Genetic adaptation to captivity can occur ina single generation
Mark R. Christie
a,1
, Melanie L. Marine
a
, Rod A. French
b
, and Michael S. Blouin
a
a
Department of Zoology, Oregon State University, Corvallis, OR 97331-2914; and
b
Oregon Department of Fish and Wildlife, The Dalles, OR 97058-4364Edited by Fred W. Allendorf, University of Montana, Missoula, MT, and accepted by the Editorial Board November 11, 2011 (received for review July 14, 2011)
Captive breeding programs are widely used for the conservationand restoration of threatened and endangered species. Neverthe-less, captive-born individuals frequently have reduced
tness whenreintroduced into the wild. The mechanism for these
tness de-clines has remained elusive, but hypotheses include environmentaleffects of captive rearing, inbreeding among close relatives, re-laxed natural selection, and unintentional domestication selection(adaptation to captivity). We used a multigenerational pedigreeanalysis to demonstrate that domestication selection can explainthe precipitous decline in
tness observed in hatchery steelheadreleased into the Hood River in Oregon. After returning from theocean, wild-born and
rst-generation hatchery
sh were used asbroodstock in the hatchery, and their offspring were released intothe wild as smolts. First-generation hatchery
sh had nearlydouble the lifetime reproductive success (measured as the numberof returning adult offspring) when spawned in captivity comparedwith wild
sh spawned under identical conditions, which is a cleardemonstration of adaptation to captivity. We also documented atradeoffamong the wild-born broodstock: Those with the greatest
tness in a captive environment produced offspring that per-formed the worst in the wild. Speci
cally, captive-born individualswith
ve (the median) or more returning siblings (i.e., offspring ofsuccessful broodstock) averaged 0.62 returning offspring in thewild, whereas captive-born individuals with less than
ve siblingsaveraged 2.05 returning offspring in the wild. These results dem-onstrate that a single generation in captivity can result in a sub-stantial response to selection on traits that are bene
cial incaptivity but severely maladaptive in the wild.
sheries
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genetics
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parentage
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rapid evolution
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salmon
C
aptive breeding programs are commonly used for the con-servation of endangered species and, more recently, for therestoration of declining populations (1
–
4). Mounting evidencesuggests that captive-born individuals released into the wild canhave substantially lower
tness than their wild-born counterpartsand that these
tness declines can occur after only a few gen-erations in captivity (5
–
8). Identifying the mechanisms that causereduced
tness in the wild is vital for deciding if, when, and howcaptive breeding programs should be applied for conservationand management purposes (5, 7). Explanations for the rapid
tness declines (8
–
12) include environmental effects of captiverearing (including heritable epigenetic effects), inbreeding amongclose relatives, relaxed natural selection, and unintentional do-mestication selection (adaptation to the novel environment).Each of these mechanisms creates subtle but testable differencesin patterns of reproductive success.Environmental effects of captive rearing, for example, couldproduce differences in
tness between captive-born and wild-born individuals but would not create differences in
tness amongindividuals that experienced identical captive environments (12,13). Relaxed natural selection in captivity is a compelling hy-pothesis because it can manifest in a myriad of forms. Lack of mate choice, for example, could result in combinations of im-mune-related genes that do not maximize
tness (14, 15). Nev-ertheless, theoretical analyses suggest that for relaxed naturalselection to cause a rapid
tness decline, the population musthave a high standing mutational load or spend many generationsin captivity (9). Unintentional domestication selection, on theother hand, can rapidly reduce
tness in the wild, especially if multiple traits are under selection (10, 16).If unintentional domestication selection is occurring, we ex-pect to observe two unique patterns. First, captive-born indi- viduals should perform better in captivity than wild-bornindividuals. Second, there should be a tradeoff among the wild-born broodstock: Those with the greatest
tness in a captiveenvironment will produce offspring that perform the worst in the wild. These predictions are not expected under relaxed naturalselection because individuals with
t and un
t genotypes (whenexpressed in the wild) would perform identically in a captiveenvironment where that genetic variation is selectively neutral.We test these competing explanations with a detailed pedigreeanalysis of a wild steelhead (
Oncorhynchus mykiss
) populationthat was supplemented with captive-reared individuals.Billions of captive-reared salmon are intentionally releasedinto the wild each year in efforts to increase
shery yields, miti-gate environmental disturbances, and bolster severely decliningpopulations (17
–
19). Steelhead from the Hood River in Oregonare listed as threatened under the US Endangered Species Act(20), and part of their recovery plan includes supplementation with juvenile
sh produced in a captive breeding program (i.e.,
sh hatchery). For winter-run steelhead from this population, weconstructed three-generation pedigrees from 15 run-years by genotyping 12,700
sh at eight highly polymorphic microsatelliteloci. Steelhead en route to their spawning grounds in the HoodRiver were
rst passed over the Powerdale Dam, which wasa complete barrier to migrating
sh (
).Because of this barrier, we were able to obtain samples of every returning
sh that spawned in the wild. Previous work from thissystem documented that captive-born
sh with two wild parentsaveraged 85% of the reproductive success of their wild-borncounterparts (6). However, the mechanism responsible for thedocumented
tness decline remained unknown.In this captive breeding program, ocean-returning wild-bornand
rst-generation hatchery adults were collected from the wildand spawned in a hatchery (hereafter,
“
broodstock
”
; Fig. 1).Their offspring (hereafter,
“
F1
”
sh) were reared in a hatchery environment and released near wild-spawning habitat as juve-niles. After release, the F1
sh went out to sea, returned asadults, and spawned in the wild. The progeny of F1
sh (here-after,
“
F2
”
sh) spent their entire lives in the wild. Using par-entage analyses, we assigned F1 hatchery
sh back to theirbroodstock parents. We again used parentage analysis to assignthe returning, wild-born F2
sh back to their F1 parents. We
Author contributions: M.R.C. and M.S.B. designed research; M.R.C., M.L.M., and R.A.F.performed research; M.R.C. analyzed data; and M.R.C. and M.S.B. wrote the paper.The authors declare no con
ict of interest.This article is a PNAS Direct Submission. F.W.A. is a guest editor invited by the EditorialBoard.
1
To whom correspondence should be addressed. E-mail:christim@science.oregonstate.edu.This article contains supporting information online atwww.pnas.org/lookup/suppl/doi:10.1073/pnas.1111073109/-/DCSupplemental.
www.pnas.org/cgi/doi/10.1073/pnas.1111073109PNAS Early Edition
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calculated the individual reproductive success of each wild-bornbroodstock
shinthehatcheryasthetotalnumberofitsF1progeny that returned as reproductively mature adults. We also calculatedthe per capita F1 reproductive success in the wild as the averagenumber of returning F2 progeny for all F1
sh assigned to a givenbroodstock. We performed separate analyses for each F1 run-yearand brood-year in addition to individual analyses for broodstock females, broodstock males, and broodstock pairs.
Results
In 7 of the 8 F1 run-years we examined, we found a substantialtradeoff between performance in the hatchery and performance inthe wild (Fig. 2 andTable S1). For broodstock families that pro-duced
ve or more returning offspring (the median), their F1offspring averaged 71% lower per capita reproductive success inthe wild than did F1 progeny from broodstock families havingfewer than
ve offspring. Thus,
sh with trait values associated with success in the captive environment produced large numbersof hatchery-reared F1 offspring that survived to become re-productively mature adults. However, the F1
sh from those largefamilies (i.e., those that were successful in captivity) had low percapita reproductive success in the wild. We observed the sametradeoff in F1 reproductive success regardless of whether weconsidered male and female broodstock separately or consideredbroodstock pairs (Fig. S1andTable S2). The
rst run-year of returning F1 hatchery
sh, 1995, did not show the tradeoff ob-served in subsequent years. However, in the year that these F1
sh were released into the wild, only a handful of broodstock
sh wereused (62% fewer than in other years) and substantially fewersmolts were released (4,600 vs. a mean of 52,700 in other years), which may have reduced the selection pressure and created lessopportunity for selection (Tables S1andS3).
The documented tradeoff is consistent with a rapid response todomestication selection. One alternate explanation is that F1
shfrom large families were more likely to mate with relatives, andsubsequently exhibit lower per capita
tness, owing to inbreedingdepression. Using our known pedigree and simulated randompairings of returning hatchery
sh with a high species-speci
cgenetic load (11 lethal equivalents) (21), we calculated the relative
tness reduction for F1
sh as a function of family size (i.e.,number of siblings). Our calculations demonstrate that inbreedingamong related hatchery
sh cannot explain the rapid decline inper capita reproductive success of F1
sh associated with in-creased family size (Fig. 3
A
). We also
t a generalized linearmodel (GLM) to establish that the slope of our explanatory var-iable was signi
cantly different from zero (
P
<
0.001; Fig. 3
A
andTable S1) and used a randomization test to demonstrate that thedocumented mean per capita F1 reproductive success cannot beexplained by the increased variance associated with smaller sam-ple sizes for broodstock with fewer offspring (
P
<
0.001; Fig. 3
B
andTable S1). Both the GLM and the randomization procedureillustrate that relaxed natural selection cannot be the predominatecause of
tness differences between hatchery and wild
sh because we would expect a
at slope (compare with Fig. 3
A
) and mostpoints to lie within the con
dence intervals (compare with Fig.3
B
). These tests remained highly signi
cant (
P
<
0.001) when theaberrant F1 run-year was included (i.e., 1995;Table S2).Because we also expect unintentional domestication selectionto cause rapid adaptation to captivity, we next examined whether
rst-generation hatchery
sh (i.e., F1
sh) had higher re-productive success than wild
sh when used as broodstock incaptivity. For 5 run-years, a portion of broodstock matings con-sisted of pairings between wild
sh and F1 hatchery
sh (6). Theremaining broodstock matings were restricted to crosses betweentwo wild
sh. We again measured reproductive success as thetotal number of returning adult offspring. In 4 of 5 run-years, theF1 hatchery broodstock had nearly twice the reproductive suc-cess of wild broodstock (Fig. 4), which is a pattern consistent with adaptation to captivity. As before, the
rst-generationhatchery broodstock collected from the
rst F1 return year(1995), for which few hatchery smolts were released (Table S3),showed no evidence for adaptation to captivity (Fig. 2).
Discussion
Under a model of domestication selection, certain traits areunintentionally selected on in the hatchery and this selectioncauses a high variance in reproductive success among thebroodstock (Fig. S2). However, the trait values associated with
Fig. 1.
Illustration of steelhead run-timing and study design. Broodstock
sh were
rst collected from the wild and spawned in captivity. The F1 offspringwere reared in a hatchery until becoming juveniles; at that time, they were released into the wild near spawning grounds. F1 juveniles went out to sea andsubsequently returned to spawn as adults in the wild. All returning adult
sh were sampled at the Powerdale Dam en route to their spawning grounds.Broodstock reproductive success was measured as the number of returning adult F1 offspring assigned to broodstock with parentage analysis. The re-productive success of F1
sh was measured by assigning F2
sh back to their F1 parents. F2
sh spent their entire lives in the wild. Each F1 hatchery run-yearconsists of
sh from multiple brood-years. In run-years 1995
–
1999, a small number of returning F1 hatchery
sh were used as broodstock. Notice that hatchery
sh return, on average, 1 y earlier than wild-born
sh owing to accelerated growth in the freshwater phase of the life cycle (1 y in the hatchery vs. an averageof 2 y in the wild).
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www.pnas.org/cgi/doi/10.1073/pnas.1111073109Christie et al.
success in the captive environment are detrimental in the wild,resulting in low reproductive success in the wild by
sh fromfamilies that were successful in captivity. Because substantial se-lection coef
cients on a single trait are required to explain thispattern, we speculate that multiple, and possibly correlated, traitsare unintentionally selected on (10). Previous work has suggestedthat growth rate may be under strong selection in hatcheries be-cause steelhead are released as yearling smolts, whereas
sh in the wild generally take 2 y or longer to smolt (22). Other possiblecontenders for selected traits include egg size, fecundity, physio-logical processes associated with smolti
cation, and individualbehaviors (e.g., predator avoidance) (10, 22
–
24). For the F1 run- year in which selection was not detected (1995), the smolts werereared in low-density conditions and the release size of the smolts was considerably larger than in other years (Table S3), whichpoints to crowding as a possible selection pressure (25). Although we have demonstrated rapid adaptation to captivity ina steelhead population, other taxa may not respond in an equiv-alent fashion. Factors that exacerbate adaptation to captivity in-clude strong selection pressures, large effective population sizes,high genetic diversity, and multiple generations in captivity (7, 9).Thus, the expected amount of genetic adaptation to captivity depends on both the intrinsic genetic composition of the desig-nated broodstock and the design and implementation of thecaptive breeding program. Steelhead are genetically diverse,highly fecund (thousands of eggs per female), and often spawnedusing dozens of families (26). Other highly fecund organisms, suchas plants, invertebrates, amphibians, and other
shes, may alsorespond quickly to domestication selection. Captive populations of less fecund animals, such as some mammals and birds, may notadapt as quickly to captivity provided that they are not kept incaptivity for many generations. One unusual feature of captivebreeding via supplementation hatcheries is that only the early lifehistory stages are kept in captivity. After release into the wild,there is very high mortality (often
>
95%), and thus ample op-portunity for directional and purifying natural selection. Whetherthe oceanic phase somehow enhances the domestication effect isnot clear. It is certainly possible that phenotypic variation gener-ated during the captive, juvenile phase (e.g., body size at release)could be under intense viability selection at sea (22).This study illustrates that domestication selection (i.e., adapta-tion to a novel environment) can cause a rapid
tness decline of hatchery
sh in the wild. Although more complex mechanisms may also be involved (e.g., relaxed purifying selection, heritable epige-netic effects), the documented patterns of reproductive successindicate that domestication selection is a primary explanation. Weconclude that (
i
) the wild population contained the requisite ge-netic variation for rapid adaptation to captivity and (
ii
) less thanone generation in captivity (i.e., fertilization through smolting)generated selection intensities necessary to produce a rapid, ge-netically based
tness reduction in the wild. Understanding thatunintentional selection in captivity can cause rapid
tness declineshas important conservation and management implications: Deter-
05101520253035
0 2 4 6 8 1 0
1995p = 0.29
05101520253035
0 2 4 6 8 1 0
1996p = 0.027
05101520253035
0 1 2 3 4 5 6
1997p = 0.037
05101520253035
0 2 4 6 1 8
1998p < 0.001
010203040506070
0 2 4 6 1 1
1999p < 0.001
010203040506070
1 2 3 4 8
2000p < 0.001
010203040506070
0 1 2 3
2001p < 0.001
010203040506070
0 1 2 3 8
2002p < 0.001
Number of F1 offspring per broodstock
M e a n F 1 r e p r o d u c t i v e s u c c e s s
Fig. 2.
Reproductive success of captive-spawned broodstock plotted againstthe per capita reproductive success of their F1 offspring (gray circles). Atradeoff between the reproductive success of
sh in captivity (broodstock)and the subsequent reproductive success of their offspring in the wild isshown in 7 of 8 F1 run-years.
P
values are shown for the slope of a GLM(
tted regression line drawn in black). Notice that the axes are scaled to eachplot and that large
y
-axis values are scaled independently (boxes) for run-years 1998, 1999, 2000, and 2002.
010203040506070
P e r c a p i t a F 1 r e p r o d u c t i v e s u c c e s s
024681118
A
0102030405060700.00.51.01.52.02.5
M e a n p e r c a p i t a F 1 r e p r o d u c t i v e s u c c e s s
B
Number of offspring per broodstock
Fig. 3.
Reproductive success of captive-spawned broodstock plotted againstthe per capita reproductive success of their F1 offspring. Results are pooled forthe 7 F1 run-years for which a substantial tradeoff was documented (comparewith Fig. 2). (
A
) Blue circles show the per capita reproductive success for eachF1 family. The solid black line represents the
tted GLM. Orange points rep-resent the expected reduction in per capita F1 reproductive success attribut-able to inbreeding as a function of F1 family size and cannot explain thedocumented pattern. (
B
) Blue circles illustrate the mean per capita F1 re-productive success (i.e., for broodstock families of a given size). The dashedlines represent the mean and 95% con
dence intervals for expected valuescalculated with random sampling of observed F1 reproductive success. Noticethat the observed pattern is consistent with unintentional domestication se-lection but is not consistent with relaxed natural selection, where we wouldexpect a
at slope and points to lay largely within the con
dence intervals.
Christie et al. PNAS Early Edition
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