Molecular Ecology (2009) 18, 2287–2296
doi: 10.1111/j.1365-294X.2009.04201.x
Glacial oceanographic contrasts explain phylogeography
of Australian bull kelp
Blackwell Publishing Ltd
C E R I D W E N I . F R A S E R , H A M I S H G . S P E N C E R and J O N AT H A N M . WAT E R S
Allan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, 340 Great King St, Dunedin
9016, New Zealand
Abstract
The evolutionary effects of Southern Hemisphere Pleistocene oceanographic conditions —
marked by fluctuations in sea levels and water temperatures, and redirected currents — are
poorly understood. The southeastern tip of Australia presents an intriguing model system
for studying the biological impacts of palaeoceanography. In particular, contrasting
oceanographic conditions that existed on eastern vs. western sides of the Bassian Isthmus
during Pleistocene glacial periods allow for natural comparisons between putative refugial
vs. re-invading populations. Whereas many western Tasmanian marine taxa were likely
eliminated by cold subantarctic water during the last glacial period, eastern Tasmanian
populations would have persisted in relatively warm temperatures mediated by the ongoing
influence of the East Australian Current (EAC). Here we test for the effects of contrasting
palaeoceanographic conditions on endemic bull kelp, Durvillaea potatorum, using DNA
sequence analysis (COI; rbcL) of more than 100 individuals from 14 localities in southeastern
Australia. Phylogenetic reconstructions reveal a deep (maximum divergence 4.7%) genetic
split within D. potatorum, corresponding to the ‘eastern’ and ‘western’ geographical
regions delimited by the Bassian Isthmus, a vicariant barrier during low Pleistocene sea
levels. Concordant with the western region’s cold glacial conditions, samples from western
Tasmania and western Victoria are genetically monomorphic, suggesting postglacial
expansion from a mainland refugium. Eastern samples, in contrast, comprise distinct
regional haplogroups, suggesting the species persisted in eastern Tasmania throughout
recent glacial periods. The deep east–west divergence seems consistent with earlier reports
of morphological differences between ‘western’ and ‘eastern’ D. potatorum, and it seems
likely that these forms represent reproductively isolated species.
Keywords: cytochrome c oxidase I, Durvillaea potatorum, palaeoceanography, phylogeography,
RuBisCo
Received 9 February 2009; revision received 18 March 2009; accepted 21 March 2009
Introduction
The evolutionary and biogeographical significance of
glacial periods is well recognized, particularly for terrestrial
systems affected by ice sheets (reviewed by Hewitt 1996,
2000; Provan & Bennett 2008). In the marine realm,
fluctuation of sea levels, water temperatures and sea ice
driven by glacial cycles are also likely to have had a strong
Correspondence: Ceridwen I. Fraser, Allan Wilson Centre for
Molecular Ecology and Evolution, Department of Zoology,
University of Otago, 340 Great King St, Dunedin 9016, New
Zealand. Fax: +64-(0)3-4797584; E-mail: [email protected]
© 2009 Blackwell Publishing Ltd
influence on species distributions and genetic connectivity
(Maggs et al. 2008). For instance, lowered sea levels during
glacial maxima can lead to the emergence of land bridges
which, while facilitating dispersal of terrestrial biota (e.g.
Tiffney 1985; reviews by Wen 1999; Sanmartin et al. 2001),
effectively divide marine populations. Scientists have
speculated on such biotic effects for centuries; Darwin
(1872), wrote ‘a narrow isthmus now separates two marine
faunas; submerge it, or let it formerly have been submerged,
and the two faunas will now blend ... or may formerly have
blended.’ The Sunda and Sahul shelves, for example,
separated many Pacific and Indian Ocean marine taxa
at Pleistocene sea level lowstands, leading to vicariant
2288 C . I . F R A S E R , H . G . S P E N C E R and J . M . WAT E R S
Fig. 1 Approximate coastlines in southeastern Australia at three points in recent geological history: the present (with the highest sea levels
in more than 100 000 years); 14 000 years ago (when Tasmania was last joined to the mainland); and 25 000 years ago (the lowstand of sea
levels during the last glacial maximum, LGM) (shoreline reconstructions modified from Lambeck & Chappell 2001). Major contemporary
surface currents — the East Australian (EAC) and Zeehan (ZC) (Baines et al. 1983; Cresswell 2000) — are shown by red arrows; altered
oceanographic conditions during the LGM, with the subtropical convergence (STC) further north and the Zeehan current blocked, are
indicated in the right panel (after Nürnberg et al. 2004). Approximate northern limits of the subtropical convergence at both modern and
LGM time slices are indicated (after Nürnberg et al. 2004). The position of the enlarged region is shown on the map of Australia (inset: lower
left). Distributional range of D. potatorum is indicated by blue arrows at the most western (Robe, South Australia) and eastern (Tathra, New
South Wales) sites where this species can be found (Huisman 2000).
divergence (e.g. Chenoweth et al. 1998; Nelson et al. 2000;
Reid et al. 2006), while similar marine biogeographical
disjunctions have been noted on either side of the Baja
California Peninsula (e.g. Bernardi et al. 2003). In Australia,
the Bassian Isthmus — a land bridge that periodically
connects Tasmania to the mainland as sea levels drop
during glaciations (Lambeck & Chappell 2001) (Fig. 1) — has
frequently been suggested as a potential vicariant barrier
to gene flow among temperate marine taxa (Dartnall 1974).
Indeed, recent phylogeographical analyses of several
marine species (e.g. cirrhitoid fish: Burridge 2000; Patiriella
sea stars: Waters et al. 2004; Catostylus jellyfish: Dawson
2005; Nerita gastropods: Waters et al. 2005; Spencer et al.
2007; Waters 2008; Catomerus barnacles: York et al. 2008) in
southeastern Australia have revealed distinct geographical
partitioning into eastern vs. western clades, generally
consistent with the vicariant hypothesis of allopatric
divergence during glacial periods.
A less-explored aspect of climate change is the effect of
altered oceanography (specifically currents) on the phylogeography of modern marine taxa. Pleistocene glacial
periods were characterized by both substantially reduced
water temperatures and redirected currents (Wells &
Okada 1996; Herbert et al. 2001), but although some
authors have suggested that ancient changes in major
Northern Hemisphere current systems may partially
explain modern phylogeographical structuring (e.g. Muss
et al. 2001; Wares 2001; Marko 2004), few studies, particularly
in the Southern Hemisphere, have directly assessed the
impacts of such palaeoceanographic features. Around
southeastern Australia, the subtropical convergence (STC),
a boundary zone between temperate and subantarctic
waters, is believed to have abutted southern Tasmania and
extended along its western coast during recent glacial
maxima, blocking the eastward flow of the warm Leeuwin/
Zeehan current (Wells & Okada 1996; McGowran et al.
1997; Nürnberg et al. 2004) (Fig. 1). The absence of the
Zeehan Current from southern Tasmania at glacial maxima
would have strengthened east–west isolation by limiting
dispersal, and the colder waters on the eastern coast may
have driven temperate marine organisms to considerably
higher latitudes; in contrast, the warm East Australian
Current (EAC) is known to have extended its southward
flow along eastern Tasmania during glacial periods (Nürnberg
et al. 2004), potentially maintaining temperate marine
conditions on the eastern, but not western, coasts of Tasmania.
© 2009 Blackwell Publishing Ltd
P O S T G L A C I A L R E C O L O N I Z AT I O N I N A U S T R A L I A N B U L L K E L P 2289
Table 1 Morphological and ecological differences between ‘eastern’ and ‘western’ forms of Durvillaea potatorum in southeastern Australia,
after Cheshire et al. (1995)
Characteristic
Western
Eastern
Primary stipe length
Primary stipe distally branched
Secondary stipes on primary stipe
Habitat
generally < 0.5 m
never
never
always subtidal, < 10 m
generally < 0.5 m or < 1.0 m
infrequently
infrequently
infrequently intertidal, or subtidal < 10 m
Here we present the first direct assessment of the expected
phylogeographical effects of these contrasting glacial
oceanographic conditions.
Australian bull kelp, Durvillaea potatorum (Labillardière),
forms a dense band in the upper subtidal and intertidal of
exposed rocky reefs from Robe in South Australia (Huisman
2000) to Tathra on the east coast of New South Wales (Millar
2007) (Fig. 1), and along the western and eastern shores
of Tasmania. It grows abundantly on King Island, on the
western sill of Bass Strait, but is rare on the Furneaux Island
Group of the eastern sill (Hay 1994). Durvillaea potatorum is
considered endemic to Australia (Cheshire et al. 1995);
additional historical records reporting D. potatorum from
the subantarctic Auckland Islands (cited in Papenfuss
1964) and from Constitución in Chile (cited in Ramirez &
Santelices 1991) are extremely dubious and require confirmation. In western Bass Strait, detached, beach-cast D. potatorum
wrack is so abundant that a flourishing kelp-wrack
harvesting industry for alginates operates on King Island
(Kirkman & Kendrick 1997). Durvillaea potatorum is an
unusually large macro-alga, with individuals commonly
reaching several metres in length (Cheshire & Hallam
1988) and weighing over 40 kg (Hay 1994); an early botanist
described it as ‘a plant which, when fully grown, is measured,
not by inches, but by fathoms’ (Harvey 1863). Cheshire &
Hallam (1989) noted morphological differences in individuals from eastern vs. western populations: those from the
east (eastern coasts of Tasmania and New South Wales)
were found to have some — albeit variable — characteristics
(such as stipe length, habitat and position of secondary
stipes) that differed from western specimens (southern and
western coasts of Victoria, and King Island in Bass Strait)
(Table 1). Like other members of its genus, D. potatorum is
dioecious, with both female and male individuals, producing
eggs and sperm, respectively. Although these gametes are
released into the water column, and could theoretically
disperse with currents, unfertilized eggs are unlikely to
survive in a viable condition for more than a few days at
sea (M. Clayton, Monash University, Melbourne, personal
communication) and fertilized eggs are rapidly — within
minutes — surrounded by adhesive secretions that effectively
attach zygotes to the substrate (Clayton & Ashburner
1994). Dispersal via gametes or zygotes seems therefore
© 2009 Blackwell Publishing Ltd
unlikely to be successful over long distances, particularly
where populations are patchy or separated by stretches of
sandy coast or open ocean (Hidas et al. 2007). As D. potatorum
is a solid-bladed, nonbuoyant member of its genus (Hay
1994), adults are also unlikely to disperse far once detached.
A kelp with such limited potential for dispersal would
be expected to show strong phylogeographical differentiation and this feature, combined with the distribution of
D. potatorum in Australia around Bass Strait, make it well
suited for studies of the effects of Pleistocence vicariance
and oceanography. Here we examine phylogeographical
structure in Australian bull kelp to test the hypotheses that:
(i) Pleistocene emergence of the Bassian Isthmus separated
this species into distinct eastern and western lineages, and
(ii) altered oceanography of Tasmania during recent glacial
periods, with subantarctic water impacting the western
(but not eastern) coasts, will be reflected in contrasting
phylogeographical patterns consistent with elimination of
the western and persistence of the eastern populations.
Materials and methods
Site selection and sample collection
Tissue samples were collected by hand, at low tide, from
the distal ends of fronds of attached Durvillaea potatorum
growing in the intertidal or shallow subtidal at 14 sites
across the species’ range (Table 2). In some cases, where
attached individuals were not obtainable due to extreme
conditions, samples were taken from fresh beach-cast
wrack (listed in Table 2). At one site — King George III Reef
— all samples were taken from attached plants in the
subtidal, using SCUBA, at between 10 and 12 m depths.
Sites were categorized on the basis of geography as either
eastern or western, and either mainland or Tasmania
(Table 2).
DNA extraction, sequencing and phylogenetic analyses
Tissue preservation, DNA extractions and polymerase
chain reactions were carried out as described in Fraser et al.
(2009a), with a 629-bp portion of the mitochondrial gene
cytochrome c oxidase I (COI) amplified using primers
2290 C . I . F R A S E R , H . G . S P E N C E R and J . M . WAT E R S
Table 2 Sample sites and localities, showing sample type (attached kelp: ‘a’; fresh beach-cast wrack: ‘w’), number of samples sequenced
and haplotypes found. For precise location of sites, refer to Fig. 2
No. of samples
sequenced
Haplotype/s
Site name
Site locality
Sample
COI
rbcL
COI
rbcL
Port Fairy
Warrnambool
Peterborough
Phillip Island
Green Point
Couta Rocks
KGIII Reef
Bruny Island
Pirates Bay
Bicheno
Binalong Bay
The Gardens
Gabo Island
Tathra
TOTAL sequenced
Western-mainland
Western-mainland
Western-mainland
Western-mainland
Western-Tasmania
Western-Tasmania
Eastern-Tasmania
Eastern-Tasmania
Eastern-Tasmania
Eastern-Tasmania
Eastern-Tasmania
Eastern-Tasmania
Eastern-Mainland
Eastern-Mainland
a
a
a
a
w
w
a
w, a
a
w
a
a
a
a
5
7
6
9
9
10
7
10
10
5
8
7
6
8
107
5
5
4
10
6
6
3
9
7
4
0
8
5
5
77
C-I
C-I
C-I
C-I
C-I
C-I
C-IV, C-V
C-I, C-IV
C-II, C-III
C-II, C-III
C-II, C-III
C-II, C-III
C-VI, C-VII, C-VIII
C-VI, C-VIII
R-I
R-I
R-I
R-I
R-I
R-I
R-III
R-I, R-III
R-II, R-III
R-I, R-II, R-III
GazF1 and GazRI (Saunders 2005), and a 886-bp region of
the chloroplast gene RuBisCO (rbcL) amplified using
primers KL2 and KL8 (Lane et al. 2006). Phylogenies for
each data set were built by maximum likelihood (ML) and
Bayesian analyses, and included outgroup sequences from
Durvillaea willana (South Island, New Zealand; GenBank
accessions: COI: EU918569; rbcL: EU918578) and Durvillaea
antarctica (Falkland Islands; GenBank accessions: COI:
FJ550107; rbcL: FJ550124). ML analyses were performed
with a HKY + G model for both COI (base frequencies
A = 0.2182, C = 0.1726, G = 0.1895, T = 0.4197; Tratio =
3.7086; gamma shape parameter = 0.0144) and rbcL (base
frequencies A = 0.2922, C = 0.1667, G = 0.2168, T = 0.3243;
Tratio = 2.9827; gamma shape parameter = 0.0081), that
was selected using the hLRT of ModelTest 3.06 (Posada &
Crandall 1998). The robustness of the ML topology was
estimated by bootstrapping (Felsenstein 1985), with heuristic
analysis of 1000 replicate data sets (Figs 2 and 3). Bayesian
posterior probability (PP) values, also indicated on the ML
phylogenies (Figs 2 and 3), were calculated using MrBayes
3.1.2 (Ronquist & Huelsenbeck 2003). Markov chain Monte
Carlo (MCMC) searches, each with four chains of 5 000 000
generations and trees sampled each 100 generations, were
carried out. The first 10 000 trees sampled were discarded
as ‘burn-in’, based on the stationarity of ln L as assessed
using Tracer version 1.4 (Rambaut & Drummond 2007); a
consensus topology and posterior probability values were
calculated with the remaining trees. An unrooted statistical
parsimony network was reconstructed using tcs 1.21
(Clement et al. 2000) in order to examine relationships
among ‘eastern’ haplotypes for COI — these analyses were
R-II, R-III
R-IV
R-IV
not performed on rbcL data due to limited diversity (only
two haplotypes in each major clade). Analysis of the
precise expansion time of the ‘western’ clade was not
possible, as robust mutation rate estimates have not yet
been developed for the Phaeophyceae (Hoarau et al. 2007).
All unique DNA sequences obtained during this study were
deposited with GenBank (Accession nos FJ872919–FJ873102).
Results
DNA sequencing of 107 Durvillaea potatorum specimens
yielded eight distinct haplotypes for COI, whereas 77 rbcL
sequences yielded a total of four haplotypes. Thirty
variable sites were found over the 629-bp fragment
amplified for COI (4.8% of sites), with approximately
one-third of the inferred changes being transversions. For
rbcL, seven variable sites were found across the 886-bp
fragment (0.8%), with all but two sites showing transitional
mutations. In both markers, variable sites occurred at the
third codon position, with the exception of one inferred
transitional mutation in COI.
ML and Bayesian phylogenetic analyses yielded trees with
consistent topologies for each genetic data set. Specifically,
both COI (Fig. 2), and rbcL (Fig. 3) analyses revealed a deep
and strongly supported genetic split within D. potatorum
(uncorrected distances up to 4.7% for COI and up to 0.9%
for rbcL; Bayesian PP values of 1.00), largely corresponding
to ‘eastern’ and ‘western’ geographical regions (Figs 2 and
3). Although both ‘eastern’ and ‘western’ haplotypes were
found along the east coast of Tasmania, the presence of all
‘eastern’ haplotypes at only eastern geographical locations,
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P O S T G L A C I A L R E C O L O N I Z AT I O N I N A U S T R A L I A N B U L L K E L P 2291
Fig. 2 Phylogeographical structure of Durvillaea potatorum in southeastern Australia, based on mitochondrial (COI) DNA sequence data.
The phylogenetic tree (inset: lower left) was generated using ML analyses, and shows Bayesian PP values (above the line) and ML bootstraps
in parentheses below. Pie charts on the map indicate the relative proportions of haplotypes at each site, with the total number of samples
per site given in parentheses after the site name. Pie charts alongside the phylogenetic tree indicate the proportions of each haplotype in
each major clade (‘east’ or ‘west’).
and the broad geographical range of ‘western’ haplotypes
across western coasts, indicates a general east–west split
despite some geographical overlap. The more informative
COI data set also revealed considerable diversity and
phylogeographical structuring within the ‘eastern’ clade,
which comprised a total of six haplotypes (uncorrected
distances 0.2–0.8%). Three were restricted to the east coast
of Tasmania (haplotypes C-III–C-V), and three were found
only at eastern mainland sites (haplotypes C-VI–C-VIII)
(Fig. 2). Although rbcL data showed relatively little
overall diversity, the genetic division between eastern
mainland and eastern Tasmania was still apparent, with a
single ‘eastern’ haplotype (R-III) across Tasmanian sites,
and another (R-IV) shared by Tathra and Gabo Island
samples (Fig. 3). Strong phylogenetic concordance was
found between mitochondrial and chloroplast markers,
with all specimens allocated to the equivalent clade
(‘eastern’ or ‘western’) for each marker.
The ‘western’ clade in both COI and rbcL data sets each
yielded just two haplotypes, one of which was particularly
geographically widespread, extending from Port Fairy on
Australia’s mainland to Bruny Island in southern Tasmania
© 2009 Blackwell Publishing Ltd
(C-I, Fig. 2 and R-I, Fig. 3). For rbcL, the widespread haplotype R-I (which differs from R-II by merely one transversion) also occurred at Bicheno in a single sample,
although the same individual yielded the less common
‘western’ haplotype for COI (C-II). Notably, D. potatorum
populations along the western coasts of both the mainland
and Tasmania were completely homogeneous for both
markers, showing no evidence of genetic division across
Bass Strait. The ‘western’ clade also extended into the
eastern coast of Tasmania, with haplotypes C-II and R-II
found from Pirates Bay northward to The Gardens (Figs 2
and 3).
Analysis of the relationships of COI haplotypes resulted
in two networks — corresponding to the ‘eastern’ and the
‘western’ clades — that could not be parsimoniously connected at the 95% confidence limit. The ‘western’ network
contained only two COI haplotypes, separated by one
mutational step, and was therefore largely uninformative.
The ‘eastern’ network (Fig. 4) showed two potentially
ancestral, central haplotypes, one from the mainland (CVI) haplogroup and one from Tasmania (C-IV). The four
remaining haplotypes radiated from an ancestral
2292 C . I . F R A S E R , H . G . S P E N C E R and J . M . WAT E R S
Fig. 3 Phylogeographical structure of Durvillaea potatorum in southeastern Australia, based on chloroplast (rbcL) DNA sequence data. The
phylogenetic tree (inset: lower left) was generated using ML analyses, and shows Bayesian PP values (above the line) and ML bootstraps
in parentheses below. Pie charts on the map indicate the relative proportions of haplotypes at each site, with the total number of samples
per site given in parentheses after the site name. Pie charts alongside the phylogenetic tree indicate the proportions of each haplotype in
each major clade (‘east’ or ‘west’).
haplotype via a single mutational step. The ‘ancestral’ haplotypes — and the mainland vs. Tasmania groups — were
themselves separated by two mutational steps, linked by a
hypothetical undetected haplotype.
Discussion
Ancient vicariant influences
The substantial phylogenetic split between ‘eastern’ and
‘western’ clades of Durvillaea potatorum (Figs 2 and 3)
supports the hypothesis that past emergence of the Bassian
Isthmus has promoted vicariant divergence in this poorly
dispersive shallow-water marine macro-alga (hypothesis
i). Although contemporary longitudinal variation in water
temperature, salinity and wave action might also be
suggested as contributing causes, the presence of both
clades across a wide geographical area and latitudinal
range, as well as their co-occurrence along the east coast of
Tasmania, would appear to refute a causal role for such
abiotic factors in generating the deep phylogeographical
structuring observed for D. potatorum. This study therefore
emphasizes the important role of vicariance in driving
diversification of Australia’s marine temperate biota (e.g.
Dartnall 1974; Burridge 2000; Waters et al. 2005; York et al.
2008). Indeed, Waters (2008) proposed that the Bassian
Isthmus had likely driven cladogenesis — with cryptic
eastern and western lineages — in many components of
southern Australia’s littoral and shallow sublittoral
communities.
The suggestion that southern Australia’s major marine
biogeographical break occurs specifically in the vicinity of
Wilsons Promontory in southern Victoria (e.g. Dawson
2005; Waters 2008) is not rejected by our findings, with the
Phillip Island site immediately to the west of this feature
fixed for the common ‘western’ haplotype. Clearly, however, finer-scale research is required to confirm the precise
location of the phylogeographical disjunction, although
the patchiness of D. potatorum would limit the possibility of
geographically intensive sampling. Wilsons Promontory
(Fig. 1) lies at the final point of contact between Tasmania
and mainland Australia during submerging of the Bassian
Isthmus; it represents the site of reunion of western and
eastern mainland geminate taxa as sea levels rose and is
therefore a natural biogeographical break. A long stretch of
uninhabitable sandy coast to the immediate east of Wilsons
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Fig. 4 Haplotype network diagram of the ‘eastern’ clade of
Durvillaea potatorum based on mtDNA (COI), with circle area
representing haplotype frequency. ‘Ancestral’ haplotypes are
indicated by asterisks.
Promontory (Ninety Mile Beach, Fig. 1) presumably inhibits
genetic exchange (or dispersal) across this region (Hidas
et al. 2007; York et al. 2008; Ayre et al. 2009), enhancing
isolation of eastern vs. western mainland populations.
An equivalent point cannot be identified in Tasmania, as
D. potatorum does not grow along the relatively sheltered
northern coast.
Ancient oceanographic influences
The broad genetic homogeneity of the ‘western’ D. potatorum,
with one particularly widespread haplotype ranging from
Port Fairy (the westernmost site sampled) to Bruny Island
in southeastern Tasmania (Figs 2 and 3), contrasts with the
relatively high diversity found in the ‘eastern’ clade for
COI. The genetic homogeneity observed across western
populations is unlikely to be due to anthropogenic
translocation (e.g. Voisin et al. 2005), as the range of
D. potatorum has apparently changed little since early
records (see Harvey 1863). Patterns of low-latitude genetic
diversity vs. high-latitude homogeneity are frequently
interpreted as evidence of postglacial recolonization in the
Northern Hemisphere, with rapid range expansion by
leading-edge migrants (Hewitt 1996, 2000; Maggs et al.
2008; Provan & Bennett 2008). Similarly, extensive sea ice
during the last glacial maximum (LGM) has been linked
© 2009 Blackwell Publishing Ltd
to patterns of high-latitude homogeneity in Durvillaea
antarctica in the Southern Hemisphere (Fraser et al. 2009b).
The monomorphism observed here in western D. potatorum
most probably reflects recent recolonization following
postglacial retraction of the subtropical convergence and
cold waters that affected western Tasmania during the last
glacial period (Fig. 1; Wells & Okada 1996; McGowran et al.
1997; Nürnberg et al. 2004) (hypothesis ii). This postglacial
expansion might have been facilitated by the strong
Zeehan Current (a continuation of the Leeuwin Current;
Ridgway & Condie 2004) that flows east from the southern
coast of mainland Australia to southern Tasmania during
interglacial periods (Fig. 1). In contrast, the southern
extension of the warm EAC during glaciations (Nürnberg
et al. 2004) presumably allowed temperate marine biota —
such as D. potatorum — to persist along the eastern coasts
of Tasmania.
If the genetic homogeneity of western D. potatorum does
indeed reflect severe glacial population decline and
subsequent postglacial range expansion, the divergence
observed between mainland and Tasmanian representatives
of the ‘eastern’ clade almost certainly predates the LGM.
This pre-LGM time frame of molecular divergence is also
supported by the findings of Fraser et al. (2009b), who
reported distinct D. antarctica haplotypes from ‘refugial’
islands in the New Zealand subantarctic. Despite the
absence of reliable mutation rate estimates for brown algae
(Hoarau et al. 2007) precluding precise dating of the time of
D. potatorum recolonization, the near-absolute genetic
homogeneity of the ‘western’ samples certainly seems
consistent with a post-LGM timeframe. For the ‘eastern’
clade, by contrast, the presence of two apparently ‘ancestral’
haplotypes (Fig. 4), one on the mainland (found at both
Tathra and Gabo Island) and one in southern Tasmania,
suggests persistence of multiple eastern populations
through the last glacial period, consistent with the warming
influence of the EAC (hypothesis ii).
To date, few marine phylogeographical studies have
directly assessed the importance of palaeoceanographic
features (but see Benzie 1999; Wares 2001). Although some
previous studies have hinted at their role (e.g. Muss et al.
2001; Marko 2004), the current analysis represents, to our
knowledge, one of the first studies to provide compelling
evidence for lasting biological effects of Pleistocene
oceanographic conditions.
Ecology and biology of D. potatorum
Although this study assesses only genetic variation, a
previous phylogenetic analysis of morphological and
ecological data (Cheshire & Hallam 1989; Cheshire et al. 1995)
has suggested a similar east–west split within D. potatorum
based on morphological and ecological characteristics. The
character states distinguishing these morphotypes were,
2294 C . I . F R A S E R , H . G . S P E N C E R and J . M . WAT E R S
‘western’ populations in northwestern Tasmania growing
intertidally (J.M. Waters, personal observation), as well as
intertidal plants at Tathra (‘eastern’ clade, C.I. Fraser,
personal observation). Nonetheless, the dominance of
‘western’ individuals in our eastern Tasmanian collections,
combined with the absence of any ‘western’ haplotypes
from the subtidally collected samples at King George III
Reef (southern Tasmania), suggests that the ‘eastern’ clade
may grow lower in the littoral and sublittoral zones. Future
studies will assess the genetic, morphological, ecological,
and taxonomical characteristics of D. potatorum to rigorously
test the hypothesis that it comprises two biologically
distinct taxa. Ideally, future genetic analyses should
also include a suite of variable markers (e.g. microsatellite loci) to further assess levels of gene flow among
D. potatorum populations.
Acknowledgements
Fig. 5 Photograph of Durvillaea potatorum retrieved from 10-m
depth at King George III Reef by SCUBA, showing secondary
stipes (s.s.) [photo: JMW].
however, somewhat variable (Table 1). Nonetheless,
when combined with our phylogeographical results, the
differentiation between ‘eastern’ and ‘western’ clades
seems likely to have a morphological, as well as genetic,
basis. Interestingly, several of the character states listed by
Cheshire et al. (1995) as ‘infrequent’ in eastern populations,
compared to entirely absent in western populations
(Table 1), were indeed observed in our ‘eastern’ samples,
such as secondary stipes emerging from the primary stipe
(Fig. 5) and stipes longer than 0.5 m. Perhaps the apparent
variability of these characteristics reflects the simultaneous
presence of both ‘eastern’ and ‘western’ genetic clades
along the east coast of Tasmania. If these clades correspond
to biologically distinct taxa, Cheshire & Hallam (1989) are
likely to have measured both sympatric forms in eastern
Tasmanian. Further morphological and physiological work,
combined with genetic identification, is clearly required to
determine whether these two clades represent separate
species, although their apparent morphological distinctness,
and their cohabitation along eastern Tasmania, certainly
suggests that they form separate taxonomic entities.
Although both clades are clearly sympatric in eastern
Tasmania, it is possible that their ecological characteristic
may differ somewhat, as noted for cryptic Durvillaea taxa in
New Zealand (Fraser et al. 2009a). Cheshire & Hallam
(1989) claimed that the ‘western’ form of D. potatorum is
never intertidal, compared to the ‘eastern’ form which is
occasionally intertidal. In contrast, we observed some
We gratefully acknowledge the following organizations and
individuals for additional sample collections: Lynda Avery and
S. Beaton of Infauna Data for collections from Peterborough; Allan
Millar for advice and a sample from Pirates Bay; Matt Edmunds
for collections from Port Fairy and Warrnambool; Roz Jessup for
collections from Phillip Island; Simon Talbot for SCUBA collections
from Tasmania; Wayne Kelly, Barry Rumbold and Sue Jones
(School of Zoology, University of Tasmania) for logistical support
in Tasmania. Thanks to Raisa Nikula for comments on the
manuscript; to Margaret Clayton and Cameron Hay for advice;
and to Tania King for laboratory assistance. This work was funded
by Department of Zoology funding allocations to C.I.F.; and
University of Otago Research grants to J.M.W.
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C.F. is a postgraduate student at the University of Otago. Her
interests include the ecology and phylogeography of Southern
Ocean marine biota, with current research focusing on southern
bull kelps (Durvillaea). She is particularly interested in applying
molecular techniques to broad-scale questions of dispersal and
climate change. H.S. is Professor of Zoology at the University of
Otago and a Principal Investigator with the Allan Wilson Centre
for Molecular Ecology & Evolution. His research covers aspects of
evolutionary biology, from theoretical population genetics and
phenotypic plasticity to the phylogenetics of birds and the
biogeography of molluscs, as well as the history of genetics. J.W.
is an Associate Professor of Zoology at the University of Otago.
His research focuses on the phylogeography and evolution of
Southern Hemisphere marine and freshwater biota. Current
projects are centered on the use of freshwater vicariant events to
calibrate molecular clocks, and the importance of macroalgae as
facilitators for oceanic rafting.
© 2009 Blackwell Publishing Ltd