Matthew P. Hare and Colin Rose Department of Biology University of Maryland THE BENEFITS AND CONSEQUENCES OF RESTORATION USING SELECTIVELY-BRED, DISEASE-TOLERANT OYSTERS
Dec 22, 2015
Matthew P. Hare and Colin Rose Department of BiologyUniversity of Maryland
THE BENEFITS AND CONSEQUENCES
OF RESTORATION USING
SELECTIVELY-BRED, DISEASE-TOLERANT
OYSTERS
Talk Outline
• Rationale behind supportive breeding using artificially-selected oyster strains– pros and cons
• Risks are now predictable
• Modeling impacts of supportive breeding– Inbred broodstock – a critical factor
• Recommendations
Supportive Breeding Goals and Impacts
• Increase population size– limit early mortality in hatchery, then release
juvenile “seed” oysters
• Hatchery broodstock and restoration seed represent a genetically bottlenecked subset of population
• Genetic diversity summarized by inbreeding effective population size, Ne
Consensus Points from Allen & Hilbish 2000
• “stocking programs [supportive breeding] will be important…” for restoration success
• “Diseases…are a major limitation” for restoration• “Continued use of selected disease resistant stocks is
warrented…”• Benefits
– Genetic measurement of restoration efficacy– Disease tolerance greater longevity of seed oysters– “genetic rehabilitation”, infusing desirable alleles
• Risks– Increase overall inbreeding– Decrease genetic variation– Lower mean fitness of population
• “Effective population size of wild populations is an essential parameter to predict genetic effects, but is unknown”
Broodstock Sources and Numbers of Seed Planted in Virginia Supportive Breeding
T. Leggett, Chesapeake Bay Foundation
0.0E+00
2.0E+06
4.0E+06
6.0E+06
8.0E+06
1.0E+07
1.2E+07
1.4E+07
1.6E+07
1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006
Year
Oysters Planted
Buyback Hatchery Selected DEBY cross 3.7x107
Oys
ters
Pla
nted
Risks of Supportive Breeding
• Can severely reduce total Ne
total Ne with % hatchery contribution x:
1 x2 (1-x)2
Ne(tot) Ne(hatchery) Ne(wild)
• No estimates for these parameters in 1999 when ‘genetic rehabilitation’ recommended
― = ― + Ryman & Laikre 1991
Predicted Consequences
• Wang & Ryman 2001• Closed hatchery line• Ne(wild) = 1500
– 95% CI = 422 - – Rose et al. 2006
• 5-10% contribution from supportive breeding in 2002, Great Wicomico, VA– Hare et al. 2006– 5% contribution graphed– N(census) annually
Hare & Rose in prep.
N e(wild) = 1500
0
200
400
600
800
1,000
1,200
1,400
1,600
0 1 2 3 4 5 6 7 8 9 10
Generation
Ne-Inbreeding
Ne - Hatchery = 50 Ne-Hatchery = 5
Ne(wild) initial = 420
0
100
200
300
400
500
600
0 1 2 3 4 5 6 7 8 9 10
Generation
Ne-Inbreeding
Ne - Hatchery = 50 Ne-Hatchery = 5
Effective Population Size – Hatchery
WILD oysters collected in DElaware BaY
and exposed to disease= DEBY strain
Disease tolerant oysters selected, = “PRIMARY” DEBY line
6 generations of selection
Hatchery amplification spawn broodstock from primary line
create lots of DEBY juvenilesplant these “seed” oysters
annual restoration broodstock
Effective Population Size – Hatchery
WILD oysters collected in DElaware BaY
and exposed to disease= DEBY strain
Disease tolerant oysters selected, = “PRIMARY” DEBY line
6 generations of selection
Hatchery amplification spawn broodstock from primary line
create lots of DEBY juvenilesplant these “seed” oysters“seed” oysters
annual restoration broodstock
BEFORE
Wild population
n = 300
AFTER
hatchery amplification of DEBY strain
n = 96 seed oysters
Loss of Alleles, locus 2j24
Allele
Effective Population Size - Hatchery• Population bottlenecks generate ephemeral correlations among alleles at
unlinked genes– gametic phase disequilibrium
• Magnitude of correlations depends on bottleneck Ne
• Waples 1991 method; Nb(LD) =
• 8 microsatellite loci, binned into biallelic data
n 300 48 100 82 100 Wild Primary LCR02 DEBY GWR02 DEBY LCR04 DEBY
LD(28) 0 5 9 11 23Nb(LD) 5.76 4.69 3.80 4.8695% CI 3.05 2.66 2.17 2.77
10.27 7.50 6.04 7.73
1
3 x (r2 – 1/S)
Effective Population Size - Hatchery
• Waples 1991 method• 8 microsatellite loci, binned into biallelic data
n 300 48 100 82 100 Wild Primary LCR02 DEBY GWR02 DEBY LCR04 DEBY
LD(28) 0 5 9 11 23Nb(LD) 5.76 4.69 3.80 4.8695% CI 3.05 2.66 2.17 2.77
10.27 7.50 6.04 7.73
Effective Population Size - Hatchery
• Waples 1991 method• 8 microsatellite loci, binned into biallelic data
n 300 48 100 82 100 Wild Primary LCR02 DEBY GWR02 DEBY LCR04 DEBY
LD(28) 0 5 9 11 23Nb(LD) 5.76 4.69 3.80 4.8695% CI 3.05 2.66 2.17 2.77
10.27 7.50 6.04 7.73
Consequences of Supportive Breeding
• Closed hatchery line• Ne(hatchery) = 5
• Initial reduction in Ne of 75 – 95%
• Recovery is slower than implied here, assumes constantly growing census N
Hare & Rose in prep.
N e(wild) = 1500
0
200
400
600
800
1,000
1,200
1,400
1,600
0 1 2 3 4 5 6 7 8 9 10
Generation
Ne-Inbreeding
Ne - Hatchery = 50 Ne-Hatchery = 5
Ne(wild) initial = 420
0
100
200
300
400
500
600
0 1 2 3 4 5 6 7 8 9 10
Generation
Ne-Inbreeding
Ne - Hatchery = 50 Ne-Hatchery = 5
What’s wrong with small Ne ??
• No problem with longstanding small Ne
• Problems caused by Ne
• Severity of problems depends on genetic load– 8 to 14 highly deleterious recessives per
genome in Pacific oyster, C. gigas
Ne
Inbreeding Depression in Oysters
• Common view: high fecundity buffers oysters from inbreeding depression– High early mortality allows ‘purging’ of load
• Correct view: even slight inbreeding causes measurable reduction in fitness-related traits
Evans et al. 2004
Aquaculture 230:89-98
40 families, n = 402
Recommendations I
• Two of three motivations for using selected strains were speculative, still no data on DEBY fitness in restoration setting
• Spawn wild oysters and use procedures that Ne(hatchery)
• Continue use of DEBY oysters only in rivers where genetic monitoring can be used to test efficacy of changing planting strategies
Recommendations II
• There is no empirical justification for using DEBY x wild broodstock crossings– Speculative benefits– Disables genetic monitoring of restoration – Known inbreeding risks still apply
Collaborators
Department of Biology &
Horn Point Laboratory,
University of Maryland
Virginia Institute of Marine Science
College of William and Mary, Virginia
C. Rose
K. Paynter
D. Meritt
S.K. Allen, Jr.
M.D. Camara
R. Carnegie
M. Luckenbach
K.S. Reece
with help from… Maryland Oyster Recovery Partnership
Charlie Frentz
Virginia Chesapeake Bay Foundation
Rob BrumbaughTommy Leggett
VA Marine Resources DivisionJim Wesson
VIMS: Cheryl MorrisonWendy RibeiroMissy Southworth
Oyster Disease Research Program, NOAA, Sea Grant
Hare Lab, UMD:
Jenna Murfree
Paulette Bloomer
Natasha Sherman
Gang Chen
Maria Murray
Peter Thompson
Safra Altman
Kristina Cammen
Andrew Ascione
Ninh Vu
Katie Shulzitski