© 2005 International Council for the Exploration of the Sea
Genetic impact of gadoid culture on wild fish populations: predictions, lessons from salmonids, and possibilities for minimizing adverse effects
Danish Institute for Fisheries Research, Department of Inland Fisheries Vejlsøvej 39, 8600 Silkeborg, Denmark
*Correspondence to D. Bekkevold: tel: +45 89213100; fax: + 45 89213150. e-mail: db{at}difres.dk.
Little is known about the effects of ranched gadoids escaping into wild populations, and plans for substantial up-scaling of gadoid mariculture raise concerns about detrimental effects on local gene pools. Genetic studies from salmonid populations subjected to intentional or unintentional releases of hatchery-produced fish suggest that wild gene pools are affected by introgression, but that the genetic impact can be minor relative to expectations from the often substantial numbers of released hatchery fish. However, even if resilience to introgression is a general trend, wild population fitness is still predicted to be jeopardized by releases. In this paper, we review theoretical genetic effects of escapes of cultivated individuals and the empirical evidence for introgression effects, which are based mainly on salmonid studies. Based on knowledge of gadoid population structure and life history traits, we make predictions for effects of gadoid mariculture on wild populations and discuss approaches for monitoring and minimizing introgression effects.
Keywords: domestication, effective population size, gadoid mariculture, hatchery, introgression, local adaptation, salmonid
Received 24 September 2004; accepted 1 November 2005.
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Introduction |
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 Top Introduction Genetic effects of ranchingGadoid population structureGene flow from mariculture...Detection of introgressionMinimizing introgression effectsReferences |
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There is growing concern about the impact of escapees from large-scale fish culture activities interbreeding with wild fish, leading to introgression of wild gene pools and, subsequently, to lowered fitness (survival and recruitment) of wild populations. It has been estimated that the annual escapees of farmed Atlantic salmon (Salmo salar Linnaeus) in the North Atlantic amount to several million individuals and, in some Norwegian rivers, more than 80% of all spawners are farm escapees (Sægrov et al., 1997). Genetic studies of salmonids have shown that accidental releases and supplemental stocking with farmed strains have influenced wild gene pools (recent studies include Berrebi et al., 2000a; Hansen, 2002; Young et al., 2004), and this has led to increased awareness of the impact of introgression (Hindar et al., 1991; Ryman et al., 1995; Ryman, 1997) and to changes in management strategies (e.g. Berg and Hansen, 2002). Nonetheless, even for the best studied salmonid populations, there is limited understanding of the long-term effects of introgression, and knowledge is virtually non-existent for marine fish. In recent years, decreasing commercial fishery harvests have led to increasing interest in the possibilities for large-scale aquaculture of gadoid fish, particularly Atlantic cod, Gadus morhua Linnaeus, which has been one of the most commercially valuable species in the North Atlantic. This paper assesses the possible genetic effects of gadoid culture on wild populations. Concerns about altering gene pools of local populations can be grouped under two headings. First, introgression from domesticated fish that are maladapted in the wild and/or genetically depauperate may cause negative fitness effects. Second, gadoids of different population background may differ in growth rate, parasite resistance, etc., and hence, in their appeal to mariculture breeding programmes (Gjerde et al., 2004). As a result, escapees from fish culture activities, even if they have not gone through a domestication process, will lead to substantial mixing of individuals that might otherwise be geographically and reproductively isolated. This causes the further concern that introgression into wild populations that are adapted to local conditions will result in outbreeding depression and disruption of co-adapted gene complexes. Here, we first treat theoretical and observed characteristics of cultured stocks. Then, we review the evidence for population structure and local adaptations in gadoid fish. Third, we discuss effects of introgression in wild populations. These discussions are based mainly on lessons from salmonid studies, and we assess how similarities and differences in salmonid and gadoid life histories and population structures affect the predictions about the effects of gadoid escapees. Fourth, we discuss ways of detecting and monitoring introgression based on genetic markers, and finally, how adverse effects of gadoid mariculture on wild populations can be minimized. Apart from being attractive from a mariculture perspective, Atlantic cod is the scientifically most intensively studied gadoid species, which is reflected in the studies cited here. However, general predictions about effects of mariculture on wild populations should be expected to hold for other cultured species, such as haddock, Melanogrammus aeglefinus Linnaeus, and pollack, Pollachius pollachius Linnaeus.
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Genetic effects of ranching |
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TopIntroductionGenetic effects of ranchingGadoid population structureGene flow from mariculture...Detection of introgressionMinimizing introgression effectsReferences |
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Most aquaculture stocks are sustained in hatcheries and farms for many generations. Usually, this is done for practical reasons and in order to breed selectively for desired traits such as high growth rate and disease resistance (Gjøen and Bentsen, 1997). Obviously, such breeding programmes lead to changes in the genetic composition in farmed stocks over time. However, genetic changes will occur even without the application of selective breeding programmes as a result of the effects of random genetic drift and what is commonly known as domestication selection. Random genetic drift is the process by which genetic variation is gradually lost as a result of stochastic changes in allele frequencies over generations. The magnitude of genetic drift is related to the genetically effective size, estimated by Ne, of the breeding population, with more drift taking place in small populations (Crow and Kimura, 1970). Hatcheries commonly use a small number of breeders compared with wild population sizes, and this results in cultured stocks losing genetic variation at a higher rate and having lower genetic diversity compared with their wild counterparts (e.g. Garcia-Marin et al., 1991; Exadactylos et al., 1999; Hansen et al., 2001b; Säisä et al., 2003; Evans et al., 2004a). The amount of genetic variation present within a breeding population has a direct relationship to its evolutionary potential, and populations with low genetic variability are less capable of responding adaptively to changing selection pressures, such as from novel parasites, altered temperature regimes, etc.
"Domestication selection" is a broad term that may in reality cover different processes. First, the captive environment is characterized by instant treatment of diseases, lowered competition for food, and absence of predators. This leads to a relaxation of natural selection pressures and to survival and propagation of phenotypes that would be disfavoured in the wild. Consequently, this process is actually the result of a lack of natural selection. Second, inadvertent directional selection may occur during hatchery propagation. For instance, individuals that show reduced shyness may be those that are most easily collected and chosen as parents for the next generation. If additive variation exists for shyness, this may therefore result in inadvertent selection for reduced shyness (i.e. boldness). Examples from salmonid fish ascribed to domestication selection include lowered predator avoidance (Berejikian, 1995; Johnsson et al., 1996; Alvarez and Nicieza, 2003), changes in morphology (e.g. Fleming and Einum, 1997), and increased boldness and aggressive behaviour (e.g. Einum and Fleming, 1997; Sundstrom et al., 2004).
The fitness of a population is also related to its genetic load, which is a measure of the fitness reduction that occurs as a result of the cumulative occurrence of deleterious mutations. The expectation is that large outbreeding populations (>>1000 individuals) harbour significant numbers of lethal or sublethal mutations occurring in a heterozygous state (Lynch et al., 1999). As long as such a population undergoes continuous outbreeding at a large effective population size, the fitness effects of these deleterious alleles remain negligible, and no significant selection occurs against them. If, however, individuals originating from large populations are inbred in a broodstock setting, this will lead to a high fixation rate and decreased fitness. This effect has been shown in plants, where self-crossing of individuals originating from large outbred populations resulted in larger fitness reductions in offspring than did self-crossings from smaller populations (Paland and Schmid, 2003). In broodstocks of rainbow trout, Oncorhynchus mykiss Walbaum, egg hatchability, fry survival, feed conversion efficiency, growth, and fecundity are highly affected by levels of inbreeding (reviewed by Kincaid, 1983). Inbreeding depression was also evident in a breeding programme for the Pacific oyster, Crassostrea gigas Thunberg, where sib-crosses exhibited significantly lower yield, growth rates, and survival compared with non-inbred individuals. Yield and growth rates were depressed even in first cousin crosses, i.e. at relatively low levels of inbreeding (Evans et al., 2004b). Thus, even though inbreeding depression is expected to occur as a result of breeding low numbers of individuals regardless of population history, individuals originating from large populations are expected to harbour more lethal or sublethal mutations, genome-wide, than those from historically small populations, and as a consequence, suffer larger fitness reductions when bred in small, isolated broodstocks. Most gadoid breeding programmes are tailored to minimizing the effects of genetic load by incorporating large numbers of breeding individuals. However, the implication to gadoid mariculture is that the magnitude of inbreeding effects may differ between salmonids and gadoids, as gadoid populations are assumed to be much larger than salmonid populations in general.
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Gadoid population structure |
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TopIntroductionGenetic effects of ranchingGadoid population structureGene flow from mariculture...Detection of introgressionMinimizing introgression effectsReferences |
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Evidence for gadoid population differences
The genetic impact of mariculture escapees will depend on the extent to which gadoids exhibit local population integrity and respond to local selection pressures. First, if reproductive behaviour differs among cod of different population backgrounds, this will affect the reproductive success in, and hence, level of gene flow from escapees. Second, if populations exhibit genetic differences of adaptive significance, introgression by fish of exogenous origin is expected to lead to decreased fitness resulting from outbreeding depression and break-up of co-adapted gene complexes. Fitness decrease caused by outbreeding depression in crosses among naturally isolated populations has been described in a multitude of species, including salmonids (see e.g. Gilk et al. (2004) for an example from pink salmon, Onchorhyncus gorbuscha Walbaum), whereas no examples are yet known from gadoids. Marine fish generally have high migratory abilities and as a consequence, potential for substantial exchange of dispersers among locations. In the absence of high local selection pressures, this should prevent establishment of population structure and local adaptations on less than very large scales (Ward et al., 1994). Nonetheless, biological differences among populations suggest that structure exists and that genetically based polymorphisms upheld by local selective pressures may have important fitness effects. Gadoids exhibit substantial population differences in growth and age at maturity (e.g. Hutchings et al., 1993; Begg et al., 1999; Otterlei et al., 1999; McIntyre and Hutchings, 2003; Salvanes et al., 2004), in morphology (e.g. Begg et al., 1999; Cardinale et al., 2004), and in biochemical properties (e.g. haemoglobin, Brix et al., 1998; allozymes, Mork et al., 1985). In vitro fertilization studies show that cod from the brackish Baltic Sea produce eggs that are buoyant at lower salinities than can be attained by cod originating from a high salinity environment, suggesting specific adaptations to local spawning conditions (Nissling and Westin, 1997). In spite of their migratory abilities, gadoids home to spawning areas (Rose, 1993; Robichaud and Rose, 2001), and migratory and resident population components apparently maintain different life history characteristics despite mixing on spawning sites (Nordeide, 1998). Gadoids exhibit complex reproductive behaviour involving both courtship displays and acoustic signals produced by specialized drumming muscles (Brawn, 1961; Engen and Folstad, 1999; Hutchings et al., 1999; Hawkins and Amorim, 2000), although there may be exceptions (Sakurai and Hattori, 1996). Rowe and Hutchings (2004) recently analysed reproductive behaviour in captive cod from two northwest Atlantic cod populations. The first, from the western Scotian Shelf, spawns December to March, and the second, from the southern Gulf of St. Lawrence, spawns several months later in May to July. Analysing male acoustic displays, the authors found that male drumming rates and somatic investment in drumming muscles differed between the two populations. Although this was not tested, the implication is that dispersers between the two populations may display suboptimal mating behaviour, and therefore, the study supports the hypothesis that behavioural differences can constitute a reproductive barrier between gadoid populations (Nordeide, 1998).
Exploring the heritable basis for population differences
Although the studies cited above suggest that individual population components have evolved in response to local selective forces, only a few studies have sought to control for environmental effects on the examined traits and, thus, to demonstrate a heritable basis for population differences (e.g. Nissling and Westin, 1997; Salvanes et al., 2004). Molecular genetic surveys of variation in non-coding DNA indicate considerable gadoid population structure across large spatial scales (such as between seas) (e.g. Ruzzante et al., 1998; Lundy et al., 1999; Pogson et al., 2001; Olsen et al., 2002) and salinity gradients (Nielsen et al., 2003). On smaller (within-sea) scales only low, albeit in some cases significant, structuring has been reported (e.g. Ruzzante et al., 1997; Arnason et al., 2000; Lundy et al., 2000; Hutchinson et al., 2001; Olsen et al., 2002; Knutsen et al., 2003). These studies suggest that, in the absence of clearly defined environmental gradients, small-scale structure is slight or non-existent. This constitutes a major contrast to genetic studies of salmonid populations, where substantial genetic differentiation can be found even on relatively small geographic scales (reviewed by Altukhov et al., 2000). This difference between gadoids and salmonids is caused by the latter spawning at discrete sites (rivers, streams, and lakes) that commonly exhibit substantial habitat heterogeneity and physical isolation. Coupled with generally smaller population sizes in salmonids, this leads to higher levels of random genetic drift and more pronounced genetic differentiation. The smaller genetic differentiation observed in gadoids as compared with salmonids does not, however, rule out adaptive variation among local populations. Traits that affect fitness are influenced by local selection pressures and have the potential to evolve despite gene flow, and may evolve much faster than traits that can be detected by neutral genetic markers. Furthermore, the stronger differentiation observed in salmonid fish reflects, at least partially, stronger genetic drift, which actually decreases the efficiency of local selection. On the other hand, in gadoid species, low genetic differentiation may reflect high effective population sizes and, thereby, reduced drift. If drift becomes unimportant, this again increases the potential for local selection to lead to adaptive differences among populations. Ultimately, predicting the potential for local adaptation based on neutral markers requires more specific knowledge of the parameters of gene flow and drift (effective population size) and cannot be based solely on the magnitude of genetic differentiation (Adkison, 1995; Hansen et al., 2002).
A direct approach to investigating population variation in selective traits is the "common garden" setup, where fish of different population origin are reared in uniform environments over generations. Persistent between-population variation in the trait under investigation (e.g. growth at temperature) demonstrates a genetic component to phenotypic differences. Studies in salmonids have not only identified genetic contribution to population differences in morphology, physiology, and parasite resistance (e.g. Taylor and McPhail, 1985a, b; Foote et al., 1999; Haugen and Vollestad, 2000; Pakkasmaa and Piironen, 2001; Glover et al., 2003), but also cases where phenotypic variance seems to be purely environmentally determined (e.g. Swain et al., 1991). Only a few such experiments have been carried out in marine fish, and most investigating growth and developmental rates (e.g. Schultz et al., 1996; Conover et al., 1997). Conover and Present (1990) used a setup to examine growth in Atlantic silverside, Menidia menidia Linnaeus, from across a latitudinal cline. They were able to show that fish originating from high latitude had a greater capacity for growth than low-latitude fish, enabling high-latitude fish to compensate for the shorter growth season. Counter-gradient genetic variation for growth rates has also been indicated in a recent experiment using two geographically separated groups of Atlantic cod from Norway (Salvanes et al., 2004).
Another approach in determining population differentiation and its heritable basis is analysing functional genes and their expression directly (e.g. Brix et al., 1998; Tsoi et al., 2003; Williams et al., 2003; DeKoning et al., 2004; Picard and Schulte, 2004) or genetic markers associated with functional genes (e.g. Pogson and Fevolden, 2003; Pogson and Mesa, 2004). Studies using this approach are still scarce because knowledge of genome architecture is limited so far to relatively few species, and the development of techniques applicable to large-scale analysis is still emerging (Ford, 2002a; Gibson, 2002). Clearly, in order to predict consequences of escaped cultured fish of exogenous origin, more studies are needed to disentangle population specific patterns of local adaptations and their genetic architecture in gadoid fish.
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Gene flow from mariculture to wild populations |
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TopIntroductionGenetic effects of ranchingGadoid population structureGene flow from mariculture...Detection of introgressionMinimizing introgression effectsReferences |
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Modelling introgression effects
A number of models have been developed to explore the genetic effects of stocking natural populations with hatchery-produced fish. In the following, we give examples of these models and discuss their relevance to estimates of the impact of gadoid mariculture. Most evaluations of effects of gene flow from captive to wild populations point to significant negative effects on population fitness. Using a quantitative genetic model, Lynch and O'Hely (2001) explored fitness effects of releasing individuals of hatchery origin into wild populations, given that the selective pressures in the two environments differ. Assuming that the hatchery stock was derived directly from the wild population, their model attempted to incorporate effects of varying levels of gene flow between the hatchery stock and wild population, their relative population sizes, and the degree to which they differ genetically. Deleterious alleles were assumed to have a measurable fitness reducing effect, whereas it was assumed that Ne in the hatchery was large enough to prevent deleterious alleles from going to fixation within the time frame under consideration. Their results show that gene flow from a hatchery environment, in which there is relaxed or positive selection on alleles that are maladaptive in the wild, can exert significant fitness reducing effects on wild populations after only a few generations. The magnitude of the fitness reduction correlates positively with the number of generations that the hatchery fish have been bred (i.e. how maladapted they have become in a natural environment) and with their relative contribution to the pool of wild breeding fish. Further, even if hatchery stocks are continuously supplemented with wild fish, a benign hatchery environment may still facilitate a way of "escape" for deleterious mutants that would otherwise have been selected against. The authors suggest that adverse effects may be substantial even when the captive population is very large, as large captive populations may harbour many rare alleles that are conditionally advantageous in a hatchery but disfavoured in nature.
Wild populations can, in principle, readapt to their natural environment following introgression. The efficiency with which maladapted alleles are selectively removed depends on several parameters, such as the magnitude of fitness reductions caused by introgression, Ne, in the wild population (as a low Ne will slow the efficiency of selection against hatchery genes), and rates of gene flow from the maladapted to the wild population. In a recent study, Theodorou and Couvet (2004) extended the model of Lynch and O'Hely (2001) and showed that if Ne in the wild population is around 100, and the captive Ne is larger than 30, adding up to five individuals of captive origin annually over 20 years, the result should have only a small effect on the genetic load and fitness of the wild population. Further, their model indicated that negative fitness effects decrease if bi-directional migration is allowed, that is, if captive broodstocks are continually supplemented with breeders of wild origin. However, the model assumes that the ratio of escapees to wild fish remains quite low (<1:20). This condition may not be met in a natural scenario, in which escapes may result both from loss of entire net pens during storms and from the continuous drift of large numbers of fertilized eggs from natural spawning in on-growth facilities, in which case, the applicability of the model is questionable (Theodorou and Couvet, 2004).
Effects of escapees on Ne in wild populations
Wang and Ryman (2001) modelled the effect of continuous gene flow from a captive stock on Ne of a wild population assumed to be below carrying capacity. Using the same basic model, Ryman and Laikre (1991) had previously shown that a single event of gene flow from a captive to a wild population would result in a decrease in Ne of the wild population, compared with the unmanipulated situation (known as the "Ryman–Laikre effect"). This would occur in spite of the increase in census population size N and be an effect of the low Ne in the captive compared with wild populations. In the approach of Wang and Ryman (2001), three different scenarios for the genetic origin of the captive broodstock were considered. Captive individuals were (i) fully bred in captivity (i.e. receiving no genes from wild populations); (ii) of wild origin (i.e. spawners are continuously sampled from the wild, crossed, and their offspring raised under captive conditions) or (iii) bred from a captive stock that is supplemented with wild-born spawners. The model showed that although Ne of the wild population initially decreased, adding captive individuals for multiple generations could lead to an increase in wild Ne, given that captive individuals originated either purely from wild fish or from broodstocks supplemented with wild spawners. This was caused by the increase in census size over generations, which had a positive effect on Ne and thus decreased genetic drift compared with a non-introgressed situation. However, the applicability of this model in predicting the consequences of gadoid mariculture escapes may be poor. The model assumes that the wild population is below carrying capacity, and it does not address effects of domestication selection in captive-bred individuals. As stated by Wang and Ryman (2001), adding captive-bred individuals is generally disadvantageous when the recipient population is at carrying capacity. The predictions of the model are also affected by the relative reproductive variance in captive and wild individuals, parameters that are difficult to estimate reliably for most gadoids.
Empirical studies of introgression effects
Numerous studies of salmonids demonstrate that hatchery fish have less success than their wild conspecifics under natural conditions. Lacroix and Stokesbury (2004) showed that only 0.09% of Atlantic salmon, S. salar, of escaped hatchery origin returned to spawn compared with an estimated 0.45% of wild fish. Although salmonids of escaped farm origin apparently are capable of adjusting to a natural feeding regime (Jacobsen and Hansen, 2001), studies of brown trout, Salmo trutta Linnaeus, show that few hatchery-produced trout released into the wild survive to maturity in the sea (Ruzzante et al., 2004), and in most cases, contribute relatively little to reproduction in local rivers (e.g. Hansen et al., 2001a, 2002). Reproductive behaviour often differs between cultured and wild salmon, and cultured fish in a semi-natural setup have lower reproductive success than fish of wild origin (Fleming et al., 1996, 2000; McLean et al., 2004). Nonetheless, introgression can be accelerated if hatchery fish follow alternative reproductive tactics such as maturation at small size and sneak spawning, which may yield substantial reproductive success in hatchery derived fish (Hansen et al., 2000; Garant et al., 2003). A recent comprehensive study of Atlantic salmon demonstrated a direct relationship between the genetic contribution from a domesticated hatchery stock and an overall fitness reduction in individuals (McGinnity et al., 2003). These authors set up a breeding experiment using fish of wild and hatchery origin to produce pure wild-type, pure hatchery fish, their first and second generation hybrids and hybrid backcrosses to both wild and hatchery fish. The survival of each of seven categories of crosses was compared for eggs, three juvenile stages, and for adults returning to spawn. The results showed that domesticated fish had an estimated lifetime success of only 2% relative to wild fish. Wild x hatchery crosses showed intermediate success with an inverse relationship between survival and the overall genetic contribution from domesticated fish. Outbreeding depression caused by the break-up of co-adapted gene complexes was evident in early developmental stages in second generation hybrid crosses. Although overall survival of both hatchery and introgressed fish was lower, hatchery fish were larger and performed better than wild fish at some life stages, thereby competitively displacing wild fish in the juvenile habitat. Thus, even though fish of captive origin generally have low success in a natural environment, they, nonetheless, can have a substantial negative effect on the fitness of wild populations owing to competitive displacement and to introgression with gene complexes that are maladapted in the wild. In conclusion, evidence from salmonids unanimously shows that domesticated strains perform poorly in the wild. Moreover, even though natural selection acts against the genetic contribution from domesticated individuals, there is evidence that introgression will have an overall negative fitness impact on wild populations.
Predictions for gadoid mariculture
Although salmonids and gadoids differ with respect to life history parameters and population structure, here we discuss and attempt to predict genetic effects of large-scale escapes from gadoid mariculture to wild conspecific populations, based on evidence from salmonid and other non-gadoid fish. Studies of the effects of gadoid introgression have not been carried out in natural or experimental settings. Otterå et al. (1999) found indications that reared juvenile cod of exogenous origin suffered reduced fitness when released into a natural habitat, compared with reared juveniles of local origin. Kristiansen et al. (1997) found that, overall, few cod that had gone through a generation of hatchery propagation survived when released into a natural environment. The authors were not able to determine the primary cause of mortality, and it was uncertain whether domestication selection had an effect per se. Thus, although there are indications that released cod of captive origin may exhibit suboptimal performance in the wild, potential introgression effects depend on a number of parameters. Direct fitness effects on local populations will depend on the demography and competitive ability of escapees. Competitive displacement of wild fish by escapees can occur at several life stages and is likely to have effects, unless escapees enter wild populations at life stages where density-dependent effects are completely absent. Little is known about the limiting factors in individual life stages of gadoids (Myers, 2001), and the relative effects of escapees of different life stages are difficult to predict.
Genetic effects of escapees are greatly influenced by their reproductive success relative to wild fish. Fish of cultured origin may exhibit spawning maturation at different (and maladaptive) times from local stocks (e.g. Nickelson et al., 1986; McLean et al., 2004; Otterå et al., 2006), and risk of interbreeding between them will depend on the overlap between spawning times of escaped and wild fish. Even if escaped captive cod reach maturity and attempt to spawn at the same time and place as local stocks, their spawning behaviour may be suboptimal, either resulting from domestication effects (Fleming et al., 2000) or from adaptive differences among populations of different origin (Rowe and Hutchings, 2004). Behavioural studies and genetic parentage estimates from Atlantic cod spawning aggregations indicate that reproductive competition and individual variance in spawning success may be substantial (Hutchings et al., 1999; Bekkevold et al., 2002; Rowe and Hutchings, 2003). It is further indicated that reproductive success varies positively with body size (Hutchings et al., 1999; Bekkevold et al., 2002), which may confer success in escapees originating from size-selected stocks, and thus facilitate introgression.
In salmonids, domesticated fish are shown to exhibit aberrant dispersal behaviour relative to wild fish (reviewed in Stabell, 1984). This has caused concern that releases lead to competitive displacement and introgression effects beyond local scales and to increased gene flow among populations. Although fine-tuned homing to spawning sites has been reported in Atlantic cod (Robichaud and Rose, 2001), it is expected that natural dispersal rates are high overall. However, this does not preclude large-scale escapes of domestic gadoids affecting migration and leading to altered patterns of gene flow among population components.
Adverse effects of introgression by cultured fish can be predicted to vary with the genetic make-up of escapees. First, the more the generations of cultured fish that have been maintained under captive conditions and undergone domestication selection, the more likely they are to contribute gene complexes that are maladapted in the wild. Second, the fewer the breeders that are maintained in broodstocks, the more likely escapees are to be genetically depauperate, and their interbreeding with wild fish to lead to reductions in genetic variability in wild populations (Ryman and Laikre, 1991). Finally, crosses between local fish and escapees of exogenous origin may lead to more severe fitness reductions owing to the breakdown of locally adapted gene complexes, although the prevalence of local adaptations is still relatively unexplored in gadoid fish. The outcome of introgression and whether it is reversible will depend on a balance between gene flow from escapees and the intensity of selection acting against them. However, negative fitness effects on wild populations may be difficult to estimate, and in most cases, may require large-scale, long-term experimental studies, in line with the salmonid study by McGinnity et al. (2003) (see above).
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Detection of introgression |
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TopIntroductionGenetic effects of ranchingGadoid population structureGene flow from mariculture...Detection of introgressionMinimizing introgression effectsReferences |
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The detection of introgression has been facilitated greatly by the use of highly variable molecular markers, such as microsatellites. Using such markers, detailed studies can be conducted to determine past and present introgression events and to assess the best strategies for re-establishing introgressed populations (e.g. Nielsen et al., 2001). One way of assessing gene flow from captive to wild populations is to analyse changes in allele and genotype compositions over time using various statistical approaches, such as hybrid indices, population admixture analysis, and population assignment tests (see Hansen (2002) for a recent application of such analyses). Genetic mixed-stock analysis represents another approach that may prove highly useful in trying to estimate proportions of farm escapees surviving in the wild (e.g. Ruzzante et al., 2004). Based on such analyses, it is possible to estimate proportions of escapees in wild populations, magnitudes of introgression, to identify introgressed and non-introgressed individuals, and to plan conservation measures. Salmonid conservation programmes have practiced identification and breeding of non-introgressed individuals as a means for restoring genetic integrity in introgressed populations (e.g. Berrebi et al., 2000b; Nielsen et al., 2001; Hansen et al., submitted for publication). Although direct conservation attempts may not be feasible in most wild gadoid populations, the information obtained from these types of analyses can yield important information about introgression dynamics and may prove highly useful in broodstock management.
Samples representing the genetic composition of populations prior to possible introgression are an important component in molecular admixture studies, although approaches have been developed that permit analyses when baseline information is incomplete (e.g. Hansen et al., 2001a). In salmonids, archived scale samples have proven a valuable source of DNA from pre-introgressed populations (Nielsen et al., 1999). In the case of gadoid populations at risk of facing introgression events, it is strongly recommended to collect samples for genetic analyses prior to the establishment of major mariculture production. This will provide a genetic baseline that can later be used to monitor gene flow from mariculture escapees. In cases where introgression has already taken place, archived otoliths may provide useful sources of DNA (e.g. Hutchinson et al., 1999).
A potentially important difference between introgression studies in gadoids and salmonids is that in the latter, hatchery fish are often based on strains of exogenous origin that have been isolated reproductively from the recipient populations for thousands of generations and are highly genetically differentiated (e.g. Largiader and Scholl, 1996). This leads to increased risk of break-up of co-adapted gene complexes during introgression, but it also facilitates genetic marker-based detection of introgressed individuals owing to the high prevalence of diagnostic loci. In marine fish exhibiting overall lower levels of genetic differentiation among populations, the molecular resolution for the detection of introgression thus may be low compared with salmonids. Whereas low genetic differentiation among wild and captive fish is not necessarily concurrent with a low fitness impact following introgression, it may constitute a challenge for the analysis framework. However, the statistical power for detecting introgression will ultimately depend on the genetic constitution of broodstocks, which may change rapidly as a result of genetic drift.
Genetic tagging of cod broodstocks has been attempted in order to estimate effects of large-scale stocking on local recruitment (Jørstad et al., 1994), and using genetically tagged farm fish may also constitute a means for detecting escapees in the wild. Genetic tagging is commonly carried out by basing broodstocks on individuals that have been crossed, allowing an otherwise rare genotype at one or more marker locus. However, as this approach commonly invokes breeding a relatively low number of individuals in order to obtain the genetically tagged broodstock, in effect, it may accelerate loss of genetic variation in introgressed populations. Unless a very large number of genetically tagged outbred families can be obtained, the procedure may thus impose a high risk of decreasing Ne in introgressed wild populations.
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Minimizing introgression effects |
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TopIntroductionGenetic effects of ranchingGadoid population structureGene flow from mariculture...Detection of introgressionMinimizing introgression effectsReferences |
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Two main strategies can be implemented into mariculture broodstock management to minimize introgression effects of gadoid escapees, namely, retaining genetic variability in broodstocks and protecting the genetic integrity of local wild populations. The strategies have additive value, but the practical relevance of each is expected to differ between large-scale broodstock programmes and smaller-scale local initiatives to farm gadoids.
Genetic variability is maximized in farmed fish by ascertaining that broodstocks are based on large numbers of individuals and that family size variation is minimized. The first is obtained by adhering to the general rule-of-thumb stating that a minimum of 50, and preferably several hundred, individuals are needed to prevent inbreeding and loss of genetic diversity in the short term (Franklin, 1980). Family size variation may occur whether broodstocks are propagated by natural spawning or via controlled dry fertilization. Individual fish may differ in their heritable viability in a way recognizable by potential mating partners but unrecognizable to broodstock managers. Allowing some level of free mate choice may promote offspring health and allow the stock to react to coevolving pathogens (see Wedekind et al. (2001) and Neff (2004) for examples in fish). On the other hand, extreme reproductive variance (e.g. in the case of a few dominant males siring large proportions of offspring) should be avoided in order to maintain an adequate Ne in the broodstock.
If broodstock propagation is carried out by artificial fertilization, behaviourally induced reproductive variance is decreased. However, as the compatibility and fertilization success may vary among individuals (see Rakitin et al. (1999) for an example from Atlantic cod), care should be taken to equalize the representation of different families, for instance by taking care not to mix sperm from multiple males during fertilization. If these precautions are followed, this should ensure a relatively high Ne in the broodstock and, hence, delay loss of genetic variation, although behavioural mate choice processes of potential importance for maintaining fitness will not be able to operate.
Domestication selection and loss of variation in broodstocks can be reduced but not avoided by regularly adding wild spawners (Ford, 2002b). However, because such an approach will slow selection programmes seeking to maximize traits that are attractive from a production perspective, the procedure is probably not appealing from a mariculture perspective. Nevertheless, fitness reduction owing to genetic load and inbreeding depression may be proximate effects in gadoid breeding programmes that are not carefully planned, underlining the importance of continuously monitoring genetic drift and divergence in broodstocks used for mariculture.
It could be argued either way that the least threat to the genetic integrity of local populations will occur (i) if broodstocks used for mariculture are based on local spawners, as this would lower risks of outbreeding depression resulting from interbreeding between escapees and wild fish; or (ii) if broodstocks are based on extant population components that exhibit differentiated reproductive behaviour, e.g. that spawn with a temporal shift compared with local populations and, thus, are reproductively isolated from wild populations. However, the first option may not be practically feasible, as it requires several individual selection programmes tailored specifically to local on-growth facilities. The second option may also be difficult to implement in practice, as reproductive behaviour such as timing of spawning is not invariably fixed, and individual variance in spawning time may result in breakdown of such isolating mechanisms and, thereby, still not preclude introgression.
It may be predicted that introgression with genetically depauperate broodstock strains of close geographic origin will exert a smaller fitness effect on wild populations, compared with introgression with exogenous and highly differentiated strains that are more likely to incur outbreeding depression and break-up of co-adapted gene complexes. The magnitude of fitness effects will depend on the efficiency of selection against introgressed gene pools in local populations, which will depend on genetic, demographic, and stochastic effects. Experimental studies are clearly needed to examine fitness effects of interbreeding between captive and wild individuals, and to determine to what extent introgression can be expected to occur in the wild.
An approach for minimizing impact on wild populations would be to prioritize locations suitable for large-scale mariculture, taking factors such as proximity to local spawning stocks and their population structure into consideration. Areas containing local populations that exhibit genetic and/or life history differentiation would, for instance, represent low suitability for the establishment of gadoid mariculture. Conversely, areas isolated from local spawning components would represent zones where mariculture would be expected to have a smaller impact. Although such an approach would necessitate fine-scale studies of local physical and population characteristics, it could be expected to minimize environmental and genetic pressures on wild populations.
In conclusion, it should be realized that large-scale escapes are costly, not just from the perspective of the on-growth fish farmer, but also from an environmental perspective if fitness costs are incurred on wild populations. Whereas approaches to minimizing introgression may have practical application in small-scale breeding and mariculture programmes, most large-scale programmes and facilities are unlikely to implement genetic considerations for minimizing introgression in wild populations along the lines discussed here. It is expected, for instance, that only a few Atlantic cod broodstock lines will be selectively bred and used throughout the northeast Atlantic, leading to most mariculture facilities containing (and leaking) fish that are highly genetically differentiated from local populations. Unless decisions are made to restrict the use of exogenous fish in areas containing wild conspecifics, the implication is that the best precaution against introgression effects lies in preventing individuals from mixing in the first place. The development of land-based facilities and sea net pens that minimize escapes should therefore have priority from both conservation and management perspectives.
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K. Kolstad, I. Thorland, T. Refstie, and B. Gjerde Body weight, sexual maturity, and spinal deformity in strains and families of Atlantic cod (Gadus morhua) at two years of age at different locations along the Norwegian coast ICES J. Mar. Sci., January 1, 2006; 63(2): 246 - 252. [Abstract] [Full Text] [PDF]
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A. Gro Vea Salvanes and V. Braithwaite The need to understand the behaviour of fish reared for mariculture or restocking ICES J. Mar. Sci., January 1, 2006; 63(2): 345 - 354. [Abstract] [Full Text] [PDF]
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