Comparative morphology of the axial complex and interdependence of internal organ systems in sea urchins (Echinodermata: Echinoidea)

Abstract

Background: The axial complex of echinoderms (Echinodermata) is composed of various primary and secondary body cavities that interact with each other. In sea urchins (Echinoidea), structural differences of the axial complex in "regular" and irregular species have been observed, but the reasons underlying these differences are not fully understood. In addition, a better knowledge of axial complex diversity could not only be useful for phylogenetic inferences, but improve also an understanding of the function of this enigmatic structure.

Results: We therefore analyzed numerous species of almost all sea urchin orders by magnetic resonance imaging, dissection, histology, and transmission electron microscopy and compared the results with findings from published studies spanning almost two centuries. These combined analyses demonstrate that the axial complex is present in all sea urchin orders and has remained structurally conserved for a long time, at least in the "regular" species. Within the Irregularia, a considerable morphological variation of the axial complex can be observed with gradual changes in topography, size, and internal architecture. These modifications are related to the growing size of the gastric caecum as well as to the rearrangement of the morphology of the digestive tract as a whole.

Conclusion: The structurally most divergent axial complex can be observed in the highly derived Atelostomata in which the reorganization of the digestive tract is most pronounced. Our findings demonstrate a structural interdependence of various internal organs, including digestive tract, mesenteries, and the axial complex.

Figure 1

Semi-schematic representation of the echinoid axial complex. Semi-schematic representation of the apical region in interradius CD (interambulacrum 2) of Sphaerechinus granularis (Echinoidea: Echinoida) showing madreporic plate, ring canal, axial complex, and rectum [after Leipoldt [26] and Strenger [61], modified]. Aboral haemal ring, Aristotle's lantern, gonads, gonoducts, and spongy (or Tiedemann's) bodies not shown. Not to scale.

Figure 2

Current understanding of sea urchin phylogeny. The hypotheses of echinozoan and echinoid relationships are based on multiple sources of morphological and molecular datasets (for further references see the Materials and methods section). This tree has not been generated using a consensus or numerical technique and reflects the views and biases of the authors.

Figure 3

Vertical magnetic resonance imaging (MRI) sections of various sea urchin specimens. The virtual sections depict the axial complex (arrow). A Cidaris cidaris (Cidaroida). B Caenopedina mirabilis (Pedinoida). C Plesiodiadema indicum (Aspidodiadematidae). D Salenocidaris hastigera (Salenioida). E Strongylocentrotus purpuratus (Echinoida). F Lytechinus variegatus (Echinoida). G Genocidaris maculata (Temnopleuroida). H Echinoneus cyclostomus (Holectypoida). I Cassidulus caribearum ("Cassiduloida"). J Echinolampas depressa ("Cassiduloida"). K Echinarachnius parma (Clypeasteroida). Tables 1 & 2 list resolutions for each MRI dataset.

Figure 4

Schematic representation of the axial complex in selected echinoid taxa. The drawings concentrate on the gross morphology of the axial complex. All other internal organs are omitted, the ring canal is depicted in part only, and the anus is not shown. The legend indicates every structure shown.

Figure 5

Schematic representation of the mesenterial suspension of the axial complex in various higher sea urchin taxa. The drawings demonstrate the impact of the gastric caecum on the architecture of the axial complex. Upper three lines: dorso-ventral mesentery always depicted on the right-hand side. Dashed lines indicate course of the oesophagus or the axial complex (Micrasterina). Lower line: Ventral view of the digestive tract and the axial complex in the vicinity of the oesophagus of highly derived irregular sea urchin taxa (Atelostomata) – note the extension of the mesentery. The grey-scale legend denominates every structure shown. dt = digestive tract, gc = gastric caecum, oe = oesophagus, re = rectum.

Figure 6

Horizontal magnetic resonance imaging (MRI) sections of various sea urchin specimens. The virtual sections were made at the level of gonads, upper digestive tract, and axial complex (arrow). Note the differing mesenterial suspensions of the axial complex. A Cidaris cidaris (Cidaroida). B Eucidaris metularia (Cidaroida). C Caenopedina mirabilis (Pedinoida). D Aspidodiadema hawaiiense (Aspidodiadematidae). E Strongylocentrotus purpuratus (Echinoida). F Lytechinus variegatus (Echinoida). G Mespilia globulus (Temnopleuroida). H Echinoneus cyclostomus (Holectypoida). Tables 1 & 2 list resolutions for each MRI dataset.

Figure 7

Horizontal light-microscopic sections through the echinoid axial complex. A, B Eucidaris tribuloides (Cidaroida); C, D Diadema setosum (Diadematidae); E, F Psammechinus miliaris (Echinoida); G, H Echinocyamus pusillus (Clypeasteroida). Left column: section at the level of head process and dorsal sac. Right column: section at the level of axial organ and axial coelom. ac = axial coelom, ao = axial organ, dm = dorso-ventral mesentery, ds = dorsal sac, fm = free mesentery, go = gonad, hp = head process, ma = madreporic ampulla, oe = oesophagus, pv = pulsating vessel, re = rectum, sc = stone canal, so = somatocoel.

Figure 8

Comparative morphology of the echinoid axial complex at the level of head process and dorsal sac. Schematic representation of the axial complex at the level of head process and dorsal sac based on light-microscopic sections. Note that although changes in shape do occur, the internal composition remains largely the same. For better comparison, the stone canal is shown towards the top of each image. The legend indicates every structure shown.

Figure 9

Comparative morphology of the echinoid axial complex at the level of axial organ and axial coelom. Schematic representation of the axial complex at the level of axial organ and axial coelom based on light-microscopic sections. Note that although changes in shape do occur, the internal composition remains largely the same. For better comparison, the stone canal is depicted towards the top of each image. The legend indicates every structure shown.

Figure 10

Horizontal electron-microscopic sections of the echinoid axial complex. A-D Psammechinus miliaris (Echinoida) and E, F Echinocardium cordatum (Micrasterina). A Dorsal sac epithelium with myoepithelial cells. B Heavily ciliated canaliculus inside the axial organ. C Axial coelom epithelium with podocyte and haemal lacunae. D Somatocoelomic epithelium. E Axial coelom epithelium with podocyte and haemal lacunae. F Heavily ciliated canaliculus inside the axial organ. ac = axial coelom, aj = adhaerens junctions, bl = basal lamina, cf = collagenous fibers, ci = cilium, cm = circumciliary microvillum, ds = dorsal sac, ec = epithelial cell, hl = haemal lacuna, mf = myofibrils, mv = microvillum, nu = nucleus, pe = pedicel, po = podocyte, so = somatocoel.

Figure 11

Schematic representation of sections through the axial complex of Sphaerechinus granularis (Echinoida). A Horizontal section through the echinoid axial complex at the level of head process and dorsal sac. B Horizontal section through the echinoid axial complex at the level of the axial organ. The insert between A and B (compare Fig. 1) roughly outlines where the virtual sections were made. C Schematic representation of the columnar epithelium of the stone canal. D Schematic representation of the flat epithelium of the somatocoel. E Schematic representation of the myoepithelium that lines head process and pulsating vessel. F Schematic representation of the specialized epithelium with podocytes found in the axial coelom. ac = axial coelom, ao = axial organ, bl = basal lamina, ca = canaliculus, ci = cilium, ct = connective tissue, dm = dorso-ventral mesentery, ds = dorsal sac, ec = epithelial cell, fm = free mesentery, hl = haemal lacuna, hp = head process, pv = pulsating vessel, sc = stone canal, so = somatocoel.