Kitada Et Al-2017-Panmixia Scomberomorus Niphonius

Journal of Fish Biology (2017)
doi:10.1111/jfb.13466, available online at wileyonlinelibrary.com
Population panmixia and demographic expansion

of a highly piscivorous marine fish Scomberomorus
niphonius
S. Kitada*, K. Nakajima and K. Hamasaki
Graduate School of Marine Science and Technology, Tokyo University of Marine Science
and Technology, Konan, Minato, Tokyo, 108-8477, Japan
(Received 14 November 2016, Accepted 17 August 2017)
Population structure and demographic history of the Japanese Spanish mackerel Scomberomorus
niphonius a highly piscivorous and migratory marine fish, were assessed using mitochondrial DNA
control region sequences (n = 720) and microsatellite genotypes at five loci (n = 1331) for samples
collected on Japanese coasts from 2001 to 2010. The population structure was panmictic and the
haplotype and allele frequencies were temporally stable even during the recent recovery process.
Demographic expansion was strongly supported throughout the Pleistocene, suggesting that the
oscillating glacial and interglacial climate conditions in the Pleistocene had no substantial impact on
the demographic history of S. niphonius.
2017 The Fisheries Society of the British Isles
Key words: Pleistocene; recruitment variation; stable population structure; type III survivorship.
INTRODUCTION
The Pleistocene glaciations were the most significant historical events to affect the
evolution of most extant species (Bernatchez & Wilson, 1998). Repeated glaciation
events in the Pleistocene had substantial effects on the population dynamics of freshwa-
ter and coastal marine fish species (Bernatchez & Wilson, 1998; Avise, 2000; Wilson &
Veraguth, 2010). Recent demographic studies with mitochondrial (mt)DNA sequences
have reported the demographic expansion of the Pacific herring Clupea pallasii Valen-
ciennes 1847 throughout the Pleistocene glaciation, since 630 000935 000 years
before present (B.P.) (Liu et al., 2011) and 710 000870 000 B.P. (Fujita et al., 2017).
The time of expansion of other marine fish has been estimated at 141 000 B.P.
for Japanese sea bass Lateolabrax japonicus (Cuvier 1828) (Liu et al., 2006),
67 000404 000 B.P. for Liza haematocheila (Temminck & Schlegel 1845) (Liu et al.,
2007), 16 00034 000 B.P. for black scorpionfish Scorpaena porcus L. 1758 in the
Mediterranean and the Black Seas (Boissin et al., 2016) and 480 000600 000 B.P. for
Monterey Spanish mackerel Scomberomorus concolor (Lockington 1879) in the Gulf
of California (Domnguez-Lpez et al., 2015). That of the Japanese Spanish mackerel,
Scomberomorus niphonius (Cuvier 1831) at 148 000503 000 B.P. and a panmictic
*Author to whom correspondence should be addressed. Tel.: +81 5463 0536; email: kitada@kaiyodai.ac.jp
1
2017 The Fisheries Society of the British Isles
2 S . K I TA D A E T A L.
38
45
Bohai
Sea Western Sea of Japan
40
Sea of Japan
36
Yellow East China
35
Sea SetoInland Sea (SIS)

Sea
3 2 1
East China Pacific Ocean 4
34
Sea
30
25
32
125 130 135 140 145 Pacific Ocean
30 128 130 132 134 136
Fig. 1. Sampling sites for Scomberomorus niphonius in Japanese waters. , The boundaries between sampling
areas. Samples from the Seto Inland Sea: , SIS_1 and , SIS_2. , Tosa Bay (TSB); , Shibushi Bay (SBS);
, Kasasa (KSA); , Ise Bay (ISB); , Wakasa Bay (WKB); , Goto (GOT).
gene pool were reported in the East China and Yellow Seas using mtDNA control
region (CR) sequences (Shui et al., 2009). Thus, precedent demographic studies of
marine fish consistently estimated that the demographic expansion has occurred in
the late Pleistocene or the last glacial maximum (LGM, c. 23 00018 000 years B.P.,
Bernatchez & Wilson, 1998).
Scomberomorus niphonius is a large piscivorous marine fish distributed in the East
China Sea, Yellow Sea and off western Japan and is an important fishery resource
for China, Korea and Japan. They spawn along the coasts of the East China, Yellow
and Bohai Seas (Shui et al., 2009) and in the Seto Inland Sea (SIS), Japan (Fig. 1).
Scomberomorus niphonius catches have substantially varied in the Japanese coasts dur-
ing the past 5 decades (Fig. 2). The SIS is the main spawning ground for the Japanese
S. niphonius population; the fisheries target high-value mature fish in the spawning
grounds during spring and early summer. The catch has decreased markedly since
1987 in the SIS and S. niphonius stock enhancement programme was initiated by fish-
ery agency in 1998 (Nakajima et al., 2013). In contrast, on the Japanese coasts of East
China Sea, Pacific Ocean and western Japan Sea, where no stock enhancement has ever
been carried out, fisheries mainly target young fish. The catch of S. niphonius started
to increase after c. 2000 in all areas. A genetic study on the Japanese S. niphonius pop-
ulations focused on the genetic effects of hatchery-releases on wild populations in the
SIS (Nakajima et al., 2014a), but the demographic history of S. niphonius populations
have not been fully investigated.
Many marine fish have very high fecundity and spawn huge numbers of eggs in their
respective spawning grounds. Mortality is very high during the pelagic larval phase
(so called type III survivorship) and survival may depend on food availability and
the environment at the time and place of spawning and hatching (Hauser & Carvalho,
2008). Such recruitment processes come under the matchmismatch hypothesis (Cush-
ing, 1990). A meta-analysis of recruitment dynamics for worldwide marine fisheries
suggested that environmental factors have a stronger influence on recruitment than
2017 The Fisheries Society of the British Isles, Journal of Fish Biology 2017, doi:10.1111/jfb.13466
D E M O G R A P H Y O F S C O M B E RO M O RU S N I P H O N I U S 3
20
15
Catch (1 000 tonnes)
10
1970 1980 1990 2000 2010
Fig. 2. Annual commercial catches of Scomberomorus niphonius 19642016 in four major fishing areas in Japan.
, Sampling years for genetic monitoring in the Seto Inland Sea ( ); , sampling years for genetic
monitoring in the East China Sea ( ), Pacific Ocean ( ), and western Sea of Japan ( ).
spawning biomass does (Szuwalski et al., 2015) and variation in local environmental
conditions may result in random sweepstake reproductive recruitment (Hedgecock,
1994). Scomberomorus niphonius is highly fecund and exhibits type III survivorship
with matchmismatch recruitment (Shoji et al., 2002; Shoji & Tanaka, 2006). Such
recruitment variations may affect the gene frequencies in populations and reproduc-
tive skews may result in multiple mergers in the genealogy as has been reported in
the Japanese sardine (Niwa et al., 2016). On the other hand, contemporary genetic
diversity and population structure may have been affected by historical demography
(Marko & Hart, 2011), particularly for species affectd by repeated glacial events over
the last 2 000 000 years (Provan & Bennett, 2008). Therefore, it is very important to
consider the effect of historical processes in the assessment of current population struc-
ture (Boissin et al., 2016; Portnoy et al., 2014).
In this study, the population structure and demographic history of S. niphonius were
estimated, based on spatiotemporal samples collected over its entire distribution range
in Japanese waters during 20012010. The results highlight the temporally stable,
panmictic genetic population structure of S. niphonius, even though the population is
currently in recovery and the demographic expansion throughout the Pleistocene.
MATERIALS AND METHODS
S E Q U E N C E A N D M I C R O S AT E L L I T E D ATA
Publicly available mtDNA-CR sequences (305 bp without gaps and missing data, n = 720) and
microsatellite genotypes at five loci (n = 1331) in wild S. niphonius were used (Nakajima et al.,
2014a, 2014bb), excluding the sample collected in South Korea and those of hatchery-reared fish
Table I. Summary statistics for each Scomberomorus niphonius sample collected in western
Japan
Sampling Sampling
locality date Age mtDNA microsatellite
(Abbreviation) (years) n H h n A AR Ho He
Seto Inland Sea MayJun 2001 Mature* 46 16 0854 00052 246 216 181 0741 0742
(SIS_1)
Seto Inland Sea AprJun 2010 25 (mature) 330 63 0846 00062 315 234 181 0757 0745
(SIS_2)
Tosa Bay (TSB) JanApr 2006 01 40 18 0833 00059 95 176 176 0756 0747
Shibushi Bay Dec 2005 0 36 18 0841 00068 121 178 169 0716 0751
(SBS)
Kasasa (KSA) Dec 2005 0 34 15 0820 00046 98 188 186 0710 0739
Ise Bay (ISB) AugSep 2005 0 120 33 0865 00060 164 204 181 0723 0755
Wakasa Bay Dec 2006 0 74 24 0845 00051 140 198 177 0767 0749
(WKB)
Goto (GOT) Dec 2005 0 40 16 0821 00048 152 214 191 0728 0745
n, Sample size; H, number of haplotypes; h, haplotype diversity; , nucleotide diversity; A, number of alleles; AR, allelic
richness; H O , observed heterozygosity; H E , expected heterozygosity. * 56106 cm fork length.
from the original data. All loci were scored by capillary electrophoresis using an ABI PRISM
3130xl Genetic Analyzer (Applied Biosystems; www.apliedbiosystems.com) with fluorescent
dye-labelled primers and there was no evidence for scoring error caused by stuttering, large allele
dropout, or null alleles (Nakajima et al., 2014a). The samples were collected from major distri-
bution areas in Japan during 20012010 (Table I and Fig. 1). In the SIS, six samples of mature
35 year old fish (56106 cm in fork length, LF ) were collected from four spawning grounds,
Osaka Bay, Harima-nada and Hiuchi-nada in 20012002 and Harima-nada, Hiuchi-nada and
Bisan-seto in 2010 (Table I and Fig. 1). The sample included some 2 year old fish, but they were
matured. As no significant difference was found in the haplotype and allele frequencies (Naka-
jima et al., 2014a) by an exact test for population differentiation (Raymond & Rousset, 1995),
the samples were combined within each sampling period and denoted as SIS_1 and SIS_2,. The
other samples were young immature fish collected in Tosa Bay (TSB), Shibushi Bay (SBS),
Kasasa (KSA), Ise Bay (ISB), Wakasa Bay (WKB) and Goto Island (GOT).
DATA ANALYSIS
The haplotypes were defined based on the sequence data excluding the invariable sites (254,
833%). The number of haplotypes, haplotype diversity (Nei, 1987) and nucleotide diversity
(Tajima, 1983; Nei, 1987) were estimated using DnaSP 5.1 (Librado & Rozas, 2009). The
exact test (Raymond & Rousset, 1995) for differences in haplotype frequencies was performed
in Arlequin 3.5 (Excoffier & Lischer, 2010). An unrooted maximum-likelihood tree of the
individual mtDNA-CR sequences was constructed under the best fit nucleotide substitution
model with minimum values of corrected Akaike information criterion (AICc) (Akaike,
1973) and the Bayesian information criterion (BIC) (Schwarz, 1978) in MEGA 7 (Kumar
et al., 2016). Genealogical relationships between haplotypes were examined by constructing
haplotype networks using a median-joining method (Bandelt et al., 1999) in Network 5 (www
.fluxus-engineering.com).
Linkage disequilibrium and conformation to HardyWeinberg equilibrium (HWE) was tested
in GENEPOP 4.2 (Raymond and Rousset, 1995) with 10 000 dememorisations, 100 batches
and 10 000 iterations. Allelic richness and heterozygosity were calculated for each locus and
population in FSTAT 2.9.3.2 (Goudet, 1995) and Arlequin 3.5.1.3, respectively. The samples
were rarefied to the smallest sample size to determine allelic richness (n = 95). An exact test
for population differentiation was also performed for the allele frequencies. The false discovery
rate (FDR) in multiple testing was controlled by the method of Benjamini & Yekutieli (2001)
using R function p.adjust (P < 005). Genetic differentiation between populations was estimated
in terms of F ST for both the haplotype and allele frequencies, based on the empirical Bayes
(EB) F ST estimator (EBF ST ) (Kitada et al., 2007) for high gene flow species (Kitada et al.,
2017) using FinePop 1.3.0 R package (www.r-project.org). Neighbour-joining unrooted phylo-
genetic trees (Saitou & Nei, 1987) were visualized in FigTree (http://tree.bio.ed.ac.uk/software/
figtree/) based on the pairwise EBF ST values. Structure 2.3.4 (Pritchard et al., 2000) analyses
were implemented given K = 1, , 5 with a burn-in period of 50 000 and 500 000 Markov chain
Monte-Carlo replicates under the correlated allele frequency model.
The historical demographic equilibrium of the mtDNA-CR was tested using Tajimas D
(Tajima, 1989) and Fus Fs (Fu, 1997) and the mismatch distribution reflecting the distribution
of pairwise differences between sequences (Rogers & Harpending, 1992) was estimated in
Arlequin 3.5. The time since population expansion was estimated using the equation = 2ut
(Rogers & Harpending, 1992), where u is the mutation rate for the whole DNA sequence
under study and t is the time since expansion. Here, u = number of bases sequences and
is the mutation rate per site. The estimated mutation rate of 28% ( = 0 028) per site per
million years (therefore, u = 0028 305 bp) was used for the mtDNA-CR of the S. concolor
(Domnguez-Lpez et al., 2015), the same genus S. niphonius. BEAST2 (Bouckaert et al.,
2014) was used to create the Bayesian skyline plot (BSP) (Drummond et al., 2005) to infer
changes in effective population size (N e ) under the mutation rate ( = 0 028). To consider
the effect of molecular rate estimates on population history (Ho et al., 2005), was considered
additionally an alternative rate that is one-tenth slower ( = 0 0028 per site per 106 years)
following the method of Liu et al., (2011). A run of 4 108 iterations with a burn-in of 4 107
was carried out under the HKY model (Hasegawa et al., 1987) as a molecular clock model.
Genealogies and model parameters were sampled every 50 000 iterations. All of the operators
were optimised automatically. The BSP were generated in Tracer 1.6 (http://tree.bio.ed.ac.uk/
software/tracer/).
RESULTS
The sequence comparisons yielded 92 haplotypes from 720 individuals (Supporting
Information Table SI). The most common haplotype SIS_2 (365%) was found in 263
individuals, but 38 individuals (53%) had a singleton haplotype. Haplotype diversity
was high, ranging from 0820 to 0854 and nucleotide diversity ranged from 000463
to 000680 (Table I). The haplotype frequency distributions were very similar in all
samples collected in different localities and years and the temporal samples SIS_1
and SIS_2 collected in 20012002 and 2010 also had similar haplotype frequencies
(Supporting Information Fig. S1). The haplotype frequencies were significantly
homogeneous for all samples and temporally stable in the SIS (Table II). The best fit
substitution model was T92 + G + I (Tamura, 1992; BIC = 19 8885, AICc = 50658)
followed by HKY + G + I (Hasegawa et al., 1987; BIC = 19 9139, AICc = 50707)
and TN93 + G + I (Tamura, 1992; BIC = 19 9226, AICc = 50691) and the unrooted
maximum-likelihood tree for 720 sequences had four major nodes with multiple
mergers despite any substitution models used out of 24 models compared (Supporting
Information Fig. S2). A star-like network diagram of the 92 haplotypes identified no
clustering and each sampling locality shared major haplotypes (Fig. 3).
The linkage equilibrium was held for all pairs of loci in all localities except three com-
binations out of 80 pairs of loci in SIS_1 and GTO (Supporting Information Table SII).
The mean number of alleles over loci ranged between 176 and 234 and allelic rich-
ness ranged between 169 and 191 and observed heterozygosity (H O = 07100767)
Table II. Significance for the pairwise difference tests on microsatellite allele (above diago-
nal) and halotype frequencies (below diagonal) in Scomberomorus niphonius. Significance after
controlling the false discovery rate (P < 005) are shown in bold (for locality abbreviations, see
Table I)
Locality SIS_1 SIS_2 TSB SBS KSA ISB WKB GTO

SIS_1 000000 013446 000020 001885 090641 001461 033776
SIS_2 073075 000000 000000 000000 000000 000001 000000
TSB 039486 011592 000356 013695 035428 016223 046121
SBS 012752 030416 027421 086622 001868 006741 066409
KSA 067870 067601 086525 094645 040488 007904 065812
ISB 048071 042375 003369 007744 064884 005543 072612
WKB 041360 049331 021829 038074 097624 007774 038087
GTO 047358 097343 018009 080144 095891 071720 094286
was similar with expected heterozygosity (H E = 07420755) (Table I). All sam-
pling localities were in HWE under controlling the FDR and all loci also met with
HWE except Sni21 locus, where only ISB departed from HWE (Supporting Informa-
tion Table SIII). HWE also held in the SIS when genotypes of SIS_1 and SIS_2 were
combined. The allele frequencies were homogeneous in all localities except SIS_2 and
SBS when all loci combined (Table II). The SIS_2 was statistically different from
others at Sni21 and Sni29 loci and the SBS was different from SIS_1 and TSB only at
Sni13 locus, but all localities were homogeneous at Sni24 and Sni26 loci (Supporting
Information Tables SIVSVI). The allele frequency distributions were stable in all
localities at all loci (Supporting Information Table SVII and Fig. S3).
The mean s.d. F ST values between pairs of populations were very small at
00000227 00000003 for mtDNA and 000056 000014 microsatellite (Table
III). The neighbour-joining unrooted trees of pairwise F ST values showed a con-
sistent population structure for both markers (Fig. 4). SBS and SIS_2 located
apart from other populations, but even the largest F ST value was very small at
00000235 for mtDNA and 0001018 for microsatellites, respectively. Structure
analyses found a panmixia with the likelihood values of 27 0713 (maximum) for
K = 1 and 27 1573, 27 3461, 27 8952 and 28 6623 for K = 2, 3, 4 and 5,
respectively.
Tajimas D (20316, P < 0001) and Fus Fs (266577, P < 0001) gave strong sup-
port to S. niphonius demographic expansion and the unimodal mismatch distribution
fitted the sudden expansion model well (P < 0001) [Fig. 5(a)]. In the analysis, the
sequences were combined for all localities because the haplotype frequencies were
homogeneous in all samples (Table II). The time of population expansion (with its
95% C.I. in parentheses) was estimated at 205 000 (183 000220 000) B.P. in late Pleis-
tocene, based on the estimate of , = 1750 (15621875) under the mutation rate of
= 0 028. Assuming the slower mutation rate ( = 0 0028), the time of population
expansion was 2 050000 (1 830 0002 200 000) B.P. in the Upper Pleistocene. The
BSP analysis obtained the effective sample size for all parameters 237 and indicated
a continuous population expansion before the LGM [Fig. 5(b)].
H_67
11
H_89 H_52 22 108
78 H_29
26
H_27
H_84 H_32
H_34 100
mv5 H_70 H_24
H_51 H_55 52
298 H_31
26H_68 116 H_92
H_50 90 49 273H_60 H_82
193 78 97
113 32 142
116 mv9 100 114 H_15
53
51 H_33 97 H_9 H_26 H_74 H_17
97 53 53
mv2 50
H_13 51H_49 H_37 H_28 97 H_57 mv6
116 H_5 97
81 H_77 116 H_21 83 116 133 H_36
67 22 H_80
H_23 260
7856 H_71 51 mv4 78 114 H_85
26 51
H_47 116 142 131 116
H_83 260 300 103 H_43
30 116 126
281 121
44 142 56 52
97 119 56 121
H_62 mv8
56 26 116 51 H_6
97 H_3 97 114
H_8 H_11 110 H_2 97
56 H_75 132 112
116 H_46
H_7 H_86 78 114 56 97
286 H_38
178 26 142
286
H_4 H_48 116 26 132
81 92 53 175 H_78
119 295 178 H_90 114142 295 mv7 H_14
132
H_63 56 44 97 114
H_42 54
44 H_40 97 26
9797 116 44 81 mv3 H_81
116 H_56
54 178 H_30 98 H_54
H_73 H_35 H_22 114 H_79
H_58 H_39
H_64 H_88 H_1
97 97 H_53 116 93 H_69
56
97 58 H_66
96 114
H_16 97 H_65
H_72 H_45 81 119
H_87 H_91
44 299 83 98
H_19 H_61
114 96H_10
H_41 H_44
H_18
116 114
51 114 96
mv1 H_20 H_25 H_76
180 119
H_59 H_12
Fig. 3. The median-joining network of 92 haplotypes for the Scomberomorus niphonius mtDNA control region
sequences. Red numbers on the connecting lines indicate the variable sites between each haplotype pair.
Node size corresponds to the haplotype frequencies; minimum node size is one individual. , SIS_1 and
,SIS_2. , Tosa Bay (TSB); , Shibushi Bay (SBS); , Kasasa (KSA); , Ise Bay (ISB); , Wakasa Bay
(WKB); , Goto (GOT); , the median vectors (hypothesised sequences).
DISCUSSION
Scomberomorus niphonius haplotype and allele frequency distributions were spa-
tiotemporally stable and the population structure was panmictic around Japan even in
the recovery process of population size after the historical minimum as indexed by
the commercial catch. Scomberomorus niphonius haplotype network was a star-like
shape and the demographic analysis inferred population expansion throughout the
Pleistocene.
The estimated time of S. niphonius population expansion in the late Pleistocene
205 000 (183 000220 000) B.P. for the mutation rate ( = 0 028) was compatible with
the 148 000503 000 B.P. estimated for S. niphonius in the East China and Yellow Seas
using mtDNA-CR sequences assuming the mutation rates of 005008 (Shui et al.,
2009). The molecular clock rate is a crucial parameter in the inference of the popu-
lation history (Ho et al., 2005; Liu et al., 2011; Grant et al., 2012; Reid et al., 2016;
Hoareau, 2016). A mutation rate of 28% per site per million years was used for the
S. concolor (Domnguez-Lpez et al., 2015) and much slower alternative of 028%.
The result is important, suggesting that S. niphonius population size has been growing
throughout the climatic changes in the Pleistocene, irrespective of mutation rate values
Table III. Empirical Bayes pairwise F ST values for microsatellite (above diagonal) and haplo-
type frequencies (below diagonal) in Scomberomorus niphonius (for locality abbreviations, see
Table I)
Locality SIS_1 SIS_2 TSB SBS KSA ISB WKB GTO
SIS_1 00006355 00004132 00006544 00004022 00003935 00004497 00004949

SIS_2 00000227 00006995 00006236 00005966 00008087 00006765 00010180
TSB 00000228 00000231 00006002 00004479 00004389 00004379 00004955
SBS 00000227 00000220 00000229 00005516 00006133 00005716 00007860
KSA 00000227 00000230 00000224 00000226 00004323 00004857 00005417
ISB 00000226 00000231 00000228 00000232 00000224 00004804 00004524
WKB 00000231 00000231 00000228 00000226 00000228 00000221 00004820
GTO 00000229 00000226 00000223 00000229 00000235 00000226 00000227
(Liu et al., 2011). The oscillations between glacial and interglacial periods over the past
3 106 years might have caused the exchange of immense amounts of water between
the ice sheets and the oceans (Lambeck et al., 2002), which should have induced great
changes in sea levels and led to a population decrease in many terrestrial animal and
plant species (Hewitt, 2000). Marine fish with long distance dispersal ability, however,
might not have been affected substantially by the severe environmental conditions. The
demographic expansion and genetic panmixia of S. niphonius populations might be
caused by the ability of disperse over long distances of this species.
(a) (b)
GT
O
_1
GT
SIS
O
_1
SIS
ISB
ISB TSB
TSB
WK WK
A B B
KS KS
A
SBS
SBS
SIS
_2
SIS
_2
60E-5 60E-5
Fig. 4. Scomberomorus niphonius neighbour-joining tree based on the empirical Bayes pairwise F ST values esti-
mated from (a) mtDNA-CR haplotype and (b) microsatellite allele frequencies. SIS_1, Seto Inland Sea;
SIS_2, Seto Inland Sea; TSB, Tosa Bay; SBS, Shibushi Bay; KSA, Kasasa; ISB Ise Bay; WKB, Wakasa
Bay; GOT, Goto.
(a) 10
Frequency (x103) 6
0
0 1 2 3 4 5 6 7 8 9 10
Number of pairwise differences
(b) 100
10
NeT
0.1
0.01
0 10 20 30 40 50 60 70 80
0 100 200 300 400 500 600 700 800

Time before present (kyr)
Fig. 5. (a) Observed ( ) and expected ( ) mismatch distributions under the sudden expansion model for
Scomberomorus niphonius mtDNA sequences for all of the samples pooled. (b) Bayesian skyline plot show-
ing changes in population size (N e T) inferred with BEAST2 based on the mtDNA sequences; N e , effective
population size, T, generation time. The separate axis at the bottom of the figure shows times under an
alternative (one-tenth slower) calibration rate for mtDNA. , Median estimates of N e T; , the 95%
upper and lower highest posterior density limits.
The haplotype frequencies were homogeneous, but SIS_2 allele frequencies differed
significantly from those of SIS_1 and other localities at two out of five loci (Sni21
and Sni29) (Supporting Information Tables SIVVI). SBS differed from SIS_1 and
TSB at Sni13 locus. The sample allele frequency distributions, however, were stable
for major alleles in all loci, suggesting that the statistical difference might have been
caused by the difference in minor allele frequencies (Supporting Information Fig. S3).
The effective population size (N e ) in the SIS was estimated at 9651 (554519521)
based on the temporal changes in microsatellite allele frequencies, which resulted in
the very small genetic drift estimate (000065) at most (Nakajima et al., 2014a). This
was equivalent to the pairwise F ST value (000064) between SIS_1 and SIS_2, suggest-
ing the differences in allele frequencies were caused by genetic drift. The sample sizes
were 246 (SIS_1) and 315 (SIS_2), therefore sampling variances in allele frequency
estimates were very small. It was concluded that the allele frequencies were spatiotem-
porally stable in Japanese S. niphonius populations. The stable haplotype and allele
frequencies in HWE suggest that the SIS is the source of S. niphonius populations, coin-
ciding that no spawning population has been reported in Japanese coasts except the SIS.
The star-like phylogenies of mtDNA sequences have been found in many marine
fishes including S. niphonius and the above mentioned fish species. Such star-like gene
trees with all nodes clustered in time show that the population has been growing expo-
nentially during its demographic history and has been large and stable (Slatkin & Hud-
son, 1991; Avise, 2000). In contrast, a recent study hypothesized that large variation
in marine fish recruitment is caused by the reproductive skew of individuals and alters
gene frequencies in the populations, based on a subset of mtDNA-CR sequences of the
Japanese sardine (Niwa et al., 2016). The large variation in S. niphonius catch history
from 1964 to 2016 indicates that recruitment success has varied substantially in the pop-
ulations (Fig. 2). Scomberomorus niphonius haplotype and allele frequency distribu-
tions, however, were stable despite sampled during the recovery process (20012010)
in the spawning ground (SIS) and other areas (Supporting Information Figs S1and S3).
The SIS_1 (collected in 2001 and 2002) and SIS_2 (in 2010) samples were mature
35 year old fish, therefore, the SIS_1 sample fish were born in and around 1998 when
the catch was at a historical minimum of 200 tons. In contrast, the SIS_2 sample fish
were spawned around 2005 when the population was clearly recovering, as shown by
the increase in catch to c. 1200 tons in the SIS (Fig. 2). The results here show that
reproductive skew might not have occurred even during the rapid population recov-
ery after the historical minimum catch. The spawning period of S. niphonius is from
mid-May to early July in the SIS and an adult fish spawns 46 times (Kishida &
Aida, 1989). Even if matchmismatch recruitment occurs in every spawning event,
all mature fish might have an equal chance for reproductive success averaging over the
long spawning period. Moreover, for fish species having group-spawning behaviour
such S. niphonius, a considerable number of individual spawn in a batch and individ-
uals that produce progenies may not be only a few in such an abundant commercially
exploited fish. Such spawning events repeated over generations should converge gene
frequencies to the population mean. This may be a reason for the spatiotemporally
stable population structure as observed in S. niphonius, even in the matchmismatch
recruitment (Shoji et al., 2002; Shoji & Tanaka, 2006). The results here suggest that S.
niphonius star-shaped phylogeny was caused by the historical population expansion,
not by the reproductive skew.
We thank the editors, B. Hnfling, S. J. Lockwood and anonymous reviewers for their
constructive comments, which improved our manuscript significantly. This study was
supported by a JSPS Grant-in-Aid for Scientific Research (B) 22 380 110 to SK.
Supporting Information
Supporting Information may be found in the online version of this paper:
Table SI. Haplotype frequencies for Scomberomorus niphonius samples.
Table SII. Significance levels for the linkage equilibrium tests for all pairs of the
Scomberomorus niphonius five microsatellite loci from each sampling location. Sig-
nificance after controlling the false discovery rate (P < 005) are shown in bold.
Table SIII. Significance levels for the HardyWeinberg equilibrium test in

Scomberomorus niphonius Significance after controlling the false discovery rate
(P < 005) are shown in bold.
Table SIV. Significance levels for the pairwise difference tests on microsatellite
allele frequencies at Sni13 (above diagonal) and Sni21 (below diagonal) in Scombero-
morus niphonius. Significance after controlling the false discovery rate (P < 005) are
shown in bold.
Table SV. Significance levels for the pairwise difference tests on microsatellite
allele frequencies at Sni 24 (above diagonal) and Sni26 (below diagonal) in Scombero-
morus niphonius. Significance after controlling the false discovery rate (P < 005) are
shown in bold.
Table SVI. Significance levels for the pairwise difference tests on microsatellite
allele frequencies at Sni 29 in Scomberomorus niphonius. Significance after controlling
the false discovery rate (P < 005) are shown in bold.
TABLE SVII. Microsatellite allele counts at the five Scomberomoru niphonius loci.
Fig. S1. Scomberomorus niphonius haplotype frequencies for each sampling locality.
n indicates sample size (individuals).
Fig. S2. An unrooted maximum-likelihood tree of 720 sequences of Scomberomorus
niphonius based on the best fit T92 + G + I model.
Fig. S3-1. Scomberomorus niphonius microsatellite allele frequencies at Sni13 locus
in each locality.
in each locality.
in each locality.
in each locality.
in each locality.
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Kitada Et Al-2017-Panmixia Scomberomorus Niphonius

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Journal of Fish Biology (2017)

doi:10.1111/jfb.13466, available online at wileyonlinelibrary.com

Population panmixia and demographic expansion

(Received 14 November 2016, Accepted 17 August 2017)

Sea SetoInland Sea (SIS)

30 128 130 132 134 136

1970 1980 1990 2000 2010

MATERIALS AND METHODS

Locality SIS_1 SIS_2 TSB SBS KSA ISB WKB GTO

SIS_1 00006355 00004132 00006544 00004022 00003935 00004497 00004949

0 100 200 300 400 500 600 700 800

Table SIII. Significance levels for the HardyWeinberg equilibrium test in

Cushing, D. H. (1990). Plankton production and year-class strength in fish popula-

(Lateolabrax japonicus) and spotted sea bass (Lateolabrax maculatus) in northwestern

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