Phylogenetic relationships of heteroscleromorph demosponges and the affinity of the genusMyceliospongia(Demospongiaeincertae sedis)

Abstract

AbstractClass Demospongiae – the largest in the phylum Porifera (Sponges) – encompasses 7,581 accepted species across the three recognized subclasses: Keratosa, Verongimorpha, and Heteroscleromorpha. The latter subclass contains the majority of demosponge species and was previously subdivided into subclasses Heteroscleromorphasensu strictoand Haploscleromorpha. The current classification of demosponges is the result of nearly three decades of molecular studies that culminated in a formal proposal of a revised taxonomy (Morrow and Cardenas, 2015). However, because most of the molecular work utilized partial sequences of nuclear rRNA genes, this classification scheme needs to be tested by additional molecular markers. Here we used sequences and gene order data from complete or nearly complete mitochondrial genomes of 117 demosponges (including 60 new sequences determined for this study and 6 assembled from public sources) and three additional partial mt-genomes to test the phylogenetic relationships within demosponges in general and Heteroscleromorphasensu strictoin particular. We also investigated the phylogenetic position ofMyceliospongia araneosa– a highly unusual demosponge without spicules and spongin fibers, currently classified as Demospongiaeincertae sedis.Our results support the sub-class relationship within demosponges and reveal four main clades in Heteroscleromorphasensu stricto: Clade 1 composed of Spongillida, Sphaerocladina, and Scopalinida; Clade 2 composed of Axinellida, Biemnida, Bubarida; Clade 3 composed of Tetractinellida and “Rhizomorina” lithistids; and Clade 4 composed of Agelasida, Polymastida, Clionaida, Suberitida, Poecilosclerida, and Tethyida. The four clades appear to be natural lineages that unite previously defined taxonomic orders. Therefore, if those clades are to be systematically interpreted, they will have the rank of superorders (hence S1-S4). We inferred the following relationships among the newly defined clades: (S1(S2(S3+S4))). Analysis of molecular data fromMyceliospongia araneosa– first from this species/genus – placed it in S3 as a sister group toMicrosclerodermasp. andLeiodermatiumsp. (“Rhizomorina”).Molecular clock analysis indicated that the origin of the Heteroscleromorphasensu strictoas well as the basal split in this group between S1 and the rest of the superorder go back to Cambrian, while the divergences among the three other superorders occurred in Ordovician (with the 95% standard variation from Late Cambrian to Early Silurian). Furthermore most of the proposed orders within Heteroscleromorpha appear to have middle Paleozoic origin, while crown groups within order date mostly to Paleozoic to Mesozoic transition. We propose that these molecular clock estimates can be used to readjust ranks for some of the higher taxa within Heteroscleromorpha.In addition to phylogenetic information, we found several unusual mtgenomic features among the sampled species, broadening our understanding of mitochondrial genome evolution in this group and animals in general. In particular, we found mitochondrial introns withincox2(first in animals) andrnl(first in sponges).