Discovery of missing link between demosponges and hexactinellids confirms palaeontological model of sponge evolution

Abstract

The two major extant groups of siliceous sponges, Demospongiae and Hexactinellida, are generally regarded as sister groups forming the clade Silicea, although the nature of their last common ancestor is uncertain. The fossil record contains a diverse range of basal demosponges that appear to have evolved from hexactine-bearing reticulosan ancestors, although a compelling morphological intermediate has not previously been discovered. Here we describe a new species of fossil sponge, Conciliospongia anjiensis gen. et sp. nov., from the Late Ordovician (~444 Ma) Anji Biota of South China. This species has a reticulate, tufted skeleton of minute monaxon spicules, characteristic of the fossil demosponge family Hazeliidae and modern heteroscleromorphs, with hexactine spicules and a globose body form inherited from reticulosan ancestors. This transitional morphology had previously been hypothesized in palaeontological studies. This morphological intermediate between two extant classes further confirms siliceous sponge monophyly and demosponge-hexactinellid spicule homology, and supports the primitive, stem-silicean interpretation of simpler-structured fossil reticulosans.

Figure 1

Reconstruction of Conciliospongia anjiensis gen. et sp. nov. (a) Overall cut-away view showing inner part of wall (right half) and outer surface (left half), with gaps in skeletal wall probably representing sites of choanocyte chambers, bounded by soft tissue walls; (b) three-dimensional cut-away reconstruction through wall thickness, illustrating tufts of fine monaxon spicules (up to 0.3 mm long), becoming more perpendicular to wall at exterior (upper) surface; (c) detail illustrating structure of inner part of wall. Sponge is approximately 35 mm wide.

Figure 2

Conciliospongia anjiensis gen. et sp. nov. (a, f–h) Paratype (specimen number NIGP 165187): (a) Overall view of dorso-ventrally flattened specimen with osculum central; (f) detail from near oscular margin, including two large hexactines amongst fine monaxons; (g) detail of central upper part of body wall, showing tufts of fine parallel monaxons; (h) oscular margin showing cuspate margin (arrow) with localized projecting spicules, and tufted texture of wall, composed of small overlapping clusters of parallel monaxons (adjacent to arrowed cusp). (b–e) Holotype (specimen number NIGP 165186): (b) Detail of upper right margin, rotated anticlockwise with respect to (c), showing walls composed of spicule tufts and occasional spicules crossing spaces of reticulation; (c) overall view of partial, laterally-compressed specimen with well preserved reticulate skeletal wall; (d) detail of the lower right region of (c) on the counterpart, showing lateral projecting spicule tufts (arrowed, with lower arrowed region magnified and inset), position of (e) (box), and finely-tufted skeleton; (e) detail of (d), showing hexactine embedded in body wall. Scale bars: (a, c) 10 mm; (b, d, h) 1 mm; (e–g) 0.5 mm.

Figure 3

Summary of early demosponge evolution. Schematic diagram showing the phylogeny and stratigraphic distribution of the stem and basal crown groups of Demospongiae, including key fossil taxa and their occurrences. The inset summary shows the simplified position of Conciliospongia anjiensis gen. et sp. nov. relative to the extant silicean classes. Phylogenetic topology of extant taxa (thick dashed lines) conforms with molecular interpretations. Primary hypothesis of fossil relationships are based on ref. for vauxiid and hazeliid relationships and ref. for Cyathophycus loydelli. Stem-group heteroscleromorph refers to ref. . The key skeletal transitions are the origination of a monaxon-based inner skeletal layer in Cyathophycus [1], subsequent loss of hexactines in the stem lineage of demosponges [2], and ultimately also the loss of monaxons within the Vauxiidae (leading to Keratosa and Verongiomorpha) [3]; the loss of a simple globose body form (and concomitant change in growth patterns) accompanied the origin of crown-group demosponges [4]. Cambrian occurrences of Heminectere (listed as Protospongia cf. conica) and Cyathophycus (described as Diagoniella cyathiformis) are after ref. , Ordovician occurrences of Heminectere and Cyathophycus are from ref. , and first appearances of Crumillospongia, Vauxia and Hazelia are from ref. .