Sponges are likely to be the earliest branching animal lineage, making them key models in studies aimed at understanding evolutionary history of animal genomes. From the morphological and developmental perspectives, sponges combine features of single-cell eukaryotic organisms and the complex multicellular animals (Eumetazoa). Analysis of the first sequenced sponge genome, the demosponge Amphimedon queenslandica, demonstrated a limited number of homologues of genes involved in eumetazoan development, suggesting a gradual assembly of the complex eumetazoan developmental toolkit.
However, sponges are a diverse phylum, composed of four distinct lineages (Demospongiae, Hexactinellida, Calcarea and Homoscleromorpha). Taking advantage of the accessibility of next generation sequencing technologies, we have sequenced genomes of five calcisponges: two calcaroneans (Sycon ciliatum and Leucosolenia complicata) and three calcineans (Clathrina lacunosa, C. laminoclathrata and C. coriacea), as well as a demosponge only distantly related to Amphimedon (Halisarca dujardini). For some of these species, we have also generated an extensive collection of transcriptome datasets representing embryonic and postembryonic development and regeneration.
Comparisons of gene content, with emphasis on developmental regulatory genes, demonstrated unexpected complexity and diversity of developmental toolkits among sponges. In particular, calcaronean and calcinean developmental regulatory gene families are significantly more complex than demosponge gene families. Overall, it appears that significant gene loss occurred independently in the calcisponge and demosponge lineages. These gene losses have been followed by gene family expansions occurring independently in the calcaronean and calcinean lineages, and, to a lesser extent, in the lineage leading to Halisarca. Strikingly, conservation of gene sequence correlates with similarity of gene expression profiles across the sponge species.
Overall, usage of developmental regulatory genes demonstrated deep conservation of body plan patterning and regeneration mechanisms between sponges and the eumetazoans. At the same time, the detailed picture – numbers of genes within individual families – revealed spectacular diversity among sponge species.