With the completion of a single unified classification, the Systema Porifera (SP) and subsequent development of an online species database, the World Porifera Database (WPD), we are now equipped to provide a first comprehensive picture of the global biodiversity of the Porifera. An introductory overview of the four classes of the Porifera is followed by a description of the structure of our main source of data for this paper, the WPD. From this we extracted numbers of all ‘known’ sponges to date: the number of valid Recent sponges is established at 8,553, with the vast majority, 83%, belonging to the class Demospongiae. We also mapped for the first time the species richness of a comprehensive set of marine ecoregions of the world, data also extracted from the WPD. Perhaps not surprisingly, these distributions appear to show a strong bias towards collection and taxonomy efforts. Only when species richness is accumulated into large marine realms does a pattern emerge that is also recognized in many other marine animal groups: high numbers in tropical regions, lesser numbers in the colder parts of the world oceans. Preliminary similarity analysis of a matrix of species and marine ecoregions extracted from the WPD failed to yield a consistent hierarchical pattern of ecoregions into marine provinces. Global sponge diversity information is mostly generated in regional projects and resources: results obtained demonstrate that regional approaches to analytical biogeography are at present more likely to achieve insights into the biogeographic history of sponges than a global perspective, which appears currently too ambitious. We also review information on invasive sponges that might well have some influence on distribution patterns of the future.

Understanding how complex traits, such as epithelia, nervous systems, muscles, or guts, originated depends on a well-supported hypothesis about the phylogenetic relationships among major animal lineages. Traditionally, sponges (Porifera) have been interpreted as the sister group to the remaining animals, a hypothesis consistent with the conventional view that the last common animal ancestor was relatively simple and more complex body plans arose later in evolution. However, this premise has recently been challenged by analyses of the genomes of comb jellies (Ctenophora), which, instead, found ctenophores as the sister group to the remaining animals (the "Ctenophora-sister" hypothesis). Because ctenophores are morphologically complex predators with true epithelia, nervous systems, muscles, and guts, this scenario implies these traits were either present in the last common ancestor of all animals and were lost secondarily in sponges and placozoans (Trichoplax) or, alternatively, evolved convergently in comb jellies. Here, we analyze representative datasets from recent studies supporting Ctenophora-sister, including genome-scale alignments of concatenated protein sequences, as well as a genomic gene content dataset. We found no support for Ctenophora-sister and conclude it is an artifact resulting from inadequate methodology, especially the use of simplistic evolutionary models and inappropriate choice of species to root the metazoan tree. Our results reinforce a traditional scenario for the evolution of complexity in animals, and indicate that inferences about the evolution of Metazoa based on the Ctenophora-sister hypothesis are not supported by the currently available data.Metazoa | Ctenophora | Porifera | phylogenomics | evolution R esolving the phylogenetic relationships close to the root of the animal tree of life, which encompass the phyla Porifera (sponges), Cnidaria (jellyfish, corals, and their allies), Ctenophora (comb jellies), Placozoa (the "plate animals" of the genus Trichoplax), and Bilateria (the group containing all remaining phyla), is fundamental to understanding early animal evolution and the emergence of complex traits [reviewed by Dohrmann and Wörheide (1)]. Traditionally, sponges have been recognized as the sister group to the remaining animals (the "Porifera-sister" hypothesis). Under this scenario, true epithelia (with belt desmosomes connecting neighboring cells) and extracellular digestion are conventionally thought to have been primitively absent in sponges, having evolved in the common ancestor of Placozoa, Ctenophora, Cnidaria, and Bilateria. Within this group, gap junctions between neighboring cells, ectodermal and endodermal germ layers, sensory cells, nerve cells, and muscle cells evolved only once in the common ancestor of Ctenophora, Cnidaria, and Bilateria. Thus, Porifera-sister is consistent with the view that the last common ancestor of the animals was relatively simple and more complex body plans evolved after sponges had separated from the other animal lineages. However, a s...

The relationships at the root of the animal tree have proven difficult to resolve, with the current debate focusing on whether sponges (phylum Porifera) or comb jellies (phylum Ctenophora) are the sister group of all other animals [1-5]. The choice of evolutionary models seems to be at the core of the problem because Porifera tends to emerge as the sister group of all other animals ("Porifera-sister") when site-specific amino acid differences are modeled (e.g., [6, 7]), whereas Ctenophora emerges as the sister group of all other animals ("Ctenophora-sister") when they are ignored (e.g., [8-11]). We show that two key phylogenomic datasets that previously supported Ctenophora-sister [10, 12] display strong heterogeneity in amino acid composition across sites and taxa and that no routinely used evolutionary model can adequately describe both forms of heterogeneity. We show that data-recoding methods [13-15] reduce compositional heterogeneity in these datasets and that models accommodating site-specific amino acid preferences can better describe the recoded datasets. Increased model adequacy is associated with significant topological changes in support of Porifera-sister. Because adequate modeling of the evolutionary process that generated the data is fundamental to recovering an accurate phylogeny [16-20], our results strongly support sponges as the sister group of all other animals and provide further evidence that Ctenophora-sister represents a tree reconstruction artifact. VIDEO ABSTRACT.

Reconstructing the phylogeny of sponges (Porifera) is one of the remaining challenges to resolve the metazoan Tree of Life and is a prerequisite for understanding early animal evolution. Molecular phylogenetic analyses for two of the three extant classes of the phylum, Demospongiae and Calcarea, are largely incongruent with traditional classifications, most likely because of a paucity of informative morphological characters and high levels of homoplasy. For the third class, Hexactinellida (glass sponges)--predominantly deep-sea inhabitants with unusual morphology and biology--we present the first molecular phylogeny, along with a cladistic analysis of morphological characters. We collected 18S, 28S, and mitochondrial 16S ribosomal DNA sequences of 34 glass sponge species from 27 genera, 9 families, and 3 orders and conducted partitioned Bayesian analyses using RNA secondary structure-specific substitution models (paired-sites models) for stem regions. Bayes factor comparisons of different paired-sites models against each other and conventional (independent-sites) models revealed a significantly better fit of the former but, contrary to previous predictions, the least parameter-rich of the tested paired-sites models provided the best fit to our data. In contrast to Demospongiae and Calcarea, our rDNA phylogeny agrees well with the traditional classification and a previously proposed phylogenetic system, which we ascribe to a more informative morphology in Hexactinellida. We find high support for a close relationship of glass sponges and Demospongiae sensu stricto, though the latter may be paraphyletic with respect to Hexactinellida. Homoscleromorpha appears to be the sister group of Calcarea. Contrary to most previous findings from rDNA, we recover Porifera as monophyletic, although support for this clade is low under paired-sites models.