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Araki Et Al 2008 Fitness of Hatchery Reared Salmonids
Araki Et Al 2008 Fitness of Hatchery Reared Salmonids
Araki Et Al 2008 Fitness of Hatchery Reared Salmonids
SYNTHESIS
Keywords Abstract
adaptation, captive breeding, conservation
genetics, selection. Accumulating data indicate that hatchery fish have lower fitness in natural
environments than wild fish. This fitness decline can occur very quickly, some-
Correspondence times following only one or two generations of captive rearing. In this review,
Michael Blouin, Department of Zoology, we summarize existing data on the fitness of hatchery fish in the wild, and we
Oregon State University, 3029 Cordley Hall,
investigate the conditions under which rapid fitness declines can occur. The
Corvallis, OR 97331, USA.
Tel.: 541 737 2362; fax: 541 737 0501;
summary of studies to date suggests: nonlocal hatchery stocks consistently
e-mail: blouinm@science.oregonstate.edu reproduce very poorly in the wild; hatchery stocks that use wild, local fish for
captive propagation generally perform better than nonlocal stocks, but often
Received: 7 November 2007 worse than wild fish. However, the data above are from a limited number of
Accepted: 2 February 2008 studies and species, and more studies are needed before one can generalize fur-
ther. We used a simple quantitative genetic model to evaluate whether domes-
doi:10.1111/j.1752-4571.2008.00026.x
tication selection is a sufficient explanation for some observed rapid fitness
declines. We show that if selection acts on a single trait, such rapid effects can
be explained only when selection is very strong, both in captivity and in the
wild, and when the heritability of the trait under selection is high. If selection
acts on multiple traits throughout the life cycle, rapid fitness declines are
plausible.
been documented. Furthermore, accumulating evidence natural environment, unless hatchery fish are intentionally
suggests that domesticated hatchery fish often exhibit excluded from spawning by weirs or traps.
differences from wild fish in predator avoidance and In Table 1 we find that the relative fitness (RF)
agonistic behavior (reviewed by Reisenbichler and Rubin between hatchery fish and wild fish is generally lower
1999) and suffer low reproductive success in the wild than one, indicating that hatchery rearing generally has
(reviewed by Berejikian and Ford 2004), and that these negative effects on RF. In the seven studies in which RF
changes can occur rapidly (Salmon Recovery Science was estimated separately for males (fathers) and females
Review Panel 2004; Araki et al. 2007a,b). Thus, the effects (mothers), point estimates show that RF in males was
of hatchery fish on wild populations remain an open smaller than that in females in four studies, about equal
question and a topic of major concern. in two, and larger in one. Thus, while hatchery females
In this review, we first summarize studies that have tend to have higher RF in the wild than hatchery males,
evaluated the relative fitness of hatchery and wild salmo- Table 1 shows no evidence for a large sex-specific bias in
nid fish. We also use quantitative genetic theory to evalu- RF. In addition, Araki et al. (2007b) showed that the sec-
ate under what conditions domestication selection alone ond generation hatchery fish from hatchery-born fathers
is a sufficient explanation for rapid fitness declines that (grandfathers of wild-born descendants) had about the
have been observed by some studies. We conclude that same reproductive success that those from hatchery-born
selection alone can be a sufficient explanation, either mothers (grandmothers of wild-born descendants) had in
when it operates on several traits throughout the life cycle the wild, suggesting no obvious grandmaternal/grandpa-
or when extremely strong selection works on a single trait ternal effects of hatchery rearing on RF.
with very high heritability. We discuss the traits under
selection that could cause the observed fitness declines.
Segregated broodstocks of nonlocal origin
While there is a need for a comprehensive consideration
of whether supplementation hatchery programs are worth The most complete information on RF of hatchery and
operating in general (Waples and Drake 2004), in this wild salmonids comes from five studies of nonlocal, seg-
review we focus more narrowly on just the fitness effects regated hatchery steelhead populations. All of these stud-
of hatchery rearing. ies indicate very low relative fitness of the hatchery fish
(Lifetime RF = 0.02–0.37, Table 1). One study of coho
salmon representing a similar broodstock management
Summary of studies evaluating fitness of hatchery
scenario (i.e. domesticated stock compared to a nonlocal
fish in the wild
wild population) used behavioral measures and estimated
We identified 14 completed studies that evaluated the fit- reduced relative breeding success (males 0.62; females
ness of hatchery fish relative that of wild fish spawning in 0.82) that was similar to the adult-to-subyearling relative
the same habitat (Table 1). Eleven out of 14 are on Paci- fitness of steelhead (75–78%) in the one study that mea-
fic salmonid spp. (Oncorhynchus), and three on Atlantic sured it (Leider et al. 1990). These segregated hatchery
salmonid spp. (Salmo). Nine of them are on steelhead stocks have been managed as more or less ‘closed’ popu-
trout (Oncorhynchus mykiss), and six of them measured lations for 5–10 generations (Table 1), during which time
lifetime fitness (typically adult-to-adult reproductive suc- there has been little genetic input from the wild popula-
cess). Here we use the term ‘relative fitness’ to mean the tion(s).
fitness of hatchery fish (either lifetime or some compo- Hatchery and wild fish experience very different envi-
nent) relative to that of wild fish spawning in the same ronments as juveniles. Differences in fitness or other char-
habitat. acteristics between hatchery and wild adults can therefore
The origin and management of the salmonid brood- be due to either genetic differences, or differences caused
stocks (parents of hatchery fish) vary substantially among by rearing in different environments as juveniles, or a
the studied systems and are expected to affect the relative mixture of these two effects. However, several lines of evi-
fitness of hatchery fish. The hatchery population can be dence suggest that genetic effects contribute to the low-
founded from either the wild population that inhabits the ered fitness of hatchery fish. Firstly, the offspring of
location of release (local hatchery stock), or from a differ- naturally spawning hatchery fish have been found to have
ent river than the one into which the stock is released lower survival to smolting and lower survival from smol-
(nonlocal hatchery stock). Hatchery populations can be ting to adulthood (Chilcote et al. 1986; Leider et al. 1990;
perpetuated solely by spawning hatchery-origin fish (seg- Kostow et al. 2003). One cannot rule out an environmen-
regated broodstock), or by spawning a combination of tal effect passed down through the gametes of the hatch-
hatchery and wild fish (integrated broodstock). In both ery parents, but this seems less likely than, say an
cases hatchery and wild fish often will be spawning in the environmental effect on the mating and spawning success
Table 1. Conditions, methodologies and estimated relative fitness (RF) in studies that compared the relative fitness hatchery and wild salmonids.
Genetic effects are presumed where hatchery and natural adults were artificially spawned and the fitness of the resulting offspring was compared
(assumes environmentally-mediated maternal effects of rearing from egg to smolt have no effect on offspring fitness). All paternal effects are also
assumed to be genetic (assuming no grandparental maternal effects). Genetic and environmental effects are considered confounded where hatch-
ery-born and wild-born fish are directly compared because they experienced very different juvenile environments. The duration of the hatchery fish
in captivity is expressed in the number of generations in captivity (NGC), which was approximated as years of hatchery operation divided by modal
age at sexual maturity. In integrated programs, where either wild fish are spawned in the hatchery or hatchery-origin fish spawn in the natural
environment, the ancestry of hatchery and wild fish may differ by only a single generation, even if the duration of the hatchery program is much
longer.
Life History
I. Completed Study Species segment Method Effect on RF NGC RF*
*m, male, f, female, when the relative fitness (RF) was estimated separately for each sex of parent.
Hatchery fish having one wild parent and one first-generation hatchery parent (NGC-2) compared to hatchery fish having two wild parents
(NGC-1).
of the hatchery parents themselves. Secondly, Araki et al. captivity (Salmon Recovery Science Review Panel 2004;
(2007a) showed that ‘traditional’ (nonlocal, segregated) Araki et al. 2007b) again points to a genetic effect because
hatchery stocks exhibited substantially lower relative fit- environmental effects are not expected to accumulate over
ness than hatchery fish produced by wild fish (in a ‘sup- generations.
plementation’ program discussed below), when each was
compared to the same wild population. Because both
Segregated broodstocks of local-origin
stocks experienced hatchery environments and were com-
pared against the same wild population, the difference An additional study of Atlantic salmon conducted as a
between them is likely to be genetic in origin. However, ‘common garden’ experiment concluded that offspring of
the two comparisons were done in different years so this a locally derived hatchery population that had been
conclusion remains tentative. Finally, evidence of a nega- completely segregated from the wild population for about
tive correlation between relative fitness and generations in five generations exhibited survival equal to offspring of
the wild fish from egg to adult (McGinnity et al. 2004). tyre 1977; Reisenbichler and Rubin 1999). The hatchery
Offspring of fish captured from an adjacent (i.e. nonlocal) fish in these studies had been propagated artificially for
population had reduced survival in both freshwater and 2–6 generations. Both types of fish were created via
seawater portions of the life cycle, emphasizing the crosses in the hatchery, so the differences are probably
importance of local adaptation in determining fitness. genetic. Similarly, hatchery steelhead derived from a wild
The apparent lack of a genetic effect of approximately five parent and a hatchery parent showed lower reproductive
generations of hatchery propagation on egg-to-adult fit- fitness than that of hatchery fish derived from two wild
ness in the locally derived hatchery population did not parents in each of 3 years of samples (Araki et al.
include an assessment of breeding performance. The 2007b). In this case overall reproductive fitness in the
locally derived hatchery population did exhibit some former hatchery fish was only 55% of the fitness in the
growth differences in the hatchery and apparent diver- latter hatchery fish (Table 1). This study also eliminated
gence in life history characteristics (e.g. age-at-smoltifica- the confounding effects of captive rearing because all
tion and maturity). fish were spawned artificially, reared in the same envi-
ronment and released on the same date. When repro-
ductive success of these two types of hatchery fish were
Integrated broodstocks of local origin
compared with that of wild fish (rather than with that
The nonlocal, segregated hatchery stocks in the above of each other), the relative fitness of the first generation
studies were derived from different geographic regions fish was 70–88% and that of the second generation fish
than the wild populations to which they were compared. was only around 30% (Table 1). Again, differences
Thus, any fitness difference could be due to local adapta- between wild-born and hatchery-born individuals are
tion or to the effects of hatchery production. The effects confounded by the different environments they experi-
of hatchery propagation, per se, can be investigated by enced, but the substantial difference between first and
studying the fitness of hatchery fish derived from the second generation hatchery fish suggests a rapid and
same local population to which they are compared. We cumulative genetic effect of hatchery culture during the
have summarized data from four such populations, two first few generations of captive rearing.
steelhead, one coho and one brown trout (Salmo trutta,
Table 1).
Limitations of existing data
The survival of offspring of hatchery brown trout
stocked into experimental channels as embryos or as juve- Even with the recent accumulations of new data above, it
niles did not differ from that of wild fish from the same is too early to draw a strong conclusion about whether
source population, even though the hatchery line had supplementation programs in general are helping or
been in production for seven generations (Dannewitz harming the wild populations, for the following reasons:
et al. 2004; Dahl et al. 2006). Similarly, the relative fitness First, the precision of the point estimates of relative fit-
of a hatchery coho salmon stock did not differ signifi- ness in above studies is limited, and we typically have low
cantly from that of wild coho salmon, even though the power to detect a biologically significant difference in fit-
hatchery population had been in operation for approxi- ness between hatchery fish and wild fish (Araki and Blou-
mately 25 generations (Ford et al. 2006). However, in in 2005; Araki et al. 2007a,b). A fitness difference of only
both these populations hatchery fish had been predomi- a few percent will have strong effects on the fate of a
nating on the spawning grounds for many years, so the population over the course of many generations (e.g.
‘wild’ populations in these cases probably consisted lar- Crow and Kimura 1970), but even the largest studies
gely of hatchery fish from previous generations. All we rarely have power to detect fitness differences of less than
can say here is that on average the hatchery fish in these 10–15% (Araki et al. 2007a,b). Second, data on the rela-
two studies experienced the hatchery environment for one tive fitness of hatchery fish compared to wild fish are
more generation than the wild fish. Or put another way, heavily biased towards steelhead. Most of the other spe-
the wild fish were in the wild for at least one full genera- cies studied (brown trout; Atlantic salmon, Salmo salar;
tion, even if their ancestors had substantial hatchery back- and coho salmon) share similar characteristics as steel-
ground. head; in particular, they reside in freshwater for at least
Evidence of reduced fitness in local-origin integrated their first year of life before they migrate to the ocean.
hatchery populations comes from two studies on steel- This characteristic leads fishery managers to rear these
head in experimental streams. Survival from egg to parr, species in hatcheries for at least a full year, usually until
or from fry to 1 year of age, of offspring of hatchery the fish change physiologically for the ocean migration
fish in enclosures in streams was approximately 80% (smoltification). In addition, most natural populations of
that of offspring of wild fish (Reisenbichler and McIn- steelhead smolt at age 2 or 3, which is usually not practical
in a hatchery. So most steelhead hatcheries accelerate the that have been proposed for why hatchery fish are less fit
growth of their fish and release them after 1 year. Some- than wild fish in nature are: (i) Deleterious mutation
times it is necessary to advance adult spawn timing to accumulation. In particular, survival from egg to smolt is
achieve the goal of creating smolts within a year. Other usually 85–95% in hatcheries versus 1–5% in the wild
species, such as some populations of Chinook salmon, (Reisenbichler et al. 2004). Thus, relaxed purifying selec-
migrate to sea after just a few months of rearing in fresh- tion during the egg-to-smolt stage is expected to result in
water, and chum salmon (O. keta) and pink salmon the accumulation of new mutations that are effectively
(O. gorbuscha) begin their migration to sea directly after neutral in the hatchery but deleterious in the wild (Lynch
emergence from the gravel. Hatchery populations of these and O’ Hely 2001). (ii) Inbreeding depression due to
species spend less time in freshwater and therefore might small broodstock sizes (reviewed by Wang et al. 2002).
be less affected by the hatchery environment than species (iii) Domestication selection, in which positive selection
that spend longer in artificial environments. Many of the for adaptation to the hatchery environment comes at the
new relative fitness studies that we are aware of focus on expense of adaptation to the natural environment (e.g.
Chinook salmon, on newly founded hatchery populations, Ford 2002).
or on hatcheries that incorporate wild born fish into the Relaxed purifying selection, coupled with the accumu-
hatchery broodstock each generation (e.g. Chiwawa River lation of new mutations, almost certainly contributes to
Chinook by A. Murdoch and M. J. Ford, in prepration). the low fitness of multi-generation hatchery stocks (Lynch
Furthermore, in most of these studies, the relative pro- and O’ Hely 2001). But relaxed selection owing to a sin-
portions of cultured fish and wild fish spawning naturally, gle generation of hatchery culture seems an unlikely
and the histories of the broodstocks, are also better explanation for dramatic declines in fitness unless salmon
known than in the studies reviewed above. Third, carry an extraordinary standing genetic load (e.g. Launey
although estimating the relative fitness of hatchery fish is and Hedgecock 2001). Typical rates of mutation to dele-
important, it is not sufficient for evaluating the effective- terious mutations are around one mutation per genome
ness of supplementation. Long-term studies comparing per generation, and the average effect of such a mutation
the demographic performance of supplemented and un- in the heterozygous state is around 2% (Lynch et al.
supplemented populations are also important, and can 1999). Thus, it should take at least a few generations for
provide a more complete understanding of the overall the effects of new mutations to accumulate. There is no
impacts of supplementation. For example, several studies evidence that salmon have unusually high mutation rates
have found widespread negative correlations between nat- (e.g. Steinberg et al. 2002). One possible explanation is
ural population productivity and intensity of hatchery that the hatchery environment somehow induces a large
production (e.g. Chilcote 2003; Nickelson 2003; Hoekstra increase in the deleterious mutation rate, but so far no
et al. 2007). The results of these studies, which primarily data exist to suggest this is happening.
focus on segregated and often nonlocal hatchery popula- Inbreeding depression is a reduction in fitness associ-
tions, are consistent with the finding that such hatchery ated with mating between relatives, and can be caused by
populations can negatively impact natural populations. either an increase in homozygosity of recessive deleterious
Similar analyses of the long-term demographic effects of alleles or a reduction in heterosis (reviewed by Charles-
supplementation should also be conducted to comple- worth and Charlesworth 1987). Unlike mutation accumu-
ment shorter-term studies of relative fitness. lation, inbreeding can potentially lead to fitness declines
in a few generations or even a single generation because
it operates on variation that is already present in a popu-
Mechanisms of fitness decline
lation. Inbreeding between close relatives (inbreeding
The data from our review suggest that the fitness of coefficient of 0.25; sib mating or equivalent) has been
hatchery fish declines with increasing generations in the shown to reduce survival rates by 10–30% in salmonids
hatchery, although confounding factors such as locality of (reviewed by Wang et al. 2002). Hatchery programs
the broodstock and interchange between the hatchery and sometimes have small breeding populations and low effec-
wild populations inhibit a firm conclusion. In studies on tive population sizes (Waples and Teel 1990), so inbreed-
steelhead, however, the fitness decline has been shown to ing depression can be a contributing factor to low
occur extremely rapidly – within the first generation or hatchery fish fitness in some cases. However, based on
two of hatchery culture in some cases (Table 1). There the studies reviewed by Wang et al. (2002), the level of
are several potential mechanisms by which captive rearing inbreeding in hatcheries would need to be unrealistically
could cause the fitness decline, but no studies have high in order to explain the fitness decline of 30%/gen-
empirically examined the mechanism of observed declines eration reported by Araki et al. (2007b). Inbreeding
of hatchery fish fitness in detail. Potential explanations depression also cannot explain the fitness decline in the
Selection could occur on adults at the time of broodstock each case is scaled to 1, so it is clear that there is ample
collection, while holding in the hatchery prior to spawn- opportunity for changes in mean fitness of 30% or larger
ing, and in the choice of fish to be spawned. Selection on due to selection within a generation. For example, in the
eggs and juveniles could occur directly at any point prior Chinook salmon study reported in Table 2 (Ford, unpub-
to release. Additional selection attributed to the hatchery lished data), a 30% reduction in mean fitness would
experience could also occur after the time of release if result from truncation selection against the 17% of the
trait distributions at the time of release differ from what population that had highest fitness in the wild. Although
they would have been had the fish been produced in the the large variance in fitness reported in these studies is
wild (Reisenbichler et al. 2004). Conceptually, one could not necessarily due to natural selection, this result is con-
construct a quantitative genetic model (Lande and Arnold sistent with strong selection potentially acting on popula-
1983; Arnold and Wade 1984; Falconer and Mackay 1996; tions and suggests that there is sufficient variance in
Ford 2002) and try to determine whether the observed fitness among individuals within a population for selec-
change in fitness was consistent with the model predic- tion to play a significant role in the short-term evolution
tions. However, to realistically model even the simple sit- of salmonids.
uation illustrated in Fig. 1 would involve a model of Next, we evaluate the plausibility of selection as an
selection on multiple traits at multiple life stages, which explanation for the inherited 30% decline in fitness per
would require estimation of a large number of parameters generation estimated by Araki et al. (2007b). Using the
for which we have limited or no data, such as the mean value of I in Table 2, heritability of relative fitness
strength of selection on each of many traits in multiple would need to be >0.07 (0.3/4.5) for males and >0.09
environments, and the genetic and phenotypic covariance (0.3/3.5) for females to explain the 30% fitness decline,
matrix for all of the traits. assuming selection attributed to the hatchery operated
Fortunately, we do not need to attempt to evaluate directly on the ‘trait’ of relative fitness in the wild. Note
such a detailed model to assess the plausibility of selec- that the lower the heritability, however, the stronger
tion as a mechanism for the 30% reduction in fitness/ selection would need to be to achieve the observed
generation found by Araki et al. (2007b). Instead, we change in mean fitness, and the strength of selection
directly evaluated the plausibility of such a change in implied by heritabilities at the low end of the range seems
mean fitness by estimating the opportunity for selection unrealistic. Although Fisher’s (1958) fundamental theory
from the observed variance in reproductive success of natural selection predicts that the heritability of fitness
reported by several studies. The opportunity for selection, itself should be zero, this prediction assumes a population
I, is the variance in individual fitness within a generation, at equilibrium in a stable environment and with no
and is also equal to the population level change in mean mutational input. The few studies that have estimated the
fitness within a generation due to selection (Crow 1958; heritability of total fitness did indeed find estimates indis-
Arnold and Wade 1984). We first evaluate the plausibility tinguishable from zero, but 95% confidence intervals
of selection as a mechanism for the 30% change in around those estimates include the values above (Gustafs-
mean fitness observed in first generation of the Araki son 1986; Kruuk et al. 2000). Thus the heritabilities for
et al. (2007b) study (W versus C[W · W]). fitness required for selection to generate the observed fit-
The estimated opportunity for selection on fish varied ness declines in steelhead are plausible (see also Carlson
considerably among studies and between the sexes: the and Seamons 2008). Because selection due to hatchery
variance in individual fitness averaged 4.5 for males and exposure would actually operate on a series of traits that
3.5 for females (Table 2). Note that the mean fitness in are correlated to an unknown degree with relative fitness
in the wild, the heritability of each trait actually under
selection due to hatchery exposure would need to be lar-
ger than these minimum values. But as we demonstrate
Table 2. Reported opportunities for selection (variance in individual
in the following section, even selection on a single trait
relative fitness) for salmon populations.
does not require implausibly large heritabilities or selec-
I tion coefficients.
Males* Females Species Reference
S2 Carlson and Seamons 2008). On the other hand, if all
RF / exp ð3Þ
2ð x 2 þ 1 Þ these conditions are met, then Fig. 3 illustrates that the
fitness decline can be very severe (even >50%) within a
Thus, in the simplest model, RF is determined by only generation. In the following sections we discuss how
three parameters, the level of truncation in a hatchery realistic each condition is for hatchery fish.
(T), the realized heritability (h2), and strength of stabi-
lizing selection in the wild (x2). In Fig. 3 we show the
Level of truncation due to domestication selection
relationship between RF and x2 with three different lev-
els of heritability (h2 = 0.2, 0.5, 0.8). It is intuitively It is commonly known that hatchery fish from wild
obvious that RF is low when the strength of natural broodstocks are difficult to rear in a hatchery and have
selection is strong, the level of truncation in a hatchery higher mortality rates than those from traditional hatch-
is high, and the heritability is high. However, Fig. 3 ery stocks (J. Gidley personal communication). This is
shows that all three conditions are required to explain a probably due to larger phenotypic variation and stronger
>30% fitness decline following a single generation of genetic maladaptation in hatchery fish from wild brood-
captive rearing if selection acts only on a single trait. stocks than in those from traditional hatchery stocks. The
For example, low levels of truncation (LT £ 0.5) cannot latter is consistent with the model of domestication selec-
explain the >30% fitness decline, and neither can x2 > 5 tion with displaced optimum because the selective shift of
or h2 £ 0.2. Thus, the conditions necessary to explain the trait values in hatcheries should be most pronounced
the >30% fitness decline per generation due to selection at the first generation (when the population values are
on a single trait are fairly extreme (e.g. h2 of various the furthest from the optimal value in captivity). Highly
traits in salmonid species are generally lower than 0.5. crowded conditions typical of hatcheries might also be a
A B
Figure 3 Relationship between relative fitness (RF) and strength of natural selection (x2). Small x2 represents strong selection in the wild. RF at
different x2 was calculated from Eqn (3) and shown with four different levels of truncation and three different levels of heritability (A–C).
part of the reasons for the strong domestication selection meta-analysis on selection gradients from 63 studies
(Frankham 2008). Even so, however, typical mortality including 62 species in the wild. Estes and Arnold (2007)
rates of hatchery fish are only 5–15% during captive rear- revisited their data to estimate x2. According to these
ing (e.g. Reisenbichler et al. 2004). According to the studies, the strength of stabilizing selection is generally
above analysis, this level of mortality by itself cannot very strong in wild populations (a modal value of
explain the >30% fitness decline even if all the mortality x2 = 3.21). The x2 we assumed (Fig. 2) is well in this
in a hatchery is due to domestication selection. However, range, so this part of our model is very plausible.
as is illustrated in Fig. 1, selection could also occur at the
broodstock collection and spawning phases, as well.
Candidate traits under selection
Another possible explanation is that the domestication
selection in a hatchery is correlated with natural selection We showed above that, given the high survival in hatch-
on hatchery fish after the release (Reisenbichler et al. eries, viability selection during the hatchery phase of the
2004). For example, mortality rate from smolt to adult is life cycle is unlikely to produce the rapid fitness declines
often >95% in natural environments. Thus, if some juve- observed in some studies. Thus, viability selection during
nile traits strongly influence survival after release, they the ocean phase, or fecundity or sexual selection during
may well be the targets of domestication selection, even the spawning phase, are also likely targets of selection
though it does not create a high mortality in a hatchery. leading to domestication. Reisenbichler et al. (2004)
Similarly, the ability to successfully spawn could somehow reported that ocean survival is highly correlated with
be influenced by traits expressed during the hatchery body size at the smolt stage, and that strong selection acts
phase of the life cycle. So in summary, viability selection on body size at release. In the high-food and predator-
in the hatchery itself is not sufficient to explain the free hatchery environment, this survival difference should
observed fitness declines. On the other hand, correlated select for high growth rate in hatchery juveniles, perhaps
selection on traits influencing phenotypes during the via a combination of physiological and behavioral
high-mortality oceanic phase, or perhaps during spawn- changes. But an excessively high growth rate is often mal-
ing, is a plausible mechanism. adaptive in natural environments (Arendt 1997).
Selection for high growth rate in the hatchery and asso-
ciated consequences for fitness are likely most severe for
Heritability
steelhead, which typically spend 2 or 3 years in freshwater
There is a large body of data on estimates of the realized before migrating to sea, and for which we have the most
heritability on various traits in various species. Although compelling evidence of rapid fitness loss. Nearly all steel-
estimated h2 values vary widely, the h2 of life history traits head hatcheries, including the Hood River Hatchery (the
tend to be low compared with h2 on other traits (i.e. subject of Araki et al. 2007b), rear and release smolts as
behavioral, physiological, and morphological traits), as yearlings. The problem is that hatcheries typically have
expected on theoretical grounds (Mousseau and Roff difficulty rearing juveniles from wild broodstock (stocks
1987; Carlson and Seamons 2008). However, some fit- that have not yet been domesticated) to a threshold smolt
ness-related traits can have high heritabilities. For exam- size (about 150 mm) in 1 year, but release all fish regard-
ple, heritabilities of egg size ‡0.6–0.8 have been reported less of size, providing the opportunity for intense selec-
in salmonids (Su et al. 1997; Kinnison and Hendry 2001; tion against slow growing individuals (as demonstrated in
Einum et al. 2004). Furthermore, the heritability of a trait Reisenbichler et al. 2004). Traits associated with rapid
depends on the environment in which it is expressed. growth in the hatchery, such as standard metabolic rate,
Thus, fitness-related traits that have low heritability in the might be selected against in nature (brown trout: Alvarez
natural environment could conceivably be highly heritable and Nicieza 2005). Growth rate has also been shown to
in the novel environment of a hatchery. Thus, although correlate positively with aggression at the both individual
the high heritabilities necessary for this model to work and population level (Lahti et al. 2001), and high levels of
(h2 = 0.5 or 0.8) would be surprising for traits closely tied aggression in domesticated steelhead populations are
to fitness in a stable natural environment, they are not associated with risk taking behavior (Johnsson and
out of the question. Abrahams 1991) and reduced ability to avoid predators
(Berejikian 1995). Therefore, when those hatchery fish
reproduce in a natural setting, their offspring could have
Strength of stabilizing selection in the wild
substantially lower fitness (Biro et al. 2004; Sundstrom
The strength of natural selection is in the wild has been et al. 2005).
the subject of extensive study. For natural selection on How the process of broodstock collection and artificial
phenotypic traits, Kingsolver et al. (2001) performed a spawning might influence subsequent spawning success is
less obvious. It is known that hatchery managers some- selection and more exotic mechanisms such as enhanced
times inadvertently and nonrandomly select which fish to mutation rates or epigenetic effects are not mutually
use in crosses (McLean et al. 2005). Also, broodstocks are exclusive. Indeed, one can imagine such effects acting in
often kept in holding pens for weeks or months before concert to cause a plunge in fitness in the second genera-
being used, and the mortality and morbidity induced has tion of culture. Research on the traits under domesti-
been shown to be nonrandom (Ford et al., 2008). Hatch- cation selection, and on possible alternative mechanisms
ery broodstock management has been the subject of con- that cause fitness declines, will be an important new
siderable scrutiny in recent years, and guidelines have direction as we search for ways to improve hatchery
been developed to maximize effective population size, and programs.
reduce intentional and unintentional artificial selection
(e.g. Campton 2005). However, artificial spawning in the
Conclusion
hatchery almost certainly results in relaxation of mate
selection (Blanchfield and Ridgway 1999; Berejikian et al. A review of studies to date shows that older, nonlocal
2000; de Gaudemar et al. 2000), intra-sexual competition, stocks generally perform worse than local stocks having
and natural selection on traits such as body size, egg size, experienced fewer generations in the hatchery. In some
fecundity and spawn timing and location (van den Berghe cases, even old stocks had fitness indistinguishable from
and Gross 1989; Fleming and Gross 1994; Einum and that of wild fish, but in most of those situations hatchery
Fleming 2000a,b). In addition to selection on the brood- fish had contributed high proportions of the natural
stock, viability selection on their offspring during the oce- breeding population for many years, making it likely that
anic phase (as discussed above) could conceivably result no ‘wild’ population remained. More studies are needed,
in surviving phenotypes that are disadvantaged during particularly on salmonids other than steelhead and on
reproduction to the extent that key behavioral traits hatchery programs that are still in their earliest phases.
under selection (e.g. aggressiveness or dominance) are Several studies in progress on other salmonid species
affected. should soon provide additional data points. One surpris-
ing recent result is large declines in fitness of steelhead
during the first two generations of hatchery culture. We
Possible other mechanisms
showed that domestication selection is a plausible expla-
We have shown that the conditions necessary for domes- nation for such large declines, especially if such selection
tication selection alone to generate fitness declines like operates on several traits throughout the life cycle. Other
those observed in studies such as Araki et al. (2007b) are mechanisms, such as an enhanced mutation rate, relaxa-
possible when certain conditions are met. Nevertheless, it tion selection, chromosomal abnormality, and epigenetic
is worth considering other explanations. We dismissed effects, might also contribute to the observed declines in
mutation accumulation as the explanation for effects fitness.
appearing during the first one or two generations because Our review indicates that salmonids appear to be very
typical rates of mutation to deleterious alleles and their susceptible to fitness loss while in captivity. The degree of
fitness effects are too small. However, an enhanced muta- fitness loss appears to be mitigated to some extent by
tion rate owing to the hatchery environment is one possi- using local, wild fish for broodstock, but we found little
bility. This could include a higher rate of chromosomal evidence to suggest that it can be avoided altogether. The
abnormalities. While there is no evidence of a high rate general finding of low relative fitness of hatchery fish,
of chromosomal abnormality in salmonids, aneuploidy in combined with studies that have found broad scale nega-
germ cells has long been known to cause meiotic errors tive associations between the presence of hatchery fish
that can result in infertility in both plants and animals and wild population performance (e.g. Hoekstra et al.
(e.g. Shi and Martin 2001; Henry et al. 2005; Hall et al. 2007), should give fisheries managers pause as they con-
2006). Another intriguing possibility is heritable epige- sider whether to include hatchery production in their
netic changes induced by the hatchery environment. conservation toolbox.
Epigenetic changes, such as alternations in DNA or
histone methylation, have been shown to affect an indi-
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