Mitochondrial DNA Sequence Variations and Genetic Relationships among Korean Thais Species (Muricidae: Gastropoda)

2011·3.6 MB·

by  Sang-Hwa Lee

Korean J. Syst. Zool. Vol. 27, No. 1: 1-17, March 2011
DOI 10.5635/KJSZ.2011.27.1.001
Mitochondrial DNA Sequence Variations and
Genetic Relationships among Korean
Thais Species (Muricidae: Gastropoda)
Sang-Hwa Lee1, Taeho Kim2, Junhee Lee1, Jong-Rak Lee3, Joong-Ki Park1,*
1Graduate Program in Cell Biology and Genetics and Department of Parasitology, College of Medicine,
Chungbuk National University, Cheongju 361-763, Korea
2Department of Plant Medicine, College of Agriculture, Life, and Environmental Sciences,
Chungbuk National University, Cheongju 361-763, Korea
3Marine Biodiversity Research Institute, INTHESEA KOREA Inc., Jeju 697-110, Korea
ABSTRACT
Thais Röding, 1798, commonly known as rock-shell, is among the most frequently found gastropod genera
worldwide on intertidal rocky shores including those of Japan, China, Taiwan and Korea. This group contains
important species in many marine environmental studies but species-level taxonomy of the group is quite
complicated due to the morphological variations in shell characters. This study examined the genetic variations
and relationships among three Korean Thaisspecies based on the partial nucleotide sequences of mitochondrial
cox1 gene fragments. Phylogenetic trees from different analytic methods(maximum parsimony, neighbor-joining,
and maximum likelihood) showed that T. bronni and T. luteostoma are closely related, indicating the most
recent common ancestry. The low sequence divergence found between T. luteostoma and T. bronni, ranging
from 1.53% to 3.19%, also corroborates this idea. Further molecular survey using different molecular marker
is required to fully understand a detailed picture of the origin for their low level of interspecific sequence
divergence. Sequence comparisons among conspecific individuals revealed extensive sequence variations
within the three species with maximum values of 2.43% in T. clavigera and 1.37% in both T. bronni and T.
luteostoma. In addition, there is an unexpectedly high level of mitochondrial genotypic diversity within eachof
the three Korean Thaisspecies. The high genetic diversity revealed in Korean Thaisspecies is likely to reflect
genetic diversity introduced from potential source populations with diverse geographic origins, such as
Taiwan, Hong Kong, and a variety of different coastal regions in South China and Japan. Additional sequence
analysis with comprehensive taxon sampling from unstudied potential source populations will be also needed
to address the origin and key factors for the high level of genetic diversity discovered within the three Korean
Thaisspecies studied.
Keywords:Thais, Korean rock-shell, mitochondrial cox1 variation, Muricidae
INTRODUCTION related to human-induced pollution, such as that from orga-
notin compounds(Shim et al., 2000; Hung et al., 2001; Tang
ThaisRöding, 1798(commonly known as rock-shell) is one and Wang, 2009) and long-term exposure to heavy metal
of the most frequently found genera of gastropods worldwide contamination(Rubio et al., 1993; Han et al., 1997; Black-
on intertidal rocky shores including those of Japan, China, more and Wang, 2004).
Taiwan, and Korea. The genus contains about a hundred Despite their significance in aforementioned environmen-
species names(Houart and Gofas, 2010), some of which tal studies, the species-level taxonomy of this group is quite
includes predatory species that cause serious damage to the complicated due to morphological variations in shell charac-
oyster culture industry by drilling through the oyster shells teristics(Tan and Sigurdsson, 1996). Indeed, the morphologi-
(Clench, 1947; Brown and Richardson, 1988). The species cal features used most frequently for species identification,
of this genus also play an important role in the marine macro- including size, shape and the absence or presence of blotches
benthic community. They have often been used as an effec- on the nodules of shell surfaces and shell apertures, are high-
tive indicator species in many marine environmental studies ly variable depending on the local environment(Hayashi,
cc This is an Open Access article distributed under the terms of the Creative *To whom correspondence should be addressed
Commons Attribution Non-Commercial License(http://creativecommons.org/ Tel: [phone], Fax: [phone]
licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, E-mail: [email protected]
and reproduction in any medium, provided the original work is properly cited.
Sang-Hwa Lee, Taeho Kim, Junhee Lee, Jong-Rak Lee, Joong-Ki Park
1999; Tan and Liu, 2001). Owing to the substantial variabili- which they were assigned to three species: T. clavigera, T.
ty in shell characteristics, species identification relying on luteostoma, and T. bronni(Fig. 1). A total of 46 specimens
shell morphology alone often leads to erroneous results creat- sampled from nine localities representing three Korean Thais
ing many synonyms. As a result, the associated nomenclature species were used for sequencing analysis. The total geno-
for Thais species is unusually complicated(Clench, 1947; mic DNA was extracted using a tissue kit(Qiagen, Valencia,
Tan, 1995). CA, USA) according to the manufacturer’s instructions. A
In Korea, Thais species have been included as part of a universal primer set(LCO1490: 5′-GGTCAACAAATCAT
species checklist in the faunal report on mollusks. Earlier AAAGATATTGG-3′, HCO2198: 5′-TAAACTTCAGGGT
studies, including some encyclopedias of Korean shells, GA CCAAAAAATCA-3′) was employed for PCR amplifi-
relied entirely on the shell characteristics without careful cation of the target gene fragment mt cox1(Folmer et al.,
appraisal of species identity(Choe, 1992; Lee and Min, 2002; 1994). PCR reactions were performed in a 50μL reaction
Min, 2004). A taxonomic investigation of Korean muricid volume consisting of 10units of Taq polymerase(Roche,
species based on a morphological comparison of shell and Mannheim, Germany), 2.5mM dNTP mixture, 2.5mM MgCl
2
radula characteristics showed that three Thais species are and 20 pmole of each primer with the following amplification
very abundant in Korean coastal areas(Choe and Park, 1997): conditions: one cycle of the initial denaturation step at 94�C
T. clavigera(Küster, 1858), T. bronni(Dunker, 1860), and for 2min, followed by 35 cycles of denaturation at 94�C for
T. luteostoma(Holten, 1803). In contrast to taxonomic assess- 30sec, primer annealing at 45�C for 30sec and elongation
ments by most earlier authorities, these species are not very at 72�C for 1min with a final extension step at 72�C for 10
morphologically discernible from each other because their min. The PCR-amplified target gene fragment was purified
shell morphology is greatly variable, creating a diverse array using a QIAquick gel extraction kit(Qiagen) according to
of local morphotypes according to their geographic origins. the manufacturer’s protocol. The sequencing reaction was
Therefore, there is considerable taxonomic confusion with performed using a BigDye®terminator v3.1 cycle sequencing
regard to species-level taxonomy in this group. kit(Applied Biosystems, Foster City, CA, USA), and the
The utility of molecular markers in modern taxonomy has reaction products were electrophoresed using an ABI 3730XL
been growing rapidly as a reliable tool for examining the DNA analyzer. Phylogenetic analysis for the mt cox1 dataset
phylogenetic relationships in different levels of taxonomic obtained from the three Thais species was performed using
groups and species identification. As in many other animal different tree-building methods(maximum parsimony [MP],
groups, molecular data from mitochondrial(mt) gene frag- neighbor-joining [NJ], and maximum likelihood [ML]) with
ments(e.g., 16S and cox1) provide a wealthy resource for PAUP 4.0b10(Swofford, 2002) using Thais turbinoides as
assessing the genetic variations and phylogenetic signals an outgroup. NJ and ML analyses were carried out using the
among closely related species of diverse molluscan taxa HKY++Γ(0.0913 of gamma shape parameter) model that
(Boudry et al., 2003; Park and Kim, 2003; Lam and Morton, was selected as the ‘best-fit’ substitution model according
2006; Reece et al., 2008). The present study examined the to the Akaike information criterion(AIC) from implementa-
genetic variations and relationships among three Korean tion of the Modeltest version 3.7 program(Posada and
Thais species based on partial nucleotide sequences of mt Crandall, 1998). The reliability of grouping in both MP and
cox1 gene fragments. In addition, the sequence data presented NJ methods was estimated using non-parametric bootstrap
here provides a very useful molecular identification tool for resampling of 1,000 pseudo-replicates.
the three Korean Thais species, which are often taxonomi-
cally complicated when based upon the morphological char-
acteristics alone. RESULTS AND DISCUSSION
Phylogenetic relationships among Korean Thais
MATERIALS AND METHODS species
The target mt cox1 gene fragment determined for all Thais
The specimens were collected from the intertidal and/or species is 658 base pairs(bp) in length with no intra- or
subtidal zones in nine localities of the Korean seashore. interspecific length variations. Table 1 lists the GenBank
Voucher specimens used for species identification and subse- accession numbers for each mt genotype and locality data
quent molecular sequencing were deposited in the Marine for the species. The MP analysis of the mt cox1 dataset show-
Mollusk Resource Bank of Korea(MMRBK; Chungbuk ed two distinct clades with very strong support(Fig. 2): one
National University, Korea). Identification of the Thaisspeci- representing the assemblage of mt genotypes from T. clavi-
mens was carried out based on the shell characteristics, from gera and the other containing two groups of mt genotypes,
2 Korean J. Syst. Zool. 27(1), 1-17
Genetic Variations of Korean Thais Species
1a 1b
2a
2c
2b
2e
2d
2f
3a
3b 3c 3d
Fig. 1.Shell morphology of three Korean Thaisspecies. T. clavigera(1a, 1b), T. bronni(2a-2f), T. luteostoma(3a-3d). Scale bars==2cm.
Korean J. Syst. Zool. 27(1), 1-17 3
Sang-Hwa Lee, Taeho Kim, Junhee Lee, Jong-Rak Lee, Joong-Ki Park
Table 1.Geographic origin, sampling locality and GenBank accession numbers for Thaisspecies used in this study
No. of individuals GenBank
Species Geographic origin Genotype
examined accession no.
Thais luteostoma Tonggumi, Ulleung-gun 10 TL01(1) HQ852742
Gyeongsangbuk-do TL02(1) HQ852743
TL03(1) HQ852744
TL04(3) HQ852745
TL05(1) HQ852746
TL06(1) HQ852747
TL10(1) HQ852751
TL12(1) HQ852753
Daeyeong, Jeju-do 6 TL02(1) HQ852743
TL04(1) HQ852745
TL07(1) HQ852748
TL08(1) HQ852749
TL09(1) HQ852750
TL11(1) HQ852752
Seogwipo-si, Jeju-do 2 TL10(2) HQ852751
Thais bronni Seogwipo-si, Jeju-do 4 TB01(1) HQ852754
TB02(1) HQ852755
TB03(1) HQ852756
TB04(1) HQ852757
Dodong, Yokji-myeon, 9 TB03(1) HQ852756
Tongyeong-si, TB05(1) HQ852758
Gyeongsangnam-do TB06(1) HQ852759
TB07(1) HQ852760
TB08(1) HQ852761
TB09(1) HQ852762
TB10(2) HQ852763
TB11(1) HQ852764
Gajin-ri, Goseong-gun, Gangwon-do 2 TB07(1) HQ852760
TB08(1) HQ852761
Wonbuk-myeon, Taean-gun, 2 TB12(1) HQ852765
Chungcheongnam-do TB13(1) HQ852766
Thais clavigera Ganwoldo-ri, Seosan-si, Chungcheongnam-do 1 TC01(1) HQ852767
Hoenggando, Chujado, Jeju-do 1 TC02(1) HQ852768
Dodong, Yokji-myeon, 2 TC03(1) HQ852769
Tongyeong-si, Gyeongsangnam-do TC04(1) HQ852770
Geoado-ri, Taean-gun, 7 TC03(1) HQ852769
Chungcheongnam-do TC04(1) HQ852770
TC05(1) HQ852771
TC06(1) HQ852772
TC07(1) HQ852773
TC08(1) HQ852774
TC09(1) HQ852775
Gajin-ri, Goseong-gun, Gangwon-do 1 TC10(1) HQ852776
Thais haemastoma 1 EU073051
Thais turbinoides South of New Caledonia 1 HQ852777
representing T. luteostomaand T. bronni. The grouping pat- respectively) also received relatively strong support. In con-
terns among the three species in the MP analysis were iden- trast to the well-structured relationships, the inferred tree
tical to those of the NJ and ML analyses(not shown). The showed no particular grouping pattern among the mitochon-
bootstrap values for these two clades were very high(100% drial genotypes within each of the three species. Irrespective
for T. clavigera in both MP and NJ methods, and 96% and of the analytical methods(MP, NJ, and ML), the reconstruct-
100% for T. bronni-T. luteostoma in MP and NJ analyses, ed phylogenetic trees consistently depicted T. bronniand T.
respectively). The branches representing T. luteostoma(92% luteostomaas being more closely related to each other than
and 96% bootstrap supports in MP and NJ, respectively) and to T. clavigera. This sister group relationship was robustly
T. bronni(88% and 81% supports in MP and NJ analyses, supported by a bootstrap value of 96%(MP) and 100%(NJ)
4 Korean J. Syst. Zool. 27(1), 1-17
Genetic Variations of Korean Thais Species
62 TL11
TL12
TL02 (2)
88 TL04 (4)
TL05
57
TL09
Thais luteostoma
TL01
TL03
80
TL07
TL08
TL10 (3)
TL06
51 TB07 (2)
100
TB13
60 TB02
TB09
TB01
TB03 (2)
74
TB04 Thais bronni
TB05
TB06
TB08 (2)
TB10 (2)
TB11
TB12
98 TC01
TC10
86 TC05
TC09
57
TC02
TC04 (2) Thais clavigera
100 TC06
TC07
TC03 (2)
TC08
Thais turbinoides Outgroup
Fig. 2.Bootstrapped consensus tree of 28 equally parsimony trees from heuristic analysis for cox1sequence data of three Korean
Thaisspecies. Bootstrap supporting values from the maximum parsimony method are indicated above the internal branches if ›50%.
The bootstrap values for each node from neighbor-joining analysis using the HKY+Γ(0.0913 of gamma shape parameter) model as
the ‘best-fit’substitution model selected under the Akaike information criterion from the implementation of Modeltest 3.7 program
(Posada and Crandall, 1998) were also shown below the branches.
in the different analytic methods(MP and NJ). This result Wu, 1965). Nevertheless, the radula characteristics are often
corresponds to the morphological similarities revealed by quite similar among closely related congeneric species,
some earlier studies using comparative analysis of morpho- making species identification rather difficult based on the
logical characters(shell, radula, and penis morphology etc.) radular traits alone(Fujioka, 1985; Tan and Liu, 2001). Some
(Choe and Park, 1997; Tan and Liu, 2001). earlier authorities reported that the rachidian teeth of T.
Aside from the shell external characteristics, traditional luteostoma and T. bronni were quite similar but noticeably
taxonomy has appreciated the radula morphology as one of different from those of T. clavigera in both the shape and
the most useful features for the classification of a wide range number of denticles. There are usually more than six denticles
of gastropod groups, including muricid species(Cooke, 1919; between the lateral and marginal cusps recorded for the
Korean J. Syst. Zool. 27(1), 1-17 5
Sang-Hwa Lee, Taeho Kim, Junhee Lee, Jong-Rak Lee, Joong-Ki Park
Korean population of T. luteostomaand T. bronni(6 and 7- and TL07 pair) to 7.75%(between TC01 and TB06 pair). In
8, respectively)(Choe and Park, 1997). Tan and Liu(2001) contrast, interspecific sequence divergence between T. luteo-
observed some variations from Hong Kong population of T. stoma and T. bronni was relatively very low, ranging from
luteostomain the denticle number, ranging from five to eight. 1.52%(for TL10 and TB03 pair) to 3.19%(for TL05 and
The rachidian tooth of T. clavigerahas fewer denticles(nor- TB06 pair). The lowest interspecific difference value(1.52%)
mally 3-4 denticles between lateral and marginal cusps). detected between T. luteostoma and T. bronni was even
Although variations in radula characteristics according to lower than the highest divergence value detected within T.
the local populations are not uncommon, particularly in the clavigera(2.43% between TC01 and TC08). This low diver-
denticle number, similarities in the radula characteristics gence value found between T. luteostoma and T. bronni
between T. bronni and T. luteostoma are in line with the implies that cladonegenetic split of these two species is very
close relationship uncovered by genetic analysis of the mol- young with a very recent common origin. Further molecular
ecular data in this study. The closer relationship between T. survey using different molecular marker is required to fully
bronniand T. luteostomais also supported by a comparison understand a detailed picture of the origin for their low level
of the penis morphology. Indeed, the morphology of the of sequence divergence. In addition, sequence comparison
male reproductive organ is generally considered species- of conspecific individuals revealed extensive sequence varia-
specific and appears to be very useful for species identifica- tions within each of the three species. The intraspecific differ-
tion in this genus. Exceptions were found for T. luteostoma ences among the T. clavigeramt genotypes were remarkably
and T. jubilaea, whose penis morphology was more or less high, with a maximum 2.43% divergence of a pairwise com-
similar(Tan and Sigurdsson, 1990; Tan and Liu, 2001). Inter- parison(found between TC01 and TC08). The sequence
estingly, the penis morphology of T. luteostoma was quite divergence within species in each of T. bronniand T. luteo-
different from that of T. clavigera, but similar to that of T. stomawas also high: the maximum value was detected bet-
bronnifrom the Korean population. T. bronnihas a recurved ween TB06-TB02 and TB06-TB07 pairs in T. bronni(1.37%)
hooklet-shaped penis with a gradually tapered terminal end and between TL05-TL06, TL05-TL07, and TL05-TL12 pairs
(Park, 1996) and these characteristics were also found in in T. luteostoma(1.37%).
Hong Kong(Tan and Liu, 2001) and Korean(personal obser- Along with the considerable genetic divergence within
vations) populations of T. luteostoma. The morphological species, there were a large number of mt genotypes discover-
similarities of both radula and penis are consistent with the ed in each of the three species. Thirty five mt genotypes were
current molecular data, indicating that T. luteostomaand T. detected from 46 individuals of the three species sequenced.
bronni are very closely related. The inclusion of broader Of these, a small fraction of mt genotypes(9 of 35; 25.7%
taxon sampling will be needed to place the Korean population of total genotypes detected) is represented by more than one
of species within the phylogenetic framework of the genus. individual(Table 1, Fig. 2). With the exception of these, all
other mt genotypes(26 of 35; 74.3% of total genotypes de-
Mt DNA variations in Korean Thaisspecies tected) were presented by a single individual. These exclu-
A total of 35 mt genotypes were discovered from 46 indivi- sive mt genotypes were shown to be unresolved polytomies
duals of nine local populations of three Korean Thaisspecies at the terminal tips in the reconstructed phylogenetic tree
(Aligned cox1 sequences for Thaisspecies are shown in Su- (Fig. 2). This unexpectedly high genotypic diversity encoun-
pplementary data, Appendix 1). Each of these three species tered within each of the three Korean Thaisspecies is assum-
included a large number of mt genotypes: 10 for T. clavigera, ed to be a reflection of the genetic diversity introduced from
13 for T. bronni and 12 for T. luteostoma. Table 2 lists the potential source populations with diverse geographic origins,
uncorrected pairwise(p) distance among mt genotypes. The such as Taiwan, Hong Kong, and many different coastal
sequence divergence of T. turbinoides(outgroup species) regions of South China and Japan. Although a large expansion
from Korean species ranged from 15.2%(between TL08 of of deep oceanic water is considered an obstacle to the long-
T. luteostomaand T. turbinoidespair and between TB07 of distance dispersal of many marine benthic taxa, some coastal
T. bronniand T. turbinoidespair) to 16.9%(between TC01 invertebrate taxa have crossed this barrier using a prolonged
of T. clavigeraand T. turbinoidespair). The highest interspe- pelagic larval form(Scheltema, 1971, 1986, 1988) or by
cific sequence divergence(17.7%) was observed between T. rafting(passive transportation of sessile-form juveniles atta-
haemastomaand the genotype TL11 from T. luteostoma. On ched to drifting objects)(ÓFoighil et al., 1999). In cases of
the other hand, sequence comparison within Korean congener- long range dispersion, the juvenile forms of these animal
ic species revealed the T. clavigerasequences to differ con- groups may have the potential to transport and establish
siderably from those of T. luteostoma and T. bronni, with successful colonies thousands of kilometers away in down-
maximum differences ranging from 7.14%(between TC01 stream habitats that are geographically distant from up-
6 Korean J. Syst. Zool. 27(1), 1-17
Genetic Variations of Korean Thais Species
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otide diff 1 - 0.61 0.46 0.46 1.06 0.61 0.61 0.46 0.61 0.15 0.61 0.61 1.98 2.28 1.67 1.82 2.13 2.43 2.28 1.82 1.98 1.98 1.98 1.82 1.82 6.84 5.93 5.62 6.08 5.78 6.08 5.78 6.23 5.62 6.23 16.72 15.65
2.Observed nucle L01 L02 L03 L04 L05 L06 L07 L08 L09 L10 L11 L12 B01 B02 B03 B04 B05 B06 B07 B08 B09 B10 B11 B12 B13 C01 C02 C03 C04 C05 C06 C07 C08 C09 C10 hais haemastoma hais turbinoides
e T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T T
bl
a 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 4 5 6 7
T 1 1 1 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 3 3
Korean J. Syst. Zool. 27(1), 1-17 7
Sang-Hwa Lee, Taeho Kim, Junhee Lee, Jong-Rak Lee, Joong-Ki Park
37 103104101103103101103100103102103105104101102103101104100101102102103103101111106103106104106104108104107119-
00992919090221019399002191212120029-9
6 11001010101111110100111101111111110 0
3 11111111111111111111111111111111111 8.
1
1100213290114623371343433458575528-76
35 4444444434444444444444444 1 6.56.2
11
396827887677028993790001927073774-221
4 43334333333344333433444431 1 1 208
3 1.7.5.
11
13124112109124011591222116929391-3221
3 44444444443444444434444441 1 1 1 1874
3 2.1.6.6.
11
8291382109003512260233322947464-76621
2 3434434443444444444444444 60778
3 1.1.0.6.5.
11
029130210900351226023132292726-176621
31 4434444443444444444444444 0.61.31.00.77.06.1
11
80793809878835122602333221696-1186671
0 34334343333344444444444441 9994088
3 0.0.1.0.1.6.5.
11
0297302109003512260233322927-10176621
9 4433444443444444444444444 93630701
2 0.0.0.1.1.0.7.6.
11
798897987677806771598887727-676622275
28 33333333333334333433333331 1.01.31.01.01.81.51.26.85.6
11
91802910989924011591222119-6010176621
7 3434434433334444443444444 0393630701
2 1.0.0.0.0.1.1.0.7.6.
11
5544657634558067715788877-72777732177
26 4444444444444544454444444 1.31.81.31.61.31.32.41.80.66.86.8
11
243372334144351246343334-432888833475
5 111111111111 126333329553
2 7.6.5.6.6.6.6.6.5.6.6.5.
11
24337243414457346876555-1432888833475
24 111111111111 0.67.16.25.66.36.36.36.36.26.26.56.85.6
11
3544834452554623576544-66088444488925
3 111111111111 74337555530606
2 0.0.7.6.5.6.6.6.6.6.6.6.7.5.
11
354483445255462357654-166088443488920
2 111111111111 674337552530675
2 0.0.0.7.6.5.6.6.6.6.6.6.6.6.5.
11
21 13151414181314141512151544235765-0.610.610.760.467.306.385.786.546.546.546.546.386.086.696.725.50 gera.
11 vi
a
0 1214131317121313141115145734687-7676769161142393383838382393545735 T. cl
2 0.0.0.0.0.7.6.5.6.6.6.6.6.5.6.16.15. TC,
576505667477684579-611166432888832370 ni;
19 111121111111 1.00.90.90.91.00.46.85.95.36.06.06.06.05.95.66.216.515.2 T. bron
Table 2.Continued 1TL012TL023TL034TL045TL056TL067TL078TL089TL0910TL1011TL1112TL1213TB0114TB0215TB0316TB0417TB0518TB0619TB0720TB0821TB0922TB1023TB1124TB1225TB1326TC0127TC0228TC0329TC0430TC0531TC0632TC0733TC0834TC0935TC1036Thais haemastoma37Thais turbinoides TL, Thais luteostoma; TB,
8 Korean J. Syst. Zool. 27(1), 1-17
Genetic Variations of Korean Thais Species
stream source populations using the oceanic current sys- nuclear DNA sequence variation of presumed Crassostrea
tems. Indeed, Thais species have a wide distribution range gigas and Crassostrea angulata specimens: a new oyster
in the Asian Pacific Ocean from the South China Sea area species in Hong Kong? Aquaculture, 228:15-25.
(including Hong Kong, Taiwan) to Northeast Asia(includ- Brown KM, Richardson TD, 1988. Foraging ecology of the
southern oyster drill Thais haemastoma(Gray): constraints
ing Japan and Korea)(Kuroda et al., 1971; Choe and Park,
on prey choice. Journal of Experimental Marine Biology
1997; Tan, 2000; Tan and Liu, 2001). It is possible to envis-
and Ecology, 114:123-141.
age that a continuous influx of larval immigrants from their
Choe BL, 1992. Illustrated encyclopedia of fauna and flora of
potential source populations might contribute to some ex-
Korea. Vol. 33, Mollusca(II). Ministry of Education, Seoul,
tent to the near-shore malacofauna of the Korean Peninsula.
pp. 1-860.
Of the western boundary currents in the North Pacific Choe BL, Park JK, 1997. Description of muricid species(Gas-
Ocean, the Kuroshio Current System is a major component tropoda: Neogastropoda) collected from the coastal areas of
of the most influential warm current that leaves the east coast South Korea. Korean Journal of Biological Sciences, 1:281-
of Taiwan. Its surface water effects travel northeastward to 296.
many regional rocky shores in eastern China, mainland Japan, Clench WJ, 1947. The genera Purpuraand Thaisin the western
and the Korean Peninsula by streams of the Tsushima Cur- Atlantic. Johnsonia, 2:61-91.
Cooke AH, 1919. The radula in Thais, Drupa, Morula, Conc-
rent and Yellow Sea Current. These current systems running
holepus, Cronia, Iopus and the allied genera. Proceedings
northeastward may be able to transport planktotrophic larvae
of the Malacological Society of London, 13:90-110.
or drifting objects that carry sessile forms of life(e.g., egg
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, 1994.
capsules of Thais species) to many different downstream
DNA primers for amplification of mitochondrial cytochrome
islands and/or continental rocky shores. The routine influx
c oxidase subunit I from diverse metazoan invertebrates.
of these types of immigrants from geographically distant Molecular Marine Biology and Biotechnology, 3:294-299.
source populations with different geographic origins(e.g., Fujioka Y, 1985. Systematic evaluation of radula characters in
Taiwan, Hong Kong, and many different coastal regions of Thaidinae(Gastropoda: Muricidae). Journal of Science of
South China and Japan) and their ability to colonize in down- the Hiroshima University, Series B, Division 1, 31:235-287.
stream habitats might act as an effective supplier of new Han BC, Jeng WL, Jeng MS, Kao LT, Meng PJ, Huang YL,
recruitment, thereby shaping the contemporary population 1997. Rock-Shells(Thais clavigera) as an indicator of As,
structure of Korean Thaisspecies. Under this assumption, the Cu, and Zn Contamination on the Putai Coast of the Black-
Foot Disease Area in Taiwan. Archives of Environmental
mt genotypic diversity found among Korean Thais popula-
Contamination and Toxicology, 32:456-461.
tions is likely to reflect a subset of the genetic diversity of
Hayashi T, 1999. Genetic differentiation between the two forms
their potential source populations. Sampling from their po-
of Thais clavigera(Küster, 1858)(Mollusca, Gastropoda)
tential source populations was not included in the present
in Tanabe Bay, Central Japan. Zoological Science, 16:81-86.
study. Therefore, further comprehensive taxon sampling from
Houart R, Gofas S, 2010. ThaisRöding, 1798 [Internet]. World
unstudied potential source populations will be needed to de- Register of Marine Species, Accessed 15 Mar 2011, <http://
termine the origin and key factors responsible for the high www.marinespecies.org/.>
level of genetic diversity discovered within each of the three Hung TC, Hsu WK, Mang PJ, Chuang A, 2001. Organotins and
Korean Thaisspecies examined. imposex in the rock shell, Thais clavigera, from oyster
mariculture areas in Taiwan. Environmental Pollution, 112:
145-152.
Kuroda T, Habe T, Oyama K, 1971. The seashells of Sagami
ACKNOWLEDGEMENTS
Bay. Maruzen Pub. Co., Tokyo, pp. 1-741(in Japanese).
Lam K, Morton B, 2006. Morphological and mitochondrial-
The authors wish to thank Roland Houart for the T. turbin-
DNA analysis of the Indo-West Pacific rock oysters(Ostrei-
oides specimens. This study was supported by a research
dae: Saccostrea species). Journal of Molluscan Studies,
grant of the Chungbuk National University in 2009.
72:235-245.
Lee JS, Min DK, 2002. A catalogue of molluscan fauna in Korea.
Korean Journal of Malacology, 18:93-217.
REFERENCES Min DK, 2004. Mollusks in Korea. Min Molluscan Research
Institute, Seoul, pp. 1-566.
Blackmore G, Wang WX, 2004. Relationships between metallo- ÓFoighil D, Marshall BA, Hilbish TJ, Pino MA, 1999. Trans-
thioneins and metal accumulation in the whelk Thais clavi- Pacific range extension by rafting is inferred for the flat
gera. Marine Ecology Progress Series, 277:135-145. oyster Ostrea chilensis. The Biological Bulletin, 196:122-
Boudry P, Heurtebise S, Lapègue S, 2003. Mitochondrial and 126.
Korean J. Syst. Zool. 27(1), 1-17 9
Sang-Hwa Lee, Taeho Kim, Junhee Lee, Jong-Rak Lee, Joong-Ki Park
Park JK, 1996. Systematic studies of Korean Muricidae(Gastro- Swofford DL, 2002. PAUP: phylogenetic analysis using parsi-
poda: Neogastropoda). PhD dissertation, Sungkyunkwan mony(* and other methods), version 4.0b10. Sinauer Asso-
University, Suwon, Korea, pp. 1-262. ciates, Sunderland, MA.
Park JK, Kim W, 2003. Two Corbicula(Corbiculidae: Bivalvia) Tan KS, 1995. Taxonomy of Thaisand Morula(Mollusca: Gas-
mitochondrial lineages are widely distributed in Asian fresh- tropoda: Muricidae) in Singapore and vicinity. Unpublish-
water environment. Molecular Phylogenetics and Evolution, ed PhD dissertation, National University of Singapore,
29:529-539. Singapore.
Posada D, Crandall KA, 1998. Modeltest: testing the model of Tan KS, 2000. Species checklist of Muricidae(Mollusca: Gastro-
DNA substitution. Bioinformatics, 14:817-818. poda) in the South China Sea. The Raffles Bulletin of Zoo-
Reece KS, Cordes JF, Stubbs JB, Hudson KL, Francis EA, 2008. logy, 8(Suppl):495-512.
Molecular phylogenies help resolve taxonomic confusion Tan KS, Liu LL, 2001. Description of a new species of Thais
with Asian Crassostrea oyster species. Marine Biology, (Mollusca: Neogastropoda: Muricidae) from Taiwan, based
153:709-721. on morphological and allozyme analyses. Zoological Science,
Rubio MR, Tineo P, Diaz J, Torreblanca A, 1993. Effects of 18:1275-1289.
cadmium exposure on the ultrastructure of hepatopancreatic Tan KS, Sigurdsson JB, 1990. A new species of Thais(Gastro-
cells of Thais haemastoma(Gastropoda, Prosobranchia). poda: Muricidae) from Singapore and peninsula Malaysia.
Marine Environmental Research, 35:47-51. The Raffles Bulletin of Zoology, 38:205-212.
Scheltema RS, 1971. Larval dispersal as a means of genetic Tan KS, Sigurdsson JB, 1996. Two new species of Thais(Mol-
exchange between geographically separated populations of lusca: Neogastropoda: Muricidae) from Peninsular Malaysia
shallow-water benthic marine gastropods. The Biological and Singapore, with notes on T. tissoti(Petit, 1852) and T.
Bulletin, 140:284-322. blanfordi(Melvill, 1893) from Bombay, India. The Raffles
Scheltema RS, 1986. Long-distance dispersal by planktonic Bulletin of Zoology, 44:77-107.
larvae of shoal-water benthic invertebrates among central Tang CH, Wang WH, 2009. Organotin accumulation in oysters
Pacific Islands. Bulletin of Marine Science, 39:241-256. and rock shells under field conditions. Journal of Environ-
Scheltema RS, 1988. Initial evidence for the transport of telepla- mental Monitoring, 11:1601-1607.
nic larvae of benthic invertebrates across the east Pacific Tang C-H, Wu SK, 1965. Studies of the radulae of Taiwanmu-
barrier. The Biological Bulletin 174:145-152. ricid gastropods(1). Bulletin of the Institute of Zoology,
Shim WJ, Kahng SH, Hong SH, Kim NS, Kim SK, Shim JH, Academia Sinica, 4:95-106.
2000. Imposex in the rock shell, Thais clavigera, as evidence
of organotin contamination in the marine environment of
Received January 14, 2011
Korea. Marine Environmental Research, 49:435-451. Accepted March 3, 2011
10 Korean J. Syst. Zool. 27(1), 1-17