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Distinct patterns of genetic differentiation among annelids of eastern Pacific hydrothermal vents

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Population genetic and phylogenetic analyses of mitochondrial COI from five deep-sea hydrothermal vent annelids provided insights into their dispersal modes and barriers to gene flow. These polychaetes inhabit vent fields located along the East Pacific Rise (EPR) and Galapagos Rift (GAR), where hundreds to thousands of kilometers can separate island-like populations. Long-distance dispersal occurs via larval stages, but larval life histories differ among these taxa. Mitochondrial gene flow between populations of Riftia pachyptila, a siboglinid worm with neutrally buoyant lecithothrophic larvae, is diminished across the Easter Microplate region, which lies at the boundary of Indo-Pacific and Antarctic deep-sea provinces. Populations of the siboglinid Tevnia jerichonana are similarly subdivided. Oasisia alvinae is not found on the southern EPR, but northern EPR populations of this siboglinid are subdivided across the Rivera Fracture Zone. Mitochondrial gene flow of Alvinella pompejana, an alvinellid with large negatively buoyant lecithotrophic eggs and arrested embryonic development, is unimpeded across the Easter Microplate region. Gene flow in the polynoid Branchipolynoe symmytilida also is unimpeded across the Easter Microplate region. However, A. pompejana populations are subdivided across the equator, whereas B. symmitilida populations are subdivided between the EPR and GAR axes. The present findings are compared with similar evidence from codistributed species of annelids, molluscs and crustaceans to identify potential dispersal filters in these eastern Pacific ridge systems.
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Molecular Ecology (2004)
13
, 2603– 2615 doi: 10.1111/j.1365-294X.2004.02287.x
© 2004 Blackwell Publishing Ltd
Blackwell Publishing, Ltd.
Distinct patterns of genetic differentiation among annelids
of eastern Pacific hydrothermal vents
L. A. HURTADO,
*†
R. A. LUTZ
and R. C. VRIJENHOEK
*
*
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA,
Department of Ecology and
Evolutionary Biology, University of Arizona, Biosciences West 310, Tucson, AZ 85721–0088, USA,
Institute of Marine and Coastal
Sciences, Rutgers University, New Brunswick, NJ 08901, USA
Abstract
Population genetic and phylogenetic analyses of mitochondrial COI from five deep-sea
hydrothermal vent annelids provided insights into their dispersal modes and barriers to gene
flow. These polychaetes inhabit vent fields located along the East Pacific Rise (EPR) and
Galapagos Rift (GAR), where hundreds to thousands of kilometers can separate island-like
populations. Long-distance dispersal occurs via larval stages, but larval life histories differ
among these taxa. Mitochondrial gene flow between populations of
Riftia pachyptila
, a
siboglinid worm with neutrally buoyant lecithothrophic larvae, is diminished across the
Easter Microplate region, which lies at the boundary of Indo-Pacific and Antarctic deep-sea
provinces. Populations of the siboglinid
Tevnia jerichonana
are similarly subdivided.
Oasisia
alvinae
is not found on the southern EPR, but northern EPR populations of this siboglinid
are subdivided across the Rivera Fracture Zone. Mitochondrial gene flow of
Alvinella
pompejana
, an alvinellid with large negatively buoyant lecithotrophic eggs and arrested
embryonic development, is unimpeded across the Easter Microplate region. Gene flow in
the polynoid
Branchipolynoe symmytilida
also is unimpeded across the Easter Microplate
region. However,
A. pompejana
populations are subdivided across the equator, whereas
B.
symmitilida
populations are subdivided between the EPR and GAR axes. The present find-
ings are compared with similar evidence from codistributed species of annelids, molluscs
and crustaceans to identify potential dispersal filters in these eastern Pacific ridge systems.
Keywords
:
Alvinella pompejana
,
Branchipolynoe symmytilida
, COI, hydrothermal vents, mitochondrial
gene flow, phylogeography,
Oasisia
,
Riftia
,
Tevnia
Received 21 April 2004; revision received 16 June 2004; accepted 16 June 2004
Introduction
Dispersal of deep-sea hydrothermal vent animals in the
vast ocean basins has been an intriguing and elusive issue
for biologists (Tyler & Young 1999; Van Dover
et al
. 2002).
For most vent animals little is known about the longevities
or transport modes of dispersing larvae or juveniles. Similarly,
the roles that deep oceanic currents play in facilitating
or constraining larval transport among vents also remain
poorly understood, although progress has been made
(Kim
et al
. 1994; Kim & Mullineaux 1998; Marsh
et al
. 2001;
Thomson
et al
. 2003). Nevertheless, the constrained distribu-
tion of deep-sea hydrothermal vent communities provides
remarkable opportunities to study the effects of benthic
topography, hydrography and geographical distance on
the dispersal of marine animals (Vrijenhoek 1997; Van Dover
et al
. 2002). Phylogeographical analyses of vent species
should shed light on the effective dispersal of individual
species and on the areas where gene flow is restricted which
may, in turn, help to identify dispersal barriers encountered
by these organisms in the deep sea.
Vent communities occur worldwide at marine hot springs
distributed along the global mid-ocean ridge system, in back
arc spreading centres and on volcanically active seamounts
(Tunnicliffe & Fowler 1996; Van Dover 2000). Because most
vent-endemic animals depend on free-living or symbiotic
chemolithoautotrophic microbes for nutrition, they must
Correspondence and present address: Luis A. Hurtado, Depart-
ment of Ecology and Evolutionary Biology, University of Arizona,
Biosciences West 310, Tucson, AZ 85721– 0088, USA. Fax: (520) 626
3522; E-mail: lhurtado@u.arizona.edu
2604
L. A. HURTADO, R. A. LUTZ and R. C . VRIJENHOEK
© 2004 Blackwell Publishing Ltd,
Molecular Ecology
, 13, 2603– 2615
live in or near hydrothermal effluents. This restriction cre-
ates island-like populations distributed intermittently
along tectonically or volcanically active spreading seg-
ments of the global mid-ocean ridge system as illustrated
by the distribution of vent fields along the East Pacific Rise
(EPR) and Galapagos Rift (GAR; Fig. 1). Discrete vent
fields are separated typically by tens to hundreds of kilo-
metres along an actively spreading ridge segment and by
hundreds of kilometres between disjunct ridge segments
that are often displaced by large transform faults. Finally,
populations can be located on separate ridge systems that
are separated by large habitat gaps (e.g. EPR vs. GAR). Fur-
thermore, frequent volcanic eruptions and tectonic events
along the EPR and GAR can destroy local vent communities
and create nascent vents that are rapidly colonized and
persist for few decades (Haymon
et al
. 1993; Lutz
et al
.
1994; Shank
et al
. 1998). Therefore, the animals found in
these ephemeral environments are expected to have ex-
ceptional colonization abilities including high rates of
dispersal, rapid individual growth rates and high fecundity
(Lutz
et al
. 1994; Vrijenhoek 1997; Tyler & Young 1999).
The adults of many vent animals are sessile or relatively
immobile, and long-distance dispersal takes place mainly
through the larvae. Negatively buoyant larvae are expected
to move primarily with along-axis bottom currents con-
strained to the axial valley of the ridge system (Kim &
Mullineaux 1998; Pradillon
et al
. 2001; Thomson
et al
. 2003).
In contrast, positively buoyant vent larvae can disperse in
hydrothermal plumes that rise several 100 m above the sea-
floor (Kim
et al
. 1994). Megaplumes generated by volcanic
eruptions rise as much as 1000 m above the axial walls and
can potentially transport buoyant larvae across vast dis-
tances (Mullineaux
et al
. 1995). Oceanic strata that transport
larvae expose them to a variety of current vectors that vary
with height above the seafloor (Tyler & Young 1999; Van
Dover
et al
. 2002).
Population genetic studies of vent animals from the
northern EPR and GAR have revealed different patterns of
population structure, some of which appear to be related to
ridge topography and geographical distance (France
et al
.
1992; Black
et al
. 1994; Craddock
et al
. 1995; Jollivet
et al
.
1995; Karl
et al
. 1996; Craddock
et al
. 1997; Vrijenhoek 1997;
Hurtado
et al
. 2003; Won
et al
. 2003). Although differences
were not surprising, given the disparate life histories of
these annelids, molluscs and crustaceans, most species dis-
perse effectively throughout the northern region. Genetic
studies of southern EPR vent animals have examined fewer
species, but present evidence suggests that two important
biogeographical filters might exist there. Populations of
Calyptogena magnifica
clams and
Bathymodiolus thermophilus
mussels exhibit concordant divergence across a region of
the southern EPR encompassing 15
°
S latitude (Hurtado
et al
. 2003; Won
et al
. 2003). Divergence of these clam and
mussel populations was hypothesized to result from strong
cross-axis currents that could disrupt along-axis gene flow
in this region (Lupton & Craig 1981; Hautala & Riser 1993;
Lupton 1998). Further south, species-level divergence between
sister-lineages separated by the Easter Microplate region
is observed for
Oasisia
tubeworms (Hurtado
et al
. 2002),
bythograeid crabs (Guinot
et al
. 2002; Guinot & Hurtado
2003) and
Bathymodiolus
mussels (Won
et al
. 2003). Phylo-
geographical studies of other vent-endemic taxa that cross
these potential biogeographical filters are needed to assess
the generality of these findings.
The present report examines patterns of mitochon-
drial differentiation and gene flow in five vent-endemic
annelids from the EPR (27
°
N to 32
°
S latitude) and GAR.
We examined three siboglinid tubeworms (
Riftia pachyptila
,
Tevnia jerichonana
and
Oasisia alvinae
), one alvinellid
worm (
Alvinella pompejana
) and a commensal polynoid
(
Branchipolynoe symmytilida
) that lives in the mantle cavity
of mussels. For each of these species, we amplified a portion
of the mitochondrial cytochrome c oxidase subunit I gene
(
mtCOI
) and examined patterns of genetic differentiation
to assess geographical subdivision and gene flow.
Materials and methods
Biological specimens
Specimens were collected during
Alvin/Atlantis
expeditions
to 12 hydrothermal vent fields along GAR and EPR axes
(Table 1). The northern EPR and GAR were sampled
Fig. 1 East Pacific Rise and Galapagos Rift. Triangles represent
known vent fields; names of transform faults are indicated.
POPULATION GENETICS OF HYDROTHERMAL VENT ANNELIDS
2605
© 2004 Blackwell Publishing Ltd,
Molecular Ecology
, 13, 2603– 2615
between 1990 and 1994, 2000, and 2002, and the southern
EPR was sampled in 1999.
The siboglinid tubeworms are completely sessile as adults.
R. pachyptila
are large worms that commonly reach 1.5 m in
length and live in smooth flexible tubes attached to sulphide
chimneys and basalts. This species produces neutrally
buoyant, small (
100
µ
m) lecithotrophic eggs with sufficient
energy reserves to persist in the water column for about
38 days (Marsh
et al
. 2001).
T. jerichonana
are thinner worms,
reach up to a metre in length and live in narrower rigid
tubes attached to solid substrates.
O. alvinae
are relatively
small worms (typically < 0.3 m) that live in narrow rigid tubes
with wide flutes. They are often attached to basaltic rocks,
clumps of
Bathymodiolus
mussels or
Riftia
tubes. No infor-
mation on the larval biology of
Tevnia
or
Oasisia
is reported.
A. pompejana
worms live in soft thin-walled tubes attached
to sulphide chimneys or to
Riftia
tubes in areas of strong
hydrothermal flow. Adults can exit their tubes and swim
vigorously, although long-distance dispersal of adults seems
improbable. This worm releases large (
200
µ
m) negatively
buoyant lecithotrophic eggs that are expected to drift with
bottom currents, and arrested embryonic development
appears to increase long-distance dispersal abilities of these
benthic larvae (Pradillon
et al
. 2001).
B. symmytilida
scale worms live in the mantle cavity of
Bathymodiolus
mussels. Larval biology of this species is
unknown, but the mid-Atlantic ridge species,
Branchipolynoe
seepensis
, has very large eggs (
500
µ
m) and lecithotrophic
larvae (Tyler & Young 1999).
Molecular methods
We examined mitochondrial cytochrome c oxidase subunit
I (
mtCOI
) sequences in this study because: (i) universal
invertebrate primers were available for a portion of this
gene (Folmer
et al
. 1994); (ii) intermolecular genetic recom-
bination appears to be absent; and (iii) this gene region has
provided useful variation for previous genetic studies of
vent taxa (e.g. Craddock
et al
. 1995; Hurtado
et al
. 2002,
2003; Won
et al
. 2003). Although doubly uniparental
inheritance (DUI) of mitochondria is reported in some
marine bivalves (Zouros
et al
. 1994 and Passamonti & Scali
2001), it has not been observed in hydrothermal vent
bivalves (Goffredi
et al
. 2003; Hurtado
et al
. 2003; Won
et al
.
2003). Strictly maternal transmission of mitochondria in
the annelids examined in this study was assumed because
we found no evidence for heteroplasmy in any of the
observed sequences. Thus, our conclusions about gene
flow apply only to females, athough we have no reason
to suspect that differential dispersal occurs between the
sexes. Previous studies of
mtCOI
and nonmitochondrial
gene markers in vent species have revealed concordant
patterns of population structure (Craddock
et al
. 1995;
O’Mullan
et al
. 2001; Hurtado
et al
. 2003; Won
et al
. 2003).
Total DNA from tissue samples was extracted using the
DNEasy kit (Qiagen, Inc., Chatsworth, CA, USA). A 710-
base pairs (bp) region of mitochondrial COI (
mtCOI
) was
amplified using primers and conditions reported by Folmer
et al
. (1994). Polymerase chain reaction (PCR) products
Table 1 East Pacific Rise and Galapagos Rift samples
Region, vent field Latitude Longitude Depth (m)
Species*
Rp Tj Oa Ap Bs
NEPR
27°N27°00N111°24W2008 10 —
21°N20°50N109°06W2636 10 — 22 7
13°N12°49N103°57W2636 † 12 11 5
11°N11°25N103°47W2515 † 9 † ††
9°N9°48N104°15W2525 19 12 10 21 10
GAR
GAR 0°48N86°09W2486 9 — 22
SEPR
7°S7°25S107°49W2747 26 28 — 8
11°S11°18S110°32W2669 24 † 10 †
14°S13°59S112°29W2626 — — 3 †
17°S17°25S113°12W2578 25 28 — 21 4
21°S21°34S114°18W2834 †† †† —
32°S31°51S112°03W2331 12 26 — 26 17
*Sample sizes: (Rp) R. pachyptila; (Tj) T. jerichonana; (Oa) O. alvinae; (Ap) A. pompejana; and (Bs) B. symmytilida.
Not recorded for this locality.
†Observed but not sampled for this study.
††Rare.
2606 L. A. HURTADO, R. A. LUTZ and R. C . VRIJENHOEK
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
were cleaned with the Qiaquick PCR Kit (Qiagen, Inc.,
Valencia, CA, USA) and sequenced in both directions with
ABI 377 or Licor 4000 L sequencers. Sequences were proof-
read and aligned with sequencher version 4.1 (Gene Codes
Corp., Ann Arbor, MI, USA). All mtCOI DNA sequences
were translated to amino acid sequences and no terminal
codons or indels were found among these sequences; thus,
we are confident to have amplified and sequenced mtCOI
and not a pseudogene.
For Riftia, most individuals were scored by restriction
digests of PCR products (see explanation in Results sec-
tion) using the BsiE I enzyme according to manufacturer’s
protocols (New England Biolabs, Beverly, MA, USA), and
fragment patterns were visualized on 1% agarose gels.
Population genetic and phylogenetic analyses
arlequin 2000 (Schneider et al. 2000) was used to estimate
gene diversity and conduct statistical tests. For each species
the following statistics were calculated: haplotype diversity,
h (equ. 8.6, Nei 1987); mean number of pairwise differ-
ences, π1 (Tajima 1983); and nucleotide diversity, π2 (equ.
10.6 Nei 1987). FST and Nm were estimated following
the method of Hudson et al. (1992) and exact tests of dif-
ferentiation were conducted following the method of
Raymond & Rousset (1995). Kimura-2-parameter (K2P)
genetic distances are reported (Kimura 1980) to correct for
mutational saturation, although at the within-species level
this is unlikely to present a problem. These K2P distances
were not used in any analyses, and are shown for comparative
purposes only. Phylogenetic analyses were conducted
with the tcs program (Clement et al. 2000), which was used
to construct statistical parsimony networks of mitochondrial
haplotypes. This method appears to provide better repres-
entations of gene genealogies at the population level than
other phylogenetic inference methods ( Templeton et al. 1992).
Demographic analyses
Tests were conducted to assess whether the populations
examined fit expectations for mutation-drift equilibrium,
and whether they fit a population size stationary model vs.
a population expansion model. Tajima’s D (Tajima 1989)
and Fu’s FS (Fu 1996) statistics were estimated to assess
evidence of population expansions. Although these statistics
were developed as tests of selective neutrality, they are
very powerful for detecting departures from population
size equilibrium caused by population expansions or
bottlenecks (Aris-Brosou & Excoffier 1996; Tajima 1996; Fu
1997; Ray et al. 2003). arlequin was used to conduct these
tests and calculate the corresponding P-values. Mismatch
distributions of DNA sequences (Harpending 1994;
Schneider & Excoffier 1999) were also examined. Ragged
and erratic distributions are expected for stationary popu-
lations, whereas smooth distributions are expected for
populations that experienced range expansions (Harpending
1994). arlequin estimates parameters related to a popu-
lation growth expansion, such as expansion time τ (= 2ut,
where u is the mutation rate and t is the number of
generations since the expansion), θ0 = 2uN0, and θ1 = 2uN1
(where N0 and N1 are the population sizes before and after
the expansion). The values reported for θ0 and θ1 are mean
values based on 100 replicates and an alpha value of
0.05. A model of population expansion is assumed if τ > 0
and θ1 > θ0, whereas a model of population stationarity is
assumed if τ = 0 or θ1 = θ0. Validity of the estimated
demographic model is tested by obtaining the distribution
of a test statistic SSD (the sum of squared differences) be-
tween the observed and an estimated mismatch distribution
obtained by a bootstrap approach (Schneider & Excoffier
1999). The P-value of the SSD statistic is computed as the
proportion of simulated cases that show a SSD value larger
than the original. A significant SSD value (P-values < 0.05)
is taken as evidence for departure from the estimated model
of population expansion (when τ > 0 and θ1 > θ0), or from
a model of population stationarity (when τ = 0 or θ1 = θ0).
Demographic tests were conducted first for each locality
and secondly for pooled localities that were determined
to be genetically homogeneous by the exact tests of popu-
lation differentiation. The same groups of pooled localities
were used to conduct Analysis of Molecular Variance (amova,
Excoffier et al. 1992), also using arlequin, to assess the pro-
portion of genetic variation attributable to differentiation
within groups.
Results
Geographic distributions
R. pachyptila has the broadest known distribution of these
five polychaetes, ranging from 27°N (Guaymas Basin) to
32°S on the EPR and on the GAR (Table 1). T. jerichonana
ranges from 13°N to 32°S on the EPR and is not known
from the GAR. Oasisia is a polytypic genus with highly
divergent evolutionary lineages that probably comprise
undescribed species (Hurtado et al. 2002). O. alvinae sensu
stricto has been found between 21°N and 9°N on the
northern EPR. Hurtado et al. (2002) report the presence of
two other very divergent lineages of Oasisia and suggest
they may constitute different species. One restricted to vents
south of the Easter Microplate (31–32°S) and the other
found at 9°N vents, with mtCOI divergences of 9% and
6% from O. alvinae s. s., respectively. The present analysis
was restricted to what we regard as O. alvinae s. s. samples,
as they formed a distinct, well-supported monophyletic
group (maximum mtCOI K2P divergence = 3.0%) that
excluded the other two divergent lineages. An earlier
allozyme study revealed no evidence for cryptic subdivision
POPULATION GENETICS OF HYDROTHERMAL VENT ANNELIDS 2607
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
in this subset of Oasisia samples (Black et al. 1998). No Oasisia
tubeworms have been observed or collected between 9°N
and the Easter Microplate region of the EPR (3000 km).
Oasisia-like tubeworms were observed at GAR vents in
1988, but specimens were not obtained then for genetic
analyses (C. Fisher, personal communication). The Pompeii
worm, A. pompejana, ranges from 21°N to 32°S on the EPR
and is not known from GAR. The range of the commensal
scale worm B. symmytilida coincides with that of its host,
the mussel B. thermophilus, from 13°N to 32°S along the EPR
and on the GAR.
Mitochondrial diversity and phylogeography
Altogether, 353 mtCOI sequences were obtained from the
five worm species (Table 2). All different haplotypes were
deposited in GenBank (Accession nos AY645949–AY646057).
Mitochondrial diversity varied greatly across the five
species. R. pachyptila and T. jerichonana exhibited very low
haplotypic diversity relative to O. alvinae, A. pompejana and
B. symmitilida, which have more segregating sites across
this 630649 bp portion of mtCOI.
R. pachyptila. A preliminary sequence analysis of EPR
individuals from 27°N (n = 10), 21°N (n = 10) and 31–32°S
(n = 12) identified only one polymorphic site. One of the
haplotypes was observed in 25 individuals (Rp-A) and the
other (Rp-B) in seven. Because so little sequence variation
was observed, 94 additional specimens were screened
from EPR localities using the restriction enzyme BsiE-I that
cuts the polymorphic site in the Rp-B haplotype. In total,
112 individuals had the Rp-A haplotype in EPR localities
north of the Easter Microplate (27°N to 17°S), and only two
individuals from 7°S had the Rp-B haplotype. However,
the frequencies of the two haplotypes shifted dramatically
to the south of the Easter Microplate, at 31–32°S, where five
individuals were observed with the Rp-A haplotype and
seven with the Rp-B haplotype. Nine individuals from
GAR were also sequenced and eight of them had the Rp-A
haplotype and the remaining individual had a third
haplotype (Rp-C) that differs from the common Rp-A by
only one position (Fig. 2A).
Limited genetic variability may limit our conclusions
about gene flow in this species. However, the severe shift
observed in the frequency of the two EPR haplotypes
between the population south of the Easter Microplate (31–
32°S) and the other populations to the north suggests very
restricted gene flow across the Easter Microplate (Table 3;
Fig. 2F). Rates of gene flow between localities north of the
Easter Microplate appear to be high, since the Rp-A haplo-
type was essentially fixed at these localities.
T. jerichonana. Sequences from 115 individuals yielded
nine polymorphic sites and nine haplotypes (Table 2). A
cluster of haplotypes (shown blue in Fig. 2B) differed by
single nucleotide substitutions from the most common
haplotype (Tj-D). A second group of haplotypes (shown red
in Fig. 2B) connects to the blue group through a ‘missing’
haplotype. Frequencies of the two groups of haplotypes
were distributed as a north–south cline (Fig. 2G). As in R.
pachyptila, populations of T. jerichonana from south of the
Easter Microplate (31–32°S) also differed from all popu-
lations to the north (Table 4). FST values between these
groups ranged from 0.38 to 0.74, and estimated rates of
gene flow were low (Nm < 0.8). The T. jerichonana group to
the north of the Easter Microplate is subdivided into two
subgroups separated by the Equator (i.e. 9 –13°N vs. 7–17°S).
FST values between these two groups ranged from 0.09 to
0.22 and estimates of gene flow between groups were at
intermediate levels (Nm range: 1.8–5.2).
O. alvinae. Sequences from 43 O. alvinae individuals yielded
33 polymorphic sites and 20 haplotypes. The statistical
Table 2 Mitochondrial COI diversity
Species NLK h k π1π2
R. pachyptila 41 640 3 0.3305
(0.0817)
2 0.3390
(0.3434)
0.0005
(0.0005)
T. jerichonana 115 630 9 0.5545
(0.0333)
9 1.1210
(0.7361)
0.0018
(0.0013)
O. alvinae 43 649 20 0.8893
(0.0345)
33 9.2270
(4.3256)
0.0142
(0.0074)
A
. pompejana 93 648 40 0.9054
(0.0254)
48 5.2382
(2.5567)
0.0081
(0.0044)
B. symmytilida 61 641 38 0.9601
(0.0161)
40 3.8727
(1.9716)
0.0060
(0.0034)
N = number of sequences; L = sequence length; K = number of
haplotypes; h = haplotype diversity; k = number of polymorphic
sites; π1 = mean number of pairwise differences; π2 = nucleotide
diversity. Standard errors in parentheses.
Table 3 Riftia pachyptila. Pairwise FST (above) and Nm values
(below diagonal). Bold-type FST values are statistically significant
(P < 0.05) based on exact tests
Locality 27°N21°N9°NGAR 7°S11°S17°S32°S
27°N000 0.01 0 0 0.52
21°N* 00 0.01 0 0 0.52
9°N**00.02 0 0 0.50
GAR * * * 0.02 0 0 0.62
7°S**21.4 * 0.04 0.04 0.48
11°S* ***13.6 0 0.66
17°S* ***12.7 * 0.66
32°S0.5 0.5 0.3 0.5 0.6 0.3 0.3
*Nm is undefined and approaches panmixia.
2608 L. A. HURTADO, R. A. LUTZ and R. C . VRIJENHOEK
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
parsimony network was partitioned into three clusters
(shown light blue, dark blue and red in Fig. 2C). The red
and dark blue clusters are connected by 10 ‘missing’
haplotypes, and the light and dark blue clusters are linked
by four haplotypes. Mean K2P divergence between the red
and blue clusters is 2.5%. Significant genetic differentiation
was observed between populations separated by the
Rivera Fracture Zone (21°N vs. 9–13°N; Table 5; Fig. 2H).
A. pompejana. Sequences from 93 individuals yielded 48
polymorphic sites and 40 haplotypes. The statistical
parsimony network revealed a clear separation between
northern and southern EPR localities (red vs. blue, Fig. 2D).
Two equally parsimonious paths separate the red and blue
Table 4 Tevnia jerichonana. Pairwise FST (above) and Nm values
(below diagonal). Bold-type FST values are statistically significant
(P < 0.05) based on exact tests
Locality 13°N11°N9°N7°S17°S32°S
13°N0.00 0.00 0.09 0.11 0.68
11°N117.0 0.01 0.17 0.20 0.71
9°N*34.9 0.19 0.22 0.74
7°S5.2 2.4 2.1 0.00 0.39
17°S4.0 2.1 1.8 * 0.38
32°S0.2 0.2 0.2 0.8 0.8
*Nm is undefined and approaches panmixia.
Fig. 2 Haplotype networks and frequencies for five eastern Pacific hydrothermal vent annelids. (A–E) Haplotype networks. (F–J)
Distribution of haplotype frequencies. Colour codes used for haplotypes in the networks correspond with those used in the pie-diagrams.
Table 5 Oasisia alvinae. Pairwise FST (above) and Nm values
(below diagonal). Bold-type FST values are statistically significant
(P < 0.05) based on exact tests
Locality 21°N13°N9°N
21°N0.48 0.49
13°N0.55 0.00
9°N0.52 *
*Nm is undefined and approaches panmixia.
POPULATION GENETICS OF HYDROTHERMAL VENT ANNELIDS 2609
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
clusters. The red cluster exhibited a star-like phylogeny
with short branches from the most frequent haplotype
(Ap-J ), whereas the blue cluster exhibited a more complex
branching topology. As expected, the northern and southern
EPR samples differed significantly (Table 6; Fig. 2I). FST
values between these groups ranged from 0.44 to 0.78, and
estimated rates of gene flow were low (Nm range: 0.14
0.65). This dramatic partitioning of mitochondrial lineages
across the Equator contrasted with homogeneity within
subdivisions. For both the northern and southern regions,
pairwise FST values revealed no appreciable genetic dif-
ferentiation and extensive gene flow within each subdivision.
Although larger samples from some localities would have
improved the FST estimates, sample sizes of these worms
generally were beyond our control. Nonetheless, this species
exhibited a large number of polymorphic sites (mean
number of pairwise differences = 5.2 ± 2.6) that may have
compensated for low sample size in some of the pairwise
estimates of FST.
B. symmytilida. Sequences from 61 individuals yielded
40 polymorphic sites and 38 haplotypes. The statistical
parsimony network was complex (Fig. 2E), exhibiting
multiple equally parsimonious links. One discrete cluster
of haplotypes (shown green in Fig. 2E) was restricted
almost entirely to the GAR; however, green haplotypes
were nearly absent from the EPR, which houses a poorly
resolved complex network of haplotypes (blue). As expected,
B. symmitilida from the GAR differed significantly from the
EPR worms. FST values between these groups ranged from
0.19 to 0.48 and estimated gene flow was fairly low
(Nm range: 0.55–2.19). However, unlike the other worms,
B. symmytilida exhibited no genetic differentiation along its
entire range on the EPR (Table 7; Fig. 2J). Pairwise FST
values indicated extensive gene flow across the EPR. Like
A. pompejana, this species also exhibited a large number of
polymorphic sites (mean number of pairwise differences
= 3.9 ± 2.0) that may have compensated for low sample
size in some of the pairwise estimates of FST.
Demographic analyses
Demographic tests were conducted for each locality
separately and on groups of localities (Roman numerals
in Fig. 2 and Table 8) that were genetically homogeneous
as determined by previous exact tests of population dif-
ferentiation. Both methods provided similar results, but
because some localities had small sample sizes, we report
only the results for pooled localities. amovas for each
species (not shown) revealed that the proportion of genetic
variation due to heterogeneity among samples within these
groups of localities did not differ from zero. Demographic
analyses suggested that population expansions might have
occurred in T. jerichonana, A. pompejana and B. symmytilida
(Table 8). Significant Tajima’s D and Fu’s FS statistics were
obtained for the northern EPR population of T. jerichonana,
the southern EPR population of A. pompejana, and the GAR
population of B. symmytilida, whereas only significant FS
values were obtained for the northern EPR population of
A. pompejana and the EPR population of B. symmytilida.
Significant test statistics in T. jerichonana from the northern
EPR and in B. symmytilida from the GAR and EPR resulted
from the presence of a few individuals (assumed to be
migrants) from very divergent clades. As expected (see
Ray et al. 2003), the D statistic was less sensitive than FS to
departures from population equilibrium.
Mismatch statistics of populations with significant D
and FS statistics were consistent with models of population
expansion. Mismatch distributions for these populations
were unimodal (not shown). Evidence of population
expansion (i.e. τ > 0; θ1 > θ0) was found in nearly all tests
except for the SEPR (7–17°S) grouping of T. jerichonana,
where the SSD statistic was significant, therefore rejecting
the population expansion hypothesis. The mismatch graph
was somewhat ragged (not shown), and the D and FS
statistics were not significant. The results for O. alvinae were
more complicated. D and FS were not significant and the
mismatch graphs may be interpreted as ragged (not shown),
suggesting population stationarity. However, mismatch
parameters were consistent with a model of population
expansion (τ > 0; θ1 > θ0). Demographic analyses were not
Table 6 Alvinella pompejana. Pairwise FST (above) and Nm values
(below diagonal). Bold-type FST values are statistically significant
(P < 0.05) based on exact tests
Locality 21°N13°N9°N11°S14°S17°S32°S
21°N0.01 0.00 0.65 0.46 0.70 0.73
13°N32.34 0.00 0.75 0.64 0.76 0.78
9°N** 0.53 0.44 0.58 0.61
11°S0.27 0.17 0.45 0.00 0.00 0.01
14°S0.60 0.29 0.65 * 0.00 0.00
17°S0.22 0.16 0.37 * * 0.07
32°S0.19 0.14 0.32 38.26 * 6.63
*Nm is undefined and approaches panmixia.
Table 7 Branchipolynoe symmytilida. Pairwise FST (above diagonal)
and Nm values (below diagonal). Bold-type FST values are
statistically significant (P < 0.05) based on exact tests
Locality 9°N7°S17°S32°SGAR
9°N0000.19
7°S* 000.32
17°S** 00.48
32°S*** 0.32
GAR 2.19 1.06 0.55 1.06
*Nm is undefined and approaches panmixia.
2610 L. A. HURTADO, R. A. LUTZ and R. C . VRIJENHOEK
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
conducted for R. pachyptila, because most of the specimens
were scored using a restriction enzyme. Nevertheless,
extremely reduced mitochondrial variability observed
among the individuals of this species suggests that a very
strong bottleneck or mitochondrial selective sweep has
occurred recently in this species. Results of an earlier allozyme
study suggest that bottlenecks might have impacted north-
ern populations of R. pachyptila (Black et al. 1994). Poly-
morphic loci carry only two alleles and the least frequent
allele generally exceeded 0.10 in frequency. Rare alleles are
lost rapidly during bottlenecks and founder events, but
heterozygosity due to remaining common alleles need not
diminish greatly if the population has a high intrinsic rate
of increase (Nei et al. 1975), or if balancing selection was
acting on the polymorphic allozyme loci ( Karl & Avise 1992).
Discussion
Population genetic and phylogenetic analyses of five poly-
chaete annelids revealed patterns of genetic differentiation
among vent fields spread across 7000 km of the East Pacific
Rise (EPR) and Galapagos Rift (GAR). Different patterns
of mitochondrial population structure exist among these
species, suggesting substantial differences in their evo-
lutionary histories, individual life histories and dis-
persal strategies. The results revealed four barriers to
dispersal that affected one or more of these annelid species:
(i) a dispersal filter around the Easter Microplate region;
(ii) a dispersal filter separating EPR and GAR populations;
(iii) a dispersal filter around the Equator separating northern
and southern EPR populations; and (iv) a dispersal filter
around the Rivera Fracture Zone. However, no evidence
was found among these annelids for restricted gene flow
across the 15°S latitude region of the EPR, where strong
cross-axis currents are hypothesized to disrupt along-
axis dispersal of the vent bivalves C. magnifica and B.
thermophilus (Hurtado 2002; Hurtado et al. 2003; Won et al.
2003). The four dispersal filters affecting these vent annelids
are discussed below, and our findings are compared with
genetic and biogeographical evidence from other vent-endemic
macroinvertebrates. The location of these filters is concordant
with genetic shifts or distributional limits of other vent
species.
The Easter Microplate region
Mitochondrial evidence suggests that the siboglinid tube-
worms R. pachyptila and T. jerichonana are subdivided
across the Easter Microplate region, but the polynoid B.
symmitilida and alvinellid A. pompejana are not. Mitochond-
rial and allozyme evidence indicate that populations of
Bathymodiolus mussels also are isolated across the Easter
Microplate region and may comprise distinct species (Won
et al. 2003). Other vent animals exhibit evidence for an
older historical barrier across the Easter Microplate. Oasisia
tubeworms from south of the Easter microplate appear
to comprise a distinct species from those found on the
northern EPR (Hurtado et al. 2002). The bythograeid crabs
Allograea tomentosa and Bythograea vrijenhoeki have only
been found south of the microplate, whereas their respective
sister-species, Cyanograea praedator and Bythograea laubieri,
are distributed widely to the north (Guinot et al. 2002;
Table 8 Population expansion tests: D = Tajima’s D-test; FS = Fu’s FS tests. P-values follow each test (significant are in bold type).
Population growth expansion parameters: τ, θ0, and θ1. SSD = sum of square deviation and corresponding P-value
Species/group DPF
SPτθ
0θ1SSD P
R. pachyptila
i (EPR, 27°N17°S) 1.15 0.15 1.18 0.06
ii (SEPR, 31–32°S) 1.38 0.95 1.15 0.62
T. jerichonana
i (NEPR, 9–13°N) 2.00 0.00 3.89 0.00 3.01 0.04 76.77 0.00 0.37
ii (SEPR, 7–17°S) 0.12 0.47 0.07 0.53 2.57 0.10 641.03 0.14 0.04
iii (SEPR, 31–32°S) 0.85 0.23 0.52 0.29 2.02 0.11 546.76 0.00 0.69
O. alvinae
i (NEPR, 21°N) 0.41 0.40 2.69 0.13 4.39 2.58 78.90 0.03 0.49
ii (NEPR, 9–13°N) 0.47 0.35 0.62 0.62 6.19 0.54 31.20 0.06 0.36
A
. pompejana
i (NEPR, 9–21°N) 0.89 0.21 7.21 0.01 9.57 0.12 17.78 0.00 0.87
ii (SEPR, 7–32°S) 2.22 0.00 –19.38 0.00 1.41 0.27 3005.66 0.01 0.07
B. symmitilida
i (EPR, 13°N32°S) 1.23 0.08 3.60 0.00 3.76 0.42 2087.79 0.00 0.37
ii (GAR) 2.05 0.00 5.84 0.00 1.94 0.06 2034.22 0.00 0.79
POPULATION GENETICS OF HYDROTHERMAL VENT ANNELIDS 2611
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
Guinot & Hurtado 2003). The Easter Microplate region also
coincides with the distributional boundaries of several
vent animals. As mentioned previously, two bythograeid
crabs, a mussel and an Oasisia tubeworm species appear to
be endemic to vents south of the microplate. Conversely,
several northern species appear to reach their southern
limits just north of the Easter Microplate (e.g. the previously
mentioned vent crabs Bythograea thermydron and C. praedator).
We did not find the clam C. magnifica south of the Easter
Microplate (Hurtado et al. 2003). However, the clam appears
to be a late colonizer at nascent vents (Shank et al. 1998),
and perhaps the 31–32°S vents had not reached a sufficiently
late stage of succession at the time of our visit in 1999.
The Easter Microplate may constitute a historical dis-
persal barrier for some taxa. It was formed between 5.25 and
2.47 million years ago (Mya) (Naar & Hey 1991; Rusby &
Searle 1995). Transform faults on the north and south
flanks of the microplate, and chains of young seamounts
extending to the east and west (Searle et al. 1989), create
topographical features that appear to entrain strong cross-
axis currents (Fujio & Imasato 1991). However, high levels
of molecular divergence in Oasisia tubeworms (Hurtado
et al. 2002) and bythograeid crabs (Guinot et al. 2002; Guinot
& Hurtado 2003) suggest that their divergence began
prior to formation of the microplate. This region lies at a
well-known zoogeographical boundary separating Indo-
Pacific and Antarctic deep-sea faunas, and defined by the
Antarctic Circumpolar Current (ACC) (Mironov et al. 1998;
Vinogradova 1979). Transitions between biogeographical
provinces are often associated with phylogeographical
breaks in taxa that cross provincial boundaries (reviewed
by Avise 2000). The ACC provides a link between the
Pacific, Atlantic and Indian Oceans that originated with
the opening of the Tasmanian Gateway between Australia
and Antarctica 34 Mya and the Drake Passage between
South America and Antarctica 20 Mya (Barker & Burrell
1977; Lawver et al. 1992). A molecular clock used to esti-
mate the time of divergence of the Oasisia lineage from 31–
32°S (Hurtado 2002), which is up to 10% divergent from
northern lineages, indicates that divergence of this lineage
occurred at least 18–21.6 Mya (assuming that the sub-
stitution rate for mtCOI in siboglinids is 0.430.48%/MY;
Chevaldonné et al. 2002). This estimate overlaps with the
time the ACC began crossing the EPR.
A filter around the Equator
Significant mitochondrial divergence exists between popu-
lations of the alvinellid A. pompejana separated by a habitat
gap that spans the Equator. Northern and southern EPR
populations of this worm are reciprocally monophyletic,
which suggests long-standing separation. Although less
dramatic, mitochondrial frequencies shift significantly
between T. jerichonana populations from north and south
of the Equator. In contrast, the annelids R. pachyptila and B.
symmytilida, the clam C. magnifica (Hurtado et al. 2003) and
the mussel B. thermophilus (Won et al. 2003) show no evidence
for restricted gene flow across the Equator. The distributional
limits of two bythograeid crabs suggest the presence of a
historical dispersal filter around the Equator. Bythograea
microps appears to be restricted to northern EPR (21–9°N)
vents, whereas B. laubieri to southern EPR vents (11–32°S)
(Guinot et al. 2002; Guinot & Hurtado 2003).
A strong, eastward, deep-sea, equatorial current creates
abrupt northern and southern gyres where it crosses the
EPR (Reid 1997). Such currents might present a barrier for
dispersal of pelagic larvae, which crabs are likely to possess,
but these currents should not impede dispersal of neg-
atively buoyant larvae that travel near the bottom, such as the
larvae of A. pompejana, a species with restricted dispersal
across this region. Topographical features associated with
the triple junction at the EPR and Galapagos Rift conver-
gence (e.g. the Hess Deep, a 6000 m depression), where the
Galapagos Microplate is formed (Lonsdale 1988), may
present a barrier to dispersal for species such as A. pompejana.
The Galapagos barrier
Hydrographic and topographical features of the equatorial
region may also create a dispersal filter between the GAR
and EPR. For example, B. symmytilida from the GAR was
nearly fixed for a unique mitochondrial lineage. Other taxa
also reveal evidence for restricted dispersal between the
EPR and GAR. C. magnifica clams from the GAR are fixed
for a unique mitochondrial variant (Hurtado et al. 2003),
and extremely reduced levels of gene flow occur between
GAR and EPR populations of the amphipod Ventiella
sulfuris (France et al. 1992). Restricted gene flow between
the EPR and GAR populations was also suggested
for the alvinellid Paralvinella grassleii ( Jollivet et al. 1995).
On the other hand, gene flow is not restricted between
B. thermophilus mussels from GAR and northern EPR popu-
lations (Craddock et al. 1995; Won et al. 2003). Distributions
of several vent species also suggest isolation of the GAR.
The vent annelids T. jerichonana and A. pompejana, and bytho-
graeid crabs C. praedator and B. laubieri (Guinot & Hurtado
2003) are not found on the GAR. Conversely, Bythograea
galapagensis (a possible synonymy of Bythograea intermedia)
is endemic to the GAR, and this species is 9.6% divergent
from its closest relative, B. thermydron, which is distributed
widely at EPR and GAR vents (Guinot & Hurtado 2003).
The Rivera Fracture Zone
The Rivera Fracture Zone (FZ) (Fig. 1) is the longest trans-
form fault (240 km) along the EPR axis. It lacks hydro-
thermal habitats and coincides with a strong westward
current at 2500 m depth (Reid 1997). Mitochondrial
2612 L. A. HURTADO, R. A. LUTZ and R. C . VRIJENHOEK
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
frequencies in O. alvinae shift significantly across this region.
The amphipod V. sulfuris also exhibits shifts in allozyme
frequencies across this region (France et al. 1992). The
Rivera FZ corresponds with the northern limit for a
number of EPR taxa, including the annelids T. jerichonana
and B. symmytilida and the mussel B. thermophilus, even
though the chemical milieu at 21°N appears to be adequate
for the missing species (Van Dover 2000). Strong currents
in this region may divert the larvae of some EPR species
away from the ridge axis.
Larval histories and genetic patterns
Unfortunately, larval life histories of most vent inverte-
brates are poorly understood (Tyler & Young 1999; Van
Dover 2000), which severely limits our ability to interpret
the present genetic patterns. In addition, it is not possible
to infer modes of larval dispersal based on similarities
of genetic differentiation patterns, because they are very
different in the species analysed. The worm A. pompejana
releases large negatively buoyant eggs (200 µm) that are
expected to drift with bottom currents (Pradillon et al.
2001), and larvae are believed to be benthic (Jollivet et al.
1998). Delayed metamorphosis in cold water and movement
through along-ridge axis currents appear to increase long
distance dispersal abilities of these benthic larvae (Pradillon
et al. 2001). For a species with such larval characteristics, an
important dispersal filter is found between 9°N and 11°S in
the EPR (i.e. the filter around the Equator), but the Easter
Microplate filter does not seem to affect dispersal of this
species. In contrast, the Easter Microplate filter appears to
restrict gene flow in R. pachyptila, a species that produces
neutrally buoyant small eggs (100 µm) with sufficient energy
reserves to persist in the water column for about 38 days
(Marsh et al. 2001). At 9°N the nonfeeding trochophore
larvae of R. pachyptila are expected to disperse a mean
distance of about 100 km, although the dispersal distance
does not appear limited by the physiological performance
of the larvae but rather by temporal oscillations in the
along-axis currents and by larval loss in cross-axis flows.
Therefore, dispersal distances of larvae of this species at
other vent sites will depend on local current regimes.
Larval biology of B. symmytilida is unknown. A related
species from the Mid-Atlantic Ridge, B. seepensis, has very
large eggs (500 µm) and lecithotrophic larvae (Tyler &
Young 1999). B. symmytilida shows no genetic differenti-
ation across the Easter Microplate. Based on this similarity
with A. pompejana, one might suggest similar larval bio-
logies, i.e. negatively buoyant eggs and arrested develop-
ment. However, population structure of the two species
differs north of the Easter Microplate, where A. pompejana
is subdivided across the Equator, while B. symmytilida is
not. Similarly, one might speculate that the larvae of T. jeri-
chonana are similar to those of its closest relative, R. pachyptila,
because both species showed significant mitochondrial
subdivision across the Easter Microplate. Another siboglinid,
O. alvinae, does not appear to disperse long distances, because
significant genetic subdivision was observed at compara-
tively small geographical scales (21°N vs. 9–13°N EPR).
Ecology and genetic patterns
A positive correlation between allozyme diversity and
levels of occupancy is reported for vent invertebrates from
the northern EPR and GAR (Vrijenhoek 1997). Species with
established populations at most of the known vent fields
are reported to have higher levels of allozyme diversity
than species that occupy fewer vent fields. However, site
occupancy is confounded with the order in which these
species establish colonies at nascent hydrothermal vents
(Vrijenhoek et al. 1998). Early colonizers (appearing within
2 years of vent formation — R. pachyptila, T. jerichonana,
P. grasslei, Alvinella caudata, A. pompejana, Lepetodrilus elevatus
and V. sulfuris) had high occupancy and nearly twice the
allozyme diversity of late colonizers (appearing after 2 years
of vent formation — O. alvinae, C. magnifica, B. thermophilus
and Eulepetopsis vitrea). However, these predictions are not
always consistent with the present mitochondrial data
obtained from approximately twice the geographical range.
For example, lower mitochondrial diversity is observed in
R. pachyptila and T. jerichonana, early colonizers with
high site occupancy, than in O. alvinae, a late colonizer
with low occupancy. Conversely, B. symmytilida and its
mussel host B. thermophilus (Won et al. 2003), which are late
colonizers with relatively low occupancy, both have
high levels of mitochondrial diversity. On the other hand,
allozyme and mitochondrial diversity are both high in A.
pompejana, an early colonizer (Jollivet et al. 1995); and the
clam C. magnifica, a late colonizer with very low occupancy,
has remarkably low diversity in allozymes and nuclear
DNAs (Karl et al. 1996), as well as low mitochondrial divers-
ity (Hurtado et al. 2003). Contrasting patterns of allozyme
and mitochondrial diversity indicate that overall genetic
diversity of vent macroinvertebrates cannot be predicted
simply from knowledge of site occupancy and succes-
sional order. More complex evolutionary and demographic
processes appear to have shaped genetic diversity in these
species. Demographic tests suggest that the ephemeral
nature of vent habitats in the EPR and GAR has had strong
effects on mitochondrial diversity of these vent annelids.
For the most part, these populations do not appear to be in
mutation-drift equilibrium, due probably to continuous
population reductions and expansions.
Conclusion
We examined patterns of population genetic differentiation
among five vent annelid species in the eastern Pacific and
POPULATION GENETICS OF HYDROTHERMAL VENT ANNELIDS 2613
© 2004 Blackwell Publishing Ltd, Molecular Ecology, 13, 2603– 2615
identified four regions where dispersal filters appear to
restrict gene flow. Comparisons with other population
genetic and phylogenetic studies indicate these filters may
affect also other vent taxa (i.e. crustaceans, molluscs and
other annelids). However, these filters work on different
time scales and to different degrees among various taxa.
For example, the Easter Microplate region has a
significant historical component, as it lies at the boundary
between two zoogeographical divisions of deep-sea fauna
(Vinogradova 1979; Mironov et al. 1998). Currents that
coincide with the Rivera FZ may create present-day filters
for some species with buoyant larvae. The equatorial
region exhibits a combination of deep-oceanic currents and
topographical features that may limit faunal exchange
between the EPR and GAR, and across the Equator along
the EPR. Finally, a strong cross-current at 15°S in the EPR,
that is hypothesized to severely disrupt along-axis dispersal
of C. magnifica clams and B. thermophilus mussels, does not
appear to impede dispersal of the annelids studied here.
The present evidence for dispersal barriers based on
patterns of mitochondrial differentiation is strengthened by
comparative genetic and biogeographical evidence from
other vent taxa. Nevertheless, studies using nuclear markers
should be conducted to assess whether our results reflect
genome-wide patterns of phylogeographical structure.
Acknowledgements
We thank the pilots and crew of DSV Alvin and R/V Atlantis for
their technical support and efforts during our oceanographic
expeditions. Mariana Mateos, Peter Smouse, Jason Wilder and
Curtis R. Young provided helpful suggestions for the manuscript;
Danielle Guinot provided valuable input on bythograeid crabs.
This study was funded primarily by the US National Science
Foundation (OCE8917311, OCE9217602, OCE9212771, OCE9302205,
OCE9529819, OCE9633131, OCE9910799 and OCE0241613), the NJ
Agricultural Experiment Station and the David and Lucile Packard
Foundation via the Monterey Bay Aquarium Research Institute.
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Luis Hurtado studies molecular ecology and evolution of marine
and terrestrial invertebrates. Robert Vrijenhoek, Senior Scientist
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... Unfortunately, there is no DNA data for L. alvini from the type locality of the Galapagos Rift hydrothermal vents (ten Hove & Zibrowius 1986), so we cannot be unequivocally certain that the EPR Laminatubus are in fact L. alvini. However, DNA studies of other annelids and other animals that occur along the EPR and the Galapagos Rift show that the same species are often found in both places (Borda et al. 2013;Hurtado et al. 2004;Johnson et al. 2013;Stiller et al. 2013) and it is a reasonable hypothesis that L. alvini is widespread at eastern Pacific vents. Interestingly, Laminatubus alvini showed little mitochondrial haplotype variation over the sampled geographic range (Fig. 3), with one of the two haplotypes found from 23°N to 38°S. ...
... Interestingly, Laminatubus alvini showed little mitochondrial haplotype variation over the sampled geographic range (Fig. 3), with one of the two haplotypes found from 23°N to 38°S. This low haplotype variability was markedly different to Laminatubus paulbrooksi n. sp., which was sampled over a much smaller geographic range (Fig. 4), but is similar to that reported for the vestimentiferan siboglinid Riftia pachyptila (Hurtado et al. 2004) and suggests larvae that disperse widely. Details on reproduction and dispersal in these species are not known, but the egg size of both L. alvini and L. joycebrooksae n. sp. was measured, and the diameter of 150 μm suggests lecithotrophic development. ...
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The bathyal serpulid Laminatubus alvini ten Hove & Zibrowius, 1986 was described from the periphery of hydrothermal vents of the Galapagos Rift and has been recorded from other vent communities of the East Pacific Rise (EPR). Here we assessed the biodiversity of serpulids collected from eastern Pacific hydrothermal vents and methane seeps using DNA sequences and morphology. Laminatubus alvini showed little genetic variation over a wide geographic range from the Alarcon Rise vents in southern Gulf of California (~23°N), to at least a point at 38°S on the EPR. Specimens from several methane seeps off Costa Rica and the Gulf of California (Mexico) differed markedly from those of Laminatubus alvini on DNA sequence data and in having seven thoracic chaetigers and lacking Spirobranchus-type special collar chaetae, thus fitting the diagnosis of Neovermilia. However, phylogenetic analysis of molecular data showed that L. alvini and the seep specimens form a well-supported clade. Moreover, among the seep specimens there was minimally a ~7% distance in mitochondrial cytochrome b sequences between a shallow-water (1000 m) seep clade restricted to Costa Rica and a deep-water clade (1800 m) from Costa Rica to Gulf of California. We describe the seep taxa here as morphologically indistinguishable L. paulbrooksi n. sp. and L. joycebrooksae n. sp.
... Habitat and geographic range. In the East Pacific, both Alvinella pompejana and Alvinella caudata live sympatrically on the walls of hydrothermal vent chimneys along the EPR and the Pacific-Antarctic Ridge from 21°N to 38°S (Hurtado et al. 2004). A. pompejana is also present on active chimneys of the Guaymas Basin. ...
... However, because of cold and oligotrophic conditions of the deep-sea waters outside areas of venting, larval development may be stopped or slowed down and the vitellus storage of the egg may be sufficient to delay settlement and metamorphosis for a long period of time until environmental conditions are appropriate (Pradillon et al. 2001). This latter hypothesis fits well with population genetics studies that indicated almost no barrier to gene flow between alvinellid populations over large portions of oceanic ridges, provided that the ridge segments are not offset by large transform faults or microplates (Jollivet et al. 1995b, Hurtado et al. 2004, Knowles et al. 2005, Plouviez et al. 2010, Jang et al. 2016). This therefore strengthens hypotheses that alvinellid larvae are entrained by bottom currents and channeled along the axial valley of the rift (Chevaldonné et al. 1997, Jollivet et al. 1999. ...
... All of them are only known from Pacific hydrothermal vent fields, with the two Alvinella species (Alvinella pompejana Desbruyères and Laubier, 1980 and Alvinella caudata Desbruyères and Laubier, 1986) and three Paralvinella species (Paralvinella grasslei Laubier, 1982, Paralvinella bactericola Desbruyères andLaubier, 1991 and Paralvinella pandorae irlandei Desbruyères and Laubier, 1986) reported from the East Pacific Rise (EPR) and Guaymas vent fields, four from the northeast Pacific (Paralvinella palmiformis Desbruyères and Laubier, 1986, Paralvinella pandorae pandorae Laubier, 1986, Paralvinella dela Detinova, 1988 and Paralvinella sulfincola Desbruyères and Laubier, 1993), two from the southwest Pacific vent ecosystems (Paralvinella fijiensis Desbruyères and Laubier, 1993 and Paralvinella unidentata Desbruyères and Laubier, 1993), and one from the Marianas back-arc spreading center and the Okinawa Trough (Paralvinella hessleri Desbruyères and Laubier, 1989). These worms usually form dense aggregations on varied hard substrata, including chimney walls, basaltic cracks with venting fluids and siboglinid tubes (Tunnicliffe et al., 1993;Desbruyères et al., 1994;Hurtado et al., 2004). Although hydrothermal vent organisms usually show a high degree of regional endemism (Rogers et al., 2012), a family endemic to the Pacific vents is still rare. ...
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Alvinellids have long been considered to be endemic to Pacific vents until recent discovery of their presence in the Indian Ocean. Here, a new alvinellid is characterized and formally named from recently discovered vents, Wocan, and Daxi, in the northern Indian Ocean. Both morphological and molecular evidences support its placement in the genus Paralvinella , representing the first characterized alvinellid species out of the Pacific. The new species, formally described as Paralvinella mira n. sp. herein, is morphologically most similar to Paralvinella hessleri from the northwest Pacific, but the two species differ in three aspects: (1), the first three chaetigers are not fused in P. mira n. sp., whereas fused in P. hessleri ; (2), paired buccal tentacles short and pointed in P. mira but large and strongly pointed in P. hessleri ; (3), numerous slender oral tentacles ungrouped in P. mira but two groups in P. hessleri . Phylogenetic inference using the concatenated alignments of the cytochrome c oxidase I (COI), 16S rRNA and 18S rRNA genes strongly supports the clustering of P. mira with two West Pacific congeners, P. hessleri and an undescribed species ( Paralvinella sp. ZMBN). The resulting Indian/West Pacific lineage suggests a possible invasion into the Indian Ocean from the West Pacific. This is the third polychaete reported from Wocan hydrothermal field. Among the three species, two including P. mira and Hesiolyra heteropoda (Annelida:Hesionidae) are present in high abundance, forming an alvinellids/hesionids-dominated polychaete assemblage distinct from that at all other Central Indian Ridge and Southwest Indian Ridge vents. Thus, this study expands our understanding of alvinellid biogeography beyond the Pacific, and adds to the unique biodiversity of the northern Indian Ocean vents, with implications for biogeographic subdivision across the Indian Ocean ridges.
... Thus, different availability of sulphides in the environment could lead to different morphological adaptations to maintain a homogeneous and stable environment for the symbionts. Interestingly, notwithstanding the potential ecological differences and the large geographic distances between types of vents, high genetic connectivity has been found across all known populations of Riftia pachyptila (Black et al., 1994;Hurtado et al., 2004). ...
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The tubeworm Riftia pachyptila is a key primarily producer in hydrothermal vent communities due to the symbiosis with sulphur-oxidizing bacteria, which provide nourishment to the worm from sulphides, oxygen and carbon dioxide. These substances diffuse from the vent water into the bloodstream of the worm through their tentacular crowns, and then to the bacteria, hosted in a specialized organ of the worm, called a trophosome. The uptake rates of these substances depend on the surface/volume relationship of the tentacles. We here describe two morphotypes, ‘fat’ and ‘slim’, respectively, from the basalt sulphide-rich vents at 9 °N and 21 °N at the East Pacific Rise, and the highly sedimented, sulphide-poor vents at 27 °N in the Guaymas Basin. The ‘fat’ morphotype has a thicker body and tube, longer trunk and smaller tentacular crowns, whereas the ‘slim’ morphotype has shorter trunk, thinner body and tube, and presents longer tentacular crowns and has a higher number of tentacular lamellae. Given the dependence on sulphides for the growth of R. pachyptila, as well as high genetic connectivity of the worm’s populations along the studied localities, we suggest that such morphological differences are adaptive and selected to keep the sulphide uptake near to the optimum values for the symbionts. ‘Fat’ and ‘slim’ morphotypes are also found in the vestimentiferan Ridgeia piscesae in similar sulphide-rich and poor environments in the northern Pacific.
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The widely distributed polychaete family Polynoidae Kinberg, 1856 is found across all oceans and from shallow to deep waters, including deep-sea hydrothermal vents and hydrocarbon seeps. Taxa inhabiting chemosynthesis-based ecosystems are often endemic to those specific habitats commonly targeted by deep-sea mining, and understanding their species diversity is essential for shaping conservation plans. Here, we report two previously undescribed scale-worms in the genus Branchinotogluma Pettibone, 1985 from the Off Hatsushima hydrocarbon seep of Sagami Bay and the Nikko Seamount hydrothermal vent on the Izu-Ogasawara Arc, and describe them as B. nikkoensis sp. nov. and B. sagamiensis sp. nov. Branchinotogluma nikkoensis sp. nov. is distinguished from the known species by the following characters: i) ventral segmental lamellae near ventral bases of neuropodia present on segments 13–17, ii) dorsal tentacular cirri being longer than ventral tentacular cirri, iii) absence of dorsal tubercles. Branchinotogluma sagamiensis sp. nov. can be differentiated from other congeners by i) 20 segments, ii) dorsal tentacular cirri being longer than ventral tentacular cirri, iii) ventral segmental lamellae near ventral bases of neuropodia present on segments 13–18, and iv) thin median antennae. The two new species are distinct in both morphology and four gene sequences from the only two species previously known from Japan including Branchinotogluma japonicus (Miura & Hashimoto, 1991) and B. elytropapillata Zhang, Chen & Qiu, 2018, originally described from Kaikata Seamount vent on the Izu-Ogasawara Arc and Okinawa Trough, respectively.
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Hydrothermal vents form archipelagos of ephemeral deep-sea habitats that raise interesting questions about the evolution and dynamics of the associated endemic fauna, constantly subject to extinction-recolonization processes. These metal-rich environments are coveted for the mineral resources they harbor, thus raising recent conservation concerns. The evolutionary fate and demographic resilience of hydrothermal species strongly depend on the degree of connectivity among and within their fragmented metapopulations. In the deep sea, however, assessing connectivity is difficult and usually requires indirect genetic approaches. Improved detection of fine-scale genetic connectivity is now possible based on genome-wide screening for genetic differentiation. Here, we explored population connectivity in the hydrothermal vent snail Ifremeria nautilei across its species range encompassing five distinct back-arc basins in the Southwest Pacific. The global analysis, based on 10 570 single nucleotide polymorphism (SNP) markers derived from double digest restriction-site associated DNA sequencing (ddRAD-seq), depicted two semi-isolated and homogeneous genetic clusters. Demo-genetic modeling suggests that these two groups began to diverge about 70 000 generations ago, but continue to exhibit weak and slightly asymmetrical gene flow. Furthermore, a careful analysis of outlier loci showed subtle limitations to connectivity between neighboring basins within both groups. This finding indicates that migration is not strong enough to totally counterbalance drift or local selection, hence questioning the potential for demographic resilience at this latter geographical scale. These results illustrate the potential of large genomic datasets to understand fine-scale connectivity patterns in hydrothermal vents and the deep sea.
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Polynoidae Kinberg, 1856 has five branchiate genera: Branchipolynoe Pettibone, 1984, Branchinotogluma Pettibone, 1985, Branchiplicatus Pettibone, 1985, Peinaleopolynoe Desbruyères & Laubier, 1988, and Thermopolynoe Miura, 1994, all native to deep-sea, chemosynthetic-based habitats. Of these, Peinaleopolynoe has two accepted species; Peinaleopolynoe sillardi Desbruyères & Laubier, 1988 (Atlantic Ocean) and Peinaleopolynoe santacatalina Pettibone, 1993 (East Pacific Ocean). The goal of this study was to assess the phylogenetic position of Peinaleopolynoe , utilizing DNA sequences from a broad sampling of deep-sea polynoids. Representatives from all five branchiate genera were included, several species of which were sampled from near the type localities; Branchinotogluma sandersi Pettibone, 1985 from the Galápagos Rift (E/V “Nautilus”); Peinaleopolynoe sillardi from organic remains in the Atlantic Ocean; Peinaleopolynoe santacatalina from a whalefall off southern California (R/V “Western Flyer”) and Thermopolynoe branchiata Miura, 1994 from Lau Back-Arc Basin in the western Pacific (R/V “Melville”). Phylogenetic analyses were conducted using mitochondrial (COI, 16S rRNA, and CytB) and nuclear (18S rRNA, 28S rRNA, and H3) genes. The analyses revealed four new Peinaleopolynoe species from the Pacific Ocean that are formally described here: Peinaleopolynoe orphanae Hatch & Rouse, sp. nov. , type locality Pescadero Basin in the Gulf of California, Mexico (R/V “Western Flyer”); Peinaleopolynoe elvisi Hatch & Rouse, sp. nov. and Peinaleopolynoe goffrediae Hatch & Rouse, sp. nov. , both with a type locality in Monterey Canyon off California (R/V “Western Flyer”) and Peinaleopolynoe mineoi Hatch & Rouse, sp. nov. from Costa Rica methane seeps (R/V “Falkor”). In addition to DNA sequence data, the monophyly of Peinaleopolynoe is supported by the presence of ventral papillae on segments 12–15. The results also demonstrated the paraphyly of Branchinotogluma and Lepidonotopodium Pettibone, 1983 and taxonomic revision of these genera is required. We apply the subfamily name Lepidonotopodinae Pettibone 1983, for the clade comprised of Branchipolynoe , Branchinotogluma , Bathykurila , Branchiplicatus , Lepidonotopodium , Levensteiniella Pettibone, 1985, Thermopolynoe , and Peinaleopolynoe .
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The hydrothermal vent fauna has a high ratio of taxa specific for vent biotopes, i.e. obligate vent taxa (> 90% at the species level). This observation, together with the dramatic difference between the vent and regular non-vent deep-sea communities, has resulted in vent fauna being treated as a separate evolutionary and biogeographic unit (e.g. DOVE Workshop Report).
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One of the most intriguing ecological questions remaining unanswered about hydrothermal vents is how vent organisms disperse and persist. Because vent species are generally endemic and their habitat is patchy and ephemeral on time scales as short as decades, they must disperse frequently, presumably in a planktonic larval stage. We suggest that dispersal occurs not only in near-bottom currents but also several hundred meters above the seafloor at the level of the laterally spreading hydrothermal plumes. Using a standard buoyant plume model and observed larval abundances near hydrothermal vents at 9°50'N along the East Pacific Rise, we estimate a mean vertical flux of approximately 100 vent larvae/h at a single black smoker. Larval abundances were extremely variable near vents, resulting in a range in estimated fluxes of at least an order of magnitude. The suitability of the plume model for these calculations was determined by releasing dyes (fluorescein and rhodamine) as larval mimics into a black smoker plume. The plume model predicted dye fluxes in the plume adequately, given the short averaging times of our measurements and the difficulty of sampling the plume centerline. Our calculations of substantial numbers of vent larvae entrained into the plume support the idea that transport in the lateral plume is an important mechanism of dispersal. Because vertical shear in flows above vents can cause larval dispersal trajectories in the plume to deviate considerably from those along the seafloor, larvae in the plume may have access to habitats that are unreachable by larvae in near-bottom flows.
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Estimating genealogical relationships among genes at the population level presents a number of difficulties to traditional methods of phylogeny reconstruction. These traditional methods such as parsimony, neighbour-joining, and maximum-likelihood make assumptions that are invalid at the population level. In this note, we announce the availability of a new software package, TCS, to estimate genealogical relationships among sequences using the method of Templeton et al. (1992) .
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Strictly considered, omitting the adjacent part of the Atlantic Ocean and the Black Sea, the Mediterranean fish fauna comprises about 550 species. Although long known, these fishes need further researches, especially in respect to their geographical distribution and differentiation. They are dispersed according to several distributional patterns. The largest group is Atlantic (Boreal, West African, or Amphi-Atlantic). Other species are endemic or cosmopolitan. Some, especially those that have been found in scattered regions of the world, pose unsolved problems, both systematic and biogeographical. Deep-sea fishes are scarce; four species only have been found below 2,000 m. The Mediterranean is usually defined as a warm-temperate sea, but it comprises several basins, in which the conditions differ more or less widely, and between which some of the faunistic features differ remarkably. These differences are evident in both west-east and north-south directions. Tropical fishes occur mainly in the southern region and in the eastern basin. In this basin there are now about 30 Indo-Pacific species, which have immigrated from the Red Sea through the Suez Canal. A number of Atlantic species, even Boreal ones, occur either regularly or occasionally in the western basin. Several Mediterranean fishes are rare or absent in the Adriatic. Some species that occur in both the Mediterranean Sea and the Atlantic Ocean exhibit geographical differentiation between the two areas. Furthermore, within the Mediterranean, related races or vicarious species occur in the various basins of the Mediterranean, which represents a center of speciation. It is quite probable that such littoral types as blennioids or gobioids will exhibit further differentiation, ecological or geographical, when they have been subjected to more critical analysis.
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In April, 1991, we witnessed from the submersible Alvin a suite of previously undocumented seafloor phenomena accompanying an in-progress eruption of the mid-ocean ridge on the East Pacific Rise crest at 9°45'N-52'N. The volume of the eruption could not be precisely determined, although comparison of pre- and post-eruption SeaBeam bathymetry indicate that any changes in ridge crest morphology resulting from the eruption were < 10 m high. Effects of the eruption included: (1) increased abundance and redistribution of hydrothermal vents, disappearance of numerous vent communities, and changes in characteristics of vent fauna and mineral deposits within the eruption area since December, 1989; (2) murkiness of bottom waters up to tens of meters above the seafloor due to high densities of suspended mineral and biogenic particulates; (3) destruction of a vent community by lava flows, mass wasting, and possible hydrovolcanic explosion at a site known as `Tubeworm Barbecue' in the axial summit caldera (ASC) at 9°50.6'N (4) near-critical temperatures of hydrothermal vent fluids, ranging up to 403°C (5) temporal variations over a 2 week interval in both temperatures and chemical/isotopic compositions of hydrothermal fluids; (6) unusual compositions of end-member vent fluids, with pH values ranging to a record low of 2.5, salinities ranging as low as 0.3 wt% NaCl (one-twelfth that of seawater), and dissolved gases reaching high concentrations (> 65 mmol/l for both CO2 and H2S); (7) venting at temperatures above 380°C of visually detectable white vapor that transformed to plumes of gray smoke a few centimeters above vent orifices; (8) disorganized venting of both high-temperature fluids (black and gray smoke) and large volumes of cooler, diffuse hydrothermal fluids directly from the basaltic seafloor, rather than from hydrothermal mineral constructions; (9) rapid and extensive growth of flocculent white bacterial mats (species unknown) on and under the seafloor in areas experiencing widespread venting of diffuse hydrothermal fluid; and (10) subseafloor downslope migration of magma normal to the ridge axis in a network of small-scale (1-5 m diameter) lava tubes and channels to distances at least 100-200 m outside the ASC. We suggest that, in April, 1991, intrusion of dikes in the eruption area to < 200 m beneath the ASC floor resulted in phase separation of fluids near the tops of the dikes and a large flux of vapor-rich hydrothermal fluids through the overlying rubbly, cavernous lavas. Low salinities and gas-rich compositions of hydrothermal fluids sampled in the eruption area are appropriate for a vapor phase in a seawater system undergoing subcritical liquid-vapor phase separation (boiling) and phase segregation. Hydrothermal fluids streamed directly from fissures and pits that may have been loci of lava drainback and/or hydrovolcanic explosions. These fissures and pits were lined with white mats of a unique fast-growing bacteria that was the only life associated with the brand-new vents. The prolific bacteria, which covered thousands of square meters on the ridge crest and were also abundant in subseafloor voids, may thrive on high levels of gases in the vapor-rich hydrothermal fluids initially escaping the hydrothermal system. White bacterial particulates swept from the seafloor by hydrothermal vents swirled in an unprecedented biogenic `blizzard' up to 50 m above the bottom. The bacterial proliferation of April, 1991 is likely to be a transient bloom that will be checked quickly either by decline of dissolved gas concentrations in the fluids as rapid heat loss brings about cessation of boiling, and/or by grazing as other organisms are re-established in the biologically devastated area.
Article
The horizontal mean circulation and diapycnal flux divergence field in the South Pacific between Tahiti and the East Pacific Rise are obtained from a nonconservative β-spiral inverse method applied to high quality hydrographic data. The diapycnal flux divergence term is found to be an essential part of the deep vorticity balance and proper resolution of this term is critical to the success of the β-spiral calculation. The subthermocline circulation in this region of the South Pacific consists of three vertical regimes. Between the thermocline and approximately 1800-2000 m a cyclonic circulation pattern exists. A zone of minimum motion is found between 1800 and 2000 m. Below this zone, northward flow along the rise and westward flow in the north indicate an anticyclonic gyre, centered on 15°S, that extends approximately 1000-2000 km to the west of the East Pacific Rise. -from Authors