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The Origins of Life History Variation in Steelhead/Rainbow Trout from Coastal California John Carlos Garza, Alicia Abadía-Cardoso, Devon Pearse
Molecular Ecology & Genetic Analysis Team Southwest Fisheries Science Center and UC Santa Cruz
Life History Variation Age- 2.0 Sex- M Length-12 cm
Age- 1.1? Sex- M Length- 41cm
Age- 5.0?? Sex- M Length- 27 cm
Age- 1.3 Sex- M Length- 88 cm
Age- 2.2 Sex- M Length- 71cm
Age- 4.0 estuarine Sex- F Length- 32 cm
Age- 3.4 estuarine? Sex- F Length- 42 cm
Age- 2.1 Sex- M Length- 53 cm
Coastal CA Steelhead Population Structure • “Snapshot” of population
structure from 60 sites, 40 basins in all five CA Coastal steelhead ESUs
• ~4500 juvenile fish non-lethally sampled from 5 sections/location
• Samples collected June-Oct. 2001 • Avg. of 66 fish/site analyzed • Data from 18 microsatellite loci • ~132,000 allele copies, 540
unique alleles sampled.
100 replicates
Redwood-Prairie
BigCk
SanL-Bear!Waddell
Pescadero Scott
SanL-Boulder!
Corralitos SanL-Zayante!
SanPedro SanL-Carbonera
Chorro SanSimeon
Carmel
BigSur WillowCk!
Mont
507 656
Redwd!Marin
Walker Lagunitas
Blueline Olema
949 Miller!
LosTrancos
558
Big-Humb
Smith-Rowdy
Klamath-Hunter WilsonCk
794
767
Klamath-HLinto Klamath-Blue!
597
831
Redwood-Panther Redwood- LostMan!
Freshwater 891
719 702
Mattole-Bear BearHumb Eel-HTree Mad-Blue
Eel-Indian Eel-Willits Eel-Lawrence Mad-Canon
Mad-Sullivan
934
647 707
777
Ten-LNFk Ten-SFk
Ten-Smith Ten-Redwd
507
Wages Usal Elk
Gualala Garcia
652 Big
Noyo NoyoSfk
Albion Noyo-Kass Noyo-LNFk
912 BigSalmon
Pudding Navarro
Russian
Steelhead Bootstrap Consensus Tree
South Central California
Klamath Mountain Northern California Central California
ESU Assignment
Strict consensus of 1000 neighbor-joining trees
Isolation by distance Regression of genetic distance on geographic distance for 59 steelhead
populations in coastal California. Geographic distance explains about 30% of the variation in genetic distance
r2=0.31! r2=0.18!
All data!Full siblings excluded!
DPS/ESU vs. Genetic Group Boundaries
Coastal CA Steelhead Population Structure
Humboldt Bay
Lost Coast
Russian Gulch
San Francisco Bay
Southern California Trout Population Structure
• Extension of population structure study to South-Central & Southern California
• Five basins with population sampling above and below dams
• Small numbers from further south • All strains of rainbow trout used in
stocking also sampled • ~1900 juvenile fish non-lethally
sampled w/ standardized protocol • Data from same 18 microsatellite
loci as previous study.
Consensus chord distance tree with bootstrap support (10,000 replicates)
Santa Clara River
Salinas River Arroyo Grande Santa Ynez River
Fillmore Hatchery Strains
Ventura River
100
S.Ynez-SalsB
S.Ynez-NFJuncalA S.Clara-SantaPaulaB
Fillmore-MtWhitLt
Fillmore-MtWhitEa
100
Fillmore-Coleman
Fillmore-Wyoming
Fillmore-Virginia03
Fillmore-Virginia02
100
91
76
99
S.Clara-LionCanB S.Clara-PiruFFA
S.Clara-LockwoodA
S.Clara-PiruGHA
100 90
76
51
S.Ynez-HiltonB
S.Ynez-S.CruzA A.Grande-LopezCanA
Ventura-NFMatilijaB
Ventura-BearB
100
Ventura-UpNFMatilijaA Ventura-MatilijaA
99
61
A.Grande- mainB
A.Grande- LosBerrosA
Salinas-NacimientoA Salinas-TassajeraB
Salinas-TassajaraB
Salinas-SanAntonioA 87
Expeditions of John Otterbein Snyder -Prominent early California ichthyologist-Student of David Starr Jordan
-Zoology professor at Stanford. Organized the National Museum fish collections.
-Published “The Fishes of the Streams Tributary to Monterey Bay, California”-1912
-Population collections of steelhead in Central California from 1897 & 1909 described.
Historical ModernWatershed Location Year N Year NEel River South Fork 1897 30 2001, 03 24Lagunitas Creek 1909 10 2001, 03 20Coyote Creek 1909 15 1998-2000 40San Lorenzo River 1897, 1909 41 2002, 04 32Pajaro River Uvas Creek 1909 19 1997, 98 16
Llagas Creek 1897 13 1997, 98 32Salinas River Arroyo Seco 1897, 1909 33 2001 32
San Antonio River 1909 27 2003 22Nacimiento River 1909 24 2003 22
TOTAL: 212 240American River Hatchery-Mt. Shasta - 2002 24Santa Clara River Hatchery-Virginia - 2003 23
Sampling for Historical Steelhead Study
Mitochondrial DNA- ~200bp section of control region
-Lagunitas population coho!
-No significant difference in number of alleles/diversity
-Four new alleles detected: 3 historically, 1 contemporary
-Differences range from very minor to dramatic
-No major replacement with hatchery stocks, although poorly sampled
Eel River
San Lorenzo
Pajaro-Llagas
Pajaro-Uvas
Salinas-Nacimiento
Coyote Creek
Salinas-Arroyo Seco
Salinas-San Antonio
Mt Shasta Virginia
Results
Mitochondrial DNA- ~200bp section of control region
-Lagunitas population coho!
-No significant difference in number of alleles/diversity
-Four new alleles detected: 3 historically, 1 contemporary
-Differences range from very minor to dramatic
-No major replacement with hatchery stocks, although poorly sampled
Eel River
San Lorenzo
Pajaro-Llagas
Pajaro-Uvas
Salinas-Nacimiento
Coyote Creek
Salinas-Arroyo Seco
Salinas-San Antonio
Mt Shasta Virginia
Results
Modern samples, River distances
r 2 = 0.0673
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9
1
0 50 100 150 200 250 300 350 400 450 500 Distance (Miles)
Fst/
(1-F
st)
Geographic versus genetic distance-mtDNA control region Modern
Historical samples, River distances
r 2 = 0.9038
-0.5
0
0.5
1
1.5
2
2.5
0 50 100 150 200 250 300 350 400 450 500
Distance (Miles)
Fst/
(1-F
st)
Geographic versus genetic distance-mtDNA control region Historical
BlKlaRi_M
Matto_M
Guala_M
AmRNF_M
UpYuL_M
McClC_M
Battl_M
DeerC_M
LosTran_M
Wadd_M
Carmel_M
Tassaja_M
BigSuRi_M
WilloCk_M
PenChor_M
Simeon_M
CuyRey_M
SisqMnz_M
Sisq_M
MnteCr_M
Quiota_M
SCrz_M
Hilt_M
Junc_M
Sals_M
VeSAnt_M
NFMati_M
BearVen_M
SPau_M
Piedra_M
LionCyn_M
Sespe_M
BuckCr_M
Piru_M
SAnita_M
NFSGab_M
SGaBear_M
DevSG_M
WFSGab_M
Cattle_M
FishFk_M
SFIronFk_M
IronFk_M
EFSGab_M
FishCyn_M
TrabCr_M
OraSnAn_M
StaAna_M
ColdCr_M
FulMil_M
NFSnJaB_M
NFSnJaE_M
Doane_M
PaumaR_M
PaumaO_M
WFSLuis_M
SDiego_M
SweetO_M
SweetR_M
nelsoni_M
FHCol_M
FHVirg_M
FHWhi_M
FHWyo_M
ARHEag_M
ARHShas_M
HCKm
lp_M
BlKlaRi_M
Matto_M
Guala_M
AmRNF_M
UpYuL_M
McClC_M
Battl_M
DeerC_M
LosTran_M
Wadd_M
Carmel_M
Tassaja_M
BigSuRi_M
WilloCk_M
PenChor_M
Simeon_M
CuyRey_M
SisqMnz_M
Sisq_M
MnteCr_M
Quiota_M
SCrz_M
Hilt_M
Junc_M
Sals_M
VeSAnt_M
NFMati_M
BearVen_M
SPau_M
Piedra_M
LionCyn_M
Sespe_M
BuckCr_M
Piru_M
SAnita_M
NFSGab_M
SGaBear_M
DevSG_M
WFSGab_M
Cattle_M
FishFk_M
SFIronFk_M
IronFk_M
EFSGab_M
FishCyn_M
TrabCr_M
OraSnAn_M
StaAna_M
ColdCr_M
FulMil_M
NFSnJaB_M
NFSnJaE_M
Doane_M
PaumaR_M
PaumaO_M
WFSLuis_M
SDiego_M
SweetO_M
SweetR_M
nelsoni_M
FHCol_M
FHVirg_M
FHWhi_M
FHWyo_M
ARHEag_M
ARHShas_M
HCKmlp_M
San Gabriel R.
The Deep South
Sta A
na-T
emas
cal-
Sn Ja
cint
o12
FH-V
irginia A
RH-Shasta
EF Sn Gabriel- Iron Fork
EF Sn Gabriel-Fish Fork NF Sn Gabriel WF Sn Gabriel-Bear
EF Sn Gabriel EF Sn Gabriel-Cattle
Klamath-Blue Santa Ana
Sta Ana-Temescal- Coldwater Canyon
O. m. nelsoni
Sta Clara-Sespe
Los Trancos
San Luis Rey
Sta Ynez-Hilton Sa
linas
-Tas
saja
ra
Sta Y
nez-
Junc
al
Waddell Chorro-Pennington Sta Ynez-Quiota
Sta Ynez-Sta Cruz Sta Ynez-Salsipuedes
93 100
69
88
75
100
67
100 67
96 92
100
62
76
Sta A
na-T
emes
cal-
Sn Ja
cint
o12
FH-V
irginia A
RH-Shasta
EF Sn Gabriel- Iron Fork
EF Sn Gabriel-Fish Fork NF Sn Gabriel WF Sn Gabriel-Bear
EF Sn Gabriel EF Sn Gabriel-Cattle
Klamath-Blue Santa Ana
Sta Ana-Temescal- Coldwater Canyon
O. m. nelsoni
Sta Clara-Sespe
Los Trancos
San Luis Rey
Sta Ynez-Hilton Sa
linas
-Tas
saja
ra
Sta Y
nez-
Junc
al
Waddell Chorro-Pennington Sta Ynez-Quiota
Sta Ynez-Sta Cruz Sta Ynez-Salsipuedes
93 100
69
88
75
100
67
100 67
96 92
100
62
76
Big Creek Falls
>> Strong, continuing selection on above-falls fish not to move downstream.
Photos: Corey Phillis"
• O. Mykiss introduced above Big Creek Falls c. 1910
• Genetic analysis supports within-basin origin of the above-falls population
(Pearse et al. 2009)
• 1.8% emigration rate over the falls, based on PIT tag data. (Hayes et al. 2012)
• 24 individuals each from above and below falls.
• 298 microsatellite loci genotyped, many mapped. (Martinez et al. 2011)
• 96 un-mapped SNP loci. (Abadía-Cardoso et al. 2011)
~400 loci distributed over all 29 linkage groups with ~10 cM coverage of the genome.
Genome Screen
Fst Histogram Micros and SNPS
0
5
10
15
20
25
30
35
40
45
50
-0.1
-0.1
-0.1 -0 -0 0
0.02
0.04
0.06
0.08 0.1
0.12
0.14
0.16
0.18 0.2
0.22
0.24
0.26
0.28 0.3
0.32
0.34
0.36
0.38 0.4
0.42
0.44
0.46
0.48 0.5
0.52
0.54
Fst
Freq
uen
cy
SNPsMicros
SH114448 SH121006 SH127236 BHMS426
Fst(298)=0.034
(Martinez et al. 2011; Pearse et al. 2014)
Hatchery Eagle Hatchery MtWhitney Hatchery Kamloops Goose Lake Bauers Upper Klamath Buckboard McCloud Butcherknife Eel CuCinger
Summer SH Willow Winter SH
ScoE Above Below
San Lorenzo San Lorenzo Carmel Carmel Salinas Tassajera
Nacimiento Santa Ynez Hilton
NF Juncal Salsipuedes Santa Cruz
Santa Clara Lion Canyon Frenchmen Santa Paula Gold Hill Pearse et al. 2014!
Populations
SNP loci
R19198R14511
SH121006R14383R34385R33562R28680R14589R40580R33010R24370R23330R18251R40252R30015
SH114448R00586R21561R40342R19633R40319R13730R30423R40152R30220R34662R24068R21285R21330
SH127236R30678R37560R33411R14225R35324R40094R34286R38346R19731R39365R12738R30589R37205R24273R38993R23044
OMS00169
OMS00143
OMS00116R37229R22570R23813
OMS00144
OMS00159R30355
ARHEagle
FHMtWhitney
Kamloops
GLBauers
UKBuckboard
McCloudBk
EelCutfinger
EelSummerSH
EelWillow
EelWinterSH
ScottAbove
ScottWeir
SanLorenzo
Carmel
Tassajera
Nacimiento
SYHilton
SYNFJuncal
SYSalsipuedes
SYSantaCruz
SCLionCan
SCFrenchmen
SCSantaPaula
SCGoldHill
0 20 40 60 80 100Pearse et al. 2014! Frequency of the allele most common in anadromous adults
Conclusions • Historical population structure relatively “intact” north of Pt. Conception:
mostly concordant with geography, no detectable hatchery impact
• Migration and drift represents natural state: corridors important
• Between Pt. Conception and the Los Angeles basin, above and below dam populations recently derived from coastal steelhead
• Deep south populations (LA, Orange and San Diego counties) highly variable, many with a strong signal of hatchery ancestry
• Little support for current DPS boundaries. Primary structuring: Local (~90%) -> Drainage -> Region
• A chromosomal region on Omy5 is strongly associated with life history variation in O. mykiss throughout its range.
Acknowledgements • Eric Anderson • Joe Anderson • Andres Aguilar • Russell Barabe • David Boughton • Anthony Clemento • Heidi Fish • Libby Gilbert-Horvath • Derek Girman • Steve Gough • David Hamm
• Terry Jackson • Sandi Jacobson • Mary Larson • Chris Lima • Jack Marshall • Andy Martinez • Edith Martinez • Dennis McEwan • Chris McKibbin • Brian Spence • Tommy Williams
Other collaborators who helped in sample collection. Funding: Fishery Restoration Grant Program, NOAA Fisheries