More questions:
•What are the closest relatives of the Trentepohliales?
•Is the order Trentepohliales a monophyletic group?
•What evolutionary processes have occurred within the
Trentepohliales?
• Two lineages in Viridiplantae
•Trentepohlialean taxa are
unequivocally within the
chlorophycean lineage
• The order Trentepohliales is
included within the
ulvophycean taxa
• The order Trentepohliales is
a monophyletic group
• Phragmoplast?
Relationships within the Ulvophyceae
• The marine orders are the most
closely related to the
Trentepohliales
In all phylogenetic analyses the
Trentepohliales emerged as a sister
group to the clade containing the
Siphonocladales/Cladophorales
complex and Dasycladales, both
containing representatives mainly
from the marine environment!
Relationships within the Trentepohliaceae
•What about the relationships inside of the family?
•Are the genera monophyletic?
•Is the species Cephaleuros virescens, with a world-wide
distribution, a monophyletic taxon?
•What is the validity of several morphological characters
used for separation at species and genus level?
Relationships within the Trentepohliaceae
Four main lineages in 18S rDNA:
 Cephaleuros clade
 Printzina lagenifera clade
 Trentepohlia aurea clade (the
generitype)
 Trentepohlia iolithus clade
Molecular data challenge traditional
classification schemes
Relationships among Trentepohlialean genera
On the basis of our results,
Cephaleuros forms a welldefined monophyletic group,
representing a more advanced
clade
Conversely, Trentepohlia is non
monophyletic and the other
genera included in the analyses
do not represent separate
lineages, suggesting the
possibility that a major
rearrangement at the genus level
may be necessary in the future
Printzina was proposed as a new
genus for nine species previously
belonging to Trentepohlia
The shape of the sporangia, the
arrangement of the sporangiatelaterals, the extensive development of
the prostrate parts of the thallus and
the occurrence in shaded habitats were
considered the key characters
separating Printzina from
Trentepohlia
The only feature that separates
conclusively the two genera is the
shape of the sporangia
•globular to reniform in Printzina
•ovoid in Trentepohlia)
The position of Phycopeltis is
surprising
Importance of the position of the
ostiole in the zoosporangium as key
character
T. umbrina (as P. umbrina) with an
ostiole opposite to the end of
attachment too
T. abietina from Hawaii shows the
ostiole clearly opposite to the end of
attachment
Our results provide therefore some
evidence that the position of the
ostiole may be a good phylogenetic
marker
Relationships within a species: Cephaleuros virescens
•Cephaleuros virescens Kunze, the generitype of Cephaleuros, is generally
considered to have a worldwide distribution in tropical and subtropical regions
•Strains of C. virescens do not form a monophyletic group; South Africa and Taiwan
are more closely related to C. parasiticus than to other C. virescens
Current analyses using the
chloroplast-encoded rbcL marker
confirm 18SSU results
*
•These data suggest that the circumscription of C. virescens should be reconsidered
•Morphological characters used to separate this species form similar taxa should be reassessed
•As currently circumscribed, C. virescens represents a complex of morphologically similar
entities
•Suriname is the type locality of C. virescens, the actual distribution of this species might be
restricted to tropical South and Central America
Lessons learned
 A subaerial habit has developed within the class Ulvophyceae
 Morphological criteria traditionally used for the circumscription of genera and
species of Trentepohliales are not correlated with evolutionary patterns
 Common and world-wide distributed species may represent a species complex
of morphologically similar entities (cryptic species)
 Many morphological characters used in taxonomy are not phylogenetically
relevant
 Another subaerial lineage has been found from a group containing
representatives mainly from the marine environment
Evolution of the subaerial flora
From textbooks to popular articles there is an appreciation that
terrestrial life emerged from the seas. And there is generally no
explanation that by “seas” is meant from oceans and lakes – that is,
from both marine and freshwater sources
Several representatives of the marine green algal class Ulvophyceae have
been found to be members of the terrestrial algal flora
The order Trentepohliales and our newly described taxa are examples of a
direct marine invasion of terrestrial environments!
This is in contrast with the general idea that terrestrial floras are
descendents of freshwater ancestors and not directly from marine ancestors
A direct marine invasion?
One intriguing, even puzzling, question is:
How marine algae, from ulvophycean ancestors, “jump” into
terrestrial habitats and became permanent representatives of the
land flora?
A probable answer may came from independent bits of
information:
• Fossils
• Ancient changes of sea level
• Pre-adaptive phenotypic plasticity
Fossil subaerial microchlorophytes
Records of fossils belonging to terrestrial microchlorophytes have been found as
early as the late Eocene (ca. 50 mya)
Reynolds and Dilcher 1984
As Cephaleuros parasiticus
Re-described as an alga
Later transfer to C. villosus
By Thompson & Wujek 1997
Dilcher 1965
As Pelicothallus villosus
Described as a fungus
Fossil trentepohlialean taxa have been
reported from the German Eocene
Trentepohlia aurea
Trentepohlia diffusa
Koeck 1939: Fossilie Kryptogamen aus der eocanean Barunkohle des
Geiseltales. Nova Acta Leopoldina 6:333-351
Printz 1939: Vorarbeiten zu einer Monographie der Trentepohliaceen.S. Nytt Mag.
Aturvidenskapene B. 80:137-210, Taf.I-XXXII
Trentepohlia aurea var. acutata
Trentepohlia rigidula
Koeck 1939: Fossilie Kryptogamen aus der eocanean Barunkohle des
Geiseltales. Nova Acta Leopoldina 6:333-351
Printz 1939: Vorarbeiten zu einer Monographie der Trentepohliaceen.S. Nytt Mag.
Aturvidenskapene B. 80:137-210, Taf.I-XXXII
Reliable fossil records established trentepohlialean
floras as far as the Eocene 50 mya
By the end of this epoch:
 Continents moved closer to their present
position
 Tropical areas shrinking
 A drying period commences
 In subtropical latitudes, open woodlands with
ferns and shrubby plants replaced forests
 Whale ancestors left the land
 Trentepohlialean taxa appeared on land over 400
my after the initial colonization of land plants in
the Paleozoic (480 mya)
http://3dparks.wr.usgs.gov/
Ancient sea level changes
•Just before Eocene (50
mya) the sea level was at
the highest and since then
it has been receding
•Much of continental
North America, Africa and
Australia were exposed
Falkowsky et al. 2004; sea level change
Evolution of floras such as
• Diatoms
• Grasses
Falkowsky et al. 2004; sea level change
Pre-adaptive phenotypic plasticity
• Intertidal marine algae live in a variable environment under great physical
stress
• This may lead to a selection for a “plastic morphology” were the same
genotype is expressing several morphologies under different ecological
conditions
• Extant ulvophyceans are examples of this adaptive phenotypic plasticity:
Terrestrial ulvophytes express this adaptive phenotypic plasticity by
their ecological ubiquity, ability to grow in several media, and their
astonishing capacity to undergo morphological modifications:
Printzina
Trentepohlia
Cephaleuros
Phycopeltis
Information from fossils, ancient sea level changes, phenotypic
plasticity and molecular data seem to indicate that:
• Terrestrial ulvophytes did not “jump” from marine to
terrestrial habitats: they were “left behind” after sea levels
receded during the Eocene
• Ancestors of terrestrial ulvophytes may had the pre-adaptive
capabilities to exploit and diversify in the new habitat and
become permanent members of the subaerial flora
Many questions still remain to be answered, for example:
•Exclusively subaerial algae have a long evolutionary history compared to other green algal
orders; however, their fossil evidence is relatively more recent; what is the evolutionary
history of this lineage between their ancestral marine origin and their transition to land?
Yakutina and Dasyclads
Cambrian
600 mya
Cladophora-like
Precambrian
700-800 mya
Trentepohliales
Eocene
50 mya
Many questions still remain to be answered, for example:
•Exclusively subaerial algae have a long evolutionary history compared to other green algal
orders; however, their fossil evidence is relatively more recent; what is the evolutionary
history of this lineage between their ancestral marine origin and their transition to land?
•Another intriguing question is about evolutionary reversals: are there any examples of
algae that originated in the continental environment and made a transition back to the sea?
Trebouxiophyceae: Stichococcus marinus?
Chlorophyceae: Dunaliella spp. ?
Trebouxiophyceae: marine Prasiolales (Prasiola and Rosenvingiella)
Some conclusions
 The terrestrial habitat has been colonized by several lineages and more than
one green algal group
 The Charophycean, Trebouxiophycean and Chlorophycean algae made
attempts to colonize the Land via freshwater habitats
 The marine Ulvophycean taxa also made this conquest (at least twice)
 Subaerial ulvophytes conquered the land using a direct strategy
 The history of the conquest of terrestrial habitats by algae is more complex
than previously recognized
 New molecular techniques (environmental cloning and phylogenomics) may
unravel more unknown lineages and unexpected discoveries!
Acknowledgments
Russell L. Chapman, Scripps Institution of Oceanography
Mike Guiry, National University of Ireland
Paul Broady, University of Canterbury, New Zealand
Thomas Friedl, University of Goettingen
Fred Brooks, American Samoa Community College
Alison Sherwood, University of Hawai’i at Mãnoa
Joe Zuccarello, Victoria University of Wellington, NZ
Bruno De Reviers, Paris Herbarium
Ricardo Tsukamoto, Sao Paulo, BZ
Jirí Neustupa, Charles University of Prague, Czech Republic
Drs. Fabio Rindi and Sarah M. Noble, graduate students Daryl W. Lam and Haj A. Allali,
several undergrads
Research at the Phycolab is funded by grants from NSF Systematics-DEB, NEP, MASGC,
CA&S/UA and from a RAC/UA to JLB
Fieldwork funds to French Guiana, South Africa, Gabon, Panama, Suriname, Europe, and
Southern Mexico partially provided by the Graduate School and the Department of
Biological Sciences at UA
The PhycoLab in the Web
http://bama.ua.edu/~jlopez
Ongoing Research at the PhycoLab
Subaerial microchlorophytes
Europe
Southeastern USA
Panama
Morocco
Gabon
Suriname
French Guiana
South Africa
and Australia
Assembling the Tree of Life Program:
UA – CUBA Seaweed research
collaboration
Lidice Clero, CIM
Dr. Ana Maria Suarez
Inst. Marine Sciences
University of La Havana
M. Sc. Ruben Cabrera
Marine Archeology
Yusimi Alfonso, Acuario
Nacional
Mayrene Guimaraes,
Cayo Coco
Antonio Vega, Holguin
Sandra Siret, Matanzas
Abdiel Jover, Santiago
Angel Moreira, Cienfuegos
Dr. Beatriz Martinez
Oceanology Institute, CITMA
Juan J. Lake, Camaguey
Ivan Martin, Villaclara