The Diploblast-Bilateria Sister hypothesis: Parallel evolution of a nervous systems may have been a simple step

Abstract

For many familiar with metazoan relationships and body plans, the hypothesis of a sister group relationship between Diploblasta and Bilateria1 comes as a surprise. One of the consequences of this hypothesis - the independent evolution of a nervous system in Coelenterata and Bilateria - seems highly unlikely to many. However, to a small number of scientists working on Metazoa, the parallel evolution of the nervous system is not surprising at all and rather a confirmation of old morphological and new genetic knowledge.2-4 The controversial hypothesis that the Diploblasta and Bilateria are sister taxa is, therefore, tantamount to reconciling the parallel evolution of the nervous system in Coelenterata and Bilateria. In this addendum to Schierwater et al.,1 we discuss two aspects critical to the controversy. First we discuss the strength of the inference of the proposed sister relationship of Diploblasta and Bilateria and second we discuss the implications for the evolution of nerve cells and nervous systems.

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[Communicative & Integrative Biology 2:5, 1-3; September/October 2009]; ©2009 Landes Bioscience
1Communicative & Integrative Biology 2009; Vol. 2 Issue 5
For many familiar with metazoan relationships and body plans,
the hypothesis of a sister group relationship between Diploblasta
and Bilateria1 comes as a surprise. One of the consequences of
this hypothesis—the independent evolution of a nervous system
in Coelenterata and Bilateria—seems highly unlikely to many.
However, to a small number of scientists working on Metazoa,
the parallel evolution of the nervous system is not surprising
at all and rather a confirmation of old morphological and new
genetic knowledge.2-4 The controversial hypothesis that the
Diploblasta and Bilateria are sister taxa is, therefore, tantamount
to reconciling the parallel evolution of the nervous system in
Coelenterata and Bilateria. In this addendum to Schierwater
et al.1 we discuss two aspects critical to the controversy. First
we discuss the strength of the inference of the proposed sister
relationship of Diploblasta and Bilateria and second we discuss
the implications for the evolution of nerve cells and nervous
systems.
The analysis in Schierwater et al.1 involved 24 ingroup taxa
and several carefully chosen outgroups. Here we present a larger
analysis of 72 taxa5 to reinforce the inference we obtained with
the smaller taxonomic sample. Figure 1A presents the results of
this analysis and shows clearly that the Bilateria and Diploblasta
are monophyletic and sister to each other with robust bootstrap
support for both parsimony and maximum likelihood analyses.
We could not overturn the sister group relationship of these two
groups regardless of the larger taxonomic sampling or the statistical
tests we used in the present analysis (Fig. 1A). It is clear to us from
analyses with broader taxonomic representation that the sister rela-
tionship of Bilateria and Diploblasta is a valid hypothesis.
With respect to the controversial aspect of parallel nervous
system evolution, we point out that a definition of a nervous
system that satisfies most is that nervous systems are spatially
organized systems of aggregated nerve cells. The simple question,
“what is a nerve cell?” then becomes the crux of the argument. But,
this question elicits a spectrum of answers from different experts.
Accurate homology statements concerning nerve cells are crucial
to the story and these have to wait for a general definition of what
a nerve cell is. The key to these definitions lies in examining the
non-bilaterian animals.2,6 In most modern views “early nervous
system evolution” is the equivalent of “early co-evolution of elec-
trical excitability and functional synapses organizing intracellular
and extracellular signaling processes spatio-temporally”.6 Most
zoologists agree that neither Placozoa nor Porifera have nerve cells
or a nervous system, but it is important to recognize that both
sponges and placozoans show behavior! They respond in a coordi-
nated way to external stimuli that must be perceived and mediated
by some kind of perception and transduction cells. Both sponges
and placozoans harbor a pre-nervous integration system with many
so-called “nerve cell typical” features, molecules and related genes,
but these characteristics cannot be co-localized with any specific
cell type.7-10 While in sponges several cell types are likely involved
in signal perception and transduction, in placozoans it seems to be
a single cell type only, the fiber cells, which form a loose connec-
tion network in the center of the placozoan body.11
Although we are far away from a general definition of a nerve
cell (and therefore a definition for nervous system), we can still
summarize our current knowledge on early nerve cell evolution
(Fig. 1B) as follows: The last common ancestor of metazoans
(LCMA) likely possessed a pre-nervous system with some kind of
unspecialized proto-nerve cells. Placozoa and Porifera cum grano
salis conserved this stage, while both Coelenterata and Bilateria
developed specialized nerve cells from this stage (top; scenario
*Correspondence to: Bernd Schierwater; ITZ; Ecology and Evolution; Tierärztliche
Hochschule Hannover; Hannover D-30559 Germany; Email: bernado@trichoplax.
com/Rob DeSalle; Sackler Institute for Comparative Genomics, American Museum
of Natural History, Central Park West at 79th Street, New York, NY 10024, USA;
Email: desalle@amnh.org
Submitted: 04/16/09; Accepted: 04/17/09
Previously published online as a Communicative & Integrative Biology
E-publication:
http://www.landesbioscience.com/journals/cib/article/8716
Addendum to: Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, et al.
Concatenated analysis sheds light on early metazoan evolution and fuels a modern
“urmetazoon” hypothesis. PLoS Biol 2009; 7:1000020; DOI:10.1371/journal.
pbio.1000020.
Article Addendum
The Diploblast-Bilateria Sister hypothesis
Parallel evolution of a nervous systems may have been a simple step
Bernd Schierwater,1,2,* Sergios-Orestis Kolokotronis,2 Michael Eitel1 and Rob DeSalle2,*
1ITZ; Ecology and Evolution; Tierärztliche Hochschule Hannover; Hannover, Germany; 2ackler Institute for Comparative Genomics, American Museum of Natural History;
New York, NY USA
Key words: placozoa, trichoplax, urmetazoon hypothesis, basal metazoan evolution, trichoplax.com, pre-nervous system, placula
hypothesis
This manuscript has been published online, prior to printing. Once the issue is complete and page numbers have been assigned, the citation will change accordingly.

www.landesbioscience.com Communicative & Integrative Biology 2
in Fig. 1B). In this light the parallel invention of nerve cells, and
consequently a nervous system, in Bilateria and Coelenterata is
hardly problematic and not much more than a morphological
and physiological specialization of already existing proto-nerve
cells. Since specialization of totipotent cells into unipotent cells is
a routine step in all metazoan lineages it seems possible to evolve
specialized nerve cells directly from proto-nerve cells. In other
words, the invention of so-called nerve cells is anything but a major
invention in metazoans, if the LCMA already possessed proto-
nerve cells, which obviously seems to be the case.
References
1. Schier water B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, et al.
Concatenated analysis sheds light on early metazoan evolution and fuels a modern
“urmetazoon” hypothesis. PLoS Biol 2009; 7:1000020.
2. Blackstone NW. A new look at some old animals. PLoS Biol 2009; 7:7.
3. Hanström B. Vergleichende Anatomie des Nervensystems der Wirbellosen Tiere.
Springer, Berlin 1928.
The Diploblast-Bilateria Sister hypothesis
Figure 1. (A) Phylogenetic tree with relationships within Bilateria, Coelenterata, and Porifera collapsed. The 72 taxa are comprised of the 64 taxa from
(5) plus eight taxa added from (1). Numbers in parentheses refer to number of species in each of these groups. Phylogenetic matrices and tree topologies
within the collapsed groups are available from the authors. We inferred the phylogeny using a maximum likelihood (ML) and maximum parsimony (MP)
optimality criterion. Node support values (ML/MP) for nodes marked by circles with inset letters are: (B) Bilateria 100/100, (C) Coelenterata 100/82,
(S) Porifera 100/100, (D) Diploblasta 100/99, (M) Metazoa 100/63; (P) Placozoa is a single taxon. Within the Bilateria: Deuterostomia 100/100,
Protostomia 100/100. (B) Phylogenetic scenarios for the evolution of nerve cells mapped onto the Diploblast-Bilateria Sister hypothesis. Five potential
characters (represented by colored boxes in the figure) important in the evolution of nerve cells are mapped onto the Diploblast-Bilateria Sister. Most
qualities of a nerve cell seem to have been present already in the last common metazoan ancestor (LCMA in light blue). In the top figure we present the
most parsimonious explanation for the evolution of these five characters (6 parsimony steps). Only the specialization of multifunctional proto-nerve cells
into unifunctional nerve cells would have occurred in parallel in Bilateria and Coelenterata in the above scenario. The middle scenario is similar to the
top only instead of hypothesizing independent gain of specialized nerve cells it hypothesizes independent loss of specialized nerve cells (7 steps). The
bottom tree shows a highly unlikely scenario where the number of steps is nearly twice that of the top scenario.

3Communicative & Integrative Biology 2009; Vol. 2 Issue 5
The Diploblast-Bilateria Sister hypothesis
4. Srivastava M, Begovic E, Chapman J, Putnam NH, Hellsten U, Kawashima T, et al. The
Trichoplax genome and the nature of placozoans. Nature 2008; 454:955-60.
5. Dunn CW, Hejnol A, Matus DQ, Pang K, Browne WE, Smith SA, et al. Broad phylog-
enomic sampling improves resolution of the animal tree of life. Nature 2008; 452:745-9.
6. Nickel M. The Pre-Nervous System and Beyond. in: DeSalle R & Schierwater B eds. Key
Transitions in Animal Evolution. Oxford University Press 2009; Oxford (in prep.).
7. Nickel M. Movements without muscles, information processing without nerves. JMBA
GME 2007; 6:8-9.
8. Sakarya O, Armstrong KA, Adamska M, Adamski M, Wang IF, Tidor B, et al. A post-
synaptic scaffold at the origin of the animal kingdom. PLoS ONE 2007; 2:506.
9. Ellwanger K, Nickel M. Neuroactive substances specifically modulate rhythmic body
contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera). Front
Zool 2006; 27:3-7.
10. Schierwater B, de Jong D, DeSalle R. Placozoa, and the evolution of Metazoa and intra-
somatic cell differentiation. Int J Biochem Cell Biol 2009; 41:370-9.
11. Hadrys T, DeSalle R, Sagasser S, Fischer N, Schierwater B. The trichoplax PaxB gene: a
putative proto-PaxA/B/C gene predating the origin of nerve and sensory cells. Mol Biol
Evol 2005; 22:1569-78.