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Nothogenia fastigiata has been reported to exhibit great morphological variability and has been considered to be widely distributed in the Southern Hemisphere. To test its current circumscription, sequences from type material of N. fastigiata and other species currently synonymized with it were compared to those from recent collections of this and other species in the genus. Eight distinct species previously subsumed under the name N. fastigiata were identified. Multiple specimens from southern Chile and a single specimen from Campbell Island (subantarctic New Zealand) were conspecific with type material of N. fastigiata from the Falkland Islands. For other species, molecular analyses of recent collections using the nuclear ITS1-5.8S-ITS2 region of the ribosomal cistron, the chloroplast rbcL and psbA genes and the mitochondrial COI gene indicated a strong geographic pattern to species relationships. Other specimens identified as N. fastigiata from Chile represented up to five species, including N. chilensis and N. fragilis, based on sequences of type material; these Chilean species occurred on a monophyletic branch. We also recognized N. lingula comb. nov. from Tasmania, which is closely related to N. fastigiata, based on sequences of type material. Specimens from mainland New Zealand identified as N. fastigiata fell into a distinct clade with New Zealand N. pulvinata and represented a previously undescribed species, described here as N. neilliae sp. nov. Another New Zealand species, N. pseudosaccata, was distantly related to N. variolosa from Auckland Island and other subantarctic islands south of New Zealand. The New Zealand species were more closely related to South African N. erinacea and N. ovalis than to species of Nothogenia from Chile, including N. fastigiata, although bootstrap support for this interpretation was weak. These genetic data demonstrate that matching DNA sequences from archival Nothogenia material to modern specimens can be used to identify and define new and old cryptic species.
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Sequencing of historic and modern specimens reveals cryptic diversity
in Nothogenia (Scinaiaceae, Rhodophyta)
SANDRA C. LINDSTROM
1
*, PAUL W. GABRIELSON
2
,JEFFERY R. HUGHEY
3
,ERASMO C. MACAYA
4
AND WENDY A. NELSON
5,6
1
Department of Botany, #3529–6270 University Blvd., University of British Columbia, Vancouver, BC V6T 1Z4, Canada
2
Biology Department & Herbarium, Coker Hall CB-3280, University of North Carolina, Chapel Hill, Chapel Hill,
NC 27599-3280, USA
3
Division of Science and Mathematics, Hartnell College, Salinas, CA 93901, USA
4
Laboratorio de Estudios Algales (ALGALAB), Departamento de Oceanograf´
ıa, Universidad de Concepci´
on,
Casilla 160-C, Chile
5
National Institute of Water and Atmospheric Research, Private Bag 14-901, Wellington 6241, New Zealand
6
School of Biological Sciences, University of Auckland, Private Bag 92-019, Auckland 1142, New Zealand
ABSTRACT:Nothogenia fastigiata has been reported to exhibit great morphological variability and has been considered to
be widely distributed in the Southern Hemisphere. To test its current circumscription, sequences from type material of N.
fastigiata and other species currently synonymized with it were compared to those from recent collections of this and
other species in the genus. Eight distinct species previously subsumed under the name N. fastigiata were identified.
Multiple specimens from southern Chile and a single specimen from Campbell Island (subantarctic New Zealand) were
conspecific with type material of N. fastigiata from the Falkland Islands. For other species, molecular analyses of recent
collections using the nuclear ITS1-5.8S-ITS2 region of the ribosomal cistron, the chloroplast rbcL and psbA genes and the
mitochondrial COI gene indicated a strong geographic pattern to species relationships. Other specimens identified as N.
fastigiata from Chile represented up to five species, including N. chilensis and N. fragilis, based on sequences of type
material; these Chilean species occurred on a monophyletic branch. We also recognized N. lingula comb. nov. from
Tasmania, which is closely related to N. fastigiata, based on sequences of type material. Specimens from mainland New
Zealand identified as N. fastigiata fell into a distinct clade with New Zealand N. pulvinata and represented a previously
undescribed species, described here as N. neilliae sp. nov. Another New Zealand species, N. pseudosaccata, was distantly
related to N. variolosa from Auckland Island and other subantarctic islands south of New Zealand. The New Zealand
species were more closely related to South African N. erinacea and N. ovalis than to species of Nothogenia from Chile,
including N. fastigiata, although bootstrap support for this interpretation was weak. These genetic data demonstrate that
matching DNA sequences from archival Nothogenia material to modern specimens can be used to identify and define new
and old cryptic species.
KEY WORDS: Biogeography, COI, ITS, Nothogenia, Phylogeny, psbA, rbcL, Sequencing type material, Species, Taxonomy
INTRODUCTION
Nothogenia Montagne, a genus of the Scinaiaceae (Order
Nemaliales), currently contains six species that occur
intertidally in the Southern Hemisphere (AlgaeBase, as of
13 March 2014): South African N. erinacea (Turner) P.G.
Parkinson and N. ovalis (Suhr) P.G. Parkinson, New
Zealand N. pseudosaccata (Levring) P.G. Parkinson and N.
pulvinata (Levring) P.G. Parkinson, Peruvian N. fragilis
Montagne and the widely distributed N. fastigiata (Bory)
P.G. Parkinson. Most of these species previously had been
assigned to Chaetangium K¨
utzing, but Parkinson (1983)
considered that genus to be a synonym of Suhria J. Agardh
ex Endlicher. A summary of Parkinson’s taxonomic conclu-
sions can be found in Silva et al. (1996, p. 104.)
The genus Nothogenia was created by Montagne (1843, p.
302) to accommodate N. variolosa (Montagne) Montagne, a
repeatedly dichotomous and linear cartilaginous species with
thin medullary filaments, a cortex of submoniliform cells and
cystocarps encircled by a dense pericarp. Montagne’s
material was collected on the Auckland Islands by Dumont
D’Urville aboard the Astrolabe (Montagne 1842, 1845). His
species, however, is considered a later heterotypic synonym
of Bory de Saint-Vincent’s Halymenia fastigiata (¼N.
fastigiata), originally collected on the Falkland Islands
(Parkinson 1983). In addition to N. variolosa, two other
species are considered synonyms of N. fastigiata:N. chilensis
(J. Agardh) Montagne (basionym: Chaetangium chilense)
and Chaetangium lingula Harvey with type localities of
Valpara´
ıso, Chile, and Brown’s River, Tasmania, Australia,
respectively.
As noted by Huisman & Womersley (1994, p. 110), ‘The
type species of Nothogenia,N. variolosa from the Auckland
Is., as illustrated by Montagne (1845, fig. 3) is a much
branched plant with narrow branches. Chapman (1969, p.
70) comments on the extreme variability of the New Zealand
taxon, and Ricker (1987, p. 168) also doubts whether this
material (and the type of N. variolosa) is the same as N.
fastigiatum [sic] from the Falkland Is. and other subantarctic
islands; clearly further study is needed’. Additionally, N.
fastigiata was described as morphologically highly plastic
along the Chilean coast (Hoffman & Santelices 1997).
* Corresponding author (Sandra.Lindstrom@botany.ubc.ca).
DOI: 10.2216/14-077.1
Ó2015 International Phycological Society
Phycologia Volume 54 (2), 97–108 Published 9 March 2015
97
Differences between two distinct morphotypes in central
Chile were attributed to adaptive responses to abiotic
factors, although genetic differentiation was also suggested
by Ram´
ırez (1988).
The present study was undertaken to authenticate the
identity of true Nothogenia fastigiata, to test the taxonomic
positions of its synonyms using DNA from modern and type
material and to determine species relationships.
MATERIAL AND METHODS
DNA was extracted from silica gel desiccated material
(Table S1) using the CTAB mini-extraction protocol as
described in Lindstrom & Fredericq (2003). Total extracted
DNA was amplified for the nuclear ribosomal ITS regions,
the chloroplast rbcL and psbA genes and the 50end of the
mitochondrial COI gene using the primers listed in Table S2.
For the ITS regions, primers ITS1 and JO6 were used
initially. If these reactions were unsuccessful in producing a
visible band, 1 ll of reaction product was used as the
template in a subsequent reaction using ITS1Pa as the
forward primer and ITS2Pa or JO6 as the reverse primer. If
the initial reaction produced multiple bands, 1 ll of crude
DNA was used as the template in a subsequent reaction
using ITS1No and ITS4No as primers. The rbcL gene was
amplified as a single fragment using the F57 and RrbcSst
primers or in two fragments using F57-R1150K and
F753No-RrbcSst as the primer pairs, and the psbA gene
was amplified using the primers psbAF1 and psbAR2. The 50
end of the COI gene was amplified using GazF1 and GazR1
as primers, or, if initially unsuccessful, CO1S1 and GazR1
were used. All reactions contained 5 or 6 ll103NEB
Thermopol buffer (New England BioLabs, Whitby, Ontar-
io), 0.5 or 1.0 ll 10 mM dNTP mix, 0.4–1.0 ll each forward
and reverse primers (at a concentration of c. 32 pmol ll
1
),
0.35 ll NEB DNA Taq polymerase, c.1ll crude DNA (or
PCR product) and distilled deionized water to a final volume
of 50 ll. The ITS regions were amplified using the protocol
of Hughey et al. (2001). If a PCR product was reamplified,
we used the protocol of Broom et al. (1999). For rbcL and
psbA, we used the PCR protocol of Lindstrom & Fredericq
(2003). For COI, we used the PCR protocol of Saunders
(2005). PCR products were sequenced using the ABI Applied
Biosystems (Foster City, California USA) Big Dye Termi-
nator v3.1 cycle sequencing kit by the Nucleic Acid Protein
Service Unit (University of British Columbia, Vancouver,
British Columbia, Canada) with the same primers used for
amplification (but at reduced concentrations).
Fully alignable rbcL, psbA and COI sequences from the
specimens listed in Table S1 were concatenated and
subjected to maximum likelihood (ML) analyses using
PAUP* 4.0b10 (Swofford 2002) and RAxML 7.2.6 [as
implemented on the T-REX website (http://www.trex.uqam.
ca/index.php?action¼raxml; Stamatakis 2006; Buc et al.
2012)]. The appropriate model of evolution for the PAUP
ML analysis using the Akaike information criterion was
determined from Modeltest 3.7 (Posada & Crandall 1998;
Table S3), and data were partitioned by gene and codon
position for the RAxML analysis. Separate analyses were
carried out for these genes individually, as well as for the ITS
region of the nuclear ribosomal cistron. Bootstrap propor-
tions were determined based on 100 replicates for PAUP ML
and 1000 replicates for RAxML. Bayesian phylogenetic
analyses were performed on the Bio-Linux7 platform (Field
et al. 2006) with MrBayes 3.2.1 (Huelsenbeck et al. 2001;
Ronquist & Huelsenbeck 2003). Markov chain Monte Carlo
runs were all executed with the GTRþIþG model. This
substitution model was used because it corresponds most
closely to the Tamura-Nei and Transitional models indicated
in Table S3 (Zakharov et al. 2009; Skillings et al. 2011). The
number of generations performed varied for each data set.
As an indicator of convergence, we followed the MrBayes
3.2 manual, which recommends continuing analyses by
increasing the number of generations until the average
standard deviation of split frequencies drops below 0.01. All
runs were performed using a sample frequency of 10 with
two independent analyses. To calculate the Potential Scale
Reduction Factor and posterior probabilities, the burn-in
values were set to discard 25%of the samples.
Out-groups were selected based on blastn searches of
GenBank. For rbcL, these included DQ787562 (Nemalion
sp.; Yang & Boo, unpublished), KC134333 [Scinaia confusa
(Setchell) Huisman; Scott et al. 2013] and AB258450 [S.
okamurae (Setchell) Huisman, Huisman & Kurihara, un-
published]. For psbA, this included DQ787638 (Nemalion
sp.; Yang & Boo, unpublished). For COI, they included
HM916493 [Nemalion multifidum (Lyngbye) Chauvin; Le
Gall & Saunders, unpublished], HM916595 (S. confusa;Le
Gall & Saunders, unpublished) and HQ544543 [S. interrupta
(A.P. de Candolle] M.J. Wynne; Le Gall & Saunders,
unpublished). We also used unpublished sequences of
Palmariaceae (Lindstrom, unpublished) since GenBank also
indicated high similarity of our Nothogenia sequences to
species in this family.
DNA from potential type material and other historical
specimens (Table S4) was extracted, amplified and sequenced
following the protocol described in Lindstrom et al. (2011)
except for using 33the primer concentration used previous-
ly. To amplify part of the rbcL gene, primers F753 and R900
were used (Table S2). Sequences were aligned with contem-
porary collections in BioEdit (Hall 1999).
RESULTS
The phylogenetic analysis of the concatenated data set of
rbcL, psbAandCOI sequences (Fig. 1) indicates that
Nothogenia is a monophyletic genus. In general, divergences
within species were universally small (mostly less than 1%
and usually much less than 1%), and divergences between
species were usually very large (often 6–13%). The two South
African species, N. ovalis and N. erinacea, occurred in a
strongly supported clade that was sister to a clade of New
Zealand species, but this relationship had weak bootstrap
support in the RAxML analysis. Among the New Zealand
species, only the sibling relationship between N. pulvinata
and N. neilliae was strongly supported. A sibling relationship
between N. pseudosaccata and N. variolosa was only
moderately supported by the PAUP and RAxML boot-
98 Phycologia, Vol. 54 (2)
straps. The third geographic clade, which was strongly
supported in all analyses, included species primarily from
Chile. This clade included N. fastigiata, which is also known
from the Falkland Islands, its type locality, and the closely
related N. lingula from Tasmania (this taxon was represented
by a GenBank rbcL sequence, KC134356, since we did not
have contemporary material). Of the remaining Chilean
species, only N. chilensis and N. fragilis have been described.
Nothogenia fragilis, the most northerly of the South
American species, occurred on a very long branch. The
remaining Chilean species occurred in a terminal cluster.
Although branches were shorter than those of other species
of Nothogenia, most branches were strongly supported. The
exception was Taxon C, which occurred along a branch from
which other species diverged, suggesting that it has
experienced little genetic differentiation.
We also examined phylogenetic relationships among
species using individual genes to assess the relative contri-
butions of these genes to the overall pattern as well as to
include additional individuals. These figures are presented as
Fig. S1 (rbcL gene), Fig. S2 (psbA gene) and Fig. S3 (COI
gene). In general, patterns for the individual genes mirrored
those of the concatenated data set. However, some of the
individual branches of the deeply diverging species showed
no clear relationships with other taxa in the psbA analysis
compared to the rbcL or concatenated analyses. These
analyses also included a single Chilean specimen (N57) that
did not cluster with any of the other taxa and may represent
an additional undescribed species. The positions of the
terminal Chilean clades (N. chilensis and Taxa A–C) varied
based on the gene analysed, but all species were moderately
to strongly supported in all analyses. We also observed
unusual COI genotypes for some of the Chilean species,
which occurred on a very long branch sister to all of the
other species of Nothogenia, and were also highly divergent
from each other (data not shown). These anomalies were
observed independently by E. Macaya and may represent
numts (nuclear mitochondrial DNA) or pseudogenes.
The ITS data set was characterized by a large number of
large indels (there were more than eight greater than 10 base
pairs [bp] in length, the longest being .100 bp). Because of
this, we analysed the data using MP with gaps treated as a
fifth base, with indels reduced to the number of steps that
might have been required to achieve the alignment of species
in our data set (data not shown but available upon request;
since other types of analyses treat gaps as missing data, they
were not performed). The resulting phylogenetic tree was
similar to those produced by other analyses but with less
resolution. Among Chilean species, N. fragilis was strongly
supported, but N. chilensis and Taxon B were intermixed on
a strongly supported branch, and most Taxa A and C
occurred on unsupported to weakly supported branches.
Nothogenia fastigiata also occurred on its own weakly
supported branch but with some strongly supported internal
branches. The subantarctic N. variolosa was also strongly
supported (and also had moderately to strongly supported
internal branches), but New Zealand N. neilliae and N.
pulvinata were intermixed. There was weak support for the
South African species occurring on the branch from which
the New Zealand and subantarctic species diverged.
Below we provide details of the species examined in this
study, including the results of sequencing type material. The
distribution of these species in the Southern Hemisphere is
shown in Fig. 2.
Fig. 1. Maximum likelihood analysis of concatentated rbcL, psbA and COI sequence data for species of Nothogenia. Bootstrap values
represent left-to-right PAUP (nreps ¼100) and RAxML (nreps ¼1000); Bayesian posterior probabilities appear below these values. An
asterisk indicates bootstrap values of 100 for the ML analyses and posterior probability of 1.000 for MrBayes. Regional provenances of
samples represented by vertical line on right: South America (100%opacity), Australia (74%opacity), New Zealand including Subantarctic
islands (48%opacity) and South Africa (24%opacity).
Lindstrom et al.: Cryptic diversity in Nothogenia 99
South African species
Nothogenia ovalis (Suhr) P.G. Parkinson 1983, p. 609
BASIONYM:Dumontia ovalis Suhr 1840, p. 274.
TYPE LOCALITY: Cape of Good Hope (see Silva et al. 1996: 112).
KNOWN DISTRIBUTION: South Africa, Namibia, Tristan da Cunha
(Guiry & Guiry 2014).
We did not sequence type material of this species, but the
morphology, genotypes and provenance of the sequenced
material suggest it is a distinctive species.
Nothogenia erinacea (Turner) P.G. Parkinson 1983, p. 609
BASIONYM:Fucus erinaceus Turner 1808, p. 55, pl. 26.
TYPE LOCALITY: Cape of Good Hope (Silva et al. 1996, p. 112).
KNOWN DISTRIBUTION: South Africa, Namibia (Guiry & Guiry
2014).
We did not sequence type material of this species. As with
N. ovalis, the morphology, genotypes and provenance of the
sequenced material suggest it is a distinctive species.
Anderson & Stegenga (1985) observed a Cruoriopsis-like
crustose tetrasporophyte in the life cycle of both South
African species. Collantes et al. (1981) had earlier illustrated
tetrasporangia in crusts from Chilean N.‘fastigiata’, and
Del´
epine et al. (1979) illustrated crusts from natural
populations from the Kerguelen Islands.
South American species
Nothogenia chilensis (J. Agardh) Montagne 1854, p. 326
BASIONYM:Chaetangium chilense J. Agardh 1847, p. 10.
TYPE LOCALITY: Valpara´
ıso, Chile.
Fig. 2. Distribution of species of Nothogenia in the Southern Hemisphere.
100 Phycologia, Vol. 54 (2)
KNOWN DISTRIBUTION: Near Valpara´
ıso, Chile (this study).
Three fragments from the three specimens comprising
Herb. Ag. 32578 in LD (6N, 9N, 17N; Table S4), identified
as ‘Chaetangium chiloense’, had rbcL sequences identical to
N06 (from Horc´
on, north of Valpara´
ıso) and N12 (from
Playa El Encanto, near Valpara´
ıso). The Herb. Ag. material
is in complete agreement with the protologue (Agardh 1847),
including the type locality of Valpara´
ıso and the material
being from the Binder herbarium (Fig. 3). Therefore, we
herein designate LD 32578 as the lectotype. Agardh (1847)
briefly noted that his species was nearly identical with
Montagne’s Nothogenia variolosa.Nothogenia chilensis can
be applied to N06, N12 and N56 among our collections. The
relationship of these specimens to N13 and N14 is discussed
below under Taxon B.
Nothogenia fastigiata (Bory) P.G. Parkinson 1983, p. 609
BASIONYM:Halymenia fastigiata Bory 1825, p. [22] 594.
TYPE LOCALITY: Iles Malouines [Falkland Islands].
KNOWN DISTRIBUTION: Falkland Islands; southern Chile, from
Corral near Valdivia south through Isla Chilo´
eto at least Magellan
Strait; Campbell Island (south of New Zealand; this study).
Despite having a widely applied name, this species appears
to be more restricted geographically than previously
understood. It has a distinct morphology of narrow,
fastigiate branches. Other taxa that have been misidentified
as this species but have distinct genetic signatures are usually
broader with fewer, sparser branches. Nothogenia fastigiata
occurs on its own well-supported branch in all analyses for
all loci (rbcL, psbA, COI and ITS). It is closely related to N.
lingula from Tasmania; these species occur on a strongly
supported branch sister to all other Chilean species.
The 102-bp fragment of type material (Herb. Ag. 32591 in
LD—11N; Table S4), ‘Dumontia fastigiata Bory herb.
Halymenia #23 fl. Mal.’, was identical to five of our
specimens (M498, N04, N37, N38 and N44) from the coast
of Chile; we therefore confirmed them as N. fastigiata.
Specimens 2N (Herb. Ag. 32576 from Ancud, Isla Chilo´
e),
13N (Herb. Ag. 32577 from Sandy Point, Fort Magellan,
Chile) and 16N (an unlocalized fragment from Chile in the
PC herbarium) also had identical 102-bp sequences to Herb.
Ag. 32591. The sequence from a specimen (N31) from
Campbell Island (south of New Zealand) indicates that this
species may indeed be widespread. The Campbell Island
specimen diverged from the Western Hemisphere specimens
by 0.2%in the rbcL gene. The morphology of the Campbell
Island specimen differed slightly from other Campbell Island
specimens identified as N. variolosa by having shorter and
broader branches.
Nothogenia fragilis Montagne 1852, p. 318
TYPE LOCALITY: Cobija, Peru.
KNOWN DISTRIBUTION: Cobija, Caleta Erra
´zuriz, Punta Talca, and
Valpara´
ıso, Chile.
The 118-bp fragment of type material (Table S4) was
identical to four contemporary specimens except for one
nucleotide in the area overlapping the reverse primer used to
amplify the type sequence (here the type sequence had the
same nucleotide as the primer rather than the nucleotide
found in the longer sequences of the contemporary material).
Three of the contemporary specimens were from Caleta
Erra
´zuriz, near Antofagasta, the fourth from Punta Talca,
south of Coquimbo; these differed by 0.3%. All of these
sequences matched an rbcL sequence from an historical
specimen (12N) said to be from Valpara´
ıso, Chile (Table S4).
These specimens occurred on a well-supported branch sister
Fig. 3. Lectotype of Nothogenia chilensis (LD 32578).
Lindstrom et al.: Cryptic diversity in Nothogenia 101
to N. chilensis and Taxa A–C. Specimens are usually 5–6 cm
high, dichotomously branched at first, then slightly irregular;
segments are of variable length and 1–3 mm diameter;
texture is firm; colour is brown-red. This species is easy to
differentiate from the other Chilean Nothogenia because
thalli are cylindrical to slightly compressed. A dark red
tetrasporophytic crust with irregular margins was described
for this species (Ram´
ırez 1988).
Taxon A
KNOWN DISTRIBUTION: Near Constituci´
on and Concepci´
on, central
Chile (this study).
Three specimens (M494, N05 and N16) were identified as
Taxon A based on similar or identical rbcL and psbA
sequences, and all were collected near Concepci´
on. These
specimens occurred on their own strongly supported branch
in the rbcL and psbA. Only a single specimen was sequenced
for COI.
In addition to the contemporary specimens we sequenced,
we matched two historic specimens (7N and 10N; Table S4)
to this species. The contemporary specimens were from near
Concepci´
on; the two historic specimens lacked information
on provenance, but the identity of their sequences with the
more recent collections suggests they may also have been
from near Concepci´
on.
Taxon B
KNOWN DISTRIBUTION: Near Valpara´
ıso (Quintay), Chile (this
study).
This taxon is closely related to N. chilensis in all analyses,
but the distinction of the two taxa is supported by strong
bootstrap values in analyses of rbcL and psbA sequences.
The two specimens (N13 and N14) identified as this species
had identical rbcL and psbA sequences and were both
collected at the same site at the same time. Despite this, they
were morphologically distinct: N13 was up to 3 cm tall with
open, spreading branches ending in acute tips; whereas N14
was up to 2 cm tall, densely branched and with truncate tips.
No historical specimens had sequences that allied them with
this taxon.
Taxon C
KNOWN DISTRIBUTION: Falkland Islands; Cobquecura, Isla Chilo´
e,
Melinka and Repollal, Chile (this study).
Specimens identified as Taxon C shared identical or nearly
identical rbcL, psbAandCOI sequences and occurred
together on moderately to strongly supported branches
(rbcL and COI analyses) or along the branch that gave rise
to Taxon B and N. chilensis (psbA). No historical specimens
had sequences that allied them with this taxon.
Naming of Taxa A to C will be done after further research
on these by E. Macaya. A single specimen (N57) not clearly
related to any of the other Chilean specimens occurred
among these taxa in rbcL, psbA and COI analyses. This
specimen remains unascribed (Figs S1–S3). Further collec-
tions are required before it can be described.
New Zealand species
Nothogenia pseudosaccata (Levring) P.G. Parkinson 1983, p.
609
BASIONYM:Chaetangium pseudosaccatum Levring 1955, p. 423.
TYPE LOCALITY: Blind Broad Bay, Stewart Island, New Zealand.
TYPE SPECIMEN: GB, Lindauer No. 7732; 21 November 1945
(Andersson & Athanasiadis 1992; Nelson & Phillips 2001).
KNOWN DISTRIBUTION: Southeast coast of South Island, Stewart
Island and Snares Islands (Adams 1994); Macquarie Island?
This species shows a moderate to weak relationship to N.
variolosa and is only distantly related (Figs 1, S1, S3). We did
not sequence type material of this morphologically distinct
species, which is inflated, club-shaped, simple or bi- or
trifurcate, with a short stalk (Levring 1955; Adams 1994;
Nelson 2013). We did sequence two specimens identified as
this species from Stewart Island, New Zealand: N21 from
Lonneker’s Nugget and N22 from Lee Bay. Ricker (1987)
reported inflated specimens from Macquarie Island that he
considered intermediate in form between N. pseudosaccata
and N. fastigiata. Recent photographic quadrats of intertidal
communities at Macquarie Island reveal specimens with a
morphology very similar to that of Stewart Island N.
pseudosaccata. Further work is required to compare material
from Macquarie Island with that from Stewart Island.
Nothogenia pulvinata (Levring) P.G. Parkinson 1983, p. 609
BASIONYM:Chaetangium pulvinatum Levring 1955, p. 422.
TYPE LOCALITY: Temple Bar, Russell, Bay of Islands, North Island,
New Zealand.
TYPE SPECIMEN: GB; Levring No. 88-5, 24 March 1948, Levring
(Nelson & Phillips 2001).
KNOWN DISTRIBUTION: North Island: mainly on the east coast
(Adams 1994).
This species shows a strong relationship to N. neilliae (Figs
1, S1–S3). We sequenced two specimens of this species: N08
from Reotahi, Whangarei Harbour, North Island, and N17
from Bayly’s Rd., Taranaki, North Island (a new southern
distribution record for this species). This distinctive species,
forming domed, densely branched tufts of narrow cylindrical
branches with pointed tips (Levring 1955; Adams 1994;
Nelson 2013), is known only from the North Island of New
Zealand.
Nothogenia neilliae W.A. Nelson sp. nov., Fig. 4
TYPE LOCALITY:46822.93 0S, 169846.980E; intertidal on rock; Kaka
Point, southeast Otago, South Island, New Zealand.
TYPE SPECIMEN: WELT A032881, 26 November 2011, Leg. W.
Nelson, K. Neill, J. Dalen.
102 Phycologia, Vol. 54 (2)
KNOWN DISTRIBUTION: Southern North Island (Cook Strait),
South Island, Stewart Island (this study).
DESCRIPTION: Thalli usually 3–5 cm high, tufted, bushy, repeatedly
dichotomously or irregularly branched; axes terete to compressed
below, becoming flattened distally. Growing from a crust-like pad
with multiple axes arising from it. Dome-shaped cystocarps with
conspicuous pore on upper branches. Texture firm, colour brown-red
to purple, bleaching ginger-red in summer.
ETYMOLOGY: In recognition of contributions made by Kate Neill to
New Zealand phycology.
This species had previously been identified as N. fastigiata
in New Zealand (Adams 1994; Nelson 2013).
Nothogenia variolosa (Montagne) Montagne 1843, p. 303
BASIONYM:Chondrus variolosus Montagne 1842, p. 6.
TYPE LOCALITY: Auckland Island.
KNOWN DISTRIBUTION: Auckland, Antipodes, and Campbell
Islands (this study).
Three specimens (3N, Herb. Ag. 32575 in LD; 14N, PC—
Gen; 15N, L 941 51 22; Table S4) represent potential type
material of Chondrus variolosus. All are from Auckland
Island. 3N and 14N had identical rbcL sequences to our
specimens from Antipodes Island (N11) and Campbell
Island (N28 and N29), and they varied at one bp position
from the contemporary specimen from Auckland Island
(N26), which had a sequence identical to 15N. We recognize
14N from PC—Gen as the lectotype specimen since PC is
where Montagne worked on these collections. We consider
the L and LD specimens to be isolectotypes.
Montagne (1845) illustrated N. variolosa with a narrow
and much-branched thallus. Further work is warranted to
clarify morphological variation in this species and N.
fastigiata within the New Zealand subantarctic region.
Australian species
Nothogenia lingula (Harvey) S.C. Lindstrom & Hughey
comb. nov.
BASIONYM:Chaetangium lingula Harvey 1860, p. 316.
TYPE LOCALITY: Brown’s River, Tasmania.
KNOWN DISTRIBUTION: Tasmania.
We sequenced the type specimen housed in TCD. The 102-
bp fragment matched exactly GenBank KC134356 from
Bicheno, Tasmania, which in turn was similar to a specimen
from Ninepin Point, Tasmania, collected in April 1958 by
W.M. Curtis and housed in HO (72638); this latter specimen
differed at two bp positions (2%divergence) from the type
specimen and at three bp (0.9%divergence) from KC134356
over a longer alignment. Sequence differences among these
Fig. 4. Holotype of Nothogenia neilliae (WELT A032881).
Lindstrom et al.: Cryptic diversity in Nothogenia 103
samples suggest possible cryptic diversity in this distinctive
species—the specific epithet referring to the flat, lanceolate
branches that distinguish it morphologically from other
species in the genus. We also examined but did not sequence
specimens in NSW (392817, 392818); these specimens were
formerly housed in AD (as A56468 and A57076) and formed
the basis of Huisman & Womersley‘s (1992) description of
postfertilization development in N. fastigiata. All of these
specimens share the same morphology as the type and HO
specimens: thalli up to 4.6 cm tall, mostly 2–4 (4.5 maximum)
mm wide, flattened, usually once or twice bifurcate (up to a
maximum of four times), with relatively long branches
tapering to narrowly rounded branch tips.
DISCUSSION
This study confirms the distinctiveness of currently recog-
nized species of Nothogenia (N. erinacea,N. fastigiata,N.
fragilis,N. ovalis,N. pseudosaccata and N. pulvinata). Also,
we were able to show that several genetic lineages, some of
them formerly subsumed under the name N. fastigiata, can
be linked to previous names based on sequencing of type
material. These include the herein resurrected N. chilensis,N.
lingula and N. variolosa. A new species name, N. neilliae, was
created for the New Zealand species formerly identified as N.
fastigiata. There are still several lineages that as yet are
unnamed, especially along the central Chilean coast.
The amount of genetic diversity uncovered in this study
among species previously subsumed in N. fastigiata is high
even considering that they occur in the upper intertidal, a
habitat previously identified by Kelly & Palumbi (2010) as
rife with genetic subdivision among invertebrates. The ITS
region of the nuclear ribosomal cistron is particularly
divergent between cryptic species, but significant divergences
were revealed by all gene regions sequenced, as evidenced in
the phylogenetic trees.
We observed the most consistent results in the rbcL and
psbA gene sequences. Janouˇ
skovec et al. (2013), who studied
the architecture of four red algal plastid genomes, found
plastid DNA to be useful for resolving relationships; they
noted that the rbcL gene was particularly good at resolving
both evolutionarily deep as well as species/subspecies-level
relationships. Our results also confirm previous observations
(e.g. Kim et al. 2006) that the rbcL gene is a more sensitive
marker compared to the psbA gene: the latter gene did not
resolve relationships nearly as clearly as the former. The
intermixing of genotypes for the nuclear ITS region in our
study, especially among closely related species, suggests the
possibility of incomplete lineage sorting, hybridization,
introgression or thallus coalescence among these species.
Problems using the ITS region, including slow genetic
coalescence and intragenomic variation, have also been
identified as reasons to use caution in employing ITS
sequence data in phylogenetic and taxonomic studies (e.g.
´
Alverez & Wendel 2003; Lane et al. 2007; Leliaert et al.
2014). Finally, we note the highly divergent COI sequences
for some Chilean specimens. Whereas the majority of COI
sequences produced a phylogenetic pattern similar to that
observed for the plastid genes, a few diverged by 20–26%
from sequences of other specimens of the same species. All of
these divergent specimens occurred together in a clade sister
to the remaining species of Nothogenia but still within the
Sciniaceae, and they were all highly divergent from each
other. Such a pattern of extreme divergence has not been
previously reported for this frequently used ‘bar-coding’
gene; these sequences may represent numts (nuclear mito-
chondrial DNA) or pseudogenes.
Another contributing factor to the large genetic diver-
gences observed among species is their geographic isolation
in the Southern Hemisphere, where there are large distances
between landmasses. An exception is the genetic diversity
observed along the Chilean coast, where species differenti-
ation appears to occur among proximate collections. In a
study of the kelp Durvillaea antarctica (Chamisso) Hariot,
Fraser et al. (2010) found low genetic connectivity across
central Chilean sampling localities, suggesting that this may
be attributable in part to habitat discontinuity. In a different
study, Montecinos et al. (2012) observed genetic discontinu-
ity in Mazzaella laminarioides (Bory) Fredericq, an intertidal
red algal species endemic to Chile and the subantarctic
islands, at 328370S–348050S and at 378380S–398400S. The
genetic differentiation between these populations for both
the rbcL and COI genes indicates that they represented
different species. In the present study, we observed breaks in
populations of species previously identified as N. fastigiata at
328570S–338110S and at 338110S–368490S. The first break
point for both Mazzaella and Nothogenia occurred in the
same area near Valpara´
ıso, indicating that the region
between 308S and 338S is an important phylogeographic
break point on this coast; this has been also reported for
other marine organisms in several phylogeographic studies
(Tellier et al. 2009; Macaya & Zuccarello 2010; Sanchez et al.
2011; Brante et al. 2012; Haye et al. 2014). The ancient origin
of this break might increase the genetic differentiation in
poorly dispersing species (Haye et al. 2014), including red
algae such as Mazzaella and Nothogenia (Alveal 2001;
Montecinos et al. 2012). However, our data also indicate
the possibility of mixed genotypes among most of these
putative species of Nothogenia from mainland Chile, where
specimens could potentially hybridize. More samples and
sites need to be analysed to provide a better understanding of
the phylogeographic structure of species of Nothogenia along
this coast.
Previously, N. fastigiata was recognized as a highly plastic
morphological species along the Chilean coast (Ram´
ırez
1988; Hoffman & Santelices 1997); however, our results
demonstrate the presence of different species. Ram´
ırez
(1988), studying two populations of N. fastigiata growing
in different ecological habitats in central Chile, found
morphological variation, with individuals from a protected
environment being flattened and samples from an exposed
site having cylindrical thalli. DNA sequence data including
sequences from type material indicate that our samples
collected from Caleta Erra
´zuriz (238S) and Punta Talca
(308S) correspond to N. fragilis and have a similar
morphology to those from the exposed site in Ram´
ırez
(1988, figs 8–13); therefore, the range of this species might
extend from Peru to central Chile. However, no contempo-
rary specimens from Peru have been analysed, and the type
104 Phycologia, Vol. 54 (2)
collection, which was indicated to be from Peru, is from an
area now part of Chile.
At most sites along the Chilean coast, only a single species
was found, with the exception of Melinka and Repollal
(438S), where both N. fastigiata and Taxon C occurred in the
mid-intertidal zone. These species are morphologically
distinct (Fig. 5). Further work is needed to understand
possible postglacial recolonization routes and/or possible
glacial refuges of these species. For example, Taxon C might
have recolonized from nonglaciated areas (e.g. Mar Brava,
Cobquecura) after the Last Glacial Maximum (LGM).
On mainland New Zealand, the distribution of a northern
species (N. pulvinata) and a southern species (N. neilliae)is
consistent with well-documented patterns of geographic and
genetic disjunctions among closely related species (e.g.
Glaphyrosiphon—Hommersand et al. 2010; Apophlaea
Nelson 2013; Melanthalia—Nelson et al. 2013).
Within the subantarctic region of the Southern Hemi-
sphere, the impacts of glaciation on the distribution of
marine taxa have been investigated using molecular sequenc-
ing data to evaluate the connectivity of populations around
the Southern Ocean and in southern South America (e.g.
Fraser et al. 2009, 2012; Macaya & Zuccarello 2010; Reisser
et al. 2011; Gonza
´lez-Wevar et al. 2012). The impact of the
LGM and the subsequent recolonization of habitats have
been investigated for both macroalgal and invertebrate
species. There is evidence that sea ice resulted in the removal
of ice-sensitive shallow marine taxa, while ice-resistant taxa
persisted through the LGM (e.g. Fraser et al. 2009, 2012;
Reisser et al. 2011). Some biogeographic studies reveal the
presence of circumpolar haplotypes and very low genetic
diversity, indicating recent dispersal and population connec-
tivity (e.g. Fraser et al. 2009; Macaya & Zuccarello 2010;
Nikula et al. 2010). Other studies have documented species
with very restricted distributions and high levels of genetic
structuring (e.g. Reisser et al. 2011). The distribution of N.
variolosa, restricted to the New Zealand subantarctic islands,
suggests that this high intertidal species persisted through the
LGM but has had limited capacity for dispersal. A more
detailed investigation of population structure within and
between islands would address questions about connectivity
amongst the New Zealand subantarctic islands.
The record of N. fastigiata from Campbell Island, the
southernmost island in the New Zealand subantarctic group,
indicates that there has been recent connection around the
Southern Ocean in this species. The most commonly invoked
mechanism for genetic connectivity across vast ocean
distances is rafting, and there is evidence of regular gene
flow amongst populations of invertebrates associated with
kelp rafts (e.g. Nikula et al. 2011a, b). It is less clear how a
high to mid-intertidal macroalga such as N. fastigiata
disperses, but in a recent article Fraser et al. (2013) reported
evidence of transoceanic dispersal between New Zealand and
South America of Adenocystis utricularis and Bostrychia
intricata, two intertidal nonbuoyant algal species. They
suggested attachment to buoyant macroalgae or floating
wood, also a possible mechanism for dispersal of N.
fastigiata. Moreover, inflated, buoyant specimens of N.
fastigiata have been observed in the field (E. Macaya,
personal observation). The single specimen of N. fastigiata
found on Campbell Island and confirmed by sequencing was
noted to be morphologically different from specimens
growing on adjacent rocky substrates later confirmed to be
N. variolosa. Further investigations of Campbell Island
populations are warranted: N. fastigiata and N. variolosa
appear to occupy the same niche within the mid- to upper
intertidal shore.
These results add yet another family and order of red
algae to a growing list in which sequenced type specimens
allow us to unequivocally apply 19th- and early 20th-century
names to modern collections (Hughey et al. 2001; Gabrielson
2008; Gabrielson et al. 2011; Lindstrom et al. 2011; Hind et
al. 2014). Because of the cryptic diversity that is being
uncovered with DNA sequencing within all orders of red
algae, coupled with the morphological variability of some
cryptic species, including Chilean species of Nothogenia,
sequencing type specimens is necessary for the correct
application of names. Moreover, Hughey et al. (2014) have
demonstrated that entire plastid and mitochondrial genomes
can be sequenced from tiny amounts of type material, a
particularly appropriate application of NextGen sequencing,
Fig. 5. Photos of the different morphologies of Nothogenia fastigiata (a) and Taxon C (b), the only species to co-occur in Chile.
Lindstrom et al.: Cryptic diversity in Nothogenia 105
which utilizes short sequences of DNA, exactly the kind of
DNA present in type specimens 100 or more years old.
ACKNOWLEDGEMENTS
Robert J. Anderson, University of Cape Town, for providing
the specimen of Nothogenia erinacea; Max Hommersand,
University of North Carolina, for sharing specimens from
South Africa, Chile, the Falkland Islands and New Zealand
and for insightful discussions; Line Le Gall for the loan of
type material of Nothogenia fragilis in PC; Geoffrey Leister
for sharing fragments of historically relevant specimens for
sequencing; John Parnell for the loan of the type of
Chaetangium lingula in TCD; Mar´
ıa Elena Ram´
ırez for
discussions; Antony Kusabs and Jenn Dalen, Museum of
New Zealand Te Papa Tongarewa, for assistance with
specimens; Sarah Wilcox and the Our Far South expedition
for material collected in 2012; Pete McClelland of the New
Zealand Department of Conservation and the captain and
crew of the HMNZS Otago for enabling W.A.N. to collect at
the subantarctic islands; Di Morris (Department of Conser-
vation) for field assistance; and Michael J. Wynne for help
with literature. Financial support for sequencing was
provided by the NaGISA programme of the Census of
Marine Life and by Emilie D. Lindstrom. Funding to
E.C.M. was provided by FONDECYT-CONICYT
11110437. Funding to W.A.N. from NIWA was provided
under the Coasts & Oceans Research Programme 2, Marine
Biological Resources (COBR1401).
SUPPLEMENTARY DATA
Supplementary data associated with this article can be found
online at http://dx.doi.org/14–077.1.s1.
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108 Phycologia, Vol. 54 (2)
... Nothogenia currently contains 10 species that are distributed only in the southern hemisphere (Guiry & Guiry 2020). It is one of only a few genera in red algae where all known species have been sequenced (Lindstrom et al. 2015). N. fastigiata, described based on material from the Falkland Islands, was reported in Peru by Montagne (1852) and Acleto (1973). ...
... Our specimens (Fig. 7E-H) agreed with these reports of N. fastigiata. Based on a short rbcL sequence (102 bp in length) from the type material of N. fastigiata, Lindstrom et al. (2015) concluded that the name N. fastigiata had been widely applied and resurrected the species N. chilensis, N. lingula, and N. variolosa (Montagne) Montagne. Currently, N. fastigiata seemed to have a more restricted distribution limited to the Falkland Islands, southern Chile from Corral (near valdivia) to the Strait of Magellan, and Campbell Island (southern New Zealand). ...
... Currently, N. fastigiata seemed to have a more restricted distribution limited to the Falkland Islands, southern Chile from Corral (near valdivia) to the Strait of Magellan, and Campbell Island (southern New Zealand). Our finding of N. chilensis on the Peruvian coast confirms the hypothesis that the distribution of N. fastigiata starts at 40 ° latitude (Lindstrom et al. 2015), whereas N. chilensis seems to be distributed from northern Peru (Yacila) to central Chile (Pichilemu). ...
Article
In Peru, an ongoing project has been to document the marine macroalgal biodiversity using molecular approaches because, to date, the Peruvian marine flora has been mostly characterized on the basis of morphological observations. We herein report on red algae collected along the coast of Peru, including specimens collected at historically important collecting sites, in order to provide a better understanding of Peruvian red algal diversity. Using phylogenetic analysis of rbcL DNA sequences, we report for the first time the occurrence of Nothogenia chilensis, Porphyra mumfordii, and Schizymenia dubyi in Peru. Results from molecular and morphological analysis of topotype material show that Chondracanthus glomeratus (M.Howe) Guiry is conspecific with C. chamissoi (C.Agardh) Kützing. Both Rhodymenia howeana E.Y.Dawson and R. multidigitata E.Y.Dawson, Acleto & Foldvik are proposed to be later taxonomic synonyms of R. corallina (Bory) Greville. Future studies will reveal more diversity of red algae from Peru with special emphasis on members of the family Bangiaceae, Delesseriaceae, and Lithophyllaceae.
... The pattern of a morphologically simple group of organisms masking considerable genetic diversity and species richness is not unique to the Thoreales, especially within the red algae. In particular, red algal studies using the cox1 barcode region in concert with other genes continue to uncover cryptic diversity and undescribed species (i.e., Salomaki et al. 2014, Lindstrom et al. 2015, Filloramo and Saunders 2016. Lindstrom et al. (2015) showed with DNA sequence data that there were eight distinct species were under the name Nothogenia fastigiata. ...
... In particular, red algal studies using the cox1 barcode region in concert with other genes continue to uncover cryptic diversity and undescribed species (i.e., Salomaki et al. 2014, Lindstrom et al. 2015, Filloramo and Saunders 2016. Lindstrom et al. (2015) showed with DNA sequence data that there were eight distinct species were under the name Nothogenia fastigiata. ...
Article
The freshwater red algal order Thoreales has triphasic life history composed of a diminutive diploid ‘Chantransia’ stage, a distinctive macroscopic gametophyte with multi-axial growth and carposporophytes that develop on the gametophyte thallus. This order is comprised of two genera, Thorea and Nemalionopsis. Thorea has been widely reported with numerous species, whereas Nemalionopsis has been more rarely observed with only a few species described. DNA sequences from three loci (rbcL, cox1 and LSU) were used to examine the phylogenetic affinity of specimens collected from geographically distant locations including North America, South America, Europe, Pacific Islands, Southeast Asia, China and India. Sixteen species of Thorea and two species of Nemalionopsis were recognized. Morphological observations confirmed the distinctness of the two genera and also provided some characters to distinguish species. However, many of the collections were in ‘Chantransia’ stage rather than gametophyte stage, meaning that key diagnostic morphological characters were unavailable. Three new species are proposed primarily based on the DNA sequence data generated in this study, Thorea kokosinga-pueschelii, T. mauitukitukii and T. quisqueyana. In addition to these newly described species, one DNA sequence from GenBank was not closely associated with other Thorea clades and may represent further diversity in the genus. Two species in Nemalionopsis are recognized, N. shawii and N. parkeri nom. et stat. nov. Thorea harbors more diversity than had been recognized by morphological data alone. Distribution data indicated that Nemalionopsis is common in the Pacific region, whereas Thorea is more globally distributed. Most species of Thorea have a regional distribution, but T. hispida appears to be cosmopolitan.
... Several recent studies have leveraged sequence data from historical specimens to address biological questions that could not be addressed as adequately, or at all, without historical specimens. For example, investigations into historical population genomics (Bi et al. 2013) and phylogenetic placement of enigmatic lineages , testing phylogeographic hypotheses for conservation (Carmi et al. 2016) and delimitating cryptic species and confirming their taxonomic status (Hind et al. 2015;Lindstrom et al. 2015;McCormack et al. 2015) have all been bolstered or made possible through sequencing historical specimens. ...
... For example, rare or difficult-to-collect specimens have added invaluable data that affected the ecological conservation status of species (Wandeler et al. 2007;Carmi et al. 2016). Sequencing nomenclatural types (the name bearers of a scientific name), and placing them into species delimited using fresh specimens, may be necessary to establish to which species a name belongs (Hind et al. 2015;Lindstrom et al. 2015;Mutanen et al. 2015). (The latter happens to be the nature of research that inspired our study.) ...
Article
Despite advances that allow DNA sequencing of old museum specimens, sequencing small-bodied, historical specimens can be challenging and unreliable as many contain only small amounts of fragmented DNA. Dependable methods to sequence such specimens are especially critical if the specimens are unique. We attempt to sequence small-bodied (3-6 mm) historical specimens (including nomenclatural types) of beetles that have been housed, dried, in museums for 58-159 years, and for which few or no suitable replacement specimens exist. To better understand ideal approaches of sample preparation and produce preparation guidelines, we compared different library preparation protocols using low amounts of input DNA (1-10 ng). We also explored low-cost optimizations designed to improve library preparation efficiency and sequencing success of historical specimens with minimal DNA, such as enzymatic repair of DNA. We report successful sample preparation and sequencing for all historical specimens despite our low-input DNA approach. We provide a list of guidelines related to DNA repair, bead handling, reducing adapter dimers, and library amplification. We present these guidelines to facilitate more economical use of valuable DNA, and enable more consistent results in projects that aim to sequence challenging, irreplaceable historical specimens. This article is protected by copyright. All rights reserved.
... Nothogenia variolosa (Montagne) Montagne which is restricted to the New Zealand subantarctic, and N. fastigiata (Bory) P.G. Parkinson which is found in Campbell Island, the southernmost island in the New Zealand subantarctic group as well as southern Chile and the Falkland Islands (Lindstrom et al. 2015); Glaphyrosiphon aucklandica (Montagne) W.A. Nelson, S.Y. Kim & S.M. Boo from Auckland and Campbell Islands in New Zealand which is more closely related to G. chilensis (found from Valdivia to Punta Arenas (39-53°S) than to the two 'mainland' New Zealand species in this genus . ...
Article
Gigartina species are very common and abundant on intertidal rocky shores in New Zealand but members of this genus and the family Gigartinaceae are still not fully documented. A well-known species, distributed as No. 164 of the Lindauer Nova-Zelandicae Exsiccatae, were labelled by Lindauer as Gigartina tuberculosa from material collected in Stewart Island. However, Gigartina tuberculosa (as Chondrus tuberculosus) was described based on specimens collected from the New Zealand subantarctic Auckland Island. Later, material from the Strait of Magellan was referred to this species. In 1993, Gigartina tuberculosa was transferred to Iridaea tuberculosa with its distribution considered to be Chile, Cape Horn, Antarctica, Falklands Islands, Tristan da Cunha, Gough Island and the Campbell Plateau. The species distributed by Lindauer is here described as Gigartina falshawiae sp. nov. These species can be differentiated morphologically: G. falshawiae has thalli that are forked, somewhat irregular and form bushy clumps, with proliferations at the margins and on the blades, and with cystocarps surrounded by lobes, whereas thalli of Iridaea tuberculosa are fan-shaped, lack proliferations, and have globose cystocarps. The distributional ranges of these species also differ: G. falshawiae is found on Stewart Island and I. tuberculosa on the New Zealand subantarctic islands (recorded from the Antipodes, Auckland and Campbell Islands), while the species co-occur on the Snares Islands.
... were aligned with MAFFT (Katoh and Standley 2013) and analyzed using RAxML executed in Trex-online (Boc and Makarenkov 2012) with the GTR + gamma model and 1,000 bootstraps. Bayesian analysis was executed with MrBayes v3.2.1 (Ronquist et al. 2012) using the search parameters described in Lindstrom et al. (2015). The trees were visualized with TreeDyn 198.3 at Phylogeny.fr ...
Article
Molecular surveys are leading to the discovery of many new cryptic species of marine algae. This is particularly true for red algal intertidal species, which exhibit a high degree of morphological convergence. DNA sequencing of recent collections of Gelidium along the coast of California, USA, identified two morphologically similar entities that differed in DNA sequence from existing species. To characterize the two new species of Gelidium and to determine their evolutionary relationships to other known taxa, phylogenomic, multigene analyses, and morphological observations were performed. Three complete mitogenomes and five plastid genomes were deciphered, including those from the new species candidates and the type materials of two closely related congeners. The mitogenomes contained 45 genes and had similar lengths (24,963 to 24,964 bp). The plastid genomes contained 232 genes and were roughly similar in size (175,499 to 177,099 bp). The organellar genomes showed a high level of gene synteny. The two Gelidium species are diminutive, turf forming, and superficially resemble several long established species from the Pacific Ocean. The phylogenomic analysis, multigene phylogeny, and morphological evidence confirms the recognition and naming of two new species, describe herein as G. gabrielsonii and G. kathyanniae. On the basis of the monophyly of G. coulteri, G. gabrielsonii, G. galapagense, and G. kathyanniae, we suggest that this lineage likely evolved in California. Organellar genomes provide a powerful tool for discovering cryptic intertidal species and they continue to improve our understanding of the evolutionary biology of red algae and the systematics of the Gelidiales. This article is protected by copyright. All rights reserved.
... ;Hayden et al., 2003;Gabrielson, 2008aGabrielson, , 2008bSaunders & McDevit, 2012;Hind et al., 2014;Sissini et al., 2014;Hernandez-Kantun et al., 2015;Lindstrom et al., 2015;Vieira et al., 2016). The biggest challenges with this approach are to deal with the highly fragmented and tiny quantities of DNA preserved in type Box 3: Bioinformatics for species delimitation ...
Article
In recent years, the use of molecular data in algal systematics has increased as high-throughput sequencing (HTS) has become more accessible, generating very large datasets at a reasonable cost. In this perspectives paper, our goal is to describe how HTS technologies can advance algal systematics. Following an introduction to some common HTS technologies, we discuss how metabarcoding can accelerate algal species discovery. We show how various HTS methods can be applied to generate datasets for accurate species delimitation, and how HTS can be applied to historical type specimens to assist the nomenclature process. Finally, we discuss how HTS data such as organellar genomes and transcriptomes can be used to construct well-resolved phylogenies, leading to a stable and natural classification of algal groups. We include examples of bioinformatic workflows that may be applied to process data for each purpose, along with common programs used to achieve each step. We also discuss possible strategies and the new skill set that will be required to fully embrace HTS as a part of algal systematics, along with considerations of cost and experimental design. HTS technology has revolutionized many fields in biology, and will certainly do the same in algal systematics.
Article
Full-text available
Conceived as a baseline for the management and conservation of the marine protected area of the French Southern Territories (réserve naturelle nationale des Terres australes françaises), the checklist of marine macroalgae of the Kerguelen Islands was updated based on an extensive review of the literature and scientific databases, from the first report of the Ross expedition, in 1840, to the most recent works. This work was also conceived as a starting point for forthcoming investigations using molecular systematics tools and for monitoring the effects of global change on sub-Antarctic marine ecosystems. After a brief history of scientific campaigns, a list of 166 species was established (103 Rhodophyta, 35 Chlorophyta and 28 Ochrophyta [Phaeophyceae]). Molecular systematics studiess have shown the existence of recurrent discrepancies between the established, morphology-based taxonomy and molecular species delimitation, calling for a revision of systematics. Nevertheless, a first analysis of biogeographical affinities of the marine flora of the Kerguelen Islands is carried out and preliminary results are partially congruent with the main regions currently recognized in the Southern Ocean suggesting the importance of long-distance dispersal to explain the observed distribution patterns.
Article
A partial rbcL sequence of the lectotype specimen of Corallina berteroi shows that it is the earliest available name for C. ferreyrae. Multilocus species delimitation analyses (ABGD, SPN, GMYC, bPTP and BPP) using independent or concatenated COI, psbA and rbcL sequences recognized one, two or three species in this complex, but only with weak support for each species hypothesis. Conservatively, we recognize a single worldwide species in this complex of what appears to be multiple, evolving populations. Included in this species, besides C. ferreyrae, are C. caespitosa, the morphologically distinct C. melobesioides, and, based on a partial rbcL sequence of the holotype specimen, C. pinnatifolia. Corallina berteroi, not C. officinalis, is the cosmopolitan temperate species found thus far in the NE Atlantic, Mediterranean Sea, warm temperate NW Atlantic and NE Pacific, cold temperate SW Atlantic (Falkland Islands), cold and warm temperate SE Pacific, NW Pacific and southern Australia. Also proposed is C. yendoi sp. nov. from Hokkaido, Japan, which was recognized as distinct by 10 of the 13 species discrimination analyses, including the multilocus BPP.
Article
The current manuscript is the first in a series intended to publish accumulating DNA barcode data to make them accessible to the scientific community. Focused on 135 specimens of red algae from the remote islands of Tristan da Cunha, part of the British Overseas Territory of Saint Helena, Ascension and Tristan da Cunha, the 47 (possibly 48; see notes with Lophurella sp. 1Tris) genetic groups uncovered during this project are compared to the only detailed floristic work for this region completed by Baardseth in 1941. A number of taxonomic anomalies are reported with indications for eventual solutions that await study of the type material of the associated morphospecies. Species previously assigned by Baardseth to the genus Epymenia Kützing are formally transferred to Rhodymenia Greville as R. elongata (Baardseth), comb. nov., (including E. marginifera Baardseth) and R. flabellata (Baardseth), comb. nov. A number of range extensions are reported including species such as Ceramium secundatum (Lyngbye) C.Agardh, Colaconema caespitosum (J.Agardh) Jackelman, Stegenga & J.J.Bolton, Helminthocladia calvadosii (J.V.Lamour. ex Duby) Setch. and Porphyra mumfordii S.C.Lindstrom & K.M.Cole, which have likely been distributed by human activities. We also note that the sporophyte of the supposedly narrowly distributed Schimmelmannia elegans has been collected from both British Columbia, Canada, and Queensland, Australia, consistent with other observations that sporophytes of red algal species with alternations of heteromorphic generations are commonly more broadly distributed than the gametophytic stage. This species, although originally described by Baardseth from these mid Atlantic islands, may also be introduced.
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Rafting on floating seaweeds facilitates dispersal of associated organisms, but there is little information on how rafting affects the genetic structure of epiphytic seaweeds. Previous studies indicate a high presence of seaweeds from the genus Gelidium attached to floating bull kelp Durvillaea antarctica (Chamisso) Hariot. Herein, we analyzed the phylogeographic patterns of Gelidium lingulatum (Kützing 1868) and G. rex (Santelices and Abbott 1985), species that are partially co-distributed along the Chilean coast (28°S-42°S). A total of 319 individuals from G. lingulatum and 179 from G. rex (20 and 11 benthic localities, respectively) were characterized using a mitochondrial marker (COI) and, for a subset, using a chloroplastic marker (rbcL). Gelidium lingulatum had higher genetic diversity, but its genetic structure did not follow a clear geographic pattern, while G. rex had less genetic diversity with a shallow genetic structure and a phylogeographic break coinciding with the phylogeographic discontinuity described for this region (29°S-33°S). In G. lingulatum, no isolation-by-distance was observed, in contrast to G. rex. The phylogeographic pattern of G. lingulatum could be explained mainly by rafting dispersal as an epiphyte of D. antarctica, although other mechanisms cannot be completely ruled out (e.g. human-mediated dispersal). The contrasting pattern observed in G. rex could be attributed to other factors such as intertidal distribution (i.e. G. rex occurs in the lower zone compared to G. lingulatum) or differential efficiency of recruitment after long-distance dispersal. This study indicates that rafting dispersal, in conjunction with the intertidal distribution, can modulate the phylogeographic patterns of seaweeds.
Article
A new genus, Glaphyrosiphon Hommersand & Leister gen. nov., is proposed to contain the generitype Glaphyrosiphon intestinalis (Harvey) Leister & W.A. Nelson comb. nov., a species known in New Zealand under the name Grateloupia intestinalis (Hooker. f. & Harvey) Setchell ex P.G. Parkinson, and two additional species: Glaphyrosiphon lindaueri W.A. Nelson & P.W. Gabrielson sp. not,. from the northern part of New Zealand and Glaphyrosiphon chilensis M.E. Ramirez, Leister, and P.W. Gabrielson sp. nov. in the southern part of Chile from Valdivia (Region de Los Rios), to Punta Arenas in the Strait of Magellan (Region de Magallanes). Thalli are borne singly or in clusters from a small discoid holdfast and consist of simple or one- to three-times-branched slippery tubes that are copiously filled with mucilage. The medulla consists of a one- to several-layered network inside the cortex composed of stellate cells that interconnect by short to long extensions linked by pit connections. Primary rhizoidal filaments are absent. Spermatangia are superficial on terminal cortical cells. Carpogonial and auxiliary-cell ampullae are formed separately and link by unsegmented tubular connecting filaments, as in other Halymeniaceae. The auxiliary-cell ampulla consists of a basal cell and four unilaterally branched filaments in which the auxiliary cell is the basal cell of one of the four filaments. The auxiliary cell and inner ampullar filaments unite forming a fusion cell. Ampullar filaments connect terminally to inner cortical cells and laterally with one another by short filaments and pit connections that form an involucral network surrounding the gonimolobes. Tetrasporangia are cruciately divided and borne laterally on filaments produced secondarily from surface cortical cells. Sequence analyses of the rbcL gene place Glaphyrosiphon sister to Polyopes in the Halymeniaceae. The two New Zealand species consist of southern and northern clades separated by 1.2% to 1.7% base-pair distances in rbcL analyses and a Chilean species that forms a single clade separated from the New Zealand clades by 3.9% to 4.4% base-pair distances. Records of Grateloupia intestinally from Tasmania have not been studied.