Impacts of beach nourishment on loggerhead and green turtles in Brevard County, Florida

1
A Comparative Study of the Evolution
of Multicellularity in the Volvocales Matthew D.
Herron and Richard E. Michod Department of
Ecology and Evolutionary Biology, University of
Arizona
Abstract The volvocine algae (Volvox and its
close relatives) represent a unique opportunity
for the study of origins of multicellularity.
Several major evolutionary transitions have
occurred within this relatively young group,
which spans a large range of sizes and several
levels of complexity. To explore the historical
and adaptive bases of these major evolutionary
transitions, we inferred phylogenetic
relationships in the colonial volvocine algae
using DNA sequence data. Using maximum parsimony
reconstructions of ancestral character states, we
traced the evolution of key innovations such as
coloniality, large size, cellular
differentiation, and novel developmental programs.

• Conclusions
• Single origin of coloniality, no evidence of
  reversal to unicellular condition.
• Most recent common ancestor of the Goniaceae
  and Volvocaceae was likely 16- or 32-celled.
• At least four independent origins of large size
  (gt32 cells), with at least two reductions in cell
  number.
• At least three separate origins of germ-soma
  differentiation (partial or complete).
• One possible reversal from complete to partial
  differentiation.
• At least two losses of the ancestral
  developmental program.

Figure 1. Subset of volvocine species (A)
Chlamydomonas reinhardtii one undifferentiated
cell, (B) Gonium pectorale a clump of 8
undifferentiated cells, (C) Eudorina elegans a
spherical colony of 32 undifferentiated cells,
(D) Pleodorina californica a spherical colony
of 32 cells of which a few are terminally
differentiated, (E) Volvox carteri a spherical
colony of up to 4000 terminally differentiated
somatic cells and a few specialized reproductive
cells, and (F) Volvox aureus a spherical colony
of up to 2000 undifferentiated cells and a few
specialized reproductive cells. Photos by C.
Solari.

• Origins of multicellularity
• Multicellularity has evolved several times
  independently.
• e.g. plants, animals, fungi, red and brown
  algae
• Complex multicellular organisms have functional
  specialization of cells.
• Specialization has a cost some cells are
  specialized for functions other than
  reproduction, lowering fecundity.
• This cost, along with multiple independent
  origins, suggests that multicellularity provides
  a substantial benefit.

• Volvocine green algae (Volvox and its close
  relatives) are an ideal system to study origins
  of multicellularity.
• More recent origin (35-60 MYA) than more
  complex multicellular groups
• Diverse group with unicellular, multicellular,
  and several intermediate stages
• Easily cultured, rapid generations
• Well-studied ecology, cytology, genetics,
  development
• Possible multiple origins of characters related
  to multicellularity

Figure 2. Numbers of cells mapped onto the
Bayesian phylogeny. At least four separate
origins of large size (gt32 cells) are evident.
Gonium octonarium and Eudorina cylindrica
represent probable reductions in cell number.
Figure 3. Three levels of germ-soma
differentiation mapped onto the Bayesian
phylogeny. At least three separate origins of
partial or complete functional specialization of
cells are evident. Pleodorina californica and P.
japonica may represent a reversal from G/S to
GS/S.

• Methods
• DNA sequences from five chloroplast genes
  (atpB, psaA, psaB, psbC, rbcL) combined into a
  supermatrix
• Best-fit model of nucleotide substitution
  inferred in Modeltest(2)
• Phylogeny inferred using Bayesian methods in
  MrBayes(3)
• Posterior probabilities calculated from 3.0 x
  106 post-burnin generations
• Ancestral character states inferred using
  maximum parsimony in Mesquite(4)

References 1. A. G. Desnitski, Eur. J.
Protistol. 31, 241 (1995). 2. D. Posada, K.
Crandall, Bioinformatics 14, 817 (1998). 3. F.
Ronquist, J. P. Huelsenbeck, Bioinformatics 19,
1572 (2003). 4. W. P. Maddison, D. R. Maddison.
http//mesquiteproject.org (2004).

• Major evolutionary transitions in the volvocine
  algae
• From unicellular to colonial
• From simple clumps of cells to structured
  hollow spheres
• From undifferentiated cells to partial
  specialization
• From partial specialization to complete
  separation of reproductive and somatic functions
• Among sizes that span five orders of magnitude
• In Volvox, among four distinct developmental
  programs(1)

Acknowledgements We thank C. Solari for
providing photographs and helpful advice, M.
Buchheim for generously providing unpublished DNA
sequences, and A. Coleman and H. Nozaki for
helpful advice.