PLoS ONEplosplosonePLoS ONE1932-6203Public Library of ScienceSan Francisco, USAPONE-D-10-0487410.1371/journal.pone.0016755Research ArticleBiologyEcologyBiogeographyEvolutionary biologyPopulation geneticsHaplotypesMarine biologyMarine ecologyPopulation biologyPopulation geneticsGenetics and GenomicsEcologyMarine and Aquatic SciencesEvolutionary BiologyGlobal Phylogeography of the Widely Introduced North West Pacific
Ascidian Styela clavaGlobal Phylogeography of Styela
clavaGoldstienSharyn J.1*DupontLise23ViardFrédérique45HallasPaul J.267NishikawaTeruaki8SchielDavid R.1GemmellNeil J.9BishopJohn D. D.27University of Canterbury, Christchurch, New
ZealandMarine Biological Association, Plymouth,
United KingdomUMR 7618 BioEMCo, Equipe IBIOS,
Université Paris-Est Creteil, Creteil, FranceUPMC Université Paris, Lab. AD2M,
Station Biologique de Roscoff, Roscoff, FranceUMR 7144 CNRS UPMC, DivCo team, Station
Biologique de Roscoff, Roscoff, FranceUniversity of Glamorgan, Pontypridd, United
KingdomUniversity of Plymouth, Plymouth, United
KingdomToho University, Miyama, Chiba,
JapanUniversity of Otago, Dunedin, New
ZealandWelchJohnEditorUniversity of Cambridge, United Kingdom* E-mail: sharyn.goldstien@canterbury.ac.nz
Conceived and designed the experiments: SJG LD FV JDDB NJG. Performed the
experiments: SJG LD PJH TN. Analyzed the data: SJG. Contributed
reagents/materials/analysis tools: NJG DS JDDB FV SJG. Wrote the paper: SJG.
Major contribution to editing the manuscript and initialising the projects:
NJG JDDB FV DRS. Developed the concepts and structure of the article,
collected data for the southern hemisphere and some U. S. and Canadian
populations, and analyzed the complete dataset: SJG. Secured funding for the
work in the southern hemisphere: NJG DRS. Secured funding and coordinated
research and data collection for the northern hemisphere: JDDB FV. Collected
data for the northern hemisphere populations: LD JPH TN. Contributed to
revisions and completion of the article: NJG JDDB FV DRS.
This study was funded by a University of Canterbury Postdoctoral Fellowship and
subcontract to NJG from NIWA as part of the FRST OBI "Biodiversity and
biosecurity" contract CO1X0502, as well as the European Network of Excellence
"Marine Genomics Europe" (contract no. 505403), the NERC (UK) Oceans 2025
programme, and the AXA Research Fund (project ‘MAAC’). This does not
alter our adherence to all the PLoS ONE policies on sharing data and
materials.
2011222201162e1675520102010291220102011Goldstien et alThis is an open-access article distributed under
the terms of the Creative Commons Attribution License, which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and
source are credited.
The solitary ascidian Styela clava Herdman, 1882 is considered
to be native to Japan, Korea, northern China and the Russian Federation in the
NW Pacific, but it has spread globally over the last 80 years and is now
established as an introduced species on the east and west coasts of North
America, Europe, Australia and New Zealand. In eastern Canada it reaches
sufficient density to be a serious pest to aquaculture concerns. We sequenced a
fragment of the cytochrome oxidase subunit I mitochondrial gene (COI) from a
total of 554 individuals to examine the genetic relationships of 20 S.
clava populations sampled throughout the introduced and native
ranges, in order to investigate invasive population characteristics. The data
presented here show a moderate level of genetic diversity throughout the
northern hemisphere. The southern hemisphere (particularly New Zealand) displays
a greater amount of haplotype and nucleotide diversity in comparison. This
species, like many other invasive species, shows a range of genetic diversities
among introduced populations independent of the age of incursion. The successful
establishment of this species appears to be associated with multiple incursions
in many locations, while other locations appear to have experienced rapid
expansion from a potentially small population with reduced genetic diversity.
These contrasting patterns create difficulties when attempting to manage and
mitigate a species that continues to spread among ports and marinas around the
world.
This study was funded by a University of Canterbury Postdoctoral Fellowship and
subcontract to NJG from NIWA as part of the FRST OBI "Biodiversity and
biosecurity" contract CO1X0502, as well as the European Network of Excellence
"Marine Genomics Europe" (contract no. 505403), the NERC (UK) Oceans 2025
programme, and the AXA Research Funds (project ‘MAAC’) (see url
http://www.axa-research.org/en/). The funders had no role in
study design, data collection and analysis, decision to publish, or preparation
of the manuscript.Introduction
An important aspect of biodiversity conservation and sustainability of marine
resources is the mitigation of non-indigenous species (NIS). To-date, there have
been no reported extinctions of native marine species caused by exotic invaders
[1].
Nonetheless, they pose a serious threat to the sustainability of aquaculture
concerns [2],
[3] and they
can alter the structure and composition of benthic communities [4], [5], thereby threatening global marine
biodiversity and resource sustainability. With only 16% of the worlds'
marine ecoregions free from NIS [6], invasive species are challenging pre- and post-border
biosecurity strategies, and threatening biodiversity and ecosystem services around
the world [7],
[8].
However, invasions can also provide insight into community ecology dynamics [9], [10], competitive
interactions [11] and the resilience of native assemblages [12] as NIS make
their way into new ecosystems.
The combined availability of high-throughput molecular techniques and analyses of the
resulting data based on explicit evolutionary models has caused a recent surge in
the number of studies seeking to use genetic patterns to assess invasion pathways
and the evolution of invasiveness [13], [14]. Recent reviews of these molecular studies show that a
wide array of taxa, geographic scales, and molecular markers have been covered over
the past decade [15], [16], with a range of results reported across both aquatic and
terrestrial NIS [14]. A comprehensive analysis of molecular studies showed
that conventional expectations of bottlenecks and reduced genetic variability for
introduced populations do not always hold true for aquatic NIS, with only around
37% of studies reporting a significant loss of genetic variation in
introduced populations [16]. However, most of these studies have sampled populations
many years after the initial introductions and global spread. Marine taxa, also
primarily sampled many years after introduction, exhibit a particularly wide range
of molecular patterns. For example, high genetic diversity has been observed for the
mitochondrial DNA gene cytochrome oxidase I (COI) in native and introduced
populations of the ascidian Microcosmus squamiger. The first
introduction of this species was recorded in1983 and it appears that extensive
sharing of haplotypes has since occurred among populations [17]. In contrast, other ascidians,
Pyura praeputialis, first recorded in 1985, and
Botryllus schlosseri, first recorded in the 1830's,
displayed genetic differentiation among native and introduced populations and
between harbours and bays for this same gene [18], [19]. Other marine taxa also
exhibit a considerable range of genetic diversities and differentiation for this
gene. For example, native populations of the seaweed Undaria
pinnatifida, first recorded outside of Asia in 1971, exhibit high
genetic differentiation but low diversity, while introduced populations exhibit
relatively high diversity [20], [21]. In contrast, the rapa whelk Rapana
venosa, first recorded in 1940s, displayed high genetic diversity
within its native range but was monomorphic throughout invaded Europe [22]. One of the
clearer genetic patterns of introduction was seen for the Pacific acorn barnacle
Balanus glandula. This species, recorded outside of North
America since the 1960's, exhibits marked genetic structure within its native
and invaded ranges, which enabled the identification of two different incursion
pathways, one to Argentina and another to Japan [23]. Finally, the European green
crab Carcinus maenus, a ubiquitous marine invader since its
transport outside of Europe in the early 19th century, has been
comprehensively studied [24], [25], [26], [27], [28], [29]. In 1997, genetic identification confirmed cryptic
invasions of this crab species [25], while two more recent studies [24], [29] found that genetic diversity
was reduced in introduced populations, particularly in the newly invaded
regions.
The solitary ascidian Styela clava Herdman, 1882 is one of many
non-indigenous marine tunicates that now dominate fouling communities of ports and
marinas around the world [30]. S. clava is native to the NW Pacific
coastal regions of Japan, Korea, northern China and the Russian Federation. The
first recorded introduction beyond this range was in California, probably in the
1920s (Lambert & Lambert 1998). In the Atlantic, this species was first observed
in Britain, in Plymouth Sound and the adjacent Lynher River Estuary, in 1953 [31]. Established
populations of S. clava are now recorded throughout the northern
hemisphere, including Atlantic Europe plus a recent record from the Mediterranean
basin [3], [32], [33], [34], Canada [2], [26], [35], both the
eastern and western coasts of the USA [36], [37], [38] and several southern hemisphere
harbours in Australia [39], [40] and New Zealand [41]. This successful invader occurs
in a diverse array of habitats including man-made structures such as subtidal
wharves, boat hulls and mussel ropes, as well as intertidal oyster racks. Large
populations exist on intertidal rocky reefs and subtidal mud flats in native and
some introduced locations. The diversity of habitats in which this species resides
makes tracking and management of its spread particularly challenging.
Two recent studies of Styela clava used microsatellite markers and
mtDNA to assess the role of human-mediated transport on regional expansion of this
introduced species in England [42] and New Zealand [43]. These two locations
respectively document one of the oldest and the newest reported incursions of
Styela clava. Both studies suggested that extensive admixture
was occurring through human-mediated transport within the regional locations. In
addition, the New Zealand study showed that recreational vessels and commercial port
vessels were both introducing new populations into New Zealand waters and
recreational vessels were also responsible for post-border expansion of S.
clava independent of the port populations [43]. Despite increased genetic
differentiation suggesting multiple incursions, microsatellite allelic diversity in
the younger New Zealand incursion was reduced in comparison to the older UK
incursion. However, mtDNA haplotype diversity was high and the genetic distance
among haplotypes was large [43] suggesting that the reduction in microsatellite allelic
richness and heterozygosity is not necessarily due to founder effects, and may be
better explained by admixture among divergent populations. A more recent study of
S. clava using microsatellite markers also showed no evidence
of reduced genetic diversity due to founder events throughout Europe, although
evidence of population expansion and/or sub-structure was observed in many
populations [44].
In this study of the solitary ascidian Styela clava, we assessed
genetic diversity and its distribution among populations in an extensive global
dataset of mitochondrial cytochrome oxidase I gene (COI) sequence. The long, well
documented, chronology of global introductions makes this an ideal species to assess
founder effects and changes in diversity with respect to time of introduction, as
well as connectivity among populations. Based on the three recent molecular studies
of this species, our expectation was that the mitochondrial diversity would not be
reduced in newer incursions and that admixture among populations would be high for
many populations due to their derivation from multiple sources. However, genetic
differentiation among geographic regions was also expected, based on the
differentiation of genotypes between the two native populations [44].
Methods
A sub-set of partial fragments of the mitochondrial DNA oxidase subunit I
mitochondrial gene (COI) for Styela clava from three different labs
were aligned. Protocols for sample collection and DNA extraction can be found in
Goldstien et al. [43] and Dupont et al. (2009). We reduced the effects of
sampling errors with an extensive geographic sampling regime, including populations
from all regions known to harbour this species. Unfortunately, we were only able to
obtain samples from two populations within the native range, which limits our
analysis to comparisons of diversity and assessing the connectivity among introduced
populations. However, each sampled population is represented by 20–30
individuals, which provides a robust measure of diversity within, and structure
among, populations. To avoid bias and oversampling in one location, only a subset of
the 2006 data from Goldstien et al. (2010) were used; essentially, regional
populations were excluded to avoid oversampling rare haplotypes.
Sequence Analyses
All sequences were checked in the respective laboratories and were brought
together for alignment. Alignments and haplotypes were identified and confirmed
manually in Bioedit v. 5.0.6 [45]. Arlequin v. 3.0 [46] was used to calculate
Nei's nucleotide diversity (π), computed as the probability that two
randomly chosen homologous nucleotides are different (Nei, 1987), and theta(S),
Watterson's theta: an estimate of the population mutation rate using the
number of estimated from the infinite-site equilibrium relationship between the
number of segregating sites, the sample size and θ (Watterson, 1975;
Tajima, 1989). Haplotype number, as well as haplotypic richness and diversity
contribution after rarefaction to a population size of 15, were estimated using
CONTRIB [47]. A
Statistical Parsimony Network was constructed in TCS 1.18 [48]. The divergence among
haplotypes was calculated using the Kimura 2-parameter distance measure (Kimura,
1980) in MEGA4 [49]. To examine population structure independent of set
population groupings and allowing for admixture, Bayesian Analysis of Population
Structure (BAPS) was used in the program BAPS v.3.2 [50]. The hierarchical
distribution of genetic variation among populations based on a
priori population groupings was also tested using Analysis of
Molecular Variance (AMOVA) [51] in Arlequin v. 3.0 [46] and was based on the
number of pairwise nucleotide differences [52]. This simple distance
measure was used due to the close genetic relationship of the sequences [53]. The
populations were partitioned into regional groups: Japan, Europe, Australia, New
Zealand, West USA, East USA, and Canada for this analysis. In addition, the
genetic distance between populations was calculated using pairwise
ΦST and Nei's average number of pairwise differences
(Nei, 1979) in Arlequin v. 3.0 (Excoffier, 1992). Finally, to determine the
relationship between ages since the introduction was reported and the genetic
diversity for the populations; diversity measures Theta(S) and haplotypic
richness, a Pearson's correlation test was done using XLstat (Addinsoft,
2006). A Non-linear regression was also performed in XLstat using the least
squares method and default functions.
Results
A partial fragment, 602 base pairs, of the mitochondrial COI gene was aligned for a
total of 554 S. clava individuals, derived from 20 populations
around the world (Table 1,
Fig. 1). Forty five
haplotypes (GenBank accession numbers: GU328006-GU328035; HQ730795-HQ730809) were
observed among the aligned sequence data from the 554 individuals sequenced and
these haplotypes exhibited 0.2%–1.3% sequence divergence.
10.1371/journal.pone.0016755.g001
Haplotype distribution for the mtDNA COI gene of Styela
clava populations sampled in 2006.
Pie colours correspond to the haplotypes in Figure 2 and population codes follow
Table 1.
10.1371/journal.pone.0016755.t001
Population locations, sample sizes (N) and summary statistics for
Styela clava.
Population
Country
Sample ID
N
H
Pb15
Crt
Crs
Crd
U:S
π
Theta(S)
Otsuchi Bay
Japan
OTS
32
11
5.99
0.014
0.023
0.000
3∶8
0.0024
3.48
Tsukumo Bay
Japan
TSU
27
8
5.19
0.064
0.015
0.049
5∶3
0.0052
3.11
Prince Edward Isl.
Canada
PEI
19
2
0.99
0.000
0.000
0.000
0∶2
0.0005
0.29
Doverodde
Denmark
DOV
24
3
1.96
0.000
0.000
0.000
0∶3
0.0015
0.54
Brest
France
BRE
30
4
2.02
0.000
0.000
0.000
0∶4
0.0006
0.76
Cork
Ireland
COR
32
7
3.96
0.000
0.003
0.000
0∶7
0.0013
1.49
Ria de Ferrol
Spain
RIA
32
8
4.57
0.000
0.000
0.000
1∶7
0.0016
1.49
Plymouth
UK
MOU
30
8
4.66
0.000
0.010
0.000
0∶8
0.0013
1.77
Avery Point
East USA
AP
27
9
5.12
0.003
0.014
0.000
0∶9
0.0016
2.08
Mumford Cove
East USA
MC
22
5
0.52
0.000
0.000
0.000
2∶3
0.0010
1.10
Mission Bay
West USA
MB
31
1
0.00
0.000
0.000
0.002
0∶1
0.0000
0.00
Niwatec River
East USA
NR
22
5
3.27
0.000
0.000
0.000
0∶5
0.0015
1.32
Puget Sound
West USA
PS
24
1
0.00
0.000
0.000
0.000
0∶1
0.0000
0.00
Santa Barbara
West USA
SB
32
3
0.94
0.008
0.000
0.035
0∶3
0.0003
0.50
Los Angeles
West USA
LA
27
8
5.03
0.036
0.013
0.023
3∶5
0.0022
1.82
San Francisco
West USA
SF
33
6
3.07
0.000
0.000
0.000
2∶4
0.0004
1.23
Woods Hole
East USA
WH
30
6
3.89
0.000
0.002
0.000
1∶5
0.0016
1.26
Hauraki Gulf
New Zealand
HG
32
12
7.21
0.050
0.035
0.015
4∶8
0.0042
3.48
Lyttelton Hbr
New Zealand
LYT
31
13
7.57
0.064
0.038
0.025
8∶5
0.0037
3.50
Melbourne
Australia
AUS
16
6
4.81
0.036
0.011
0.025
0∶6
0.0035
1.81
The identification code for each population is included. Summary
statistics are: H, number of haplotypes; Pb[15], haplotypic
richness with rarefaction; Crt, contribution to total haplotypic
richness; U:S, proportion of unique: shared haplotypes; π,
nucleotide diversity; and Theta(S), the population mutation rate
estimated from the number of segregating sites.
Note: Bold text highlights the populations with the highest diversity
across multiple measures.
The observed nucleotide diversity was low for almost all populations
(π≤0.0052), while haplotype diversity was moderate, ranging between 1 and 13
haplotypes per population. New Zealand and Japan were the most genetically diverse
populations and contributed most of the diversity to the total data set, as shown
with π, Theta(S), and haplotypic richness (Table 1). The Lyttelton population was also
consistent in its majority contribution to haplotypic and nucleotide diversity due
to within population haplotype diversity (Crs) and haplotype divergence among
populations (Crd), supported by the high number of unique haplotypes in this
population, as well as nucleotide diversity and Theta(S) (Table 1). The remaining populations differed in
contribution due to diversity or divergence of haplotypes, as well as nucleotide and
θS diversity. The statistical parsimony network (Fig. 2) shows that unique
haplotypes occurring in New Zealand, in particular, are more divergent than
haplotypes in all other populations, contributing to the higher Theta(S) and
Contribution (Crd,) values. Linear and non-linear equations did not show any
significant correlation between age of incursion and the haplotypic richness (Pb15)
or Theta(S) of the introduced populations, although an apparent positive trend is
seen among the five populations from west coast USA (Fig. 3).
10.1371/journal.pone.0016755.g002
Statistical parsimony network for the mtDNA COI gene of Styela
clava populations sampled in 2006.
Unique haplotypes are not coloured and those unique haplotypes observed in
the Lyttelton population are circled. Haplotypes that appear in the text are
numbered accordingly.
10.1371/journal.pone.0016755.g003
Scatter plots of theta(S) and haplotypic richness (Pb[15]), against years since the first
reported incursion of Styela clava from 20 populations
sampled globally (Table
1).
Data points are coloured to represent populations from geographic regions:
Europe (black), east coast Nth America (light grey), west coast USA (black
stripe), and southern hemisphere (white).
Two populations from the east (Otsuchi Bay) and west (Tsukumo Bay) coast of Honshu,
mainland Japan, represent the native populations in this study, albeit a small area
of the entire range. Both of these populations exhibit high genetic diversity (Table 1), and significant
differentiation was observed between the two populations (Table S1).
Eight of the eleven haplotypes from Otsuchi are spread throughout the introduced
populations (Fig. 1; 01, 02, 03,
06, 07, 08, 09, 14), while only three of eight Tsukumo haplotypes are shared among
other populations (Fig. 1; 01,
02, 06). One haplotype is shared among all populations (01), although this haplotype
is less frequent in the southern hemisphere populations (Fig. 1). The frequency of each of the shared
haplotypes differs among populations, particularly those in different ocean basins,
such as between the west and east coast of the USA. For instance, the second most
frequent haplotype (07) observed in west coast USA populations is rare in all other
populations of the northern hemisphere, excluding Denmark, where it also occurs in
high frequency. Similarly, the third most frequent haplotype (06) in Atlantic coast
populations (i.e., Europe, east USA and east Canada), excluding France, occurs in
very low frequency in west coast USA populations. Europe exhibits extensive
admixture with generally low diversity; one unique haplotype is observed in Spain
and one haplotype (24) is unique to the European countries of Spain (RIA), Ireland
(COR) and France (BRE). Similarly, most of the North American populations exhibited
low genetic diversity and extensive admixture. Los Angeles, San Francisco and
Mumford Cove populations were the most diverse populations within the North American
region.
The statistical parsimony network (Fig.
2) reflects the high frequency of some haplotypes and the large number of
unique haplotypes observed among populations. There are also several missing, or
hypothetical, haplotypes in the data most likely present in unsampled populations
within the native range. The network also shows the wide range of divergence among
haplotypes (0.2%–1.3%) with many of the unique haplotypes at the
higher end of the divergence scale. Many of these divergent haplotypes occur in the
Lyttelton population (Fig. 1).
Genetic distance among populations (Table S1) shows that the two Japanese and two New
Zealand populations are significantly different from most other populations.
Lyttelton is the only population that is significantly different from all other
populations. The Australian population is significantly different from all
populations except the population of Huaraki Gulf, New Zealand. The southern
hemisphere is genetically distinct from the northern hemisphere and from the native
populations sampled. New Zealand populations exhibit a high number of unique
haplotypes that are likely to be present in a native population not sampled. In
particular, the Lyttelton population shares only five of its 13 haplotypes with
other populations (one of these, 17, being shared only with the Los Angeles
population), and two haplotypes (26 and 47) are unique to the Hauraki Gulf
(Auckland, NZ) and Melbourne (Australia).
BAPS groupings (Fig. 4) indicate
genetic similarities among populations of the east coast of America and west coast
of Europe, and Otsuchi; between Australia and Hauraki Gulf; between Prince Edward
Island and Mumford Cove; between Doverode and San Francisco; and between Puget Sound
and Mission Bay. Lyttelton, Tsukumo, Los Angeles and Santa Barbara did not group
with any other populations. Analysis of Molecular Variance (AMOVA) was undertaken to
quantify the components of genetic variance within the data (Table 2). Data were partitioned in two ways: 1)
geographic location: Japan, Europe, west USA, east USA, east Canada, Australia, New
Zealand, and 2) concordant with BAPS groupings (Figure 4). Both partitions show significant
genetic structure among groups, but the degree of variation explained by the group
was greater for BAPS partitions (ΦCT, 0.25) than for among
geographic regions (ΦCT, 0.08). The variation within groups
(ΦSC) is also reduced for the BAPS groups
(ΦSC, 0.00) indicating that these groupings contain less variation
than occurs within geographic regions (ΦSC, 0.15).
10.1371/journal.pone.0016755.g004
Bayesian population structure groups for the mtDNA COI gene of
Styela clava determined using BAPS v.3.2.
Circles are coloured to represent genetically similar populations. The
unfilled circles represent populations that do not group with any others.
Population codes follow Table
1.
10.1371/journal.pone.0016755.t002
F-statistics for Styela clava AMOVA results.
Source of variation
Among groups (ΦCT)
Among populations, within groups
(ΦSC)
Within populations (ΦST)
BAPS Groups
0.25
0.00
0.24
Geographical Regions
0.08
0.15
0.22
The data were partitioned in two ways: 1) BAPS Groups obtained from
Bayesian analysis without prior population designation; 2) Populations
grouped by geographical region. All results are significant
(p<0.01).
Geographical regions: Japan, Europe, Australia, New Zealand, West USA,
East USA, and Canada.
Discussion
The aim of this study was to assess genetic diversity and its distribution among
populations of Styela clava and to test the link between age of
incursion and genetic diversity of this widely introduced ascidian. The COI gene
revealed a moderate level of haplotype diversity (45 haplotypes in 554 individuals)
with low to moderate nucleotide diversity (0.000–0.005), useful in identifying
genetic similarities among populations. This level of haplotype diversity is similar
to that observed for the star sea squirt, Botryllus schlosseri, for
which 16 haplotypes were identified from 181 individuals throughout Europe [18];
however, the nucleotide diversity for this species was much higher (0.008 –
0.08). In contrast, two other ascidians exhibited high haplotype diversity across
native and introduced populations: 52 COI haplotypes were observed in 258
individuals of an Australian ascidian, Microcosmus squamiger, now
present in northern hemisphere locations [17], and 34 haplotypes were
identified from 67 individuals of the Mediterranean ascidian Cystodytes
dellechiajei[54].
Microcosmus squamiger, however, exhibited low nucleotide
diversity (0.002 – 0.008) compared to the other ascidians, excluding
S. clava, while for Cystodytes dellechiajei
nucleotide diversity was also high (0.006 – 0.08) [17], [54].
Molecular studies have shown that genetic diversity of many introduced populations is
equal to or greater than that of corresponding native populations, thereby
contradicting theoretical expectations and possibly enhancing the success of
invasive organisms [55], [56]. This observation is thought to result primarily through
continuing introductions from multiple sources enhancing genetic diversity and
increasing novel genotypes [14], [16]. The two native populations of S. clava
sampled here exhibit significant genetic diversity and genetic differentiation from
each other, and have high genetic diversity compared to most populations of the
introduced range, with only New Zealand populations exhibiting similar genetic
diversity (Table 1). The
abundance of unique haplotypes in populations such as New Zealand and Los Angeles
(Fig. 1) also suggests that
a substantial component of the genetic variation in the native range of this species
has not been sampled in this study. However, most of the haplotypes observed
throughout the introduced range are observed in at least one of the native
populations sampled.
Most of the haplotypes shared among northern hemisphere populations are also present
in the Otsuchi Bay population, while haplotypes shared between Tsukumo Bay and
introduced populations were also present in the Otsuchi Bay population (Fig. 1). The high frequency of
unique haplotypes in Tsukumo Bay suggests that this population is not a likely
source for any of the introduced populations sampled. Microsatellite data for Europe
and USA populations showed a similar pattern of population clustering in the
northern hemisphere [44]. As for this study, Tsukumo Bay was distinct from all
other populations and links were suggested between Atlantic Europe and the eastern
seaboard of the USA and between northern Denmark and the west coast of the USA,
although for the microsatellite data it was the latter grouping that clustered with
Otsuchi Bay. In Europe, neither the COI data presented here nor the microsatellite
data of Dupont et al. (2010) shows a clear correlation between genetic diversity at
a site and the time since S. clava was first reported there. In
contrast, Los Angeles, which is very close to Newport Harbour where S.
clava was first reported on the west coast of the USA (Abbott &
Johnson 1972), did show higher COI diversity than other sites on this coast (Dupont
et al. (2010) did not include this locality).
Molecular data for other marine invasive species of NE Asian origin have displayed
weaker links with Japanese populations than were observed between introduced
populations of S. clava and the Otsuchi Bay sample. For instance,
native populations of the amphipod Caprella mutica in Japan were
genetically diverse and all exhibited unique haplotypes that were not observed in
any other locations in the data set [57]. Similarly, introduced populations of the brown seaweed
Undaria pinnatifida, particularly in Europe but also in New
Zealand and America, were genetically similar to aquaculture populations in Japan
and Korea but less similar to natural Japanese populations [21].
The southern hemisphere S. clava populations are genetically
distinct from the northern hemisphere introduced populations and from the native
populations sampled, a pattern also observed for U. pinnatifida[20], [21]. New Zealand
populations of S. clava exhibit a high number of unique haplotypes
that are likely to be present in a native region not sampled. The significant
genetic differentiation between the two New Zealand populations, Hauraki Gulf and
Lyttelton, suggests that these ports received founders from different sources, most
likely from vessels arriving from different locations. The same result was shown for
microsatellite markers in New Zealand populations [43], but the more comprehensive
data set presented here shows that Hauraki Gulf populations have stronger genetic
affinities to Japan and the northern hemisphere populations than does the more
southern port of Lyttelton.
It has been suggested that the build-up of genetic diversity from multiple sources is
creating more successful invaders and that the founder effect may be overstated for
NIS [14], [16], [58]. Our study does
not support the idea that neutral genetic diversity is linked to invasive potential.
Populations such as Prince Edward Island, Puget Sound and Mission Bay may well have
received smaller incursions to account for their low diversity, but the invasiveness
of these populations does not appear to be affected by their low genetic diversity.
In particular, Prince Edward Island has experienced population numbers in pest
proportions [59], [60], suggesting that the low founder diversity is not
affecting the successful invasion of the species at this location. The species was
also seasonally very abundant in Mission Bay during the surveys reported by Lambert
& Lambert (1998). In addition, the high level of diversity within the Lyttelton
population of New Zealand has not translated to high abundance, distribution, or
competitive ability in this location (SJG unpublished data). Santa Barbara shows
anomalously low diversity adjacent to a coastal region of high diversity (Los
Angeles); in this case, chance events or selective processes may be acting within
the enclosed environment of the marina to reduce genetic diversity subsequent to
introduction.
One of the difficulties for biosecurity management of marine invasions is our ability
to identify and date incursions. This species, like many others, shows a range of
genetic diversities within populations and differentiation among them, independent
of the age of incursion. Multiple incursions appear to be associated with the
successful establishment of this species in many locations, while other locations
have potentially experienced rapid expansion from a small founding population with
reduced genetic diversity. The potential for multiple incursions blurs the line
between founder events and the time required for genes to spread into established
populations. These mixed patterns create difficulties when attempting to manage and
mitigate a species that continues to spread.
Supporting Information
Pairwise comparisons for ΦST (above diagonal) and Nei's
pairwise distance within populations (diagonal) and corrected distance among
populations (below diagonal) of S.clava for mtDNA gene
COI.
(DOC)
We are very grateful to the numerous people who contributed time and effort to the
collection of samples. This list includes: The National Institute of Water and
Atmospheric Research (NZ), the Sanford Seafood Company Ltd (NZ), The Cleveland
Oyster Company Ltd (NZ), Jeff Davidson (UPEI, Canada), Jason Bram (UC Santa Barbara,
USA), Robert Whitlatch (UConn, USA), Gretchen and Charles Lambert (U Washington,
USA), Jørgen Lützen (Copenhagen University), Dan Minchin (MOI Ltd,
Ireland), and Xavier Turon (Blanes, Spain). We thank John Darling (US EPA) for
exchanging data.
Biosketches. This article results from a collaboration of
multi-disciplinary research groups. The expertise of the groups covers areas of
marine bioinvasions, reproductive biology, ecological processes, evolution and
molecular ecology.
http://www.biol.canterbury.ac.nz/
www.crg.org.nz
http://www.sb-roscoff.fr/en/divco.html
http://www.mba.ac.uk/
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