SC/J09/JR31
Do not cite without written permission from the authors

Stock structure of Bryde’s whales in the western North Pacific
as revealed by microsatellite and mitochondrial DNA analyses
Naohisa Kanda, Mutsuo Goto, and L.A. Pastene
The Institute of Cetacean Research, 4-5, Toyomi-cho, Chuo-ku, Tokyo 104-0055, Japan
Contact email:kanda@cetacean.jp

ABSTRACT
Genetic variations at 17 microsatellite loci and 299 bp of mitochondrial DNA (mtDNA) control region
were analyzed from JARPNII samples of Bryde’s whales (Balaenoptera edeni) to describe their stock
structure in the western North Pacific off Japan. Up to 50 individuals per year were collected each year
from 2000 to 2007. Our main focus was to look for evidence of existence of genetically differentiatedsub-stocks in the sub-area 1: one in the west of 155°E (sub-area 1W) and other in the east of 155°E(sub-area 1E). For this purpose, we conducted conventional hypothesis testing for both genetic markers
and a Bayesian clustering approach for microsatellites. No genetic differences were detected among thesamples collected from the different survey years within the 1W as well as 1E. We also failed to detect
any evidence of genetic differentiation between the samples from the 1W and 1E, indicating these
JARPNII samples came from a genetically same group of Bryde’s whales. In order to examine stock
differentiation in a wider geographic range in the western North Pacific, samples of Bryde’s whales
obtained during past commercial whaling in the central western North Pacific in 1979 and aroundOgasawara Islands in 1983 and 1984 were compared to the JARPNII samples. No evidence of genetic
differentiation was detected between these two and JARPNII samples. All of the results indicated thatthe sub-area 1 was occupied exclusively by the individuals from a single stock.
KEY WORDS: BRYDE’S WHALE, MICROSATELLITE, MTDNA, STOCK STRUCTURE, JARPNII,INTRODUCTION
Bryde's whales (Balaenoptera edeni) are a unique baleen whale species because they are restricted totropical and warm temperate waters warmer than 20°C in major oceans between approximately 40°N and
40°S year-round (Omura, 1959; Best, 1977; Kato, 2002). As typical baleen whale species, Bryde’s
whales undergo seasonal movement from winter breeding grounds in low latitudes to summer feeding
grounds in higher latitudes. Their latitudinal migration, however, appeared to be short compared toother baleen whale species (e.g., Kishiro, 1996).
The comprehensive assessment of North Pacific Bryde’s whale has begun since the 47th meeting of
the International Whaling Commission (IWC) Scientific Committee (IWC, 1996, 1999, 2007). In thewestern North Pacific, two sub-areas (sub-area 1 and 2) divided at 180° were set within which only asingle stock of Bryde’s whales was highly likely distributed. Some members of the Committee, however,has argued against the single stock scenario in the sub-areas and, during Implementation Simulation Trials
in 2007, possibility of the presence of two sub-stocks was further suggested in the sub-area 1. These
two sub-stocks were thought to occupy west (1W) and east (1E) of 155°E, respectively (IWC, 2007).
All of these concerns were derived from that the defined area, especially sub-area 1, was very large andwide and that supportive evidence for the scenario was limited due to lack of samples from some parts ofthe sub-area 1 (see Appendix 14 of Annex D in IWC, 1999).
Since 2000, JARPN second phase (JARPNII) has begun taking up to 50 Bryde’s whales each year
from the western North Pacific feeding ground in order primarily to study feeding ecology and fisheriesinteractions of whales in this area and secondary to acquire information essential for effective
management of this species. The research area of JARPNII covers northwestern part of the Bryde’s
whales’ sub-area 1 (approximately one sixth of the whole area) where no genetic samples was collected in
the past.
On the basis of genetic variation at 17 microsatellite loci and 299 bp of mitochondrial DNA(mtDNA) control region sequences analyzed in individuals obtained from the western North Pacific,
South Pacific, and eastern Indian Ocean, Kanda et al. (2007) showed that Bryde’s whales were structured

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within as well as between oceanic basins with evidence of limited gene flow (see also Wada & Numachi,
1991; Pastene et al., 1997). Low mtDNA sequence divergence among populations and a lack ofconcordance between geographic and phylogenetic position of mtDNA haplotypes suggested recent
separation of populations rather than frequent trans-equatorial and inter-oceanic movement.
Nevertheless, the whales from the western North Pacific were shown to belong to the single stock. The
western North Pacific samples in that past study included whales collected during the JARPNII surveys
from 2000 to 2003.
The primary objective of this study was to better understand stock structure of Bryde’s whales fromthe sub-area 1 of the western North Pacific using hypervariable microsatellite analysis and mtDNA
control region sequencing. We first looked for any evidence of genetic differentiation between the
JARPNII samples collected from the 1W and 1E. We then looked for any evidence of genetic
differentiation among the samples from JARPNII and past commercial whaling conducted at outside the
JARPNII area. Genetically different stocks might co-occur in the feeding ground, and incomplete
knowledge about stock structure can cause unsound management, for instance, over-exploitation ofcertain stocks if separate stocks are erroneously treated as a single unit.
MATERIALS AND METHODS
Samples
JARPNII samples of Bryde’s whales were obtained off the Japanese coast from the IWC defined
sub-areas 7, 8, and 9 in the western North Pacific (Fig. 1). Up to 50 individuals per year were collectedeach year from 2000 to 2007. These samples were divided into sub-area 1W (West: Japanese coast and155ºE) and 1E (East: 155ºE-180º). Table 1 shows survey year, survey period, and sample size (West,East) from 2000 to 2007. Sampling dates and locations of scientific surveys slightly differed year by
year depending on the sampling plan of a given year. All samples were collected during spring andsummer in the feeding ground. Details of offshore part of JARPNII survey can be found in Tamura et al.
(2009).
In order to examine stock differentiation in a wider geographic range in the western North Pacific,
samples of Bryde’s whales obtained during past commercial whaling around Ogasawara Island in 1983
and 1984 (Ogasawara) and in the central western North Pacific in 1979 (pelagic) were used forcomparison (Fig. 1). Individuals in the Ogasawara sample (N=102 in the microsatellite and N=103 in
the mtDNA analyses) were archived specimens from past Japanese coastal commercial whaling
operations. A total of 545 whales in 1983 and 528 whales in 1984 were caught according to a catch
history (e.g., Table 2 of Appendix 2 in IWC, 1997). Individuals in the pelagic sample (N=98 in the
microsatellite and N=113 in the mtDNA analyses) were archived specimens of past Japanese pelagic
commercial whaling operations. Pelagic commercial whaling landed a total of 402 Bryde’s whales in1979 according to the catch history (IWC, 1997). More detail information on genetic characteristics ofthese commercial whaling samples was available in Kanda et al. (2007).
DNA extraction
Total DNA was extracted from 0.05 g of skin, muscle, heart, or liver tissue using the protocol ofSambrook et al. (1989) and then was stored in TE buffer (10 mM Tris-HCl, 1 mM EDTA, pH 8.0).
Microsatellite analysis
Genetic variations at microsatellites were analyzed using 17 sets of primers, none of which was designed
specifically from Bryde's whales: EV1, EV14, EV21, EV94, EV104 (Valsecchi & Amos, 1996), GT011(Bérubé et al., 1998), GT23, GT310, GT575 (Bérubé et al., 2000), GATA28, GATA53, GATA98,
GATA417, GGAA520, TAA031 (Palsbøll et al., 1997), DlrFCB14, and DlrFCB17 (Buchanan et al.,1996). Primer sequences and PCR cycling profiles followed those of the original authors. PCR
amplifications followed the manufacture’s instructions for the use of Ex Taq DNA polymerase (Takara
Shuzo). Amplified products were electrophoresed on a 6% polyacrylamide denaturating gel using a
BaseStation 100 DNA fragment analyzer (Bio-Rad), and alleles were sized manually in relation to aninternal size standard (Genescan 400HD, Applied Biosystems) and to Bryde’s whale microsatellites ofknown size that were included on each gel.
mtDNA analysis
Sequencing analysis of the 299 bp control region of mtDNA was conducted using the primers light-strand
MT4 (Árnason et al., 1993) and heavy-strand P2 (5'-GAAGAGGGATCCCTGCCAAGCGG-3' ; Hori etal., unpublished). PCR products were purified by MicroSpin S-400HR columns (Pharmacia Biotech).

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Cycle sequencing was performed with the same primers, using BigDye terminator cycle sequence Kit(Applied Biosystems, Inc). The cycle sequencing products were purified by AutoSeq G-50 spin
Columns (Pharmacia Biotech). The labeled sequencing fragments were resolved by electrophoresis
through a 5% denaturing polyacrylamide matrix on an ABI 377 or ABI3100 Automated DNA
Sequencer (Applied Biosystems, Inc), following the protocols of the manufacture. For each sample bothstrands were sequenced.
Genetic diversity analysis
For the microsatellite analysis, the number of alleles per locus and expected heterozygosity per locus wascalculated using the software FSTAT 2.9.3 (Goudet, 1995). Statistical tests for the deviations fromexpected Hardy-Weinberg genotypic proportions were conducted using the software GENEPOP 4.0(Rousset, 2008). When simultaneous multiple tests were conducted, Rice (1989) correction for themultiple tests was performed.
For the mtDNA, the number of haplotypes and haplotype diversity were calculated following Nei(1987). The nucleotide diversity (Nei, 1987: equation 10.5) and its standard error for population
sampling and stochastic processes were calculated from the pair-wise differences between the mtDNA
sequences using the Kimura’s 2- parameter adjustment (Kimura, 1980).
Genetic divergence analysis
Conventional hypothesis testing procedure was conducted using heterogeneity test in microsatellite allele
and mtDNA haplotype frequencies among the samples, respectively. Our null hypothesis to be tested isif the samples came from a genetically same group of Bryde’s whales. If a statistically significant allele
frequencies differences exist, then it could indicate these samples came from genetically different stocksof Bryde’s whales. Probability test (or Fisher’s exact test) implemented in GENEPOP was used to
conduct the heterogeneity tests for the microsatellites. Sequential Bonferroni correction (Rice, 1989)
was applied when multiple tests were conducted. Weir and Cockerham estimator of FST was calculatedusing FSTAT 2.9.3 (Goudet, 1995). The randomized chi-square test of Independence (Roff and Bentzen,
1989) was used to investigate the temporal/spatial differentiation of mtDNA variation. In each test a
total of 10,000 permutations of the original data were performed. Tests were conducted for all samples
combined as well for males and females separately. A p-value smaller than 0.05 was used as a criterion
to reject the null hypothesis of panmixia. FST for mtDNA was calculated based on the analysis ofmolecular variance (AMOVA) (Excoffier et al., 1992).
A Bayesian clustering approach implemented in the software STRUCTURE (Pritchard et al., 2000)
was also applied to determine the most likely number of genetically distinct stocks present in our samples.
STRUCTURE is a model-based clustering method for inferring stock structure using multi-locus
genotype data. Spatial differentiation of samples was assessed assuming that the sampled individuals
belong to an unknown number of K stocks. We conducted three independent runs for each value of K
between 1 and 5 with no prior information (i.e., only genetic information was considered). All of thesimulations were based on a burn-in period of 10,000 iterations and runs of 100,000 iterations. The
ancestry model we used for the simulation was the admixture model, which assumes individuals may
have mixed ancestry. The allele frequency model used was the correlated allele frequencies model,
which assumes frequencies in the different stocks are likely to be similar due to migration or sharedancestry.
RESULTS AND DISCUSSION
Genetic diversity within samples
Microsatellie. All 17 microsatellite loci were polymorphic within all the JARPNII samples (Table 2).
Total number of alleles at each locus overall the samples ranged from two at DlrFCB14 to 18 at GATA28
with an average of 8.2. Expected heterozygosity ranged from 0.285 at TAA31 to 0.913 at GATA28 withan average of 0.673. None of the 17 loci showed significant deviation from expected Hardy-Weinberg
genotypic proportions after correction for the simultaneous multiple tests.
The levels of allelic diversity and heterozygosity in the JARPNII samples were compatible to thosespecies used for primer design (Buchanan et al., 1996; Valsecchi and Amos, 1996; Palsbøll et al., 1997;
Bérubé et al., 1998, 2000) and others reported (Bérubé et al., 2000; Kanda et al., 2006). Thisobservation was the same to that in Kanda et al. (2007), even the sample size had been doubled since then.
Although some loci contained low number of alleles, it is unlikely that this low variability is due too thenegative effect on genetic diversity at a population level. This is because the low diversity is notconsistent over all of the 17 loci.

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mtDNA. Sequence variations at 299bp of the mtDNA control region resulted in 38 unique haplotypes.
Haplotype diversity was 0.814 and nucleotide diversity was 0.0107 (standard error = 0.00058). Genetic
diversity at the mtDNA control region was similar to that of other large baleen whales in the North Pacific,
such as common minke whales (Goto et al., 2009) and sei whales (Kanda et al., 2009).
Genetic divergence among samples
Bryde’s whales in the JARPNII samples were divided into two on the basis of individual’s sighting sites(IWC, 2007): sub-area 1W sample (1W) was those initially sighted at west of 155°E, while sub-area 1Esample (1E) was those at east of 155°E. We first tested for genetic allele frequency differences among
the samples collected from different survey years within 1W as well as within 1E. No statisticallysignificant yearly heterogeneity was detected within each after correction for multiple tests at the
microsatellite as well as mtDNA sequence analysis (Table 3). We combined the year samples into one
for each of the areas as 1W and 1E samples. Then, we looked for evidence of genetic differences
between the 1W and 1E samples. No statistically significant heterogeneity was observed after thecorrection for multiple tests at the microsatellite as well as mtDNA sequence analysis (Table 3),indicating that the JARPNII samples came from a genetically same group of Bryde’s whales. All of thesamples were then combined into a single JARPNII sample for further analyses.
The commercial whaling samples of Bryde’s whales obtained around Ogasawara Island in 1983 and1984 (Ogasawara) and in the central western North Pacific in 1979 (pelagic) were used to examine stock
differentiation in a wider geographic range in the subarea 1. The Ogasawara sample was collected fromwest of 155°E and the pelagic sample from east of 155°E, and these samples corresponded to the SWNP
and CWNP samples in Kanda et al. (2007), respectively. No evidence of genetic differentiation wasobserved among the JARPNII, Ogasawara, and pelagic samples after the corrections for multiple loci.
These results indicated that all the three samples were obtained from a genetically same group of Bryde’s
whales. FST values calculated from microsatellite allele and mtDNA haplotype frequencies, respectively,
between pairs of these three samples were not statistically different from zero (Table 4). Bayesianclustering analyses conducted without information on geographic sampling origins presented the lowest
likelihood probability at K = 5 and the highest likelihood probability at K = 1 (Table 5). This result also
provided support for a single stock.
Both conventional hypothesis testing and Bayesian clustering method failed to detect evidence ofexistence of multiple stocks in the sub-area 1 in this study. Kanda et al. (2007) has already reached thesame conclusion that only a genetically single stock occupies the JARPNII survey area using the samples
collected from 2000 to 2003. Because sampling locations of the 2000 to 2003 samples were restricted towest of 160°E, however, the conclusion of the single stock was tentative. In the current study, Bryde’s
whales in the samples of another four years from 2004 to 2007 included those collected further east up to
170°E (eastern boundary of sub-area 9). We, therefore, think that these individuals from JARPNII andcommercial whaling samples fairly well covered the sub-area 1, allowing us to detect whether or not
multiple sub-stocks existed in the sub-area 1. All of the results indicate that the sub-area 1 is occupied
exclusively by the individuals from a single stock.
As described in Kanda et al. (2007), our results were consistent with previous genetic studies ofBryde’s whale (Wada and Numachi, 1991; Pastene et al., 1997) as well as field studies (Nemoto, 1959;
Ohsumi, 1978; Kishiro, 1996). Wada (1996) analyzed GOT-1 allozyme allele frequencies in 2521
individuals collected from 1974 to 1984, divided along the 10-degree squares based on their catch
positions between 20°N and 40°N and between 140°E and 160°W, and failed to show existence ofmultiple stocks in the western North Pacific. Past mark-recapture data demonstrated that tagged whales
regularly moved within the sub-area 1 as well as from near the equator to coastal and pelagic areas off thecoast of Japan.
ACKNOWLEDGEMENT
We gratefully acknowledge the researchers and crew members that participated in JARPNII survey. Our
sincere gratitude also goes to H. Oikawa and S. Azumi for their assistance in DNA extraction, and H.
Hatanaka for valuable comments on the manuscript.
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Kanda, N., Goto, M., and Pastene, L.A. 2006. Genetic characteristics of western North Pacific sei
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Kanda, N., Goto, M., Kato, H., McPhee, M.V., and Pastene, L.A. 2007. Population genetic structureof Bryde’s whales (Balaenoptera brydei) at the inter-oceanic and trans-equatorial levels. Cons.
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Tamura, T., Matsuoka, K., and Fujise, Y. 2009. Methodology and survey procedure under the JARPN
II - offshore component- with special emphasis on whale sampling procedures. Paper SC/J09/JR4
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Fig. 1. Sampling locations of Bryde’s whales used in this study.
Triangle = JARPNII, diamond = Ogasawara, square = pelagic.

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Table 1. Survey year and period, sample size (west, east)* of Bryde’s
whales collected from JARPNII surveys from 2000 to 2007.
Year

Survey period

Sample size (west, east)*

2000
August - September
42 (42, 0)
2001
May - July
43 (43, 0)
2002
July - August
50 (36, 14)
2003
May - July
50 (37, 13)2004
June - September
50 (0, 50)
2005
June - July
50 (46, 4)
2006
June - August
50 (12, 38)
2007
June - August
50 (20, 30)* west=west of 155°E, east=east of 155°E

Table 2. The number of alleles (A), expected heterozygosity(He), and test result for expected Hardy-Weinberg genotypic
proportions (HW) at 17 microsatellite loci analyzed in the JARPNII
samples of Bryde’s whales. n.s. = not significant.
A

He

HW

2
15
11
7
8
7
8
18
7
7
8
7
8
3
5
11
7
8.2

0.490
0.885
0.735
0.755
0.769
0.645
0.549
0.913
0.617
0.796
0.755
0.765
0.741
0.495
0.608
0.646
0.285
0.673

n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.
n.s.

DlrFB14
DlrFB17
EV1
EV104
EV14
EV21
EV94
GATA28GATA53
GATA98GATA417GGAA520
GT23
GT011
GT310
GT575
TAA31
average
mtDNA
Haplotype number
Haplotype diversity
Nucleotide diversity(standard error)

38
0.814
0.0107(0.00058)

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Table 3. Test results (p-values) for genetic differentiation at the 17
microsatellite loci and mtDNA sequences among the samples of Bryde’s
whales.
Locus

1W

1E

1Wx1E

Sub-area 1*

Microsatellite
DlrFB14
DlrFB17
EV1
EV14
EV21
EV94
EV104
GATA28GATA53
GATA98GATA417GGAA520
GT23
GT011
GT310
GT575
TAA31

0.014
0.811
0.987
0.430
0.616
0.183
0.284
0.522
0.218
0.147
0.079
0.589
0.334
0.502
0.513
0.723
0.620

0.310
0.490
0.152
0.316
0.780
0.100
0.190
0.333
0.078
0.688
0.026
0.594
0.128
0.713
0.523
0.814
0.204

0.411
0.043
0.893
0.686
0.143
0.309
0.529
0.138
0.639
0.241
0.904
0.723
0.537
0.793
0.778
0.765
0.461

0.894
0.922
0.321
0.526
0.629
0.004
0.848
0.328
0.771
0.080
0.651
0.158
0.113
0.043
0.749
0.302
0.216

mtDNA
0.332
0.160
0.225
0.055
* among JARPNII, Pelagic, and Ogasawara (see text for sample details)

Table 4. Level of genetic differentiation (FST) calculated from mtDNA haplotype
frequencies (above diagonal) and microsatellite allele frequencies (below diagonal)
among the samples of Bryde’s whales from the sub-area 1.

JARPNII
Pelagic-E*
Ogasawara-W**

JARPNII

Pelagic-E

Ogasawara-W-----0.0002
0.0004-0.0020-----0.0009

0.0035-0.0021-----* Pelagic-E: commercial whaling in the central western North Pacific in 1979 (sub-area 1 east)** Ogasawara-W: commercial whaling around Ogasawara island in 1983 and 1984 (sub-area 1 west)

Table 5. Estimated posterior probability of number of stocks (K)for the pooled samples of Bryde's whales collected from JARPNII
and past commercial whaling computed using STRUCTURE.
K

Log P (x/k)

s.d.

Probability

1
2
3
4
5

-28477.4-28791.8-29177.9-30503.8-32488.0

64.7
849.9
1694.64420.58446.0

~1.0
~0.0
~0.0
~0.0
~0.0

8