Deceptive Desmas: Molecular Phylogenetics Suggests a New Classification and Uncovers Convergent Evolution of Lithistid Demosponges

Abstract

Reconciling the fossil record with molecular phylogenies to enhance the understanding of animal evolution is a challenging task, especially for taxa with a mostly poor fossil record, such as sponges (Porifera). ‘Lithistida’, a polyphyletic group of recent and fossil sponges, are an exception as they provide the richest fossil record among demosponges. Lithistids, currently encompassing 13 families, 41 genera and >300 recent species, are defined by the common possession of peculiar siliceous spicules (desmas) that characteristically form rigid articulated skeletons. Their phylogenetic relationships are to a large extent unresolved and there has been no (taxonomically) comprehensive analysis to formally reallocate lithistid taxa to their closest relatives. This study, based on the most comprehensive molecular and morphological investigation of ‘lithistid’ demosponges to date, corroborates some previous weakly-supported hypotheses, and provides novel insights into the evolutionary relationships of the previous ‘order Lithistida’. Based on molecular data (partial mtDNA CO1 and 28S rDNA sequences), we show that 8 out of 13 ‘Lithistida’ families belong to the order Astrophorida, whereas Scleritodermidae and Siphonidiidae form a separate monophyletic clade within Tetractinellida. Most lithistid astrophorids are dispersed between different clades of the Astrophorida and we propose to formally reallocate them, respectively. Corallistidae, Theonellidae and Phymatellidae are monophyletic, whereas the families Pleromidae and Scleritodermidae are polyphyletic. Family Desmanthidae is polyphyletic and groups within Halichondriidae – we formally propose a reallocation. The sister group relationship of the family Vetulinidae to Spongillida is confirmed and we propose here for the first time to include Vetulina into a new Order Sphaerocladina. Megascleres and microscleres possibly evolved and/or were lost several times independently in different ‘lithistid’ taxa, and microscleres might at least be four times more likely lost than megascleres. Desma spicules occasionally may have undergone secondary losses too. Our study provides a framework for further detailed investigations of this important demosponge group.

First record of the genus Vetulina Schmidt, 1879 (Porifera: Demospongiae: Sphaerocladina) from the Indian Ocean with the description of two new species: biogeographic and evolutionary significance

“…Our result shows that the 1065-bp-long fragment of both holotypes are 100% identical. Thus, our generated gene tree, which is based on a reduced taxa set of Schuster et al 2015, confirms the previous findings. Presently, we are not aware of a generally accepted molecular species concept for sponges and CO1 is known to be highly conserved in Demospongiae (Shearer et al 2002).…”

“…5). In this study, we additionally sequenced the extended 'Erpenbeck' fragment of the CO1 gene (Erpenbeck et al 2006) for both published specimens (LN624212 and LN62421) (Schuster et al 2015) in order to elucidate ambiguous sites at the 3′ end, which caused the 1% difference. Our result shows that the 1065-bp-long fragment of both holotypes are 100% identical.…”

“…Pisera and Lévi (2002) noted the similarity of Vetulinidae to Mesozoic sphaerocladine lithistids, suggesting Vetulina may be the only extant genus of this lineage. Schuster et al (2015) formerly placed Vetulinidae into its own order Sphaerocladina. Until the discovery of these two new species, Vetulina was a monospecific genus in the monogeneric Vetulinidae.…”

“…With recent molecular studies, this has been formally abandoned and lithistid species have been allocated to 13 families in 4 orders (Morrow and Communicated by P. Martinez Arbizu This article is registered in ZooBank under urn: lsid:zoobank.org: pub:0895227E-C2F8-41F3-B227-036C80BF83A5 Cárdenas 2015; Schuster et al 2015). The Vetulinidae Von Lendenfeld 1903 are a single family in the Sphaerocladina, an order that already existed in the fossil classification (Morrow and Cárdenas 2015).…”

Molecular biodiversity of Red Sea demosponges

“…This marker shows considerable phylogenetic signal on lower taxonomic levels (e.g., Chombard et al, 1998;Erpenbeck et al, 2007a;Cardenas et al, 2009;Schuster et al, 2015) and has also been successfully applied for the molecular taxonomy of Calcarea (Voigt and Wörheide, 2016).…”