurity strategies, based on risk assessments, should be developed to reduce pathogen exchange and mitigate the consequences.     

Factors that contribute to the ecological risks of salmon and steelhead hatchery programs and some mitigating strategies

State and federal agencies in the United States annually release millions of hatchery salmon and steelhead into public waters. Many of the hatchery programs are located in areas where the wild populations are now listed under the U.S. Endangered Species Act (ESA) (16 U.S.C. §§ 1531–1544). These hatchery programs pose genetic and ecological risks to wild fish populations. Genetic risks occur when hatchery and wild fish interbreed and usually occur within a taxonomic species. Ecological risks occur when the presence of hatchery fish affects how wild fish interact with their environment or with other species and may affect whole species assemblages. This paper reviews some of the factors that contribute to ecological risks. Important contributing factors include the relative abundance of hatchery and wild fish in natural production areas, hatchery programs that increase density-dependant mortality, residual hatchery fish, some physical advantages that hatchery fish can have over wild fish, and life history characteristics that may make some species especially vulnerable to the effects of ecological risks. Many of these risk factors can be mitigated by management activities that reduce the level of interactions between hatchery and wild fish. This paper concludes by recommending twelve mitigation strategies that may be useful when agencies need to bring hatchery programs into compliance with the take provisions of the ESA.     

Different prevalences of Renibacterium salmoninarum detected by ELISA in Alaskan chinook salmon Oncorhynchus tshawytscha spawned from freshwater and seawater

Soluble antigen of Renibacterium salmoninarum (Rs) was detected by a polyclonal enzyme-linked immunosorbent assay (ELISA) at significantly higher prevalences in adult chinook salmon Oncorhynchus tshawytscha that matured in freshwater than in the same cohort of fish spawned after maturation in seawater. The cumulative results were consistent during 4 yr of comparison at the Little Port Walter Hatchery on Baranof Island, Alaska, USA. Possible causes for this difference are discussed. Maturation of chinook salmon broodstock in seawater has become a practical strategy at this hatchery to reduce the prevalence of Rs-positive parent fish and the numbers of culled eggs.     

Lopsided Fish in the Snake River Basin — Fluctuating Asymmetry as a way of Assessing Impact of Hatchery Supplementation in Chinook Salmon, Oncorhynchus tshawytscha

The use of developmental instability (an individual's failure to produce a consistent phenotype in a given environment) was evaluated to detect the effects of outplanting hatchery fish on wild salmon. Juvenile chinook salmon were collected in 1989, 1990, and 1991 from five drainages in the Snake River Basin. In each drainage we attempted to collect fish from streams with no hatchery supplementation (wild), naturally spawning fish from streams with hatchery supplementation (natural), and fish collected at a hatchery. Forty fish were collected per site and the number of elements in bilateral characters were counted on each side of the fish. Indices of fluctuating asymmetry (FA), a measure of minor, random deviations in perfect symmetry of bilateral counts, were calculated as an estimator of developmental instability. Analysis of character counts from seven paired characters revealed normal distributions. Only one of the characters displayed counts that were statistically larger on one side than the other, indicating that directional asymmetry (DA) or antisymmetry was not a major bias of FA. However, the means of all individual characters revealed a non-statistically significant left side bias. We analyzed our data using two indices of FA (FA1 and FA5) with different levels of sensitivity to DA. Differences in both FA indices were found among years, with collection sites in 1989 having significantly larger FA values than in 1991 (FA p < 0.01). Levels of FA among wild, natural, and hatchery fish were comparatively small (FA1 p = 0.17). This suggests developmental conditions were different in the first year of the study than in the last. The cause of these differences may be linked to either genetic or environmental variation or to gene—environment interactions, but the general population declines of salmon that occurred during this time obscures more specific conclusions.     

Source-Sink Estimates of Genetic Introgression Show Influence of Hatchery Strays on Wild Chum Salmon Populations in Prince William Sound,Alaska

The extent to which stray, hatchery-reared salmon affect wild populations is much debated. Although experiments show that artificial breeding and culture influence the genetics of hatchery salmon, little is known about the interaction between hatchery and wild salmon in a natural setting. Here, we estimated historical and contemporary genetic population structures of chum salmon (Oncorhynchus keta) in Prince William Sound (PWS), Alaska, with 135 single nucleotide polymorphism (SNP) markers. Historical population structure was inferred from the analysis of DNA from fish scales, which had been archived since the late 1960’s for several populations in PWS. Parallel analyses with microsatellites and a test based on Hardy-Weinberg proportions showed that about 50% of the fish-scale DNA was cross-contaminated with DNA from other fish. These samples were removed from the analysis. We used a novel application of the classical source-sink model to compare SNP allele frequencies in these archived fish-scales (1964–1982) with frequencies in contemporary samples (2008–2010) and found a temporal shift toward hatchery allele frequencies in some wild populations. Other populations showed markedly less introgression, despite moderate amounts of hatchery straying. The extent of introgression may reflect similarities in spawning time and life-history traits between hatchery and wild fish, or the degree that hybrids return to a natal spawning area. The source-sink model is a powerful means of detecting low levels of introgression over several generations.     

Genetic implications of hatchery rearing in Atlantic salmon: effects of rearing environment on genetic composition

In an experiment to investigate genetic consequences of hatchery rearing in salmon, allozyme variation at five polymorphic loci was examined in Atlantic salmon of known initial genetic composition, which were reared throughout freshwater life in the hatchery or stocked into the wild as swim-up fry. The genetic composition of the juveniles in the hatchery remained homogeneous from fertilization up to stocking, and from stocking to 2+ in the wild, however, those remaining at the hatchery developed genetic differences among smolting and nonsmolting 1+ parr. These differences were attributed to conditions leading to early smolting at 1+ among the hatchery fish, with 1+ smolts diverging from the gene pool from which they were derived, whereas those stocked into the wild did not smolt until a year later and retained the original genetic composition. The results are discussed in relation to hatchery rearing of salmon and implications for the use of reared fish in stocking and enhancement programmes.     

Non-indigenous brook trout and the demise of Pacific salmon: a forgotten threat?

Non-indigenous species may be the most severe environmental threat the world now faces. Fishes, in particular, have been intentionally introduced worldwide and have commonly caused the local extinction of native fish. Despite their importance, the impact of introduced fishes on threatened populations of Pacific salmon has never been systemically examined. Here, we take advantage of several unique datasets from the Columbia River Basin to address the impact of non-indigenous brook trout, Salvelinus fontinalis, on threatened spring/summer-run chinook salmon, Oncorhynchus tshawytscha. More than 41 000 juvenile chinook were individually marked, and their survival in streams without brook trout was nearly double the survival in streams with brook trout. Furthermore, when brook trout were absent, habitat quality was positively associated with chinook survival, but when brook trout were present no relationship between chinook survival and habitat quality was evident. The difference in juvenile chinook survival between sites with, and without, brook trout would increase population growth rate (lambda) by ca. 2.5%. This increase in lambda would be sufficient to reverse the negative population growth observed in many chinook populations. Because many of the populations we investigated occur in wilderness areas, their habitat has been considered pristine; however, our results emphasize that non-indigenous species are present and may have a dramatic impact, even in remote regions that otherwise appear pristine.     

Natural selection acts on Atlantic salmon major histocompatibility (MH) variability in the wild

Pathogen-driven balancing selection is thought to maintain polymorphism in major histocompatibility (MH) genes. However, there have been few empirical demonstrations of selection acting on MH loci in natural populations. To determine whether natural selection on MH genes has fitness consequences for wild Atlantic salmon in natural conditions, we compared observed genotype frequencies of Atlantic salmon (Salmo salar) surviving in a river six months after their introduction as eggs with frequencies expected from parental crosses. We found significant differences between expected and observed genotype frequencies at the MH class II alpha locus, but not at a MH class I-linked microsatellite or at seven non-MH-linked microsatellite loci. We therefore conclude that selection at the MH class II alpha locus was a result of disease-mediated natural selection, rather than any demographic event. We also show that survival was associated with additive allelic effects at the MH class II alpha locus. Our results have implications for both the conservation of wild salmon stocks and the management of disease in hatchery fish. We conclude that natural or hatchery populations have the best chance of dealing with episodic and variable disease challenges if MH genetic variation is preserved both within and among populations.