Maybe steelhead and salmon are particularly susceptible to this captivity-induced loss of fitness (when released in the wild) because of their anadromous life history, or maybe it's true with many kinds of fish. Also, I wonder to what extent it's reversible. Might the next generation (wild-born grandkids of hatchery fish) have higher repro success?


Christie et al. 2011. Genetic adaptation to captivity can occur in a single generation. Proceedings of the National Academy of Sciences. www.pnas.org/cgi/doi/10.1073/pnas.1111073109

ABSTRACT: Captive breeding programs are widely used for the conservation
and restoration of threatened and endangered species. Nevertheless,
captive-born individuals frequently have reduced fitness when
reintroduced into the wild. The mechanism for these fitness declines
has remained elusive, but hypotheses include environmental
effects of captive rearing, inbreeding among close relatives, relaxed
natural selection, and unintentional domestication selection
(adaptation to captivity). We used a multigenerational pedigree
analysis to demonstrate that domestication selection can explain
the precipitous decline in fitness observed in hatchery steelhead
released into the Hood River in Oregon. After returning from the
ocean, wild-born and first-generation hatchery fish were used as
broodstock in the hatchery, and their offspring were released into
the wild as smolts. First-generation hatchery fish had nearly
double the lifetime reproductive success (measured as the number
of returning adult offspring) when spawned in captivity compared
with wild fish spawned under identical conditions, which is a clear
demonstration of adaptation to captivity. We also documented a
tradeoff among the wild-born broodstock: Those with the greatest
fitness in a captive environment produced offspring that performed
the worst in the wild. Specifically, captive-born individuals
with five (the median) or more returning siblings (i.e., offspring of
successful broodstock) averaged 0.62 returning offspring in the
wild, whereas captive-born individuals with less than five siblings
averaged 2.05 returning offspring in the wild. These results demonstrate
that a single generation in captivity can result in a substantial
response to selection on traits that are beneficial in
captivity but severely maladaptive in the wild.

No different than our eastern trout fisheries. Hatchery trout are junk. No natural selection is taking place in a hatchery. The trout that consume the most trout chow, get larger and produce more eggs. Produce more progeny, and a large percentage lives. You know where that goes. The bigger question is whether these fish are spawning with wild fish, and producing a fish that is inferior at surviving in the wild?

Fishes have a very plastic phenotype, even with no changes in gene frequencies. The classic studies on this are by Sean Lema and others with Death Valley Cyprinodon species, if you change the temperature or food regimes individuals can bulk up or become much smaller with the loss of pelvic fins.

Nice to see this point being established so clearly with good numbers. It should go a long way toward driving better hatchery practices.

The actual number of mechanisms behind this effect is likely bewildering, but I can likely outline a lot of them very generally. I'll outline a few I think are the most relevant. This also goes toward some of the issues I have brought up elsewhere concerning over-protection and imposing too much ecological stability in protected environments.

[1]Epigenetics:
One of the main ones is epigenetics, or functionally relevant modifications of the genome not involving changes in nucleotide sequences. We tend to think of DNA as a master program that determines who and what we are. However, the makeup of the cells in which the DNA operates plays a large role in what DNA gets expressed, and these are also inheritable. It's like a computer operating system that has one set of bugs when installed on brand X computer and another set of bugs when installed on brand Y computers. Not only that but the environment (computer users) with which it operates also plays a role in which of these bugs gets expressed. More often called phenotypic plasticity. So when you clone (reproduce) this computer on another machine it is effectively a different operating system in spite of the fact that the base code (DNA) is the same. Many the forthcoming mechanisms will refer back to this epigenetic effect in some way.

[2] Predatory responses:
Tadpole responses to predators are well studied. Here is a study showing phenotypic variantions in Hyla chrysoscelis (my favorite frog) resulting from the presents or lack of predatory dragonfly larvae with the tadpoles. Tadpoles also release hormones in the presents of predators that modify the predator avoidance behavior of all the tadpoles whether subjected to predation or not. Here's a review of antipredator pheromones. This study demonstrates where early protection from predators lead to increased growth rates which resulted in lower adult sizes as a result of later intraspecific competition. An effect that is highly relevant to fish hatcheries. All of these environmental responses contribute to the epigenetics of subsequent generations per [1].

[3) Beneficial gene reduction:
Suppose you have a population with a significantly valuable wild adaptation. You then protect their environment from certain stressors (say predators) required to trigger the expression of this gene. This population then moves out into an unprotected environment. The presents, or lack of, now plays no role in survivability in spite of the genes presents. Which is passed on by way of [1]. The best fit individuals have no better chance of breeding than those in which a bad mutation of this gene occurred. Hence, for this particular generation, certain benefits of evolutionary pressures has been lost on average for the last two generations (assuming you started with wild stock). This is exacerbated even further from pressures from below (genetics) and pressures from above (environment and population dynamics) to be added below.

4) Lotka–Volterra and population dynamics:
In [2] and [3] the effects were single generational via [1] with a hint at population dynamics in [2]. It is not just the predators that caps the population of a prey. With the predators the prey has essentially the same population cap as a result of intraspecific competition. A large boom cycle can hurt a population worse than predation by predators that remain dependent on that prey for their own survival. For big game hunters this illustrates why the removal of predators is not an effective strategy, and can actually harm the populations hunters want in abundance. Fish hatcheries tend to operate in this mode of maxing out intraspecific competition. Thus even in the absents of epigenetic effects the wild fit individuals are stressed in unnatural ways against the shear weight of numbers produced by the hatcheries. Hatchery stock then have a breeding success way out of proportion to their future survival capacity. Yet by replenishing the hatchery stock to full ecological support potential every generation the survival capacity of the wild stock provides a negative mean benefit to high survival fitness. Hatcheries replace the need for fitness by sheer weight of offspring numbers. The survival strategy is changed to something more akin to certain insect survival strategies, where only a few individuals are required for the entire capacity of the next generation.


It is the resource constraints that limit the size of particular populations, thus allowing hierarchical predation to increase the total biomass without producing an overall reduction in the population capacities at the bottom of the food chain. Just not in an intraspecific manner, though it in general doesn't harm intraspecific population capacities. This is why the biomass number at coral reefs in Palmyra seem obvious to me. In effect predation extends the effective lifespan of the biomass in a given ecosystem, but only if predator numbers are confined by the available prey. Human predators are not so confined. The higher up on this food chain something is the more dependent individual survival success becomes to species survival. The lower down the food chain the more breeding success becomes dependent on sheer numbers for species survival. Due to predation these sheer numbers do not result in significant intraspecific competition, such as what happened in the tadpole study were predator removal resulted in intraspecific competition that reduced their growth potential.

I'm happy to see these issues addressed in a more limited and specific but sufficient manner to justify changes to our hatchery practices.

Edited by mywan, 12 January 2012 - 04:00 AM.

This is a very interesting article. I currently work on a project that monitors the success of a coho salmon broodstock program in North-Central California. The goal of this program is to re-establish wild runs of coho salmon. We sometimes struggle with this issue and are always trying to find ways to reduce the impacts of hatchery rearing. Here is a link to our website any of you are interested: Russian River Coho Salmon Captive Broodstock Program