Poster presented at the first EukRef workshop (Vancouver 2015)

1. What Are the Red Algae? Nemaliophycidae
Rhodomeniophycidae
Rhodophyta: A cornucopia of cryptic diversity
Eric D. Salomaki, Christopher E. Lane
Department of Biological Sciences, University of Rhode Island, Kingston RI, USA
Figure 3. This phylogeny from Verbruggen et al. 2010 contains the most recent
comprehensive Rhodophyte taxonomic classification. Coloration of the branches
shows statistical support of the clades with black being well supported and orange
indicating weak support. Maximum likelihood bootstrap support and Bayesian
posterior probabilities are listed at the nodes.
Cyanidiaceae
Galdieriaceae
Porphyridiaceae
Phragmonemataceae
Stylonemataceae
Boldiaceae
Compsopogonaceae
Rhodochaetaceae
Erythrotrichiaceae
Rhodellaceae
Bangiaceae
Rhodachlyaceae
Psilosiphonaceae
Lemaneaceae
Batrachospermaceae
Thoreaceae
Colaconemataceae
Acrochaetiaceae
Rhodothamniellaceae
Rhodophysemataceae
Palmariaceae
Scinaiaceae
Liagoraceae
Galaxauraceae
Balbianiaceae
Balliaceae
Rhodogorgonaceae
Sporolithaceae
Hapalidiaceae
Corallinaceae
Ahnfeltiaceae
Pihiellaceae
Atractophora
Acrosymphytaceae
Calosiphoniaceae
Inkyuleeaceae
Naccariaceae
Bonnemaisoniaceae
Cruoriaceae
Polyideaceae
Gainiaceae
Dumontiaceae
Rhizophyllidaceae
Kallymeniaceae
Sphaerococcaceae
Nizymeniaceae
Phacelocarpaceae
Gloiosiphoniaceae
Endocladiaceae
Haemeschariaceae
Phyllophoraceae
Gigartinaceae
Furcellariaceae
Tichocarpaceae
Acrotylaceae
Mychodeophyllaceae
Mychodeaceae
Callophycus
Areschougiaceae
Cubiculosporaceae
Schmitziellaceae
Solieriaceae
Dicranemataceae
Caulacanthaceae
Cystocloniaceae
Sarcodiaceae
Plocamiaceae
Schizymeniaceae
Nemastomataceae
Tsengiaceae
Halymeniaceae
Sebdeniaceae
Rhodymeniaceae
Hymenocladiaceae
Fryellaceae
Champiaceae
Faucheaceae
Lomentariaceae
Peyssonneliaceae
Pterocladiaceae
Gelidiaceae
Gelidiellaceae
Gracilariaceae
Pterocladiophilaceae
Spyridiaceae
Ceramiaceae
Callithamniaceae
Wrangeliaceae: Ptiloteae
Wrangeliaceae: Griffithsieae
Delesseriaceae: Nitophylloideae
Delesseriaceae: Phycodryoideae
Dasyaceae: Heterosiphonia group
Caloglossa
Dasyaceae: Dasya group
Delesseriaceae: Delesserioideae
Rhodomelaceae
Sarcomeniaceae
Hildenbrandiaceae
0.2 subst/site
Nemaliophycidae
Stylonematophyceae
Porphyridiophyceae
Cyanidiophyceae
Compsopogonophyceae
Rhodellophyceae
Bangiophyceae
Hildenbrandiophycidae
Corallinophycidae
Ahnfeltiophycidae
Rhodymenio-
phycidae
Palmariales
Acrochaetiales
Colaconematales
Nemaliales
Balliales
Balbianiales
Rhodachlyales
Thoreales
Batrachospermales
Corallinales
Rhodogorgonales
Pihiellales
Ahnfeltiales
Gigartinales
Ceramiales
Ceramiales
Gracilariales
Gigartinales
Gelidiales
Acrosymphytales
Rhodymeniales
Sebdeniales
Halymeniales
Nematostomatales
Plocamiales
Gigartinales
Bonnemaisoniales
Gigartinales
Florideo-
phyceae
Cyanidiales
Bangiales
Compsopogonales
Rhodochaetales
Erythropeltidales
Porphyridiales
Rhodellales
Stylonematales
A
B
C
99 | 1.00
100 | 1.00
93 | 1.00
100 | 1.00
55 | 0.99
– | –
– | –
96 | 1.00
– | –
– | 1.00
99 | 1.00
100 | 1.00
100 | 1.00
60 | 0.98
57 | 0.99
93 | 1.00
– | 0.99
68 | 1.00
– | –
100 | 1.00
57 | 0.97
100 | 1.00
100 | 1.00
100 | 1.00
– | 1.00
98 | 1.00
91 | 1.00
54 | –
100 | 1.00
– | –
100 | 1.00
100 | 1.00
93 | 1.00
58 | –
100 | 1.00
95 | 1.00
– | –
– | –
– | –
57 | –
– | –
– | –
– | –
– | 0.97
– | –
96 | 1.00
98 | 1.00
61 | –
– | –
– | –
– | –
99 | 1.00
86 | 1.00
– | 1.00
96 | 1.00
99 | 1.00
90 | 1.00
64 | 1.00
100 | 1.00
82 | 1.00
– | 0.98
100 | 1.00
64 | 0.99
100 | 1.00
– | 0.98
– | 1.00
– | 0.98
– | 1.00
70 | 1.00
100 | 1.00
– | –
100 | 1.00
– | –
– | –
86 | 1.00
– | –
63 | 0.97
86 | 1.00
50 | 0.99
67 | 1.00
79 | 1.00
97 | 1.00
59 | –
100 | 1.00
99 | 1.00
– | –
– | –
100 | 1.00
100 | 1.00
100 | 1.00
100 | 1.00
100 | 1.00
100 | 1.00
– | 1.00
100 | 1.00
D
E
bootstrap support in ML analysis
<50 60 70 80 90 100
Sporolithales
Table 1. Classes of Rhodophyta with major defining morphological characteristics
from Gantt et al. 2010.
Figure 2. Rhodophyte
phylogenetic hypothesis
from Saunders and
Hommersand 2004, based
on a compilation of
molecular studies. Putative
evolutionary scenarios for
type of Golgi association
(ER = exclusively ER; ERm =
ER and mitochondrial; NU
= nuclear) and presence vs.
absence of peripheral
encircling thylakoids (PT or
NPT respectively, or mix for
both)are mapped on the
tree
Conspecifics
Convergent morphologies
Conspecifics
a b
c
Evolutionary history of the lineage
Hypothetical species 1
Hypothetical species 3
Hypothetical species 2
Figure 1. Traditionally red algae have been classified
based on morphology. The morphological classification
often reflects molecular data (a), however, distantly
related species can develop similar morphologies (b) as
a result of convergent evolution. The use of molecular
data has been essential to recognizing these situations,
as well as cases where morphologically dissimilar
specimens are in fact the same species (c). Image
adapted from Cianciola et al. 2010.
Cianciola, E.N., Popolizio, T.R., Schneider, C.W. & Lane, C.E. 2010. Using molecular-assisted alpha taxonomy to better
understand red algal biodiversity in Bermuda. Diversity. 2:946–58.
Freshwater, D.W., Fredericq, S., Butler, B.S., Hommersand, M.H. & Chase, M.W. 1994. A gene phylogeny of the red algae
(Rhodophyta) based on plastid rbcL. Proc. Natl. Acad. Sci. U. S. A. 91:7281–5.
Gantt, E., Berg, G.M., Brodie, A., Chan, C.X.I.N., Collén, J., Jr, F.X.C., Gross, J. et al. 2010. Prophyra: Complex life histories in a
harsh environment: P. umbilicalis, an intertidal red alga for genomic analysis. In Seckbach, J. & Chapman, D. [Eds.] Red
Algae in the Genomic Age: Cellular Origin, Life in Extreme Habitats and Astrobiology. Springer-Verlag, pp. 112–29.
Saunders, G.W., Chiovitti, A. & Kraft, G.T. 2004. Small-subunit rDNA sequences from representatives of selected families
of the Gigartinales and Rhodymeniales (Rhodophyta). 3. Delineating the Gigartinales sensu stricto. Can. J. Bot. Can. Bot.
82:43–74.
Saunders, G.W. & Hommersand, M. 2004. Assessing red algal supraordinal diversity and taxonomy in the context of
contemporary systematic data. Am. J. Bot. 91:1494–507.
Verbruggen, H., Maggs, C. a, Saunders, G.W., Le Gall, L., Yoon, H.S. & De Clerck, O. 2010. Data mining approach identifies
research priorities and data requirements for resolving the red algal tree of life. BMC Evol. Biol. 10:16.
References
• The phylum Rhodophyta contains more than 6,000
described species that are classified into seven distinct
classes (Table 1)
• Primary endosymbiotic lineage estimated to have
diverged from its common ancestor with other primary
endosymbionts over 1 billion years ago
• Morphologically diverse (Table 1), ranging from
microscopic unicellular individuals to large and/or highly
branched multicellular specimens more than a meter in
length
• Predominately marine, though approximately 5% of
the species diversity is found in freshwater habitats
• Lacking flagella and centrioles throughout all stages of
their life history
• The red algal plastid contains the photosynthetic
pigments chlorophyll-a, phycocyanin, and phycoerythrin
which are located on phycobilisomes for light harvesting
Taxonomic Classification
• The traditional framework of red algal taxonomy was
based largely upon morphological characteristics
• The use of molecular tools for understanding red algal
biodiversity uncovered a plethora of phenotypic
plasticity and cryptic diversity (Figure 1)
• Much of the traditional morphological framework is
supported by molecular analyses, especially at the
higher taxonomic ranks (Figure 2)
• Molecular analyses have revealed non-monophyletic
orders and additional data for under-represented clades
is needed to resolve the evolutionary histories of many
red algal orders (Figure 3)
• Numerous unsuccessful attempts have been made to
resolve the phylogenetic relationships of orders within
the Nemaliophycidae (Figure 3 - Red).
• The Nemaliophycidae (Figure 2 - Lineage 2; Figure 3 -
Red) are a biologically diverse lineage of particular
interest for studying evolutionary transitions.
• Of the 10 orders in Nemaliophycidae, 6 are strictly
marine, 3 are strictly freshwater, and species from the
last order are found in either habitat (Figure 4, a & b)
• Species are morphologically diverse (Figure 4, c-f),
and can be found to maintain the typical Florideophyte
triphasic life cycle, or a biphasic or monophasic life
history.
• Despite low support values for several deep nodes in
the Florideophyceae, molecular data has revealed that
two orders within the Rhodomeniophycidae (Figure 3 -
Grey) are non-monophyletic.
• The Ceramiales comprise two distinct polyphyletic
clades (Figure 3 - Green)
• The Gigartinales resolve as polyphyletic since the
earliest molecular based studies (Freshwater et al.
1994). To date, additional 18S data from all families in
the Gigartinales have been unsuccessful at recovering a
monophyletic order (Saunders et al. 2004)
Figure 4. Images depicting morphological diversity in
the Nemaliophycidae. Species are found in both marine
(a) and freshwater habitats (b). Members can range
from being simple filaments (c) to having a complex
thallus (d), and with (e) or without calcification (f).
a b microscopesandmonsters.comanbollenessor.wordpress.com
biogeodb.stri.si.edu www.notteesale.it
www.reefcleaners.org www.aphotomarine.com
c d
e f