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University of Leuven
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University of Leuven
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MARGEN-00322; No of Pages 10
Marine Genomics xxx (2015) xxxxxx
Marine Genomics
journal homepage: www.elsevier.com/locate/margen
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a r t i c l e
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Article history:
Received 16 February 2015
Received in revised form 28 April 2015
Accepted 28 April 2015
Available online xxxx
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Keywords:
Adaptation
Atlantic Ocean
Fish
Population genomics
Departamento de Gentica, Universidad de Santiago de Compostela, Facultad de Biologa, Santiago de Compostela E-15706, Spain
University of Leuven, Laboratory of Biodiversity and Evolutionary Genomics, Charles Deberiotstraat 32, B-3000 Leuven, Belgium
Departamento de Gentica, Universidad de Santiago de Compostela, Facultad de Veterinaria, Lugo E-27002, Spain
i n f o
a b s t r a c t
Partitioning phenotypic variance in genotypic and environmental variance may benet from the population
genomic assignment of genes putatively involved in adaptation. We analyzed a total of 256 markers (120
microsatellites and 136 Single Nucleotide Polymorphisms SNPs), several of them associated to Quantitative
Trait Loci (QTL) for growth and resistance to pathologies, with the aim to identify potential adaptive variation
in turbot Scophthalmus maximus L. The study area in the Northeastern Atlantic Ocean, from Iberian Peninsula
to the Baltic Sea, involves a gradual change in temperature and an abrupt change in salinity conditions. We
detected 27 candidate loci putatively under selection. At least four of the ve SNPs identied as outliers are
located within genes coding for ribosomal proteins or directly related with the production of cellular proteins.
One of the detected outliers, previously identied as part of a QTL for growth, is a microsatellite linked to a
gene coding for a growth factor receptor. A similar set of outliers was detected when natural populations were
compared with a sample subjected to strong articial selection for growth along four generations. The observed
association between FST outliers and growth-related QTL supports the hypothesis of changes in growth as an
adaptation to differences in temperature and salinity conditions. However, further work is needed to conrm
this hypothesis.
2015 Published by Elsevier B.V.
Romn Vilas a,, Sara G. Vandamme b,1, Manuel Vera c,2, Carmen Bouza c, Gregory E. Maes b,3,
Filip A.M. Volckaert b, Paulino Martnez c
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1Q3
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1. Introduction
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Partitioning the phenotypic variance into genetic and environmental components can be challenging due to statistical correlations
between genetic and environmental variation and the constitutive
interaction between both effects. However, phenotypic differences
may reect differences in the underlying genetic variation caused
by natural selection acting over generations in a process of adaptation to particular environmental conditions. This effect has been
demonstrated through genetic variation of candidate genes within
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http://dx.doi.org/10.1016/j.margen.2015.04.011
1874-7787/ 2015 Published by Elsevier B.V.
Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
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Q5
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2.1. Sampling
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that behave differently is useful for detecting adaptive polymorphisms, particularly if combined with complementary strategies
such as the use of functional information and appropriate QTL
(Vasemgi and Primmer, 2005; Stinchcombe and Hoekstra, 2007;
Hansen et al., 2012; Schoville et al., 2012). However, it is important
to emphasize the limited status of candidates for outlier loci, which
begs for additional experimental conrmation because of important
limitations of the population genomics approach (Bierne et al.,
2013). Correlations across populations and variation in effective
population size can substantially increase the FST variance among
loci and therefore make it difcult to separate historical or demographic effects from natural selection in highly subdivided species
(Nei and Maruyama, 1975; Robertson, 1975). Furthermore, the
effects of selection and genetic drift are frequently intertwined. For
example, when selection is involved in the reinforcement of
reproductive barriers, this may facilitate genome-wide neutral
divergence via genetic drift (Nosil et al., 2009). In combination
with population subdivision, the hitchhiking effect and the presence
of intrinsic genetic incompatibilities in hybrid zones, may cause a
correlation between genetic and environmental variation (Bierne,
2011; Bierne et al., 2011). Furthermore, other factors besides a
complex demography and cryptic genetic structure, can also
determine the appearance of selective effects on particular loci
(Barrett and Hoekstra, 2011; Roesti et al., 2012).
The turbot (Scophthalmus maximus L.; Scopththalmidae) is a
marine sh with high fecundity and vagility, which probably
explains high levels of gene ow between large panmictic populations. This hypothesis is concordant with the evidence of low genetic
structure along its geographic range (Blanquer et al., 1992; Bouza
et al., 1997, 2002; Coughlan et al., 1998; Vandamme et al., 2014).
The observed spatial genetic homogeneity of neutral markers is an
advantage in relating FST-outlier loci with signatures of divergent
selection because it suggests a low genetic drift scenario
(Beaumont, 2005; Nielsen et al., 2009). Vandamme et al. (2014)
found evidence for putative divergent selection at both sides of a
hydrodynamic front in the North Sea. However, the very wide
distribution range across several environmental gradients implies
the capacity of the sh to survive and reproduce in very different
conditions. The Atlantic area involves a gradient in light, temperature and salinity. Temperature differences range between 16 C in
the Iberian Peninsula to 8 C in the southern part of the Baltic Sea
and differences in salinity range from 35 in the Iberian Peninsula
to 8 in the Baltic (HELCOM, 2003; lvarez et al., 2005). Whereas
temperature changes gradually with latitude, an abrupt salinity
drop is observed between the Baltic and the North Sea. The transition
zone between the Baltic and the North Sea is recognized as a
biogeographical barrier for many marine species (Johanneson and
Andr, 2006). Differences in temperature and photoperiod are
expected to particularly affect the survival and reproduction of a
sh such as turbot that lives in relatively shallow waters near the
coast. Although populations living across these gradients have
usually shown low genetic structure for presumably neutral
markers, differentiation between them is statistically signicant
(Nielsen et al., 2004; Suzuki et al., 2004; Florin and Hglund, 2007;
Vilas et al., 2010; Vandamme et al., 2014). An explanation for this
result is that turbot consist of several demes locally adapted to
environmental differences in a background of relatively high levels
of gene ow (Nielsen et al., 2004; Vilas et al., 2010).
With the aim to identify genes with an adaptive genetic pattern we
perform a genome scan analysis of ve natural populations living in
different environmental conditions by using a total of 256 codominant
markers, most of them closely linked to functionally annotated genes
(Bouza et al., 2012). The analysis included 13 microsatellites located at
QTL related to growth and resistance to pathologies and the genetic
variation in natural populations was also compared with an additional
sample subjected to strong growth selection during several generations.
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Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
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Q6
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Fig. 1. Map of Europe showing the location of collecting sites: Atlantic Galician coast (AG), Cantabric Sea (CS), English Channel (EC), North Sea (NS) and Baltic Sea (BS).
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C
O
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Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
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Q7
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t1:1
t1:2
t1:3
t1:4
Table 1
Gene diversity (He), HardyWeinberg equilibrium departures (FIS) and test for conformance to expected values by locus and population for 58 microsatellite loci of turbot, analyzed by
Vilas et al. (2010), of which 28 are anonymous (left) and 30 EST-linked (right) in two new populations: the English Channel (EC) and the farmed population (FAR). Signicance level
*: P b 0.0008.
t1:5
EC
FAR
EC
FAR
He
FIS
He
FIS
Locus
He
FIS
He
FIS
Sma284
Sma42
Sma168
Sma247
2/5TG14
Sma135
Sma22
Sma147
Sma14
Sma137
Sma142
Sma149
F8I11/8/17
Sma113
Sma117
Sma34
Sma18
Sma184
Sma185
Sma38
Sma100
Sma144
Sma175
Sma205
Sma19
Sma146
Sma282
Sma77
0.862
0.938
0.785
0.759
0.867
0.910
0.867
0.804
0.903
0.320
0.936
0.889
0.865
0.808
0.859
0.868
0.882
0.666
0.723
0.833
0.594
0.962
0.418
0.510
0.920
0.829
0.691
0.831
0.084
0.007
0.197*
0.033
0.061
0.053
0.067
0.053*
0.081
0.037
0.304*
0.043
0.153
0.193
0.095
0.053
0.019
0.217*
0.047*
0.119
0.214*
0.026
0.021
0.183
0.005
0.079
0.076
0.064
0.867
0.906
0.631
0.646
0.825
0.821
0.878
0.691
0.765
0.377
0.873
0.801
0.497
0.699
0.731
0.802
0.868
0.257
0.525
0.807
0.408
0.876
0.341
0.459
0.895
0.770
0.551
0.759
0.183
0.058
0.057
0.054
0.041
0.015
0.075
0.085
0.007
0.051
0.269
0.037
0.112
0.043
0.083
0.142
0.069
0.028
0.213
0.123
0.081
0.001
0.024
0.053
0.022
0.101
0.112
0.018
SmaE1
SmaE2
SmaE3
SmaE7
SmaE4
SmaE29
SmaE8
SmaE12
SmaE14
SmaE16
SmaE25
SmaE28
SmaE38
SmaE20
SmaE35
SmaE40
SmaE41
SmaE42
SmaE19
SmaE22
SmaE26
SmaE32
SmaE30
SmaE43
SmaE10
SmaE13
SmaE31
SmaE33
SmaE36
SmaE39
0.869
0.284
0.586
0.617
0.510
0.367
0.610
0.879
0.862
0.379
0.789
0.430
0.887
0.666
0.347
0.854
0.693
0.432
0.703
0.799
0.645
0.706
0.527
0.116
0.383
0.858
0.846
0.814
0.766
0.856
0.250
0.617*
0.066
0.139*
0.184
0.074
0.080
0.052
0.226
0.598*
0.076
0.135
0.026
0.086
0.624*
0.029
0.066
0.169
0.005
0.040
0.360*
0.085
0.115
0.053
0.104
0.027
0.133*
0.189
0.051
0.111
0.770
0.172
0.505
0.516
0.469
0.308
0.662
0.797
0.870
0.043
0.656
0.245
0.727
0.427
0.000
0.793
0.660
0.538
0.508
0.262
0.461
0.574
0.576
0.354
0.164
0.781
0.745
0.680
0.583
0.647
0.080
0.093
0.010
0.111
0.066
0.084
0.119
0.046
0.101
0.011
0.027
0.154
0.024
0.287
0.000
0.051
0.177
0.071
0.024
0.032
0.123
0.160
0.121
0.057
0.063
0.048
0.225
0.073
0.014
0.130
261
3. Results
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R
O
P
T
C
E
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269
270
267
268
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266
Locus
t1:7
t1:8
t1:9
t1:10
t1:11
t1:12
t1:13
t1:14
t1:15
t1:16
t1:17
t1:18
t1:19
t1:20
t1:21
t1:22
t1:23
t1:24
t1:25
t1:26
t1:27
t1:28
t1:29
t1:30
t1:31
t1:32
t1:33
t1:34
t1:35
t1:36
t1:6
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Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
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t2:1
t2:2
t2:3
Table 2
Gene diversity (He), HardyWeinberg equilibrium departures (FIS) and test for conformance to expected values by locus and population of 62 new EST-linked microsatellites of turbot. EC,
BS, NS, CS, AG, and FAR are samples from the English Channel, Baltic Sea, North Sea, Cantabric Sea, Atlantic Galician coast, and the farmed population, respectively. Signicance level *: P b
t2:4
0.0008.
t2:5
EC
BS
NS
CS
AG
FAR
He
FIS
He
FIS
He
FIS
He
FIS
He
FIS
He
FIS
t2:7
t2:8
t2:9
t2:10
t2:11
t2:12
t2:13
t2:14
t2:15
t2:16
t2:17
t2:18
t2:19
t2:20
t2:21
t2:22
t2:23
t2:24
t2:25
t2:26
t2:27
t2:28
t2:29
t2:30
t2:31
t2:32
t2:33
t2:34
t2:35
t2:36
t2:37
t2:38
t2:39
t2:40
t2:41
t2:42
t2:43
t2:44
t2:45
t2:46
t2:47
t2:48
t2:49
t2:50
t2:51
t2:52
t2:53
t2:54
t2:55
t2:56
t2:57
t2:58
t2:59
t2:60
t2:61
t2:62
t2:63
t2:64
t2:65
t2:66
t2:67
t2:68
Smax144
Smax272
SmaE139
Smax187
Smax218
Smax261
SmaE84
SmaE86
Smax194
Smax315
SmaE120
SmaE96
Smax154
Smax159
SmaE127
SmaE61
SmaE99
Smax244
SmaE100
Smax205
Smax283
Smax290
Smax170
Smax220
Smax254
Smax310
Smax158
Smax255
SmaE118
SmaE128
SmaE52
Smax164
Smax189
Smax215
Smax225
SmaE97
SmaE316
Smax231
SmaE117
SmaE82
Smax270
Smax302
SmaE137
Smax183
Smax184
Smax277
SmaE79
Smax180
Smax248
Smax284
SmaE78
Smax191
Smax197
Smax227
SmaE105
SmaE112
SmaE50
SmaE71
Smax276
SmaE72
SmaE167
Smax168
0.823
0.149
0.776
0.069
0.450
0.439
0.781
0.902
0.693
0.368
0.531
0.855
0.942
0.640
0.716
0.707
0.499
0.710
0.549
0.691
0.752
0.725
0.739
0.190
0.779
0.747
0.553
0.506
0.578
0.908
0.045
0.477
0.586
0.333
0.591
0.605
0.736
0.429
0.148
0.638
0.454
0.554
0.790
0.142
0.839
0.734
0.881
0.595
0.853
0.748
0.343
0.506
0.210
0.342
0.632
0.819
0.542
0.695
0.568
0.823
0.290
0.504
0.132
0.040
0.520*
0.016
0.260*
0.111
0.072
0.081
0.050
0.038
0.559*
0.644*
0.0590
0.201*
0.130
0.186
0.043
0.405*
0.240
0.035
0.058*
0.096
0.065
0.094
0.117
0.026
0.162
0.038
0.046
0.028
0.012
0.048
0.001
0.085
0.257
0.008
0.046
0.108
0.250
0.103
0.032
0.279
0.240
0.071
0.153
0.022
0.069
0.030
0.053
0.318*
0.444
0.227
0.290
0.058
0.031
0.065
0.088
0.166
0.043
0.077
0.200
0.009
0.758
0.155
0.802
0.021
0.409
0.475
0.595
0.841
0.724
0.118
0.411
0.762
0.914
0.441
0.676
0.757
0.327
0.587
0.501
0.691
0.610
0.687
0.650
0.061
0.701
0.680
0.575
0.505
0.707
0.870
0.022
0.264
0.615
0.410
0.564
0.626
0.754
0.298
0.021
0.593
0.494
0.648
0.784
0.245
0.685
0.788
0.843
0.533
0.781
0.731
0.340
0.697
0.121
0.230
0.586
0.746
0.585
0.664
0.504
0.832
0.000
0.538
0.032
0.192
0.376
0.000
0.068
0.096
0.001
0.007
0.177
0.056
0.482*
0.497*
0.015
0.009
0.140
0.295*
0.053
0.218
0.040
0.045
0.116
0.114
0.025
0.021
0.129
0.049
0.047
0.032
0.182
0.193
0.000
0.195
0.175
0.116
0.245
0.054
0.181
0.428
0.000
0.076
0.033
0.410
0.279
0.391
0.365*
0.054
0.074
0.059
0.081
0.064
0.248
0.405
0.057
0.243
0.076
0.060
0.109
0.098
0.132
0.028
0.000
0.225
0.847
0.041
0.712
0.062
0.406
0.473
0.631
0.897
0.709
0.345
0.505
0.705
0.935
0.448
0.724
0.716
0.328
0.401
0.463
0.626
0.621
0.724
0.663
0.155
0.677
0.576
0.514
0.491
0.635
0.922
0.118
0.558
0.589
0.287
0.591
0.611
0.769
0.462
0.138
0.595
0.345
0.581
0.781
0.154
0.825
0.691
0.859
0.584
0.829
0.752
0.339
0.623
0.271
0.342
0.606
0.789
0.606
0.665
0.621
0.771
0.349
0.504
0.008
0.010
0.648*
0.014
0.126
0.056
0.022
0.094
0.029
0.025
0.440*
0.471*
0.048
0.066
0.059
0.284
0.200
0.099
0.099
0.098
0.039
0.035
0.101
0.192
0.133
0.093
0.012
0.103
0.147
0.119
0.056
0.028
0.115
0.258
0.154
0.174
0.011
0.217
0.057
0.124
0.025
0.398
0.136
0.080
0.267
0.054
0.040
0.212
0.020
0.002
0.005
0.388*
0.020
0.181
0.138
0.019
0.037
0.064
0.211
0.134
0.512*
0.048
0.813
0.160
0.754
0.085
0.442
0.482
0.751
0.911
0.713
0.427
0.293
0.778
0.913
0.425
0.794
0.758
0.229
0.630
0.493
0.629
0.643
0.678
0.747
0.160
0.597
0.562
0.616
0.505
0.488
0.899
0.065
0.287
0.583
0.520
0.628
0.553
0.787
0.441
0.321
0.614
0.428
0.588
0.683
0.022
0.815
0.730
0.847
0.573
0.838
0.766
0.368
0.677
0.196
0.334
0.639
0.755
0.609
0.662
0.574
0.814
0.374
0.443
0.117
0.084
0.557*
0.025
0.065
0.323
0.044
0.171
0.055
0.325
0.667*
0.608*
0.070
0.023
0.014
0.283*
0.052
0.275
0.179
0.002
0.019
0.049
0.041
0.084
0.020
0.033
0.144
0.100
0.070
0.085
0.023
0.060
0.029
0.060
0.074
0.115
0.181
0.013
0.053
0.114
0.118
0.331
0.051
0.000
0.146
0.071
0.152
0.289
0.118
0.092
0.064
0.261
0.111
0.042
0.191
0.021
0.124
0.093
0.109
0.014
0.048
0.129
0.817
0.100
0.776
0.082
0.260
0.499
0.876
0.876
0.698
0.426
0.332
0.767
0.921
0.475
0.762
0.711
0.281
0.611
0.451
0.675
0.672
0.705
0.731
0.172
0.669
0.596
0.593
0.499
0.671
0.920
0.082
0.361
0.605
0.524
0.603
0.675
0.780
0.439
0.195
0.621
0.334
0.598
0.716
0.137
0.819
0.742
0.846
0.530
0.871
0.745
0.320
0.660
0.154
0.192
0.623
0.792
0.609
0.674
0.554
0.807
0.339
0.461
0.081
0.044
0.592*
0.021
0.117
0.127
0.023
0.023
0.194
0.027
0.579*
0.429*
0.029
0.051
0.012
0.296
0.039
0.522*
0.108
0.018
0.023
0.086
0.053
0.093
0.034
0.091
0.175
0.194
0.287*
0.017
0.033
0.180
0.173
0.046
0.070
0.043
0.041
0.288
0.069
0.060
0.252
0.359
0.093
0.068
0.124
0.032
0.040
0.099
0.051
0.049
0.105
0.084
0.080
0.085
0.063
0.033
0.145
0.050
0.210
0.098
0.121
0.031
0.725
0.395
0.711
0.000
0.448
0.496
0.737
0.729
0.592
0.313
0.510
0.641
0.893
0.490
0.722
0.769
0.607
0.605
0.192
0.657
0.724
0.726
0.563
0.333
0.700
0.267
0.313
0.498
0.460
0.806
0.082
0.259
0.525
0.157
0.408
0.491
0.658
0.631
0.126
0.591
0.504
0.410
0.677
0.157
0.765
0.702
0.771
0.505
0.788
0.729
0.282
0.556
0.061
0.543
0.500
0.772
0.397
0.558
0.444
0.657
0.193
0.299
0.190
0.084
0.330
0.000
0.138
0.139
0.086
0.169
0.162
0.088
0.433
0.701*
0.182
0.172
0.116
0.190*
0.111
0.402
0.108
0.029
0.035
0.053
0.171
0.000
0.012
0.034
0.011
0.102
0.138
0.181
0.033
0.035
0.070
0.060
0.084
0.151
0.113
0.207
0.296
0.127
0.115
0.220
0.690*
0.082
0.101
0.098
0.034
0.010
0.022
0.028
0.408
0.250
0.021
0.036
0.167
0.136
0.055
0.082
0.329
0.059
0.338
0.066
324
325
326
327
328
329
330
331
N
C
O
R
O
Locus
t2:6
332
333
Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
334
Q8
335
336
337
338
6
t3:1
t3:2
t3:3
t3:4
Table 3
Pairwise FST values from SNPs (above diagonal) and microsatellites (below diagonal). EC,
BS, NS, CS, AG and FAR are samples for the English Channel, Baltic Sea, North Sea, Cantabric
Sea and Atlantic Galician coast, respectively. P b 0.0033.
t3:5
t3:6
Q1
t3:7
t3:8
t3:9
t3:10
t3:11
339
EC
BS
NS
CS
AG
FAR
Table 5
Outlier analysis based on BayeScan of SNPs in natural populations of turbot. is the locus
specic effect; P is the posterior probability that the locus is under selection and FST is the
xation index.
EC
BS
NS
CS
AG
FAR
Outlier
FST
t5:5
0.034*
0.020*
0.022*
0.025*
0.047*
0.034
0.026*
0.031*
0.030*
0.075*
0.001
0.032*
0.009*
0.015*
0.064*
0.003
0.041*
0.000
0.004
0.067*
0.008
0.043*
0.002
0.003
0.071*
0.046*
0.085*
0.037*
0.041*
0.043*
SmaSNP247
SmaSNP281
SmaSNP314
SmaSNP298
SmaSNP181
2.114
1.432
1.485
1.346
1.316
1.000
0.967
0.985
0.914
0.993
0.0765
0.0469
0.0491
0.0441
0.0412
t5:6
t5:7
t5:8
t5:9
t5:10
365
366
373
Because the outlier analysis was performed with samples from populations living along a temperature cline, it is likely that the presumed
adaptive process is related to differences for this variable or any other
correlated with it. Many environmental variables are dependent on
temperature, including differences in metabolism, the distribution of
food, predators, parasites and competitors. Differences in temperature
as an explanation for the atypical behavior of several markers is consistent with the result that most outliers remained signicant when the
analysis did not include the two atypical samples (BS because of the
low salinity and FAR because of farming), but only those populations living along a temperature gradient (AG, CS, EC, and NS). Although temperature is gradually changing within the Atlantic Ocean, population
genetic structure of turbot appears to be mostly associated with a relatively strong break within the North Sea (Vandamme et al., 2014). Four
of these outliers (Sma22, SmaE7, 2/5TG14 and Sma149) are located at a
growth-related QTL (Snchez-Molano et al., 2011; Rodrguez-Ramilo
et al., 2014). Locus SmaE7 is linked to a gene coding for the receptor
for a broblast growth factor, which is likely involved in adaptation
374
375
355
4. Discussion
356
364
t4:1
t4:2
t4:3
Q2
t4:4
Table 4
Outlier analysis based on BayeScan of the microsatellite loci in all ve turbot populations including the Baltic Sea and the farmed population (5p/BS and 5p/FAR, respectively) and in four
populations excluding the Baltic and the farmed population (4p/noBS-FAR). is the locus specic effect; P is the posterior probability that the locus is under selection and FST is the xation
index. Outliers identied by Vilas et al. (2010) and Vandamme et al. (2014) are indicated as V10 and V14, respectively. Signicance level ***: P N 0.99; **: P = 0.970.99; *: P = 0.910.97.
357
358
359
360
361
362
363
R
O
352
353
350
351
348
349
346
347
344
345
t4:5
342
343
354
340
341
5p/BS
Sma42
Sma117
Sma22
Sma144
Sma147
Sma146
SmaE7
SmaE22
F8I11/8/17
SmaE33
2/5TG14
SmaE84
SmaE137
SmaE112
SmaE167
Sma168
SmaE99
SmaE117
SmaE12
SmaE4
Sma149
Sma142
t4:7
t4:8
t4:9
t4:10
t4:11
t4:12
t4:13
t4:14
t4:15
t4:16
t4:17
t4:18
t4:19
t4:20
t4:21
t4:22
t4:23
t4:24
t4:25
t4:26
t4:27
t4:28
V10
Outlier
t4:6
t5:1
t5:2
t5:3
t5:4
V10
V10V14
V10
V10V14
1.198
1.240
1.541
1.113
1.552
1.333
2.487
0.974
1.071
1.099
1.257
3.016
1.751
1.842
1.911
1.021
1.328
1.636
0.751
1.096
0.546
0.055
5p/FAR
4p/noBS-FAR
FST
FST
FST
***
***
***
***
***
***
***
***
***
***
***
***
***
***
***
**
**
**
*
*
ns
ns
0.0064
0.0649
0.0048
0.0068
0.0887
0.0700
0.1883
0.0520
0.0553
0.0582
0.0656
0.2737
0.1051
0.0038
0.1313
0.0555
0.0774
0.1061
0.0415
0.0584
0.0335
0.0188
1.097
1.508
1.192
0.528
1.854
1.317
2.694
1.384
1.328
1.502
1.401
2.961
1.855
1.140
0.033
1.120
1.773
1.250
1.228
0.127
0.971
0.616
***
***
***
*
***
***
***
***
***
***
***
***
***
**
ns
**
***
ns
**
ns
***
**
0.0122
0.1184
0.0114
0.0203
0.1539
0.1022
0.2611
0.1091
0.1032
0.1187
0.1091
0.3023
0.1552
0.0123
0.0407
0.0904
0.1504
0.1084
0.0115
0.0415
0.0779
0.0573
1.170
1.659
1.354
1.075
2.060
1.552
2.752
1.380
1.410
1.656
1.605
3.227
2.073
1.494
0.047
1.400
1.540
1.459
0.946
0.245
0.994
0.500
*
***
***
***
***
***
***
***
***
***
***
***
***
**
ns
***
***
ns
ns
ns
***
ns
0.0044
0.0631
0.0037
0.0046
0.0940
0.0566
0.1680
0.0500
0.0494
0.0644
0.0594
0.2355
0.0965
0.0034
0.0188
0.0531
0.0627
0.0667
0.0057
0.0210
0.0340
0.0201
Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
367
368
369
370
371
372
376
377
378
379
380
381
382
383
384
385
386
387
388
389
390
391
R
O
Fig. 2. FST outliers identied by BayeScan analysis of the global dataset with ve natural samples (136 SNPs). A log10 Bayes factor (BF) of 1.0, 1.5 and 2.0 corresponds to posterior probabilities that a locus is under selection of 0.91, 0.97 and 0.99, respectively. For a log10BF N 2 the evidence is commonly interpreted as decisive.
409
410
411
412
413
414
415
416
417
418
419
420
421
407
408
405
406
403
404
N
C
O
401
402
399
400
t6:7
Outlier
BS/EC
BS/NS
BS/CS
BS/AG
t6:8
t6:9
t6:10
t6:11
t6:12
SmaSNP247
SmaSNP281
SmaSNP314
SmaSNP298
SmaSNP181
1.000
0.846
0.830
0.963
0.986
0.998
0.711
0.860
0.779
0.995
1.000
0.579
0.967
0.679
0.949
1.000
0.488
0.972
0.859
0.963
423
Table 7
Markers linked to loci likely under selection in turbot. LG is the linkage group in the genetic
map of Bouza et al. (2012). Outliers within the condence interval of QTL for growth
(G) and resistance (R) are indicated.
t7:1
t7:2
t7:3
t7:4
Table 6
Outlier analysis of SNPs between pairs of natural populations of turbot. EC, BS, NS, CS, AG,
and FAR are samples from the English Channel, Baltic Sea, North Sea, Cantabric Sea,
Atlantic Galician coast, and the farmed population, respectively. Posterior probability of
being under selection of ve SNPs identied as outliers in the global analysis is shown.
The remaining six pairwise comparisons (which do not involve BS) revealed no outliers.
397
398
t6:1
t6:2
t6:3
t6:4
t6:5
t6:6
395
396
422
393
394
392
Outlier
LG QTL Annotation
Sma42
Sma117
Sma22
Sma144
Sma147
Sma146
SmaE7
SmaE22
F8I11/8/17
SmaE33
2/5TG14
SmaE84
SmaE137
SmaE112
SmaE167
Sma168
SmaE99
SmaE117
1
21
11
3
6
14
6
12
24
23
19
7
16
22
2
9
9
G
R
R
SmaE12
SmaE4
Sma149
Sma142
SmaSNP247
SmaSNP281
SmaSNP314
SmaSNP298
SmaSNP181
17
8
15
17
13
21
4
G/R
Cathepsin O
Fibrinogen alpha chain-like
Villin-1
T-complex protein 1 subunit gamma-like
Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
424
425
426
427
428
429
430
431
432
433
434
435
436
t7:5
t7:6
t7:7
t7:8
t7:9
t7:10
t7:11
t7:12
t7:13
t7:14
t7:15
t7:16
t7:17
t7:18
t7:19
t7:20
t7:21
t7:22
t7:23
t7:24
t7:25
t7:26
t7:27
t7:28
t7:29
t7:30
t7:31
t7:32
444
445
446
447
448
449
450
451
Q9
452
453
454
455
458
Acknowledgments
538
539
References
548
Alberto, F.J., Derory, J., Boury, C., Frigerio, J.M., Zimmermann, N.E., Kremer, A., 2013.
Imprints of natural selection along environmental gradients in phenology-related
genes of Quercus petraea. Genetics 195, 495512.
lvarez, I., de Castro, M., Gmez-Gesteira, M., Prego, R., 2005. Inter- and intra-annual
analysis of the salinity and temperature evolution in the Galician Ras Baixas-ocean
boundary (northwest Spain). J. Geophys. Res. 110 (C04008).
Barrett, R.D.H., Hoekstra, H.E., 2011. Molecular spandrels: test of adaptation at the genetic
level. Nat. Rev. Genet. 12, 767780.
Beaumont, M.A., 2005. Adaptation and speciation: what can FST tell us? Trends Ecol. Evol.
20, 435440.
Beaumont, M.A., Balding, D.J., 2004. Identifying adaptive genetic divergence among
populations from genome scans. Mol. Ecol. 13, 969980.
Beaumont, M.A., Nichols, R.A., 1996. Evaluating loci for the use in the genetic analysis of
population structure. Proc. Biol. Sci. 263, 16191626.
Bierne, N., 2011. The distinctive footprints of local hitchhiking in a varied environment
and global hitchhiking in a subdivided population. Evolution 64, 32543272.
Bierne, N., Welch, J., Loire, E., Bonhomme, F., David, P., 2011. The coupling hypothesis:
why genome scans may fail to map local adaptation genes. Mol. Ecol. 20, 20442072.
549
550
551
552
553
554
555
556
557
558
559
560
561
562
563
564
565
566
459
460
443
4.2. SNP based outliers and the unique position of the Baltic Sea
441
442
501
502
R
O
457
439
440
456
SmaE117 and SmaE167. Locus SmaE12 was an outlier only when the
analysis included BS or FAR. Nonetheless, this locus showed higher FST
than expected under neutrality when the analysis includes BS and the
opposite pattern when this sample was replaced by FAR. This suggests
that the variation at SmaE12 is driven in opposite directions by these
two populations under different evolutionary pressures, including
those potentially imposed by differences in salinity and growth rate.
This marker is closely linked to the gene coding for the trap alphatranslocon protein, which is related to membrane processes (Vilas
et al., 2010). An explanation for these contrasting patterns is the adaptation to varying conditions of salinity, negatively affecting the reproductive success. Consistent with this hypothesis, it has been observed
that eggs of turbot from the Baltic populations have high survival rates
in salinities between 10 and 15, conditions under which no or
only low survival occurs among the turbot from the North Sea (Karas
and Klingsheim, 1997; Nissling et al., 2006). Recent observations suggest that selection for a high fecundity result in lower somatic growth
in the Baltic Sea (Nissling et al., 2013). However, as in the case of temperature, it is likely that other environmental factors correlated with
differences in salinity may be operating (Vandamme et al., 2014).
437
438
Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
503
504
505
506
507
508
509
510
511
512
513
514
515
516
517
518
519
520
521
522
523
524
525
526
527
528
529
530
531
532
533
534
535
536
537
540
541
542
543
544
545
546
547
N
C
O
R
O
Nielsen, E.E., Hemmer-Hansen, J., Larsen, P.F., Bekkevold, D., 2009. Population genomics of
marine shes: identifying adaptive variation in space and time. Mol. Ecol. 18,
31283150.
Nissling, A., Johansson, U., Jacobsson, M., 2006. Effects of salinity and temperature conditions on the reproductive success of turbot (Scophthalmus maximus) in the Baltic Sea.
Fish. Res. 80, 230238.
Nissling, A., Florin, A.B., Thorsen, A., Bergstrm, U., 2013. Egg production of turbot,
Scophthalmus maximus, in the Baltic Sea. J. Sea Res. 84, 7786.
Nosil, P., Funk, D.J., Ortiz-Barrientos, D., 2009. Divergent selection and heterogeneous genomic divergence. Mol. Ecol. 18, 375402.
Oh, J.H., Moon, H.B., Choe, E.S., 2009. Changes in differentially expressed genes in the liver
of Oryzias latipes by binary exposure to carcinogenic polycyclic aromatic hydrocarbons. Kor. J. Environ. Biol. 27, 391396.
Orsini, L., Spanier, K.I., De Meester, L., 2012. Genomic signature of natural and anthropogenic stress in wild populations of the waterea Daphnia magna: validation in space,
time and experimental evolution. Mol. Ecol. 21, 21602175.
Pardo, B.G., Hermida, M., Fernndez, C., Bouza, C., Prez, M., Llavona, A., Snchez, L.,
Martnez, P., 2006. A set of highly polymorphic microsatellites useful for kinship
and population analysis in turbot (Scophthalmus maximus L.). Aquac. Res. 37,
15781582.
Pardo, B.G., Fernndez, C., Hermida, M., Vzquez-Lpez, A., Prez, M., Presa, P., Calaza, M.,
lvarez-Dios, J.A., Comesaa, A.S., Raposo-Guilln, J., Bouza, C., Martnez, P., 2007. Development and characterization of 248 novel microsatellites markers in turbot
(Scophthalmus maximus). Genome 50, 329332.
Pereiro, P., Balseiro, P., Romero, A., Dios, S., Forn-Cuni, G., Fuste, B., Planas, J.V., Beltrn, S.,
Novoa, B., Figueras, A., 2012. High throughput sequence analysis of turbot
(Scophthalmus maximus) transcriptome using 454-pyrosequencing for the discovery
of antiviral immune genes. Plos One 7 (e35369).
Raymond, M., Rousset, F., 1995. GENEPOP (version 1.2): population genetics software for
exact test and ecumenicism. J. Hered. 86, 248249.
Ribas, L., Pardo, B.G., Fernndez, C., lvarez-Dios, J.A., Gmez-Tato, A., Quiroga, M.I., Planas,
J.V., Sitja-Bobadilla, A., Martnez, P., Piferrer, F., 2013. A combined strategy involving
Sanger and 454 pyrosequencing increases genomic resources to aid in the management of reproduction, disease control and genetic selection in the turbot
(Scophthalmus maximus). BMC Genomics 14, 180.
Robertson, A., 1975. Remarks on the LewontinKrakauer test. Genetics 80, 396.
Rodrguez-Ramilo, S.T., Toro, M.A., Bouza, C., Hermida, M., Pardo, B.G., Cabaleiro, S.,
Martnez, P., Fernndez, C., 2011. QTL detection for Aeromonas salmonicida resistance
related traits in turbot (Scophthalmus maximus). BMC Genomics 12, 541.
Rodrguez-Ramilo, S.T., Fernndez, J., Toro, M.A., Bouza, C., Hermida, M., Fernndez, C.,
Pardo, B.G., Cabaleiro, S., Martnez, P., 2013. Uncovering QTL for resistance and survival time to Philasterides dicentrarchi in turbot (Scophthalmus maximus). Anim. Genet.
44, 149157.
Rodrguez-Ramilo, S.T., De la Herrn, R., Ruiz-Rejn, C., Hermida, M., Fernndez, C.,
Pereiro, P., Figueras, A., Bouza, C., Toro, M.A., Martnez, P., Fernndez, J., 2014. Identication of quantitative trait loci associated to resistance to viral haemorrhagic
septicaemia (VHS) in turbot (Scophthalmus maximus): a comparison between bacterium, parasite and virus diseases. Mar. Biotechnol. http://dx.doi.org/10.1007/s10126013-9544-x.
Roelofs, D., Morgan, J., Sturzenbaun, S., 2010. The signicance of genome-wide transcriptional regulation in the evolution of stress tolerance. Evol. Ecol. 24, 527539.
Roesti, M., Hendry, A.P., Salzburger, W., Berner, D., 2012. Genome divergence during evolutionary diversication as revealed in replicate lake-stream stickleback population
pairs. Mol. Ecol. 21, 28522862.
Rogers, S.M., Bernatchez, L., 2005. Integrating QTL mapping and genome scans towards
the characterization of candidate loci under parallel selection in the lake whitesh
(Coregonus clupeaformis). Mol. Ecol. 14, 351361.
Rogers, S.M., Bernatchez, L., 2007. The genetic architecture of ecological speciation and
the association with signatures of selection in natural lake whitesh (Coregonus sp.,
Salmonidae) species pairs. Mol. Biol. Evol. 24, 14231438.
Snchez-Molano, E., Cerna, A., Toro, M.A., Bouza, C., Hermida, M., Pardo, B.G., Cabaleiro, S.,
Fernndez, C., Martnez, P., 2011. Detection of growth-related QTL in turbot
(Scophthalmus maximus). BMC Genomics 12, 473.
Schltterer, C., 2002. A microsatellite-based multilocus screen for the identication of
local selective sweeps. Genetics 160, 753763.
Schoville, S.D., Bonin, A., Franois, O., Lobreaux, S., Melodelima, C., Manel, S., 2012. Adaptive genetic variation on the landscape: methods and cases. Annu. Rev. Ecol. Evol.
Syst. 43, 2343.
Slate, J., 2005. Quantitative trait locus mapping in natural populations: progress, caveats
and future directions. Mol. Ecol. 14, 363379.
Stankus, S., 2003. The peculiarities of turbot (Psetta maxima L.) biology and their role in
the ecosystem of the Baltic Sea coastal zone of Lithuania. Acta Zool. Lit. 13, 217238.
Stinchcombe, J.R., Hoekstra, H.E., 2007. Combining population genomics and quantitative
genetics: nding the genes underlying ecologically important traits. Heredity 100,
158170.
Storz, J.F., 2005. Using genome scans of DNA polymorphism to infer adaptive population
divergence. Mol. Ecol. 14, 671688.
Suzuki, N., Nishida, M., Yoseda, K., stnda, C., ahin, T., Amaoka, K., 2004. Phylogeographic relationships within the Mediterranean turbot inferred by mitochondrial
DNA haplotype variation. J. Fish Biol. 65, 580585.
Tsakas, S., Krimbas, C.B., 1976. Testing heterogeneity of F-values: suggestion and a correction. Genetics 84, 399401.
Vandamme, S.G., Maes, G., Raeymaekers, J., Cottenie, K., Imsland, A.K., Hellemans, B.,
Lacroix, G., Mac Aoidh, E., Martinsohn, J., Martnez, P., Robbens, J., Vilas, R.,
Volckaert, F., 2014. Environmental selective pressure reinforces historical differentiation in turbot (Scophthalmus maximus). Mol. Ecol. 23, 618636.
Bierne, N., Roze, D., Welch, J., 2013. Pervasive selection or is it? Why are FST outliers
sometimes so frequent? Mol. Ecol. 22, 261264.
Blanquer, A., Alayse, J.P., Berrada-Rkhami, O., Berrebi, P., 1992. Allozyme variation in
turbot (Psetta maxima) and brill (Scophthalmus rhombus) (Osteichtyes,
Pleuronectiformes, Scophthalmidae) throughout their range in Europe. J. Fish Biol.
41, 725736.
Bouza, C., Snchez, L., Martnez, P., 1997. Gene diversity analysis in natural populations
and cultured stocks of turbot (Scophthalmus maximus L.). Anim. Genet. 28, 2836.
Bouza, C., Presa, P., Castro, J., Snchez, L., Martnez, P., 2002. Allozyme and microsatellite
diversity in natural and domestic populations of turbot (Scophthalmus maximus) in
comparison with other Pleuronectiformes. Can. J. Fish. Aquat. Sci. 59, 14601473.
Bouza, C., Hermida, M., Pardo, B.G., Fernndez, C., Fortes, G.G., Castro, J., Snchez, L., Presa,
P., Prez, M., Sanjun, A., de Carlos, A., lvarez-Dios, J.A., Ezcurra, S., Cal, R.M., Piferrer,
F., Martnez, P., 2007. A microsatellite genetic map of turbot (Scophthalmus maximus).
Genetics 177, 24572467.
Bouza, C., Hermida, M., Milln, A., Vilas, R., Vera, M., Fernndez, C., Calaza, M., Pardo, B.G.,
Martnez, P., 2008. Characterization of EST-derived microsatellites for gene mapping
and evolutionary genomics in turbot. Anim. Genet. 39, 666670.
Bouza, C., Hermida, M., Pardo, B.G., Vera, M., Fernndez, C., de la Herrn, R., Navajas-Prez,
R., lvarez-Dios, J.A., Gmez-Tato, A., Martnez, P., 2012. An Expressed Sequence Tag
(EST)-enriched genetic map of turbot (Scophthalmus maximus): a useful framework
for comparative genomics across model and farmed teleosts. BMC Genet. 13, 54.
Bowden, T.J., 2008. Modulation of the immune system of sh by their environment. Fish
Shellsh Immunol. 25, 373383.
Campbell, P.M., Devlin, R.H., 1997. Increased CYP1A1 and ribosomal protein L5 gene
expression in a teleost: the response of juvenile Chinook salmon to coal dust
exposure. Aquat. Toxicol. 38, 115.
Colosimo, P.F., Hosemann, K.E., Balabhadra, S., Villareal, G., Dickson, M., Grimwood, J.,
Schmutz, J., Myers, R.M., Schluter, D., Kingsley, D.M., 2005. Widespread parallel
evolution in sticklebacks by repeat xation of ectodysplasin alleles. Science 307,
19281933.
Coughlan, J.P., Imsland, A.K., Galvin, P.T., Fitzgerald, R.D., Naevdal, G., Cross, T.F., 1998.
Microsatellite DNA variation in wild populations and farmed strains of turbot from
Ireland and Norway: a preliminary study. J. Fish Biol. 52, 916922.
DeFaveri, J., Viitaniemi, H., Leder, E., Meril, J., 2013. Characterizing genic and nongenic
molecular markers: comparison of microsatellites and SNPs. Mol. Ecol. Resour. 13,
377392.
Florin, A.B., Hglund, J., 2007. Absence of population structure of turbot (Psetta maxima)
in the Baltic Sea. Mol. Ecol. 16, 115126.
Foll, M., Gaggiotti, O., 2008. Estimating selection with different markers and varying
demographic scenarios: a Bayesian perspective. Genetics 180, 977993.
Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and xation
indices (version 2.9.3). Available from. http://www.unil.ch/izea/softwares/fstat.html.
Handley-Goldstone, H.M., Grow, M.W., Stegeman, J.J., 2005. Cardiovascular gene
expression proles of dioxin exposure in zebrash embryos. Toxicol. Sci. 85,
683693.
Hansen, M.M., Olivieri, I., Waller, D.M., Nielsen, E.E., GeM Working Group, 2012.
Monitoring adaptive genetic responses to environmental change. Mol. Ecol. 21,
13111329.
HELCOM, 2003. The Baltic marine environment 19992002. Balt. Sea Environ. Proc. N 87.
HELCOM, 2011. The fth Baltic Sea pollution load compilation (PLC-5). Balt. Sea Environ.
Proc. No. 128.
Hemmer-Hansen, J., Therkildsen, N.O., Meldrup, D., Nielsen, E.E., 2014. Conserving marine
biodiversity: insights from life-history trait candidate genes in Atlantic cod (Gadus
morhua). Conserv. Genet. 15, 213228.
Hermida, M., Bouza, C., Fernndez, C., Sciara, A.A., Rodrguez-Ramilo, S.T., Fernndez, J.,
Martnez, P., 2013. Compilation of mapping resources in turbot (Scophthalmus
maximus): a new integrated consensus genetic map. Aquaculture 414, 1925.
Hoffman, A.A., Willi, Y., 2008. Detecting genetic responses to environmental change. Nat.
Rev. Genet. 9, 421432.
Hong, B., Swaney, D.P., Mrth, C.M., Smedberg, E., Hgg, H.E., Humborg, C., Howarth, R.W.,
Bouraoui, F., 2012. Evaluating regional variation of net anthropogenic nitrogen and
phosphorus inputs (NANI/NAPI), major drivers, nutrient retention pattern and
management implications in the multinational areas of Baltic Sea basin. Ecol.
Model. 227, 17135.
Iglesias, R., Param, A., lvarez, M.F., Leiro, J., Fernndez, J., Sanmartn, M.L., 2001.
Philasterides dicentrarchi (Ciliophora: Scuticociliatida) as the causative agent of the
scuticociliatosis in farmed turbot Scophthalmus maximus in Galicia (NW Spain). Dis.
Aquat. Org. 46, 4755.
Imsland, A.K., Sunde, L.M., Folkvord, A., Stefansson, S.O., 1996. The interaction of
temperature and sh size on growth of juvenile turbot. J. Fish Biol. 49, 926940.
Johanneson, K., Andre, C., 2006. Life on the margin: genetic isolation and diversity loss in a
peripheral marine ecosystem, the Baltic Sea. Mol. Ecol. 15, 20132029.
Karas, P., Klingsheim, V., 1997. Effects of temperature and salinity on embryonic
development of turbot (Scophthalmus maximus L.) from the North Sea, and
comparisons with Baltic populations. Helgol. Mar. Res. 51, 241247.
Lewontin, R., Krakauer, J., 1973. Distribution of gene frequency as a test of the theory of
the selective neutrality of polymorphisms. Genetics 74, 175195.
Luikart, G., England, P.R., Tallmon, D., Jordon, S., Taberlet, P., 2003. The power and promise
of population genomics: from genotyping to genome typing. Nat. Rev. Genet. 4,
981994.
Nei, M., Maruyama, T., 1975. LewontinKrakauer test for neutral genes. Genetics 80, 395.
Nielsen, E.E., Nielsen, P.H., Meldrup, D., Hansen, M.M., 2004. Genetic population structure
of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones
for marine shes in the transition zone between the Baltic Sea and the North Sea.
Mol. Ecol. 13, 585595.
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Please cite this article as: Vilas, R., et al., A genome scan for candidate genes involved in the adaptation of turbot (Scophthalmus maximus), Mar.
Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
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Vasemgi, A., Primmer, C.R., 2005. Challenges for identifying functionally important genetic variation: the promise of combining complementary research strategies. Mol.
Ecol. 14, 36233642.
Vera, M., lvarez-Dios, J.A., Milln, A., Pardo, B.G., Bouza, C., Hermida, M., Fernndez, C., de
la Herrn, R., Molina-Luzn, M.J., Martnez, P., 2011. Validation of single nucleotide
polymorphism (SNP) markers from an immune Expressed Sequenced Tag (EST)
turbot (Scophthalmus maximus) data base. Aquaculture 313, 3141.
Vera, M., lvarez-Dios, J.A., Fernndez, C., Bouza, C., Vilas, R., Martnez, P., 2013.
Development and validation of single nucleotide polymorphisms (SNPs) markers
from two transcriptomic 454-run of turbot (Scophthalmus maximus) using high
throughput genotyping. Int. J. Mol. Sci. 14, 56945711.
Vilas, R., Bouza, C., Vera, M., Milln, A., Martnez, P., 2010. Variation in anonymous and
EST-microsatellites suggests adaptive population divergence in turbot. Mar. Ecol.
Prog. Ser. 420, 231239.
Vitalis, R., Dawson, K., Boursot, P., 2001. Interpretation of variation across marker loci as
evidence of selection. Genetics 158, 18111823.
Weir, B.S., Cockerham, C.C., 1984. Estimating F-statistics for the analysis of population
structure. Evolution 38, 13581370.
R
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Genomics (2015), http://dx.doi.org/10.1016/j.margen.2015.04.011
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