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JOURNAL OF CRUSTACEAN BIOLOGY, 21(4): 1007–1013, 2001
INTRASPECIFIC VARIATION AND GEOGRAPHIC ISOLATION IN
IDOTEA BALTHICA (ISOPODA: VALVIFERA)
J. P. Wares
University of New Mexico, Department of Biology, Castetter Hall,
Albuquerque, New Mexico 87131-1091, U.S.A. ([email protected])
A B S T R A C T
There is often more genetic diversity in a given ecosystem than is represented by current taxonomy. Historical patterns of isolation among populations play an important role in studying the variation in behavior, habitat, and other ecological interactions among different populations of a species
or species group. Idotea balthica (Isopoda: Valvifera) is a common intertidal grazer of the North
Atlantic which has been well-studied in Europe for intraspecific differentiation. Using DNA sequence data from a mitochondrial protein-coding gene (cytochrome c oxidase I), I studied the relationships among different populations of I. balthica in European and American coastal populations. It is apparent that there are at least three historically isolated populations of I. balthica on
the North American coast, while the European Atlantic coast contains populations that are closely
related to each other and to one of the North American populations. It appears that populations of
I. balthica on the North American coast represent both recently arrived colonists from Europe as
well as populations which have survived recent glacial maxima.
With the advent of molecular techniques it
has become apparent that there is often more
biological diversity in a given ecosystem than
is represented by current taxonomy (e.g.,
Henry, 1994; Foltz et al., 1996; Bastrop et al.,
1998). Even brief periods of population isolation may permit rapid differentiation of various mating recognition mechanisms such as
mating calls (Henry, 1994) or gamete recognition proteins (Metz and Palumbi, 1996;
Hellberg, 1998; Pernet, 1999). These historical patterns of isolation among populations
play an important role in studying the variation in behavior, habitat, and other ecological interactions (Travis, 1996) among different populations of a species or species group.
The Valviferan isopod Idotea balthica (Pallas, 1772) is a common intertidal grazer of
the North Atlantic which has been well-studied in Europe for intraspecific differentiation
(Bulnheim and Fava, 1982; Legrand-Hamelin
and Legrand, 1982a, b; Bulnheim, 1984) and
the ecological significance of color polymorphisms (e.g., Salemaa, 1978; Guarino et al.,
1993; Jormalainen et al., 1995; Merilaita,
1998). While I. balthica tends to be competitively displaced by congeneric grazers on
European shorelines (Franke and Janke,
1998), it is a dominant grazer on the North
American coast where it may be found feeding on a different suite of macroalgae and sea-
grasses than in Europe (J. P. Wares, personal
observation). The diet of I. balthica includes
both rocky intertidal macroalgae (Shacklock
and Croft, 1981; Schaffelke et al., 1995) and
other algae and grasses (Robertson and Mann,
1980). There are undoubtedly both ecological and historical foundations for the geographic variation in dominance and diet of I.
balthica (Endler, 1982; Travis, 1996).
In particular, this system is of interest because of the changes in community composition of the North American Atlantic coast
due to Pleistocene glaciation (Pratt and
Schlee, 1969; Smith et al., 1998; Holder et
al., 1999). Populations of species found in the
rocky intertidal of New England and the
Canadian Maritimes must be derived from
refugial populations in Europe, the mid-Atlantic coast of North America, and a small
portion of eastern Canada north of the glacial
margin (Dyke and Prest, 1987; Ingólfsson,
1992; Wares, 2000). Studying the pattern of
population recolonization in I. balthica invites comparisons to the current and historical distributions of its habitat and competitor species, allowing a better description of
the ecology of this species.
Using DNA sequence data from a mitochondrial protein-coding gene (cytochrome
c oxidase I), the relationships among different populations of I. balthica in European and
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 4, 2001
American coastal populations were analyzed.
The primary goal of this study was to determine whether or not the populations of I.
balthica in the North Atlantic represent a single panmictic population. The alternative
finding, that there are populations which have
been historically isolated, may indicate that
the amount of morphological and ecological
diversity found in this species is partly attributable to localized adaptation.
MATERIALS AND METHODS
Specimens of I. balthica, I. metallica Bosc, 1802, I.
granulosa Rathke, 1834, and I. emarginata Fabricius,
1793, were collected from intertidal sites listed in Table
1. The congeneric taxa were used for outgroup rooting.
All species were identified using key morphological characters described in Hayward and Ryland (1995) and Gosner (1978). Individual specimens were placed in 95%
ethanol or DMSO buffer (0.25M EDTA pH 8.0, 20%
DMSO, saturated NaCl, Seutin et al., 1991) immediately.
DNA Extraction and Amplification
DNA was phenol-extracted from each specimen following the protocol in Hillis et al. (1996). PCR amplification of a portion of the mitochondrial cytochrome c oxidase I (COI) protein-coding gene was performed using
the primers LCO1490 5′-ggtcaacaaatcataaagatattgg-3′ and
HCO2198 5′-taaacttcagggtgaccaaaaaatca-3′ from Folmer
et al. (1994). Amplification took place in 50-µl reactions
containing 10–100 ng DNA template, 0.02 mM of each
primer, 5 µl Promega 10× polymerase buffer, 0.8 mM
dNTPs (Pharmacia Biotech), and 1 u Taq polymerase
(Promega). A Perkin-Elmer 480 thermocycler with a temperature profile of 94° (60 sec)–40° (90 sec)–72° (150
sec) for 40 cycles was used.
Double-stranded PCR products were purified using
Promega (Madison, Wisconsin) Wizard PCR preps and
resuspended in 30 µl ddH2O. The template was cyclesequenced using BigDyes fluorescently labeled dideoxy
terminators according to manufacturer’s recommended
conditions (Perkin-Elmer). Unincorporated dideoxynucleotides were removed by gel filtration using Sephadex
G-25 (Sigma, St. Louis, Missouri). The products were
then electrophoresed on an ABI 377 automated DNA sequencer. All DNA samples were sequenced completely
in both directions using PCR primers. Sequence data was
aligned and edited for ambiguities using complementary
fragments in Sequencher 3.0 (GeneCodes Corporation,
Cambridge, Massachusetts). No gaps or poorly aligned
regions existed in the sequence alignment. Consensus sequences were exported as a NEXUS file for subsequent
analysis using PAUP* 4.0b4a (Swofford, 1998).
Phylogenetic Analysis
Characters that were missing or ambiguous were removed from the analysis. A heuristic search for the set
of most-parsimonious trees was performed in PAUP*
4.0b4a. These trees were used to estimate starting parameters for additional maximum-likelihood (ML) analysis. Starting trees were obtained via stepwise addition,
with simple addition sequence. Tree-bisection-reconnection was used for branch swapping, and branches were
collapsed if the maximum branch length was zero.
Table 1. Location of intertidal sites from which specimens of Idotea were collected for this study. The sample
size of individuals sequenced from each population is also
indicated; not all sequence data is included in Fig. 1 for
clarity, as many of the sequences were identical.
Location
Gloucester Point, Virginia
Beavertail State Park,
Rhode Island
Damariscotta, Maine
Antigonish, Nova Scotia
Reykjavik, Iceland
Galway, Ireland
Roscoff, France
Helgoland, Germany
Species Collected (n)
I. balthica (5)
I. balthica (1)
I.
I.
I.
I.
I.
I.
I.
I.
balthica (10)
balthica (7)
balthica (5),
emarginata (1)
balthica (5),
granulosa (1)
balthica (7)
metallica (4)
Maximum-likelihood analysis of these data was then
performed in PAUP* 4.0b4a, using the best-fit model (see
Felsenstein, 1988; Goldman, 1993; Cunningham et al.,
1998). ModelTest (Posada and Crandall, 1998) was used
to determine the best-fit model for likelihood analysis;
likelihood ratio tests were used to generate the statistical
fit of each model to the data. Support for clades within
the ML tree was estimated using maximum parsimony
bootstrapping (1,000 replicates). Likelihood-ratio tests
(Felsenstein, 1988; Goldman, 1993) were used to test that
the data collected were consistent with a constant-rate
Poisson-distributed process of substitution (molecular
clock model). First, the ML phylogeny was estimated using the best-fit model only, then this estimate was repeated
under constraint of the molecular clock model. These estimates were used to calculate the likelihood-ratio test statistic δ = 2[ln(Lo) – ln(L1)], with (n – 1) d.f. where n is
the number of taxa in the tree.
RESULTS
A total of 419 nucleotides of mtDNA sequence data were collected from the specimens listed in Table 1. Sequence data may
be accessed in GenBank (AF241889–
241935). Of this data set, 288 characters are
constant, 36 are autapomorphic, and 95 are
parsimony-informative. Base composition for
this fragment was AT-biased (A: 0.209, C:
0.181, G: 0.239, T: 0.371). ModelTest (Posada
and Crandall, 1998) indicated that HKY + Γ
is the best-fit model for these data, and it was
chosen for all subsequent analyses.
Maximum-likelihood analysis of these data
produced the phylogeny in Fig. 1. The estimated transition : transversion ratio was 24.8,
and the Gamma shape parameter α = 0.101.
These data reject the molecular clock model
(δ = 530.95, P < 0.001). Parsimony analysis
produced topologically identical phylogenies
to ML, so maximum parsimony was used as
WARES: GEOGRAPHIC ISOLATION IN IDOTEA BALTHICA
the criterion for bootstrap analysis (1,000
replicates) of this data set in the interest of
saving computational time. Bootstrap support
is very strong for several geographically distinct clades in this phylogeny (Fig. 1). For example, all individuals of I. balthica collected
in Virginia form a distinct clade, as do the
individuals collected in Iceland. Another
clade nested within I. balthica contains two
individuals collected in Nova Scotia; this
clade and the Virginia clade are well-supported sister clades.
All other haplotypes found in North America are closely related or identical to individuals collected throughout western Europe,
and all individuals identified morphologically
as I. balthica comprise a clade with 100%
bootstrap support (Fig. 1), suggesting that initial identification was not in error. While it
is apparent that the genetic relationships
among the clades of North American I. balthica populations represent a series of historical discontinuities in gene flow, the separations are too large to suggest that any clade
is ancestral to another.
The outgroup taxa are all quite divergent
from I. balthica and each other. Based on
HKY (transitions weighted greater than transversions) calculated distances, the four
species in this study are 17–25% divergent
from each other at this locus (Table 2). Precise estimates of the actual time of divergence
based on a taxon-specific molecular clock are
not available, but estimates of divergence in
the COI gene fragment have been calibrated
in other species to about 2% divergence per
million years (for review see Knowlton and
Weigt, 1998; Wares, 2000). This divergencerate estimate suggests that diversification of
these taxa was probably in the Miocene and
took place within the North Atlantic prior to
the trans-Arctic Interchange 3.5 million years
ago (Vermeij, 1991; Cunningham and Collins,
1998). Diversification of the I. balthica populations, however, encompasses only 2.5–
4.7% sequence change (Table 2), suggesting
that North American populations diverged in
the Pleistocene.
DISCUSSION
Studies of historical relationships among
populations require that long-range dispersal
events are relatively infrequent, so that the
genetic signal may be used to estimate the
timing of divergence (Nielsen and Slatkin,
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2000). Long-range dispersal events are probably rare in I. balthica because this genus
broods its offspring. However, I. balthica is
frequently found rafting on mats of drift algae (Tully and O’Ceidigh, 1986, 1987; Tuomi
et al., 1988; Ingólfsson, 1995). This appears
to be a primary mechanism of dispersal and
recolonization of populations affected by cold
winters and sea ice (Locke and Corey, 1989),
and individuals have occasionally been found
on drifting mats of algae hundreds of kilometers off the shore of Iceland (Ingólfsson,
1995). Even near shore, some studies have
shown that I. balthica tends to be found in
marginal driftweed habitats (Naylor, 1955;
Franke and Janke, 1998). Thus, while dispersal distances may tend to be low for each
generation it seems that there is a capacity for
long-range dispersal over geologic time. The
phylogeographic pattern found in this study
supports this conclusion. It is apparent that
there are at least three historically isolated
populations of I. balthica on the North American coast, while the European Atlantic coast
contains populations that are closely related
to each other and to one of the North American populations.
The North American populations, separated
by genetic distances of 2.5–4.7%, have been
isolated from each other since well before the
most recent glacial maximum (~20 kya,
Holder et al., 1999), based on the mtDNA
sequence data presented here. This Pleistocene separation of populations is easily explained by focusing on glacial refugia, which
seem to be found south of the glacial margin
in both North America and Europe, and also
in Newfoundland and Iceland (Dyke and
Prest, 1987; Holder et al., 1999). The genetically distinct populations from Virginia,
Nova Scotia, Iceland, and mainland Europe
may represent historical isolates which have
survived many of the Pleistocene glacial maxima. Recent dispersal events have connected
European and North American populations in
the amphi-Atlantic group (Fig. 1); although
eastward dispersal might be predicted based
on the directionality of the Gulf Stream and
North Atlantic Drift currents, patterns of haplotype diversity and genealogical signal indicate that post-glacial expansion from Europe is more likely (Wares, 2000).
The geographically isolated populations of
I. balthica in this study do not appear to be
misidentified congeners. The genetic diver-
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 4, 2001
Fig. 1. ML phylogeny of Idotea individuals in this study, using the HKY + Γ model. All members of divergent clades
(Iceland, Nova Scotia, and Virginia) are present, but some identical DNA sequences have been pruned from the
basal amphi-Atlantic group for clarity. This tree does not fit the molecular clock model (P < 0.001). Numbers below
branches indicate bootstrap support from 1,000 MP replicates.
WARES: GEOGRAPHIC ISOLATION IN IDOTEA BALTHICA
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Table 2. Genetic distances between populations of I. balthica and congeneric species in this study. Populations are
delineated according to the cladistic structure in Fig. 1. Amphi-Atlantic population represents the basal cluster of I.
balthica which are found in both European and American collection localities. Distances were calculated using the
HKY model in PAUP* 4.0b4a (Swofford, 1998).
Amphi-Atlantic
Virginia
Iceland
Nova Scotia
I. metallica
I. granulosa
I. emarginata
Amphi-Atlantic
Virginia
Iceland
Nova Scotia
I. metallica
I. granulosa
I. emarginata
0.002
0.041
0.010
0.047
0.213
0.222
0.172
0.004
0.044
0.025
0.206
0.255
0.189
0.002
0.046
0.215
0.222
0.178
0.00
0.219
0.243
0.181
0.00
0.246
0.187
n/a
0.215
n/a
gences among these populations are still
lower than those among other Idotea species
(Table 2), and these populations identified as
I. balthica form a monophyletic clade (Fig.
1). This is important, as the North American
endemic species I. phosphorea Harger, 1828,
was not available for analysis; genetic similarity between populations of I. phosphorea
and isolated populations of I. balthica could
suggest mitochondrial introgression. There is
no evidence for introgression of I. metallica,
another North American species, however.
The specimens of I. metallica from the North
Sea are clearly divergent from I. balthica, and
permanent European populations have only
recently been established from North American source populations (Franke et al., 1999),
though dispersal from North America via the
Gulf Stream may be common (Naylor, 1955).
A large amount of morphological and genetic diversity has been described for I. balthica in European populations (Bulnheim and
Fava, 1982; Legrand-Hamelin and Legrand,
1982b; Bulnheim, 1984). This includes subspecific populations in the Adriatic Sea (I. b.
basteri Audouin, 1826), North Sea (I. b.
triscuspidata Audouin, 1826), and Baltic Sea
(I. b. baltica), which are all distinct based on
allozyme data (Bulnheim, 1984). The genus
is also considered to be diverse and is distributed worldwide (Brusca, 1984; Rafi and
Laubitz, 1990), although Idotea may contain
many species which actually belong to other
Valviferan genera (Poore and Lew Ton,
1993).
It should not be assumed that the diverse
ecological and morphological characters
found in this species, and in this genus, are
simply due to labile development and ecological parameters. This study illustrates that
there may often be unrecognized populations
within a species that have been historically
isolated from one another. Isolation among
populations will also generate variation in
morphological and life-history traits, and
more molecular data may continue to indicate
the importance of historical isolation on producing variation within and among species.
For example, many of the polymorphic
characters used to define subspecies may be
genetically sex-linked (Legrand-Hamelin and
Legrand, 1982a, b), and these characters also
influence habitat choices via predator avoidance (Jormalainen and Tuomi, 1989; Merilaita and Jormalainen, 1997). Variable predation on different color morphs is the most
promising explanation for the maintenance of
color polymorphism (Jormalainen et al.,
1995), and these color morphs actually
change in frequency following seasonal
changes in substrate composition (Guarino et
al., 1993). Populations that are historically
isolated in different geographic locations may
develop different patterns of response to local predators and algal communities; this hypothesis has not been tested with direct reference to populations that are known to be
historically isolated. However, other species
seem to share this pattern of divergence.
Dahlgren et al. (2000) report a highly differentiated allele found in Nova Scotia populations of the quahog Arctica islandica
(Linnaeus, 1767), and Chopin et al. (1996)
indicate that the red alga Chondrus crispus
also has a genetically divergent population in
Nova Scotia. The fact that I. balthica is commonly found grazing on Chondrus in North
American populations, and the concordance
of these population divergences, suggests that
historical isolation due to Pleistocene glaciation has certainly played a role in genetically
structuring many North American populations.
In conclusion, history and ecology appear
to be intimately intertwined in I. balthica.
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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 21, NO. 4, 2001
There appear to be distinct grazing habits and
patterns of color polymorphism among different populations of this species. While most
of this variation may be attributed to varying availability of algal habitat or the geographic distribution of congeneric competitors (Shacklock and Croft, 1981; Shacklock
and Doyle, 1983; Salemaa, 1987; Schaffelke
et al., 1995), there are also historical discontinuities among populations of I. balthica,
signified by the genetic differentiation in this
study. Any of these factors may interact in
promoting ecological diversification. Further
studies of the ecology and evolution of I.
balthica must consider the historical isolation
of populations within the North Atlantic.
ACKNOWLEDGEMENTS
Thanks go to Cliff W. Cunningham who supported this
molecular work, V. A. Miller for technical assistance, E.
Sotka, H. D. Franke, J. E. Duffy, L. Watling, and R. Wetzer for assistance in obtaining and identifying specimens
as well as valuable discussions of Idoteid ecology. T. H.
Oakley, R. Wetzer, M. J. Hickerson, E. Naylor, and two
anonymous reviewers provided helpful suggestions for
improving this manuscript. J.P.W. was financially supported by Sigma Xi, a National Science Foundation Dissertation Improvement Grant, and NSF research grant
DEB-96-15461 (C. W. Cunningham).
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RECEIVED: 5 July 2000.
ACCEPTED: 16 April 2001.