Abstract
Bilateria are the predominant clade of animals on Earth. Despite having evolved a wide variety of body plans and developmental modes, they are characterized by common morphological traits. By default, researchers have tried to link clade-specific genes to these traits, thus distinguishing bilaterians from non-bilaterians, by their gene content. Here we argue that it is rather biological processes that unite Bilateria and set them apart from their non-bilaterian sisters, with a less complex body morphology. To test this hypothesis, we compared proteomes of bilaterian and non-bilaterian species in an elaborate computational pipeline, aiming to search for a set of bilaterian-specific genes. Despite the limited confidence in their bilaterian specificity, we nevertheless detected Bilateria-specific functional and developmental patterns in the sub-set of genes conserved in distantly related Bilateria. Using a novel multi-species GO-enrichment method, we determined the functional repertoire of genes that are widely conserved among Bilateria. Analyzing expression profiles in three very distantly related model species—D. melanogaster, D. rerio and C. elegans—we find characteristic peaks at comparable stages of development and a delayed onset of expression in embryos. In particular, the expression of the conserved genes appears to peak at the phylotypic stage of different bilaterian phyla. In summary, our study illustrate how development connects distantly related Bilateria after millions of years of divergence, pointing to processes potentially separating them from non-bilaterians. We argue that evolutionary biologists should return from a purely gene-centric view of evolution and place more focus on analyzing and defining conserved developmental processes and periods.
Highlights
Bilateria comprise about 99% of the extant eumetazoans [1] and are classified into 32 phyla [2].The taxon “Bilateria” has been defined based on morphological key innovations, namely bilateral symmetry, triploblasty, an enhanced nervous system and a complex set of cell types [3]
Analyzing the set of 85 orthogroups in more detail we found that these genes are retained in species separated by a billion years of independent lineage evolution, but that most of them act in key developmental processes
Previous investigations concluded that essentially all important developmental regulators precede the origin of bilaterians, and that rewiring of already existing factors was a hallmark of bilaterian evolution [22,23,24,63,66] and our results enhanced by a second BLAST and phylogeny-based control step are in support of this
Summary
Bilateria comprise about 99% of the extant eumetazoans [1] and are classified into 32 phyla [2].The taxon “Bilateria” has been defined based on morphological key innovations, namely bilateral symmetry, triploblasty, an enhanced nervous system and a complex set of cell types [3]. Bilateria comprise about 99% of the extant eumetazoans [1] and are classified into 32 phyla [2]. It is difficult to define unifying morphological properties for larval or adult Bilateria, as their descendants underwent extensive re-modellings (including secondary reductions and simplifications). Support for the hypothesis that the developmental transcriptome might be a conserved trait across diverse groups of animals has been found [9,10]. Several studies described a conserved phylotypic period mid development based on transcriptomic analyses [11,12,13], akin to the morphological hourglass model of developmental progression [14,15], itself an extension of von Baer’s reverse funnel model of development in animals [16]
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