Rhodophyta: A cornucopia of cryptic diversity
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.com anbollenessor.wordpress.com biogeodb.stri.si.edu www.notteesale.it www.reefcleaners.org www.aphotomarine.com c d e f
Transcript of Rhodophyta: A cornucopia of cryptic diversity
What Are the Red Algae? Nemaliophycidae
Rhodomeniophycidae
Rhodophyta: A cornucopia of cryptic diversityEric 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 classi�cation. 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.
CyanidiaceaeGaldieriaceae
PorphyridiaceaePhragmonemataceae
StylonemataceaeBoldiaceae
CompsopogonaceaeRhodochaetaceae
ErythrotrichiaceaeRhodellaceae
Bangiaceae
Rhodachlyaceae
Psilosiphonaceae
LemaneaceaeBatrachospermaceae
Thoreaceae
ColaconemataceaeAcrochaetiaceae
RhodothamniellaceaeRhodophysemataceaePalmariaceae
Scinaiaceae
LiagoraceaeGalaxauraceae
BalbianiaceaeBalliaceae
RhodogorgonaceaeSporolithaceae
HapalidiaceaeCorallinaceae
AhnfeltiaceaePihiellaceae
Atractophora
Acrosymphytaceae
CalosiphoniaceaeInkyuleeaceae
NaccariaceaeBonnemaisoniaceae
Cruoriaceae
PolyideaceaeGainiaceae
DumontiaceaeRhizophyllidaceae
Kallymeniaceae
SphaerococcaceaeNizymeniaceaePhacelocarpaceae
GloiosiphoniaceaeEndocladiaceae
Haemeschariaceae
PhyllophoraceaeGigartinaceae
FurcellariaceaeTichocarpaceae
AcrotylaceaeMychodeophyllaceae
Mychodeaceae
CallophycusAreschougiaceae
CubiculosporaceaeSchmitziellaceae
Solieriaceae
DicranemataceaeCaulacanthaceae
Cystocloniaceae
SarcodiaceaePlocamiaceae
SchizymeniaceaeNemastomataceae
TsengiaceaeHalymeniaceae
SebdeniaceaeRhodymeniaceae
HymenocladiaceaeFryellaceae
ChampiaceaeFaucheaceae
Lomentariaceae
Peyssonneliaceae
PterocladiaceaeGelidiaceae
Gelidiellaceae
GracilariaceaePterocladiophilaceae
SpyridiaceaeCeramiaceae
CallithamniaceaeWrangeliaceae: Ptiloteae
Wrangeliaceae: GriffithsieaeDelesseriaceae: Nitophylloideae
Delesseriaceae: PhycodryoideaeDasyaceae: Heterosiphonia group
CaloglossaDasyaceae: Dasya group
Delesseriaceae: DelesserioideaeRhodomelaceae
Sarcomeniaceae
Hildenbrandiaceae
0.2 subst/site
Nemaliophycidae
StylonematophyceaePorphyridiophyceae
Cyanidiophyceae
Compsopogonophyceae
RhodellophyceaeBangiophyceae
Hildenbrandiophycidae
Corallinophycidae
Ahnfeltiophycidae
Rhodymenio-phycidae
Palmariales
AcrochaetialesColaconematales
Nemaliales
BallialesBalbianialesRhodachlyales
Thoreales
Batrachospermales
Corallinales
RhodogorgonalesPihiellalesAhnfeltiales
Gigartinales
Ceramiales
Ceramiales
GracilarialesGigartinales
Gelidiales
Acrosymphytales
Rhodymeniales
Sebdeniales
Halymeniales
Nematostomatales
Plocamiales
Gigartinales
Bonnemaisoniales
Gigartinales
Florideo-phyceae
Cyanidiales
Bangiales
CompsopogonalesRhodochaetalesErythropeltidales
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 | 1.00100 | 1.00
100 | 1.0060 | 0.98
57 | 0.9993 | 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 | 1.0082 | 1.00
– | 0.98
100 | 1.00
64 | 0.99
100 | 1.00
– | 0.98
– | 1.00
– | 0.98
– | 1.00
70 | 1.00100 | 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 de�ning morphological characteristicsfrom 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
ConspecificsConvergent 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 classi�ed based on morphology. The morphological classi�cation often re�ects 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 identi�es 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 classi�ed 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 Classi�cation• 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 �laments (c) to having a complex thallus (d), and with (e) or without calci�cation (f ).
a b microscopesandmonsters.comanbollenessor.wordpress.com
biogeodb.stri.si.edu www.notteesale.it
www.reefcleaners.org www.aphotomarine.com
c d
e f
