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Genetic structure of Linckia laevigata and Tridacna crocea populations in the Palawan shelf and shoal reefs

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Allozyme variation of 10 populations of Linckia laevigata at 8 polymorphic loci and 13 populations of Tridacna crocea at 6 polymorphic loci were analyzed to compare genetic variability and genetic affinities among reefs in Palawan, Philippines. Two to five populations were sampled from each of four regions: the shelf reefs in (1) northern Palawan and (2) southern Palawan and the offshore reefs in (3) the Kalayaan island group (KIG) in the South China Sea and (4) the Tubbataha shoals in the Sulu Sea. Heterozygosity was highest in populations of L. laevigata from the south shelf of Palawan and populations of T. crocea from the Tubbataha shoals of the Sulu Sea. The lowest heterozygosity estimates were from the reefs of the KIG in the South China Sea, for both species. Overall FST values for both species were significant, with an estimated average number of effective migrants per generation (NEM) of 4.85 (~5 individuals) for L. laevigata and 3.54 (~4 individuals) for T. crocea. Within-region comparisons showed NEM ranging from 6.29 to 92.34 for L. laevigata and from 3.40 to 6.30 for T. crocea. The higher gene flow among L. laevigata populations relative to T. crocea is consistent with the greater dispersal potential of the former species. Finer scale genetic structuring was evident in T. crocea populations. For both species, the Tubbataha reefs in the Sulu Sea have higher genetic affinity with the populations from the southern shelf of Palawan, while the reefs in the KIG had higher affinity with the northern Palawan shelf reefs. The north and south shelf populations have the least genetic affinity. Genetic patchiness among reefs within regions suggests the importance of small-scale physical factors that affect recruitment success in structuring populations in small island and shoal reef systems in Palawan.
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Genetic structure of
Linckia laevigata
and
Tridacna crocea
populations
in the Palawan shelf and shoal reefs
Received: 27 May 2002 / Accepted: 20 November 2002 / Published online: 11 February 2003
Springer-Verlag 2003
Abstract Allozyme variation of 10 populations of Linc-
kia laevigata at 8 polymorphic loci and 13 populations of
Tridacna crocea at 6 polymorphic loci were analyzed to
compare genetic variability and genetic affinities among
reefs in Palawan, Philippines. Two to five populations
were sampled from each of four regions: the shelf reefs in
(1) northern Palawan and (2) southern Palawan and the
offshore reefs in (3) the Kalayaan island group (KIG) in
the South China Sea and (4) the Tubbataha shoals in the
Sulu Sea. Heterozygosity was highest in populations of
L.laevigata from the south shelf of Palawan and pop-
ulations of T.crocea from the Tubbataha shoals of the
Sulu Sea. The lowest heterozygosity estimates were from
the reefs of the KIG in the South China Sea, for both
species. Overall F
ST
values for both species were signif-
icant, with an estimated average number of effective
migrants per generation (N
EM
) of 4.85 (5 individuals)
for L.laevigata and 3.54 (4 individuals) for T.crocea.
Within-region comparisons showed N
EM
ranging from
6.29 to 92.34 for L.laevigata and from 3.40 to 6.30 for
T.crocea. The higher gene flow among L.laevigata
populations relative to T.crocea is consistent with the
greater dispersal potential of the former species. Finer
scale genetic structuring was evident in T.crocea pop-
ulations. For both species, the Tubbataha reefs in the
Sulu Sea have higher genetic affinity with the popula-
tions from the southern shelf of Palawan, while the reefs
in the KIG had higher affinity with the northern Pala-
wan shelf reefs. The north and south shelf populations
have the least genetic affinity. Genetic patchiness among
reefs within regions suggests the importance of small-
scale physical factors that affect recruitment success in
structuring populations in small island and shoal reef
systems in Palawan.
Introduction
Palawan Island is among the largest islands in the
Philippine archipelago. It represents a unique biogeo-
graphic province because of its dynamic geologic history
(Hall 1996). It is bound in the west by the South China
Sea (SCS), the largest marginal sea in the Indo–West
Pacific region (see Fig. 1). On the east it is bounded by
the Sulu Sea, a small marginal basin in the southern
Philippines that is interconnected to the SCS by a
topographic sill via the Mindoro Strait in the northern
section and the Balabac Strait in the southern portion.
The island province has the highest reef area in the
Philippines, with 37.85% cover. Off the western coast of
the province is the Kalayaan island group (KIG) which
is part of the Spratly Island chain in the South China
Sea. These offshore atoll reefs are hypothesized to be a
critical support system to surrounding shelf habitats by
providing a rich source of pelagic propagules of fish and
invertebrates (McManus 1994; McManus and Men
˜ez
1997; Alin
˜o et al. 1998). On the Sulu Sea side lies
another cluster of offshore reefs, the Tubbataha shoals,
which is renowned for its high diversity of corals and
reef fish (Sandalo 1996; Dantis et al. 1999).
There is an increasing interest in establishing the ge-
netic affinities of reef-associated populations within the
SCS system and among bordering continental reefs,
particularly the shelf and shoal areas of Palawan Island.
Population genetic studies on selected reef organisms
from different shoal and shelf reef systems in Palawan
provide an opportunity to investigate reef connectivity
in this region. Together with hydrodynamic studies,
information on the life-history traits of the selected
species and benthic recruitment patterns derived from
Marine Biology (2003) 142: 717–726
DOI 10.1007/s00227-002-0998-z
M.A. Juinio-Men
˜ez ÆR.M. Magsino
R. Ravago-Gotanco ÆE.T. Yu
Communicated by T. Ikeda, Hakodate
M.A. Juinio-Men
˜ez (&)ÆR.M. Magsino ÆR. Ravago-Gotanco
E.T. Yu
The Marine Science Institute, College of Science,
University of the Philippines, Diliman,
1101 Quezon City, Philippines
E-mail: meneza@upmsi.ph
Tel.: +63-2-9205301
Fax: +63-2-9247678
the resource monitoring surveys, insights on probable
sources and sinks of larvae in this significant geographic
area can be gained.
The blue coral reef starfish Linckia laevigata and the
boring giant clam Tridacna crocea are among the most
ubiquitous reef-associated invertebrates in the shoal and
shelf reefs of Palawan. Both species have planktonic
larval stages, which provide a mechanism for long-dis-
tance dispersal. L.laevigata has a longer larval duration
of 21–28 days (Yamaguchi 1977) compared to the 7- to
14-day potential planktonic period of T.crocea (Shokita
et al. 1991). Previous studies on the population genetics
of L.laevigata (Williams and Benzie 1993, 1996, 1998)
and other tridacnid clams (Benzie and Williams 1992a,
1992b; Macaranas et al. 1992; Benzie and Williams 1995,
1997) using allozyme markers indicate high gene flow
among populations of these species over wide geo-
graphical scales.
The objective of the present study was to compare the
genetic variability and genetic affinities of populations of
these species in order to infer gene flow patterns within
and among small island and shoal reef systems in four
geographic regions in Palawan. The relationships be-
tween genetic structure, dispersal potential and ocean
circulation patterns are discussed.
Materials and methods
Sample collection
Various shoals and fringing reefs of small islands were sampled in
the Linapacan Strait in northern Palawan, the Balabac Strait in
southern Palawan, the Kalayaan island group in the South China
Sea, and the Tubbataha shoals in the Sulu Sea (Fig. 1). Two to
five reefs from each of these regions were sampled for each spe-
cies. The reefs sampled were: El Nido, Pangaldauan, Nangalao,
Cotad and Cambari in northern Palawan; Mantangule, Can-
abungan and Bugsuk in southern Palawan; Panata, Parola, Pag-
asa, Lawak, and Northeast Investigator Shoal in the KIG; and
Jessie Beazley Reef, North and South Islets of the Tubbataha
reefs. A total of 10 populations of Linckia laevigata and
13 populations of Tridacna crocea were sampled. For each reef,
20–38 individuals of each of the target species were collected
during the SCS–Sulu Sea scientific cruises in November 1997,
April 1998 and May 1999.
In the field, collection for both species was done by SCUBA
and snorkeling across shallow reef areas. L.laevigata samples
were maintained in recirculating seawater on board the ship.
Total body weight (g) and arm radius (mm) were determined
prior to the dissection of the pyloric caecum of individual starfish.
For T.crocea, mantle tissues were snipped from individual clams.
Tissue samples were frozen immediately in liquid nitrogen,
transported in dry ice and stored at )70C prior to electropho-
retic analysis.
Fig. 1 Linckia laevigata,Tridacna crocea. Sample collection sites in
the four Palawan regions [i.e. Kalayaan island group, South China
Sea (KIG,SCS); Tubbataha, Sulu Sea; North Palawan; South
Palawan]. Major ocean surface currents in the South China Sea
(Shaw and Chao 1994) and Sulu Sea (Villanoy, personal commu-
nication) during the southwest monsoon. The predominant surface
currents vary with the monsoon winds
718
Allozyme electrophoresis
Standard electrophoretic procedures were followed (Macaranas
1991; Williams 1992). Tissue samples were homogenized in the
presence of extraction buffer (0.04% mercaptoethanol colored with
bromophenol blue), and exudates applied with filter paper wicks to
a 12% horizontal starch gel (Sigma) using Tris-citrate (TC) pH 7.0
buffer. Gels were electrophoresed at 350 V, 40–60 mAmp for
6–8 h. Staining procedures followed Shaw and Prasad (1970). Each
electrophoretic run incorporated a set of reference samples (i.e.
previously characterized allele variants) to ensure consistency of
scoring alleles between gels. Loci were numbered in order of de-
creasing anodal mobility. Alleles were labeled according to their
mobility relative to the most common allele.
Statistical analyses
Genotypic allele frequencies and genetic variability parameters
were calculated using the BIOSYS-1 package (Swofford and
Selander 1981). Conformance of genotype frequencies to Hardy–
Weinberg equilibrium expectations were assessed using a v
2
good-
ness-of-fit and exact-probability tests, both employing Levene’s
(1949) correction for small sample sizes, with levels of significance
adjusted for multiple comparisons with a standard Bonferroni
correction (Lessios 1992). Standardized genetic variance estimates
(F-statistics) were calculated according to Weir and Cockerham
(1984) using ‘‘Tools for Population Genetic Analysis’’ (TFPGA;
Miller 1997). The statistical significance of F
IS
and F
ST
were eval-
uated using the equations given in Waples (1987) to estimate v
2
.
Cluster analysis was performed, and a dendrogram based on un-
biased genetic distance (Nei 1978) was constructed using the un-
weighted pair-group method with arithmetic means (UPGMA).
Pairwise comparisons of F-statistics were conducted to determine
significant genetic differences within and among populations in a
cluster or region. The average number of migrants per generation
(N
EM
) over all populations, within and between each region were
calculated with the equation for an island model, N
EM
=[(1/
F
ST
)·1]/4, using the unbiased estimate of F
ST
.
Results
Around 25–30 enzyme systems were screened for poly-
morphic activity, scorability and resolution in three to
four electrophoretic buffers. Out of these, eight and six
polymorphic loci were used to analyze genetic variation
in Linckia laevigata (Table 1) and Tridacna crocea
(Table 2) populations, respectively. LGG-1* was
resolved for L.laevigata, but was not included in the
analysis, because later screening produced inconsistent
and smeared banding patterns. GPI-1*,LAP-1*,LGG*
and LT* loci for T.crocea were also not included in the
analysis, because they were not scored in all of the
populations.
Population genetic variability
The allele frequencies for eight polymorphic loci of the
ten reef populations of L.laevigata are shown in
Table 1. A single most common allele was found for all
polymorphic loci in L.laevigata, except for LP-1*,
where the most common allele was different (i.e.
LP-1
B
) in both Pangaldauan Is. and El Nido popula-
tions. GPI-1* had the greatest number of alleles, al-
though GPI-1
A
was found only in the El Nido and
Cambari samples. In addition, a rare allele (LT-1
D
) was
found only at NE Investigator. For T.crocea, the most
common allele was the same for all populations, except
in the case of AK-1
C
in Parola (Table 2). Of the six
polymorphic loci, MDH-1* was the most variable with
five alleles, although MDH-1
E
was found only in El
Nido and N. Islet-1 populations. Likewise, both LDH-
1
A
and LDH-1
C
were present in only three populations
at very low or critical levels, indicating the possibility of
losing the two alleles. Exact significance probabilities
and v
2
analysis corrected with Bonferroni procedure
(P<0.05) showed that out of 110 tests, only the LP-1*
locus in two populations of L.laevigata (i.e. Panata and
Cambari Is.) deviated significantly from the Hardy–
Weinberg equilibrium (HWE) expectations. For
T.crocea, out of 78 tests, only the MDH-1* locus in one
population (i.e. Bugsuk) deviated significantly from
HWE expectations.
Table 3 shows the overall percentage polymorphism
and the average heterozygosity of reef populations of
L.laevigata and T.crocea from the four regions sampled
in Palawan. The mean heterozygosity was higher for
L.laevigata (H
o
=0.282) than T.crocea (H
o
=0.199).
Overall, the starfish populations also showed greater
percentage of polymorphism (72%) compared with the
clam populations (63%). The average number of alleles
per polymorphic locus ranged from two to five alleles for
both species. Of the four regions, the KIG populations
had the lowest average heterozygosity for both inverte-
brate species. The highest average heterozygosity esti-
mates were observed in southern Palawan for
L.laevigata and in the Tubbataha shoals for T.crocea.
Population genetic structure
The standardized genetic variance in L.laevigata based
on eight polymorphic loci is shown in Table 4. There
was significant within-population variation for LP-1*,
but multiloci F
IS
was not significant (F
IS
=0.0669) in the
populations sampled. Three loci (HK-1*,PGM-1* and
LP-1*) contributed to the significant overall interpopu-
lation genetic variation (F
ST
=0.0490). Based on F
ST
, the
estimated number of effective migrants per generation
(N
EM
) is 4.85 individuals. The standardized genetic
variance based on six polymorphic loci in T.crocea
populations is shown in Table 5. Significant intrapopu-
lation variation was found in all loci. Thus, overall
within-population genetic differentiation across all loci
(F
IS
=0.2763) was highly significant. Likewise, all poly-
morphic loci, except MDH-2*, were significant between
populations, resulting in a highly significant overall in-
terpopulation variation (F
ST
=0.0660). The estimated
N
EM
for T.crocea is 3.54 individuals.
Within-region analysis revealed significant genetic
structure within populations of T.crocea in the KIG
(Table 6). Likewise, pairwise F
IS
values between regions
719
were significant, with the exception of pairwise estimates
between Tubbataha and south Palawan for T.crocea.In
contrast, there was no intrapopulation genetic structur-
ing in L.laevigata populations within or between re-
gions. Significant interpopulation (F
ST
) differences were
observed in all regions for T.crocea and only in north
and south Palawan for L.laevigata.
The dendrogram based on unbiased genetic distance
of Nei (1978) for the ten sampled reef populations of
L.laevigata is shown in Fig. 2. Genetic distance values
ranged from 0.003 to 0.064 (matrix not shown). In
general, there is clustering of geographically close pop-
ulations, but with some exceptions. Pairwise F
ST
com-
parisons indicate three significantly different clusters:
KIG populations in the SCS with Cambari in north
Palawan; Sulu Sea populations with Canabungan in
south Palawan; and El Nido–Pangaldauan reefs, both in
northwest Palawan. In addition, Nangalao Island (north
Table 1 Linckia laevigata. Allele frequencies for the eight polymorphic loci in ten populations from Palawan shelf and shoal reefs (KIG
Kalayaan island group; SCS South China Sea; Tubb Tubbataha; SS Sulu Sea; NP North Palawan; SP South Palawan)
Locus Population
KIG, SCS Tubb, SS NP SP
Panata NE Inves-
tigator
S. Islet N. Islet Cambari Pangal-
dauan
El
Nido
Nanga-
lao
Cana-
bungan
Mantan-
gule
HK-1* (N)2630 292229 3032262625
A 0.346 0.183 0.293 0.500 0.190 0.267 0.281 0.173 0.346 0.040
B 0.462 0.550 0.586 0.386 0.466 0.317 0.531 0.519 0.404 0.380
C 0.192 0.267 0.121 0.091 0.259 0.267 0.156 0.135 0.250 0.440
D 0.000 0.000 0.000 0.023 0.086 0.150 0.031 0.173 0.000 0.140
SOD-1* (N)2630 292229 3032262625
A 0.019 0.050 0.052 0.068 0.069 0.083 0.094 0.038 0.135 0.080
B 0.962 0.917 0.879 0.886 0.931 0.850 0.875 0.904 0.827 0.860
C 0.019 0.033 0.069 0.045 0.000 0.067 0.031 0.058 0.038 0.060
MDH-1* (N)2630 292229 3032262625
A 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000
IDHP-1* (N)2630 292229 3032262625
A 0.019 0.033 0.086 0.023 0.017 0.033 0.031 0.038 0.038 0.020
B 0.923 0.883 0.724 0.864 0.828 0.783 0.828 0.827 0.827 0.820
C 0.000 0.017 0.190 0.091 0.086 0.117 0.109 0.058 0.058 0.120
D 0.058 0.067 0.000 0.023 0.069 0.067 0.031 0.077 0.077 0.040
PGM-1* (N)2630 292229 3032262625
A 0.308 0.217 0.328 0.477 0.172 0.250 0.313 0.173 0.346 0.040
B 0.500 0.517 0.552 0.409 0.483 0.350 0.469 0.538 0.423 0.400
C 0.192 0.267 0.121 0.091 0.259 0.250 0.188 0.115 0.221 0.440
D 0.000 0.000 0.000 0.023 0.086 0.150 0.031 0.173 0.000 0.120
MPI-1* (N)2630 292229 3032262625
A 0.019 0.033 0.086 0.023 0.017 0.050 0.031 0.058 0.058 0.020
B 0.923 0.867 0.741 0.841 0.828 0.783 0.828 0.827 0.827 0.820
C 0.000 0.017 0.172 0.114 0.086 0.100 0.094 0.038 0.038 0.120
D 0.058 0.083 0.000 0.023 0.069 0.067 0.047 0.077 0.077 0.040
LGG-2* (N)2630 292229 3032262625
A 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000
LT-1* (N)2630 292229 3032262625
A 0.250 0.183 0.293 0.227 0.155 0.350 0.250 0.327 0.385 0.320
B 0.000 0.067 0.000 0.000 0.000 0.150 0.063 0.019 0.000 0.000
C 0.750 0.733 0.707 0.773 0.845 0.500 0.688 0.654 0.615 0.680
D 0.000 0.017 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000
LT-2* (N)2630 292229 3032262625
A 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000
LP-1* (N)2630 292229 3032262625
A 0.077 0.017 0.052 0.000 0.000 0.050 0.094 0.346 0.115 0.100
B 0.231 0.033 0.017 0.091 0.431 0.600 0.563 0.077 0.000 0.000
C 0.519 0.683 0.741 0.727 0.500 0.283 0.250 0.519 0.885 0.900
D 0.173 0.200 0.069 0.114 0.069 0.033 0.063 0.000 0.000 0.000
E 0.000 0.067 0.121 0.068 0.000 0.033 0.031 0.058 0.000 0.000
GPI-1* (N)2630 292229 3032262625
A 0.000 0.000 0.000 0.000 0.017 0.000 0.016 0.000 0.000 0.000
B 0.038 0.033 0.086 0.023 0.000 0.033 0.016 0.038 0.038 0.020
C 0.904 0.883 0.741 0.841 0.828 0.800 0.828 0.846 0.846 0.820
D 0.000 0.000 0.172 0.114 0.086 0.100 0.094 0.038 0.038 0.120
E 0.058 0.083 0.000 0.023 0.069 0.067 0.047 0.077 0.077 0.040
H
e
0.168 0.209 0.307 0.244 0.251 0.373 0.259 0.325 0.357 0.331
No. of alleles 2.5 2.9 2.5 2.9 2.7 3.1 3.2 3.0 2.5 2.7
Percent polymorphism 63.7 72.7 72.7 72.7 72.7 72.7 72.7 72.7 72.7 72.7
720
Table 2 Tridacna crocea. Allele frequencies for the six polymorphic loci in 13 populations from Palawan shelf and shoal reefs (abbreviations, see Table 1)
Locus Populations
KIG, SCS Tubb, SS NP SP
NE Inves-
tigator
Pag–
asa
Parola Panata Lawak J. Beazley N. Islet-1 N. Islet-2 Pangaldauan Cotad El Nido Canabungan Bugsuk
AK-1* (N)32 311020 34 35 28 29 19 3015 31 34
A 0.219 0.452 0.100 0.400 0.265 0.300 0.268 0.034 0.211 0.167 0.300 0.145 0.059
B 0.703 0.516 0.400 0.525 0.603 0.700 0.732 0.638 0.579 0.517 0.433 0.790 0.794
C 0.078 0.032 0.500 0.075 0.132 0.000 0.000 0.328 0.211 0.317 0.267 0.065 0.147
CK-1* (N)32 312020 36 35 28 29 27 3023 32 34
A 0.063 0.032 0.050 0.425 0.014 0.129 0.232 0.034 0.315 0.133 0.239 0.047 0.029
B 0.828 0.613 0.650 0.475 0.875 0.857 0.750 0.845 0.630 0.650 0.543 0.859 0.853
C 0.109 0.355 0.300 0.100 0.111 0.014 0.018 0.121 0.056 0.217 0.217 0.094 0.118
IDHP-1* (N)32 331620 38 35 28 29 27 3037 32 34
A 0.063 0.015 0.156 0.075 0.013 0.000 0.036 0.000 0.000 0.017 0.135 0.047 0.250
B 0.094 0.182 0.031 0.150 0.132 0.100 0.161 0.086 0.222 0.317 0.014 0.125 0.132
C 0.797 0.773 0.688 0.775 0.855 0.857 0.786 0.914 0.778 0.667 0.757 0.813 0.529
D 0.047 0.030 0.125 0.000 0.000 0.043 0.018 0.000 0.000 0.000 0.095 0.016 0.088
LDH-1* (N) 32 33 4 13 36 35 28 29 27 30 37 32 34
A 0.000 0.000 0.000 0.000 0.014 0.029 0.000 0.000 0.000 0.000 0.000 0.000 0.147
B 1.000 1.000 1.000 1.000 0.972 0.971 0.964 1.000 1.000 1.000 1.000 0.984 0.853
C 0.000 0.000 0.000 0.000 0.014 0.000 0.036 0.000 0.000 0.000 0.000 0.016 0.000
LDH-2* (N)32 332016 38 35 28 29 27 3037 32 34
A 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000
MDH-1* (N)31 302020 32 29 25 24 20 2636 30 32
A 0.016 0.000 0.000 0.000 0.328 0.069 0.000 0.042 0.000 0.115 0.000 0.133 0.234
B 0.145 0.083 0.200 0.175 0.016 0.293 0.200 0.438 0.375 0.000 0.000 0.150 0.219
C 0.839 0.767 0.775 0.800 0.438 0.483 0.400 0.500 0.625 0.577 0.750 0.483 0.484
D 0.000 0.150 0.025 0.025 0.219 0.155 0.320 0.021 0.000 0.308 0.194 0.233 0.063
E 0.000 0.000 0.000 0.000 0.000 0.000 0.080 0.000 0.000 0.000 0.056 0.000 0.000
MDH-2* (N)31 311315 38 35 27 28 16 2837 31 31
A 0.016 0.048 0.000 0.000 0.000 0.043 0.074 0.054 0.000 0.107 0.230 0.129 0.016
B 0.145 0.048 0.192 0.233 0.184 0.129 0.111 0.107 0.156 0.107 0.054 0.210 0.145
C 0.839 0.758 0.769 0.700 0.816 0.829 0.815 0.821 0.844 0.786 0.716 0.613 0.823
D 0.000 0.145 0.038 0.067 0.000 0.000 0.000 0.018 0.000 0.000 0.000 0.048 0.016
ME-1* (N)32 331020 38 35 28 29 27 3037 32 34
A 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000 1.000
H
e
0.166 0.188 0.206 0.19 0.178 0.211 0.226 0.2 0.188 0.22 0.214 0.177 0.223
No. of alleles 2.4 2.5 2.4 2.3 2.5 2.4 2.5 2.4 1.9 2.3 2.4 2.8 2.8
Percentpolymorphism 62.5 62.5 62.5 62.5 62.5 62.5 62.5 62.5 62.5 62.5 62.5 62.5 75
721
Palawan) and Mantangule Island (south Palawan) were
significantly different from each other as well as from the
other three clusters. The El Nido–Pangaldauan reef
cluster was the most genetically distinct. These popula-
tions were different even from Cambari and Nangalao,
which are also in the northern Palawan region although
on the Sulu Sea side.
Genetic distance among the 13 reef localities sampled
for T.crocea ranged from 0.001 to 0.067 (matrix not
shown). The populations were divided into two signifi-
cant major clusters (Fig. 3). The first cluster includes all
the populations from the Sulu Sea and southern Pala-
wan, with the addition of Lawak in the KIG. The second
Table 3 Linckia laevigata,Tridacna crocea. Overall measures of percentage polymorphism and average heterozygosity (SD in parentheses)
of reef populations from four geographical regions of Palawan shelf and shoal reefs
No. ofsites L.laevigata No. ofsites T.crocea
Mean heterozygosity 0.282 (0.067) 0.199 (0.022)
Kalayaan is. group, South China Sea 2 0.189 (0.029) 5 0.183 (0.053)
Tubbataha, Sulu Sea 2 0.276 (0.045) 3 0.212 (0.064)
North Palawan 4 0.302 (0.058) 3 0.206 (0.063)
South Palawan 2 0.344 (0.018) 2 0.201 (0.054)
Percentpolymorphism 72 63
Table 4 Linckia laevigata. Standardized genetic variance at eight
polymorphic loci in ten populations from Palawan shelf and shoal
reefs (**significant at P<0.01; N
EM
=4.85 individuals)
Locus F
IS
F
ST
HK-1* –0.0245 0.0370**
SOD-1* –0.0886 –0.0013
IDHP-1* 0.0573 0.0045
PGM-1* 0.0086 0.0292**
MPI-1* 0.0584 0.0016
LT-1* –0.0919 0.0227
LP-1* 0.4810** 0.1917**
GPI-1* 0.0683 0.0023
Mean 0.0669 0.0490**
Table 5 Tridacna crocea. Standardized genetic variance at 6 poly-
morphic loci in 13 populations from Palawan shelf and shoal reefs
(**significant at P<0.01; N
EM
=3.54 individuals)
Locus F
IS
F
ST
AK-1* 0.3664** 0.0657**
CK-1* 0.2582** 0.0823**
IDHP-1* 0.2573** 0.0415**
LDH-1* 0.2995** 0.0654**
MDH-1* 0.2443** 0.0966**
MDH-2* 0.2317** 0.0180
Mean 0.2763** 0.0660**
Table 6 Linckia laevigata,Tridacna crocea. Average Nei’s unbiased genetic distance (D), F
ST
averaged overall loci and the average
number of migrants per generation (N
EM
) for various sets ofpopulations from Palawan shelf and shoal reefs (Snumber of populations; N
total number of individuals; *P<0.05,**P<0.01)
Regions considered SN Nei’s DF
IS
F
ST
N
EM
Within-region comparisons
T.crocea Kalayaan island group, South China Sea 5 143 0.0226 0.2995* 0.0689** 3.40
Tubbataha reefs, Sulu Sea (Tubb) 3 92 0.0115 0.1656 0.0410** 5.80
North Palawan (NP) 3 94 0.0155 0.3292 0.0387** 6.20
South Palawan (SP) 2 66 0.0134 0.3307 0.0380** 6.30
L.laevigata KIG, South China Sea 2 56 0.0020 0.3049 0.0027 92.34
Tubbataha reefs, Sulu Sea 2 51 0.0041 0.0801 0.0121 20.41
North Palawan 4 117 0.0110 0.0747 0.0316** 7.66
South Palawan 2 51 0.0096 0.1907 0.0382** 6.29
Between-region comparisons
T.crocea KIG+Tubb 2 235 0.0096 0.2787** 0.0354** 6.81
KIG+NP 2 237 0.0052 0.3417** 0.0164** 14.99
KIG+SP 2 209 0.0130 0.3342** 0.0428** 5.59
Tubb+NP 2 186 0.0135 0.2667* 0.0454** 5.26
Tubb+SP 2 158 0.0076 0.2582 0.0249** 9.79
NP+SP 2 160 0.0180 0.3347** 0.0538** 4.40
L.laevigata KIG+Tubb 2 107 0.0073 0.1941 0.0227** 10.76
KIG+NP 2 173 0.0096 0.1556 0.0295** 8.22
KIG+SP 2 107 0.0092 0.0617 0.0305** 7.95
Tubb+NP 2 168 0.0165 0.0946 0.0501** 4.74
Tubb+SP 2 102 0.0104 –0.0394 0.0351** 6.87
NP+SP 2 168 0.0193 0.0205 0.0593** 3.97
722
cluster includes all the north Palawan populations and
the other populations from the KIG. However, com-
parison of standardized genetic variance revealed finer
scale genetic differentiation among populations both
between and within each of the major clusters. For ex-
ample, samples from two sites at N. Islet in the first
major cluster were significantly different from each
other. Likewise, the two populations from southern
Palawan were significantly different from each other. In
the second cluster, Panata and Parola samples (KIG)
showed greater genetic affinities, with north Palawan
populations, Pangaldauan and El Nido respectively,
than with other KIG populations (i.e. Northeast Inves-
tigator and Pag-asa).
Gene flow estimates within the four regions are
higher in L.laevigata than T.crocea (Table 6). The
highest N
EM
was over 90 individuals in the KIG for
L.laevigata populations, with gene flow higher in the
offshore reef populations than the shelf reefs. In con-
trast, relative gene flow levels among T.crocea popula-
tions in the north and south shelf reefs were higher than
those in the KIG and Tubbataha reefs. All pairwise
comparisons between the four regions showed signifi-
cant interpopulation (F
ST
) genetic differences for both
species. Interestingly, relative gene flow patterns between
regions are similar for both species. Results indicate the
least gene flow was estimated between north and south
Palawan. Gene flow between KIG and north Palawan is
greater than that with south Palawan. Moreover, gene
flow between Tubbataha and south Palawan is greater
than that with north Palawan. The relative gene flow
between the KIG and Tubbataha was intermediate for
T.crocea, but was highest of all regional pairwise
comparisons for L.laevigata, suggesting higher gene
flow between the SCS and Sulu Sea for the latter species.
Discussion
Genetic variability
The relatively higher genetic variability of populations
of Linckia laevigata and Tridacna crocea in the Palawan
shelf reefs and the Tubbataha shoals compared to the
KIG reefs may be due to the greater potential sources of
propagules in these regions. The north and south shelf
reef samples were collected in the Linapacan and Bala-
bac Straits, where there is regular exchange of waters
between the Sulu and South China Sea. In the case of the
Tubbataha shoals, Pacific Ocean waters passing through
the San Bernardino Strait, as well as those from the
Mindanao and Celebes Seas, provide rich sources of
larvae. In addition, the more adverse atmospheric
and hydrographic elements in the KIG result in lower
recruitment success in this region.
The mean heterozygosity estimates for both species in
this study were lower compared to reported values from
other populations of the blue coral starfish and other
giant clam species listed in Table 7. Although different
sets of loci were analyzed, the lower average hetero-
zygosity may be due to the lower mean number of alleles
per locus found in the present study. For example, the
GPI-1* locus of L.laevigata in the Great Barrier Reef
had seven alleles (Williams and Benzie 1993) compared
to only five in the Palawan reefs. This is consistent with
results reported by Williams and Benzie (1996) for
populations collected from other localities in the Phil-
ippines.
Gene flow
The relatively lower genetic affinity between north and
south shelf reefs may be due to distance and the presence
of a land barrier that minimizes gene flow between these
shelf reefs. Despite the long distance between the Tub-
bataha reefs and the southern shelf reefs, high genetic
Fig. 2 Linckia laevigata. Dendrogram showing genetic relation-
ships of ten reef populations based on Nei’s (1978) unbiased genetic
distance D. Populations with the same superscript are not
significantly different (P<0.01) (abbreviations, see Table 1)
Fig. 3 Tridacna crocea. Dendrogram showing genetic relationships
of 13 reef populations based on Nei’s (1978) unbiased genetic
distance D. Populations with the same superscript are not
significantly different (P<0.01) (abbreviations, see Table 1)
723
exchange may occur through a stepwise mechanism of
larval dispersal and recruitment along the series of reefs
between the two regions. This may be facilitated by
longshore currents and the prevailing southern surface
drift in the Sulu Sea (Fig. 1). However, the same cannot
be invoked for exchange between the KIG and northern
Palawan, which are separated by a wide distance of open
waters. Larval dispersal models based on surface ve-
locity fields and mean monthly geostrophic velocities in
the KIG region indicate that larval advection from the
KIG to other regions in Palawan is weak and very
variable (Villanoy and Salamante, unpublished data). In
particular, strong horizontal gradients in the KIG sur-
face currents showed a lack of distinct and persistent
flow from the KIG towards northern Palawan. How-
ever, currents from the SCS, passing through the KIG,
move towards western Palawan, merging with a north-
ward longshore current. Thus, shelf reefs along north-
western Palawan are potential staging posts for the
northward dispersal of both species. In the case of the
two offshore reef systems, gene flow between these re-
gions were intermediate compared to that between other
regions, for T.crocea, and was highest for L.laevigata.
This indicates effective larval dispersal between the SCS
and Sulu Sea populations through the northern and
southern shelf reefs of Palawan.
Genetic structure
The generally higher gene flow and lower genetic struc-
turing among L.laevigata populations relative to
T.crocea within and among the different regions in
Palawan are consistent with expectations, considering
the longer larval duration (i.e. greater dispersal poten-
tial) of the former species. Results of the present study
conform to previous studies on giant clams and the blue
coral starfish (i.e. see F
ST
values, Table 7) as well as
those for other marine species, in which the length of
planktonic larval period and the degree of population
subdivision are broadly correlated (e.g. reviewed in
Shaklee and Bentzen 1998).
The genetic structuring of populations of L.laevigata
and T.crocea in Palawan (i.e. within a region of less
than four degrees latitude and longitude) is very fine
scale compared to previous reports. For instance, ge-
netic structuring of L.laevigata in Palawan is higher
than structuring among the vast Pacific and Indian
Ocean populations (Williams and Benzie 1998). No ge-
netic structuring was reported for the species in the East
Indian–West Pacific (Williams and Benzie 1996) and the
Great Barrier Reef (Williams and Benzie 1993). Fine-
scale genetic structuring in L.laevigata populations was
evident within north and south shelf reef populations,
which are only 5–35 km apart. Larval retention in the El
Nido–Pangaldauan reefs may be favored by the presence
of embayments and the strong northern currents run-
ning along the western portion of Palawan (Villanoy and
Salamante, unpublished data). In addition, larval dis-
persal and recruitment in the Linapacan and Balabac
Straits maybe influenced by highly variable tidal flows
within these shallow reef shelf areas.
Earlier population genetic studies on giant clams in
the Pacific revealed little genetic differentiation between
widely separated populations (reviewed in Benzie and
Williams 1995). However, more recent studies showed
structuring between reef groups on different archipela-
goes in the Pacific (Benzie and Williams 1997). The lack
of correspondence between major oceanic surface cur-
rents and the routes of gene flow of three giant clam
species, suggests strong historical influence on the giant
clams’ population genetic structure in the West and
Central Pacific. No previous studies have been con-
ducted for T.crocea, but the reported F
ST
for T.maxima
(which is most similar to T.crocea in habit) from the
Western Coral Sea (Benzie and Williams 1992a) is
markedly lower than that of the populations of T.crocea
in Palawan. Although F
ST
estimates for T.maxima
populations across the Pacific are higher (F
ST
=0.156;
Benzie and Williams 1997), F
ST
among the Central Pa-
cific islands is comparable to the Palawan samples, de-
spite the large difference in geographic scales. In the
same study, no significant genetic differentiation was
observed among two reef sites in the Philippines, i.e.
Bantayan Island and Tawi-Tawi (F
ST
=–0.002), which
are separated by greater geographic distance compared
to the Palawan sites in the present study.
The difference in geologic history of the Sulu Sea and
the South China Sea (Hall 1996; Schluter et al.1996) may
contribute to genetic structuring of reefs in Palawan.
Table 7 Linckia laevigata,Tridacna crocea. Comparison of the standardized genetic variance (F
ST
) for both invertebrates from other
geographic scales (* significant atP<0.01)
L.laevigata Tridacnaspp. Source
Pacific Ocean and Indian Ocean 0.030* Williamsand Benzie (1998)
West and Central Pacific Ocean 0.096* (T.gigas) Benzieand Williams (1995)
0.156* (T.maxima) Benzieand Williams (1997)
Indo-WestPacific 0.002 Williamsand Benzie (1996)
0.098* (T.derasa) Macaranas et al. (1992)
Great Barrier Reefs, Australia 0.001 Williamsand Benzie (1993)
0.000 (T.gigas) Benzieand Williams (1992a)
Western Coral Sea 0.019* (T.maxima) Benzieand Williams (1992b)
Kalayaan island group, South China Sea, and Sulu Sea 0.049* 0.066* (T.crocea) Presentstudy
724
Based on studies of the tectonics and sea-level changes in
Southeast Asia, the Sulu Sea basin was intermittently
isolated from the South China Sea (reviewed by McM-
anus 1985). Notably, despite the history of isolation and
the presence of a persistent land barrier (i.e. Palawan
land mass), gene flow between the two offshore reef
systems is high. Given the small geographic scale, all
populations within each of the four regions in Palawan
would have been influenced by similar past events and
oceanic currents. However, there was significant struc-
turing within all four regions in T.crocea populations
and in two regions for L.laevigata. The pronounced
genetic structuring among reefs in the KIG, particularly
in the case of T.crocea (e.g. Lawak is only 110 and
160 km from Northeast Investigator and Panata, re-
spectively), may reflect highly random recruitment pat-
terns as influenced by adverse environmental conditions
in this region relative to the other regions in Palawan.
Information on larval behavior and local hydrographic
conditions as affected by reef topographies (e.g.
Wolanski and Sarsenki 1997) could provide more
insights on how these may influence larval dispersal and
recruitment success. Nonetheless, fine-scale genetic
patchiness reported in the present study is concordant
with reef variation in the genetic structure and distri-
bution of L.laevigata color morphs in the KIG (Mag-
sino et al. 2002; Juinio-Men
˜ez, personal observations),
the patterns of coral reef community structure, and
differences in survivorship and growth of coral recruits
in Palawan reefs (Quibilan and Alin
˜o, unpublished da-
ta). The reef systems sampled in Palawan are shoals and
fringing reefs on small isolated islands surrounding the
island province. The Sulu and South China Sea differ-
entially influence these diverse reef habitats with respect
to atmospheric (e.g. storms) and hydrographic processes
(e.g. seasonally reversing currents, tidal flows). Thus,
effective gene mixing over wider geographical scales may
be reduced, resulting in genetic patchiness.
In conclusion, despite the potential for long larval
dispersal across large geographic areas, fine-scale genetic
structuring of L.laevigata and T.crocea populations
was evident between and within four geographical reef
areas in Palawan, Philippines. These results provide in-
sights into the importance of present-day local physical
processes that may affect recruitment success among the
diverse reefs of Palawan, including the relatively isolated
reef system in the KIG. The lower heterozygosity and
genetic patchiness in the KIG reefs suggest that larval
recruitment is highly variable and may be limited by
higher mortality rates compared to other reef areas in
Palawan. The patterns of genetic affinities among the
four regions for both species indicate considerable gene
flow among offshore and shelf reefs and high connec-
tivity between the South China Sea and the Sulu Sea,
despite the presence of a land barrier and past basin
isolation. Further studies are needed to test hypotheses
on local ecological processes that influence the fine-scale
genetic structure of reef organisms in the Palawan reefs.
Likewise, studies over a broader geographic area in the
South China Sea may provide better insights into the
influence of past biogeographic events.
Acknowledgements The authors thank the SCS–Sulu Sea dive col-
lection team for assistance in the sample collection, particularly
Dr. P. Alin
˜o, who also provided assistance on various aspects of
this study, and Dr. C. Villanoy for valuable oceanographic inputs.
This research is part of the South China Sea research program
funded by Department of Science and Technology–Philippine
Council for Aquatic and Marine Research and Development
(DOST–PCAMRD). We are also grateful for the comments of an
anonymous reviewer, which helped improve the manuscript. This is
contribution number 327 from the University of the Philippines
Marine Science Institute (UPMSI).
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726
... Taking into account all of these eco-biological aspects, considerable genetic differentiation is highly expected among populations of T. maxima. Various population genetic studies, reporting on nuclear and mitochondrial DNA variation in T. maxima, supported this assumption (Laurent et al., 2002;Juinio-Meñez et al., 2003;DeBoer et al., 2008;Kochzius and Nuryanto, 2008;Nuryanto and Kochzius, 2009;Ahmed Mohamed et al., 2016;Hui et al., 2016). Indeed, restricted gene flow was revealed within and among various Indo-Pacific giant clam populations. ...
... Pattern of genetic homogeneity was also recorded within other marine species across the same surveyed geographic spectrum, such as in the reef-building coral Pocillopora verrucosa (Robitzch et al., 2015). However, our finding clearly contrasts with those of earlier population genetic studies of T. maxima (using nuclear and mitochon-drial DNA markers) unveiling significant genetic differentiation and marked patterns of restricted gene flow across other parts of the distribution zone (Laurent et al., 2002;Juinio-Meñez et al., 2003;DeBoer et al., 2008;Kochzius and Nuryanto, 2008;Nuryanto and Kochzius, 2009;Ahmed Mohamed et al., 2016;Hui et al., 2016). ...
... Taking into account all of these eco-biological aspects, considerable genetic differentiation is highly expected among populations of T. maxima. Various population genetic studies, reporting on nuclear and mitochondrial DNA variation in T. maxima, supported this assumption (Laurent et al., 2002;Juinio-Meñez et al., 2003;DeBoer et al., 2008;Kochzius and Nuryanto, 2008;Nuryanto and Kochzius, 2009;Ahmed Mohamed et al., 2016;Hui et al., 2016). Indeed, restricted gene flow was revealed within and among various Indo-Pacific giant clam populations. ...
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... Taking into account all of these eco-biological aspects, considerable genetic differentiation is highly expected among populations of T. maxima. Various population genetic studies, reporting on nuclear and mitochondrial DNA variation in T. maxima, supported this assumption (Laurent et al., 2002;Juinio-Meñez et al., 2003;DeBoer et al., 2008;Kochzius and Nuryanto, 2008;Nuryanto and Kochzius, 2009;Ahmed Mohamed et al., 2016;Hui et al., 2016). Indeed, restricted gene flow was revealed within and among various Indo-Pacific giant clam populations. ...
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The present investigation focuses on population genetic structure analysis of the endangered giant clam species Tridacna maxima across part of the Red Sea, with the main aim of assessing the influence of postulated potential barriers to gene flow (i.e., particular oceanographic features and marked environmental heterogeneity) on genetic connectivity among populations of this poorly dispersive bivalve species. For this purpose, a total of 44 specimens of T. maxima were collected from five sampling locations along the Saudi Arabian coast and examined for genetic variability at the considerably variable mitochondrial gene cytochrome c oxidase I (COI). Our results revealed lack of population subdivision and phylogeographic structure across the surveyed geographic spectrum, suggesting that neither the short pelagic larval dispersal nor the various postulated barriers to gene flow in the Red Sea can trigger the onset of marked genetic differentiation in T. maxima. Furthermore, the discerned shallow COI haplotype genealogy (exhibiting high haplotype diversity and low nucleotide diversity), associated with recent demographic and spatial expansion events, can be considered as residual effect of a recent evolutionary history of the species in the Red Sea.
... Despite this high biodiversity, studies on the genetic population structure and gene flow in marine taxa of the PA are rather rare. The few studies conducted investigated L. laevigata and T. crocea in Palawan (South China Sea and Sulu Sea; Magsino et al., 2002;Juinio-Meñez et al., 2003), T. crocea at the Western Pacific coast of the Visayas (Ravago-Gotanco et al., 2007), the anemonefish Amphiprion clarkii in Cebu (Pinsky et al., 2010), rabbitfishes along the eastern coast (Magsino & Juinio-Meñez, 2008) and the sea urchin Tripneustes gratilla (Malay et al., 2000). Hence, information on connectivity of marine population within the PA and their connectivity to other regions in the IMA is limited. ...
... Only on an ocean-wide scale, could a significant differentiation between populations of the Indian and Pacific Oceans be detected (Williams & Benzie, 1997;Crandall et al., 2008;Kochzius et al., 2009). However, investigations on a much smaller scale in Palawan (PA) revealed a low but significant differentiation (Juinio-Meñez et al., 2003), indicating that probably local oceanographic and geographic conditions can limit connectivity among populations. In the Visayas, other taxa such as the anemonefish A. clarkii (Cebu) and the giant clam T. crocea (Eastern Philippine seaboard) also show restricted gene flow (Ravago-Gotanco et al., 2007;Pinsky et al., 2010). ...
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Coral reef associated marine invertebrates, such as the blue sea star Linckia laevigata , have a life history with two phases: sedentary adults and planktonic larvae. On the one hand it is hypothesised that the long pelagic larval duration facilitates large distance dispersal. On the other hand, complex oceanographic and geographic characteristics of the Visayan seascape could cause isolation of populations. The study aims to investigate the genetic diversity, genetic population structure and gene flow in L. laevigata to reveal connectivity among populations in the Visayas. The analysis is based on partial sequences (626 bp in length) of the mitochondrial cytochrome oxidase I gene (COI) from 124 individuals collected from five localities in the Visayas. A comparative analysis of these populations with populations from the Indo-Malay Archipelago (IMA) published previously is also presented. Genetic diversity was high ( h = 0.98, π = 1.6%) and comparable with preceding studies. Analyses of molecular variance (AMOVA) revealed a lack of spatial population differentiation among sample sites in the Visayas (Φ ST -value = 0.009; P > 0.05). The lack of genetic population structure indicates high gene flow among populations of L. laevigata in the Visayas. Comparative analysis with data from the previous study indicates high connectivity of the Visayas with the central part of the IMA.
... The absence of much older T. gigas in TRNP suggests that these recruits came from other areas within the Sulu Sea or other localities. The hydrographic flow within Palawan are interconnected from different areas within the West Philippines Sea (WPS) and Sulu Sea (Juinio-Meñez et al. 2003;Tangunan and Peleo-Alampay 2018), and we do not discount the possibility of recruits coming from the different successfully managed restocking sites in the country. A genetic study could help verify the origin of these recruits. ...
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Tridacna gigas (Cardiidae: Tridacninae) is the largest extant reef-associated bivalves that occur abundantly in the Indo-West Pacific Region. However, unregulated exploitation had caused localized extinction in many parts of its distribution range. In Palawan, the species was considered virtually extinct in the 1980s, and since then, no study has been done to monitor their status in the wild. In the absence of updated studies about T. gigas, we gathered information through field reports, key informants, and field visits. Within five months of data gathering, we recorded 97 empty shells (14 in pairs and 83 single shells) with 65.86 cm (range: 42-112 cm) average shell length, which were estimated to be from 5 to >76 years old. Most (78.36%) of the empty shells were used for decoration and landscaping. On the other hand, 29 live individuals with 73.69 cm (range: 42-109 cm) average shell length were estimated to be 5 to >76 years old. Tubbataha Reefs Natural Park and some island resorts harbored the highest number of live T. gigas. The presence of live T. gigas in these areas reflects years of effective management and the resorts' essential contribution to resource conservation. These remaining live individuals could be used in breeding and restocking programs to restore their lost populations.
... Furthermore, sub-population structure within the SCS was revealed on other fish species, for example, the six bar wrasse (Thallassoma hardwicki) (Chen et al., 2004) and the mottled spinefoot Siganus fuscescens (Ravago-Gotanco & Juinio-Men̈ez, 2010). Fine-scale population structure within the SCS system was also revealed in the blue starfish Linckia laevigata and the giant clam Tridacna crocea (Juinio-Meñez et al., 2003). By contrast, the sea urchin (Tripneustes gratilla) did not show any significant genetic differentiation in this region (Casilagan et al., 2013). ...
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Seagrass plays important ecological roles and ecosystem services, yet degrading alarmingly in the South China Sea (SCS), one of the largest marginal seas of the Western Pacific. As connectivity is a vital component in population persistence, understanding of connectivity is of importance for effective seagrass conservation management. In the South China Sea, our understanding of connectivity is mainly based on studies in fishes and invertebrates. Connectivity in seagrass populations, on the other hand, is still poorly investigated. In this review, I predict that genetically structured population of seagrass is likely to occur in the SCS. Future research on seagrass connectivity should include (i) investigation on the pattern of connectivity at a local and broader-regional scale, and (ii) investigation on processes involved in the seagrass connectivity. These investigations are aimed to improve our knowledge of seagrass connectivity and to contribute in providing a solid framework for seagrass restoration/transplantation and spatial planning of seagrass management.
... Observed differences in the populations in the northwestern South China Sea, Gulf of Thailand, Karimata Strait, and the Philippines [94] can be explained by the limited larval exchanges modelled between these reefs. Contrastingly, the modelled high interconnectivity between the Spratly Islands and western Palawan [98] reflects the strong gene flow detected across these reef sites. The perceived distinction of the Philippine internal seas [94] is concordant with the high likelihood of retention simulated around the Visayan and Sibuyan Seas, and the limited range of interconnections of the internal reefs with the Sulu Sea. ...
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Coral reefs of the North Indo-West Pacific provide important ecosystem services to the region but are subjected to multiple local and global threats. Strengthening management measures necessitate understanding the variability of larval connectivity and bridging global connectivity models to local scales. An individual-based Lagrangian biophysical model was used to simulate connectivity between coral reefs for three organisms with different early life history characteristics: a coral (Acropora millepora), a sea urchin (Tripneustes gratilla), and a reef fish (Epinephelus sp). Connectivity metrics and reef clusters were computed from the settlement probability matrices. Fitted power law functions derived from the dispersal kernels provided relative probabilities of connection given only the distance between reefs, and demonstrated that 95% of the larvae across organisms settled within a third of their maximum settlement distances. The magnitude of the connectivity metric values of reef cells were sensitive to differences both in the type of organism and temporal variability. Seasonal variability of connections was more dominant than interannual variability. However, despite these differences, the moderate to high correlation of metrics between organisms and seasonal matrices suggest that the spatial patterns are relatively similar between reefs. A cluster analysis based on the Bray-Curtis Dissimilarity of sink and source connections synthesized the inherent variability of these multiple large connectivity matrices. Through this, similarities in regional connectivity patterns were determined at various cluster sizes depending on the scale of interest. The validity of the model is supported by 1) the simulated dispersal kernels being within the range of reported parentage analysis estimates; and, 2) the clusters that emerged reflect the dispersal barriers implied by previously published population genetics studies. The tools presented here (dispersal kernels, temporal variability maps and reef clustering) can be used to include regional patterns of connectivity into the spatial management of coral reefs.
... In the Philippines, the current research has focused on the phylogeographic distribution of some fishes, bent-toed geckoes, as well as bivalves across established biogeographic margins that limit some other terrestrial and marine taxa (Carpenter & Springer, 2005;Esselstyn et al., 2010;Gaither & Rocha, 2013;Huxley, 1868;Lemer et al., 2016;Siler, Oaks, Esselstyn, Diesmos & Brown, 2010;Wallace, 1860Wallace, , 1863. Local analysis of the distribution and connectivity of some marine taxa across the Philippines has also been investigated in western populations of the sea star Linckia laevigata and the giant clam Tridacna crocea near the island of Palawan, as well in the western portion of the Central Visayas (Alcazar & Kochzius, 2016;Juinio-Menez, Magsino, Ravago-Gotanco & Yu, 2003;Magsino, Ravago & Juinio-Menez, 2002; Ravago-Gotanco, Magsino & Juinio-Menez, 2007) Across the globe, sepiolid squids (Cephalopoda: Sepiolidae) form mutualistic associations with bioluminescent bacteria from the genera Vibrio and Photobacterium (γ-Proteobacteria: ...
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Abstract Marine microbes encounter a myriad of biotic and abiotic factors that can impact fitness by limiting their range and capacity to move between habitats. This is especially true for environmentally transmitted bacteria that cycle between their hosts and the surrounding habitat. As geologic history, biogeography, and other factors such as water temperature, salinity, and physical barriers can inhibit bacterial movement to novel environments, we chose to examine the genetic architecture of Euprymna albatrossae (Mollusca: Cephalopoda) and their Vibrio fischeri symbionts in the Philippine archipelago using a combined phylogeographic approach. Eleven separate sites in the Philippine islands were examined using haplotype estimates that were examined via nested clade analysis to determine the relationship between E. albatrossae and V. fischeri populations and their geographic location. Identical analyses of molecular variance (AMOVA) were used to estimate variation within and between populations for host and symbiont genetic data. Host animals demonstrated a significant amount of variation within island groups, while symbiont variation was found within individual populations. Nested clade phylogenetic analysis revealed that hosts and symbionts may have colonized this area at different times, with a sudden change in habitat. Additionally, host data indicate restricted gene flow, whereas symbionts show range expansion, followed by periodic restriction to genetic flow. These differences between host and symbiont networks indicate that factors “outside the squid” influence distribution of Philippine V. fischeri. Our results shed light on how geography and changing environmental factors can impact marine symbiotic associations at both local and global scales.
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We present a new record and information on the distribution of the IUCN listed Tridacna crocea Lamarck, 1819 in the Philippines. The new record in Patnanungan Island extends the known distribution of this species by 80 km east of the nearest previously known occurrence. The collected specimens are found in shallow water at a depth of 3 m, exhibit a relatively small size, and showed the characteristic of completely burrowing its valves in coral substrates. DNA barcoding was also done, and the constructed phylogenetic tree demonstrated that the giant clams created a monophyletic group. Tridacna crocea has a wide distribution and is relatively abundant throughout the Philippine reefs. We recommend updating the population status and stock assessment of giant clams in the country for local regulation and conservation management.
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The collection sites of Tridacna crocea in the Philippines was listed based on the previous studies from 1986 up to the present date. Eighteen (18) studies showed the wide distribution of T. crocea within the country. New samples were also added to the collection by the present study from Ulugan Bay and Honda Bay in Puerto Princesa Palawan. First record of T. crocea in Batanes Island was also presented by this study using molecular approach identification. The amplified mitochondrial DNA cytochrome c oxidase I gene (COI) sequences of T. crocea and the sequences from Genbank of the Tridacna maxima, Tridacna squamosa, Tridacna noae and outgroup were used to construct Neighbour Joining and Maximum Likelihood tree. The information in this study contributes to the growing data on genetics of the giant clams (Cardiidae: Tridacninae). This can serve as a guide to the possible population structure and adaptation patterns of habitat associated marine invertebrate species.
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The Spratly Islands encompass a dense system of several hundred coral reefs in the most biodiverse of the world's seas. They serve as breeding grounds for a wide variety of organisms. A study of pelagic larval survival times and current patterns indicates that they may supply recruiting organisms for marine ecosystems throughout the South China Sea. Strategic concerns and vague possibilities of hydrocarbon deposits have led to military build-up in the area, resulting in violent confrontations and environmental stress. Future oil drilling could have widespread impacts. A more sustainable-use strategy would be to freeze current claims on the islands and establish an international marine park. Such a park could generate on the order of USD 1B annually from tourism. Carefully managed, the park would safeguard substantially-sized populations of tens of thousands of species, and help to ensure a steady supply of recruits to regional fisheries. -from Author
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Analysis of allozyme data and nucleotide sequences for a region of the mitochondrial cytochrome oxidase I (COI) gene was em- ployed to elucidate genetic relationships among Linckia laevigata color morphs. Allozyme variation at 8 polymorphic loci was examined for six reef populations of L. laevigata, representing blue and orange morph populations collected from the Kalayaan Islands Group (KIG), South China Sea, and Tubbataha Reef, Sulu Sea. Analysis revealed grouping of populations according to color morph, with significant genetic differentiation detected between blue and orange morph populations (Fst=0.1149). In two sites where blue and orange morphs are sympatric (Panata and NE Investigator shoal), significant genetic differentiation was detected, possibly due to reproductive isolation among morphs. Notably, allele frequency shifts were observed between blue and orange morph populations at three loci, HK, PGM, and LP-1, although there was no fixation for alternative alleles. Preliminary analysis of nucleotide sequences for a limited number of L. laevigata collected from Panata Island reveal genetic patterns congruent with those obtained from allozyme data. Neighbor-joining analysis of sequence data reveal divergence of blue morphs from orange or mix-color morphs. Genetic differentiation of blue and orange morphs in the KIG are congruent with observed genetic patterns of L. laevigata color morphs across larger spatial scales, between the Indian and Pacific Ocean. In addition, fine-scale population genetic structure of L. laevigata in the South China Sea and Sulu Sea was revealed. Factors which may contribute to the observed fine-scale genetic patchiness are discussed.
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The Pacific marine biota, particularly species with long planktonic larval stages, are thought to disperse widely throughout the Pacific via ocean currents. The little genetic data available to date has supported this view in that little or no significant regional differentiation of populations has been found over large geographical distances. However, recent data from giant clams has demonstrated not only significant regional differentiation of populations, but routes of gene flow that run perpendicular to the main present-day ocean currents. Extensive surveys of genetic variation at eight polymorphic loci in 19 populations of the giant clam Tridacna maxima, sampled throughout the West and Central Pacific, confirmed that the patterns of variation seen so far in T. gigas were not unique to that species, and may reflect a fundamental genetic structuring of shallow-water marine taxa. Populations of T. maxima within highly connected reef systems like the Great Barrier Reef were panmictic (average FST < 0.003), but highly significant genetic differences between reef groups on different archipelagos (average FST = 0.084) and between West and Central Pacific regions (average FST = 0.156) were found. Inferred gene flow was high (Ne m usually > 5) between the Philippines and the Great Barrier Reef, between the Philippines and Melanesia (the Solomon Islands and Fiji), and between the Philippines and the Central Pacific island groups (Marshall Islands, Kiribati, Tuvalu and Cook Islands). Gene flow was low between these three sets of island chains (Ne m < 2). These routes of gene flow are perpendicular to present-day ocean currents. It is suggested that the spatial patterns of gene frequencies reflect past episodes of dispersal at times of lower sea levels which have not been erased by subsequent dispersal by present-day circulation. The patterns are consistent with extensive dispersal of marine species in the Pacific, and with traditional views of dispersal from the Indo-Malay region. However, they demonstrate that dispersal along present-day ocean surface currents cannot be assumed, that other mechanisms may operate today or that major dispersal events are intermittent (perhaps separated by several thousands of years), and that the nature and timing of dispersal of Pacific marine species is more complex than has been thought.
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BIOSYS-1 is a FORTRAN IV program designed to aid biochemical population geneticists and systematists in the analysis of electrophoretically detectable allelic variation. It can be used to compute allele frequencies and genetic variability measures, to test for deviation of genotype frequencies from Hardy-Weinberg expectations, to calculate F-statistics, to perform heterogeneity chi-square analysis, to calculate a variety of similarity and distance coefficients, and to construct dendrograms using cluster analysis and Wagner procedures. The program, documentation, and test data are available from the authors.
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Ten species of marine shore fishes with a wide range of life-history strategies were collected from four areas in southern California, U.S.A., and Baja California, Mexico, and examined for patterns of genetic differentiation. Multilocus D and FST values (based on 32-42 presumptive gene loci in each species) were both negatively correlated with estimated dispersal capability. These results were robust to variations in the number and type of loci used in the analysis and are compatible with the hypothesis that levels of genetic differentiation in these shore fishes are determined primarily by gene flow and genetic drift. There is no a priori reason to expect the observed correlation to result from natural selection or historical factors. The findings thus suggest that populations of these shore fishes are in at least a quasi-equilibrium with respect to migration, mutation, and genetic drift. Present data were also used to compare estimates of mNe obtained by three different methods. Estimates based on FST values calculated by the methods of Nei and Chesser (FST(N)) and Weir and Cockerham (FST(W)) were highly correlated, but FST(N) ≤ FST(W) for every species, leading to generally higher mNe estimates for Nei and Chesser's method. Estimates of mNe based on the frequency of private alleles (Slatkin, 1985a) were not as strongly correlated with dispersal capability as were FST and D values. A low incidence of private alleles in many species may be responsible for this relatively weak correlation and may limit the general usefulness of Slatkin's method. In spite of their sensitivity to natural selection, FST and D may be better indicators of relative gene flow levels for high gene flow species.
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The-Pacific marine biota, particularly species with long planktonic larval stages, are thought to disperse widely throughout the Pacific via ocean currents. The little genetic data available to date has supported this view in that little or no significant regional differentiation of populations has been found over large geographical distances. However, recent data from giant clams has demonstrated not only significant regional differentiation of populations, but routes of gene flow that run perpendicular to the main present-day ocean currents. Extensive surveys of genetic variation at eight polymorphic loci in 19 populations of the giant clam Tridacna maxima, sampled throughout the West and Central Pacific, confirmed that the patterns of variation seen so far in T. gigas were not unique to that species, and may reflect a fundamental genetic structuring of shallow-water marine taxa. Populations of T. maxima within highly connected reef systems like the Great Barrier Reef were panmictic (average FST 5) between the Philippines and the Great Barrier Reef, between the Philippines and Melanesia (the Solomon Islands and Fiji), and between the Philippines and the Central Pacific island groups (Marshall Islands, Kiribati, Tuvalu and Cook Islands). Gene flow was low between these three sets of island chains (Nem
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Reconstructions of SE Asia at 5 Ma intervals for the past 50 Ma are presented. They are constrained by new data from the Philippine Sea plate, which forms the eastern boundary of the region, by recent interpretations of the South China Sea and Eurasian continental margin, forming the western boundary, and by the known motions of the Indian-Australian plate to the south. There are two regionally important periods of change during the past 50 Ma. Both appear to be the expression of arc-continent collision and resulted in major changes in the configuration of the region and in the character of plate boundaries. At c. 25 Ma the collision of the Australian continent with the Philippine Sea plate arc caused major effects which propagated westwards through the region. At c. 5 Ma collision of the Philippine arc and the Eurasian continental margin occurred in Taiwan. This appears to be a key to the recent tectonics of the region. Principal features of the model are described. -from Author