Estimation of divergence times in the volvocine algae
Matthew D. Herron, Jeremiah D. Hackett, Frank Aylward, and Richard E. Michod
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA
INTRODUCTION
MATERIALS AND METHODS
Phylogenetic reconstruction of red algae, green algae, and land plants using Bayesian
Markov Chain Monte Carlo methods in MrBayes.
The volvocine green algae (Volvox and its close relatives) are an important
model system for the evolution of multicellularity and cellular differentiation.
Three chloroplast genes: P700 chlorophyll a-apoprotein A1 (psaA), P700 chlorophyll aapoprotein A2 (psaB), and photosystem II CP43 apoprotein (psbC) partitioned by
codon.
The evolutionary transition from single cells to completely differentiated
multicellular individuals can be describe as a series of small steps, many
represented in extant volvocine algae (Kirk 2005).
One nuclear gene: small ribosomal subunit (SSU).
Divergence times estimated using Langley-Fitch (local molecular clock method; LF), nonparametric rate smoothing (NPRS), and penalized likelihood (PL) in r8s (Figure 1).
Reconstructing the history of these changes allows us to describe an increase
in the level of complexity within a gradualist framework.
Sample of 300 posterior trees.
Multiple fossil calibrations (see inset, Figure 1).
Rausch et al. (1989) estimated the divergence of colonial volvocine algae from
unicellular relatives at 50-75 MYA using nuclear genes; these estimates
assume a constant substitution rate across lineages.
Analyses evaluated by fossil cross-validation.
Divergences within the volvocine algae estimated using LF (Figure 2).
Sample of 300 posterior trees from the five chloroplast gene analysis of Herron &
Michod (2008).
We used multiple genes with multiple fossil calibrations to estimate divergence
times among unicellular and colonial volvocine algae.
Beta subunit of ATP synthase (atpB), large subunit of Rubisco (rbcL), psaA, psaB, and
psbC, partitioned by codon.
RESULTS
Compsopogon coeruleus
1
Rhodella violacea
Porphyra yezoensis
Gracilaria tenuistipitata
Rhodophyta
Porphyridium aeruginium
Tetrabaenaceae
0.97
8
9
Palmaria palmata
2
5
6
Chaetosphaeridium globosum
Psilotum nudum
3
Pinus
4
Nymphaea / Cabomba
5
Streptophyta
Marchantia polymorpha
7
2
0.84
1
3
4
Arabidopsis thaliana
6
0.96
Goniacaceae
0.88
Mesostigma viride
9
10
Euvolvox
8
0.88
Triticum aestivum
0.67
Ostreococcus tauri
Chlorella vulgaris
7
8
Oltmannsiellopsis viridis
8
Stigeoclonium helveticum
Paulschulzia pseudovolvox
Fossil calibrations from Yoon et al. (2004), Berney &
Pawlowski (2006):
1. 1174-1222 MYA for Bangiomorpha (red alga)
2. 596-603 MYA for Florideophyte red algae
3. 432-476 MYA for first land plants
4. 355-370 MYA for first seed plants
5. 290-320 MYA for angiosperm vs. gymnosperm split
6. 115 MYA min. for oldest known Nymphaeales
7. 90-130 MYA for monocot vs. dicot split
8. 750 MYA min. for Proterocladus (Cladophoraceae)
1800
1600
1400
1200
1000
Chlamydomonas debaryana
8
9
Chlamydomonas reinhardtii
0.99
800
600
400
9
Tetrabaena socialis
Volvox tertius
# Gains and
Volvox carteri
# losses of characters defined by Kirk (2005):
200
MYA
Figure 1. Chronogram of red algae, green algae and land plants based on three chloroplast
genes (psaA, psaB, and psbC) and one nuclear gene (SSU) using LF. Gray boxes are
ranges of estimates across the sample of 300 posterior trees. Outlined boxes are fossil
calibrations from Yoon et al. (2004); gray boxes for these nodes are ranges inferred during
fossil cross-validation. Bayesian posterior probabilities below 1.0 are shown.
Volvocaceae
0.97
8
Chlorophyta
Pseudendoclonium akinetum
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
300
Incomplete cytokinesis
Partial inversion
Rotation of basal bodies
Organismal polarity
Transformation of cell wall into ECM
Genetic control of cell number
Complete inversion
Increased volume of ECM
Sterile somatic cells
Specialized germ cells *
Asymmetric division
Bifurcated cell division program
250
200
0.94
9
10
0.98
0.94
8
0.97
10*
0.99
11
12
0.59
150
Lobomonas monstruosa
Paulschulzia pseudovolvox
Chlamydomonas reinhardtii
Vitreochlamys pinguis
Vitreochlamys aulata
Vitreochlamys aulata
Vitreochlamys ordinata
Chlamydomonas debaryana
Basichlamys sacculifera
Tetrabaena socialis
Astrephomene perforata
Astrephomene gubernaculifera
Astrephomene gubernaculifera
Gonium pectorale
Gonium viridistellatum
Gonium viridistellatum
Gonium viridistellatum
Gonium quadratum
Gonium octonarium
Gonium multicoccum
Gonium multicoccum
Volvox globator
Volvox barberi
Volvox rousseletii
Platydorina caudata
Volvulina compacta
Volvulina pringsheimii
Volvulina steinii
Volvulina steinii
Volvulina steinii
Pandorina morum
Pandorina morum
Pandorina morum
Pandorina colemaniae
Pandorina morum
Pandorina morum
Volvulina boldii
Yamagishiella unicocca
Yamagishiella unicocca
Yamagishiella unicocca
Eudorina elegans
Eudorina elegans
Eudorina unicocca
Eudorina unicocca
Eudorina elegans
Volvox gigas
Pleodorina indica
Pleodorina illinoisensis
Eudorina cylindrica
Pleodorina californica
Pleodorina japonica
Volvox aureus
Volvox aureus
Volvox aureus
Volvox africanus
Volvox dissipatrix
Volvox tertius
Volvox tertius
Volvox obversus
Volvox carteri f. nagariensis
Volvox carteri f. kawasakiensis
Volvox carteri f. weismannia
100
50
MYA
CONCLUSIONS
The colonial volvocine algae (Tetrabaenaceae, Goniaceae, and Volvocaceae)
diverged from unicellular relatives at least 200 MYA.
An early, rapid radiation established all of the major colonial lineages
(Tetrabaenaceae; Astrephomene; Gonium; Euvolvox; Pandorina + Volvulina;
Yamagishiella; Eudorina + Pleodorina + remaining Volvox) by 150 MYA.
Most colonial body plans are not recent innovations but ancient adaptations
that have been stable over a time scale of tens of millions of years.
Several nominal species include divergences over 50 MYA (Astrephomene
gubernaculifera, Gonium multicoccum, Volvulina steinii, Pandorina morum,
Yamagishiella unicocca, Eudorina elegans)
A body plan similar to that of modern Eudorina, with complete inversion and a
large volume of extracellular matrix (ECM) was present at least 180 MYA.
Sterile somatic cells originated at least 30 MYA in Euvolvox (V. globator + V.
barberi + V. rousseletii), at least 80 MYA in the clade including the remaining
Volvox and Pleodorina, and at least 125 MYA in Astrephomene.
Figure 2. Chronogram of volvocine algae based on five chloroplast genes using LF,
calibrated with the divergence between Paulschulzia (Tetrasporales) and Volvox carteri
derived from analysis in Figure 1. Gray boxes are ranges of estimates across the sample of
300 posterior trees. Bayesian posterior probabilities below 1.0 are shown.
* It is unclear if the MRCA of V. aureus and V. carteri had specialized germ cells.
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