146
F. Raible and P.R.H. Steinmetz
Over the past few decades, molecular biology has provided many additional
ways of assessing complexity. Beyond the global comparison of gene repertoires
(counts of genes or gene families), the diversity of conserved gene families provides
entry points into molecular features of different species. In an increasing number
of species, such analyses can now be complemented by molecular techniques that
address the expression dynamics and site of activity of individual genes, allowing
researchers to characterise individual cell populations and tissues on the molecular
level. Likewise, gene knockdown techniques are becoming available for more and
more species, allowing more detailed analyses of the regulatory networks governing
animal systems.
The fastest progress, however, has been made on the level of sequencing, and several whole-genome or transcriptome sequencing projects now provide a much better
view of molecular evolution during animal diversification. In this chapter, we review
recent progress in molecular analysis of different animal taxa and discuss what they
reveal about the origin of complex features during animal evolution. A particular
focus will be on the evolutionary changes that accompanied the origin and diversification of multicellular animals (Metazoa) from unicellular eukaryotic ancestors, as
well as the differences in complexity found in different bilaterian groups.
5.2 Choanoflagellates: The Evolution of Multicellularity
in Metazoa
Choanoflagellates form a phylum of flagellated, mostly unicellular organisms. They
possess an apical flagellum surrounded by a bacteria- and detritus-catching collar
of actin-rich microvilli. Their cell morphology and ability to form extracellular silicate spicules are very reminiscent of sponge choanocytes (Clark 1866, 1868), and
recent molecular phylogeny studies have confirmed the phylogenetic position of
choanoflagellates as a monophyletic sister group to all Metazoa (Carr et al. 2008,
Clark 1868, Haeckel 1874, King et al. 2008, Shalchian-Tabrizi et al. 2008). Some
extant choanoflagellate species can form colonies (e.g. Proterospongia) or differentiate into amoeboid cells and reproductive cysts (Bütschli 1883–1887, Leadbeater
1983, Siewing 1985). Hence, it is conceivable that the unicellular common ancestor of choanoflagellates and metazoans had the capacity of cell differentiation
or colony formation and therefore exhibited primitive features of multicellularity
(King et al. 2008, Lang et al. 2002). If true, extant colony-forming choanoflagellates might still resemble ancient, primitive multicellular life forms informative
for the evolution of all animals on the metazoan line of evolution. Alternatively,
colony formation and cell differentiation may have evolved independently in animals after the choanoflagellate-metazoan split. To distinguish between these two
scenarios, searches were carried out for metazoan genes important in multicellular
processes such as cell adhesion, cell–cell-communication and the division of labour
in differentiated cell types in the genomes of the strictly unicellular choanoflagellate Monosiga brevicollis (using EST and genome data) and the colony-forming
F. Raible and P.R.H. Steinmetz
Over the past few decades, molecular biology has provided many additional
ways of assessing complexity. Beyond the global comparison of gene repertoires
(counts of genes or gene families), the diversity of conserved gene families provides
entry points into molecular features of different species. In an increasing number
of species, such analyses can now be complemented by molecular techniques that
address the expression dynamics and site of activity of individual genes, allowing
researchers to characterise individual cell populations and tissues on the molecular
level. Likewise, gene knockdown techniques are becoming available for more and
more species, allowing more detailed analyses of the regulatory networks governing
animal systems.
The fastest progress, however, has been made on the level of sequencing, and several whole-genome or transcriptome sequencing projects now provide a much better
view of molecular evolution during animal diversification. In this chapter, we review
recent progress in molecular analysis of different animal taxa and discuss what they
reveal about the origin of complex features during animal evolution. A particular
focus will be on the evolutionary changes that accompanied the origin and diversification of multicellular animals (Metazoa) from unicellular eukaryotic ancestors, as
well as the differences in complexity found in different bilaterian groups.
5.2 Choanoflagellates: The Evolution of Multicellularity
in Metazoa
Choanoflagellates form a phylum of flagellated, mostly unicellular organisms. They
possess an apical flagellum surrounded by a bacteria- and detritus-catching collar
of actin-rich microvilli. Their cell morphology and ability to form extracellular silicate spicules are very reminiscent of sponge choanocytes (Clark 1866, 1868), and
recent molecular phylogeny studies have confirmed the phylogenetic position of
choanoflagellates as a monophyletic sister group to all Metazoa (Carr et al. 2008,
Clark 1868, Haeckel 1874, King et al. 2008, Shalchian-Tabrizi et al. 2008). Some
extant choanoflagellate species can form colonies (e.g. Proterospongia) or differentiate into amoeboid cells and reproductive cysts (Bütschli 1883–1887, Leadbeater
1983, Siewing 1985). Hence, it is conceivable that the unicellular common ancestor of choanoflagellates and metazoans had the capacity of cell differentiation
or colony formation and therefore exhibited primitive features of multicellularity
(King et al. 2008, Lang et al. 2002). If true, extant colony-forming choanoflagellates might still resemble ancient, primitive multicellular life forms informative
for the evolution of all animals on the metazoan line of evolution. Alternatively,
colony formation and cell differentiation may have evolved independently in animals after the choanoflagellate-metazoan split. To distinguish between these two
scenarios, searches were carried out for metazoan genes important in multicellular
processes such as cell adhesion, cell–cell-communication and the division of labour
in differentiated cell types in the genomes of the strictly unicellular choanoflagellate Monosiga brevicollis (using EST and genome data) and the colony-forming