Ziegler A et al. (2010), Origin and evolutionary plasticity of the gastr...

ECB-ART-41802

BMC Evol Biol 2010 Oct 18;10:313. doi: 10.1186/1471-2148-10-313.

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Origin and evolutionary plasticity of the gastric caecum in sea urchins (Echinodermata: Echinoidea).

Ziegler A , Mooi R , Rolet G , De Ridder C .

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BACKGROUND: The digestive tract of many metazoan invertebrates is characterized by the presence of caeca or diverticula that serve secretory and/or absorptive functions. With the development of various feeding habits, distinctive digestive organs may be present in certain taxa. This also holds true for sea urchins (Echinodermata: Echinoidea), in which a highly specialized gastric caecum can be found in members of a derived subgroup, the Irregularia (cake urchins, sea biscuits, sand dollars, heart urchins, and related forms). As such a specialized caecum has not been reported from "regular" sea urchin taxa, the aim of this study was to elucidate its evolutionary origin. RESULTS: Using morphological data derived from dissection, magnetic resonance imaging, and extensive literature studies, we compare the digestive tract of 168 echinoid species belonging to 51 extant families. Based on a number of characters such as topography, general morphology, mesenterial suspension, and integration into the haemal system, we homologize the gastric caecum with the more or less pronounced dilation of the anterior stomach that is observed in most "regular" sea urchin taxa. In the Irregularia, a gastric caecum can be found in all taxa except in the Laganina and Scutellina. It is also undeveloped in certain spatangoid species. CONCLUSIONS: According to our findings, the sea urchin gastric caecum most likely constitutes a synapomorphy of the Euechinoidea. Its occurrence in "regular" euechinoids is linked to the presence of an additional festoon of the anterior stomach in ambulacrum III. Both structures, the additional festoon and the gastric caecum, are absent in the sister taxon to the Euechinoidea, the Cidaroida. Since the degree of specialization of the gastric caecum is most pronounced in the predominantly sediment-burrowing irregular taxa, we hypothesize that its evolution is closely linked to the development of more elaborate infaunal lifestyles. We provide a comprehensive study of the origin and evolutionary plasticity of a conspicuous digestive tract structure, the gastric caecum, in a major taxon of the extant invertebrate macrozoobenthos.

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Species referenced: Echinodermata
Genes referenced: LOC100887844 stk36

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	Figure 1. Historic and contemporary representations of the general anatomy of the irregular and "regular" sea urchin digestive tract. (A) and (B) constitute the first graphic representations of the gastric caecum (black arrow in A) as well as the dilation of the anterior stomach (white arrow in B). (A) Spatangus purpureus - aboral view, modified from Hoffmann [8]. (B) Paracentrotus lividus - aboral view, modified from Tiedemann [20]. Numbers indicate homologous body parts in "regular" and irregular sea urchins according to Lovén's system [29]: Roman numerals (I-V) indicate ambulacra, whereas Arabic numerals (1-5) indicate interambulacra. (C) Spatangus purpureus - aboral view of a dissected specimen. (D) Paracentrotus lividus - aboral view of a dissected specimen. di = dilation, es = esophagus, gc = gastric caecum, in = intestine, re = rectum, st = stomach. Not to scale.
	Figure 2. List of higher sea urchin taxa analyzed in this study. Note that the monophyly of several of these taxa is still under debate. The numbers in brackets designate the number of species analyzed in each family in the course of this study. This diagram is based upon results obtained by numerous authors [74-84].
	Figure 3. Digestive tract anatomy of selected "regular" sea urchin taxa (Histocidaridae - Aspidodiadematidae). Histocidaridae (A), Cidaridae (B, C), Phormosomatidae (D), Echinothuriidae (E-G), Pedinidae (H, I), Micropygidae (J), and Aspidodiadematidae (K, L). AB = aboral view, OR = oral view. d = dilation, e = esophagus, f = festoon. Not to scale.
	Figure 4. Digestive tract anatomy of selected "regular" sea urchin taxa (Diadematidae - Temnopleuridae). Diadematidae (A-D), Glyptocidaridae (E), Stomopneustidae (F), Arbaciidae (G, H), Saleniidae (I-K), and Temnopleuridae (L). (G) from [22, Fig. 2, Pl. II] - reproduced in modified form with kind permission from L'Institut Océanographique, Fondation Albert Ier, Prince de Monaco. AB = aboral view, LA = lateral view, OR = oral view. d = dilation, e = esophagus, f = festoon. Not to scale.
	Figure 5. Digestive tract anatomy of selected "regular" sea urchin taxa (Parechinidae - Toxopneustidae). Parechinidae (A-D), Echinidae (E, F), Echinometridae (G, H), Strongylocentrotidae (I, J), and Toxopneustidae (K, L). (A) from [27, Fig. 9] - reproduced in modified form with kind permission from Mr. Thierry Powis de Tenbossche. (C, F, K) from [22, Figs. 1, 4, 7, Pl. II] - reproduced in modified form with kind permission from L'Institut Océanographique, Fondation Albert Ier, Prince de Monaco. (H) from [23, Fig. 9] - reproduced in modified form with kind permission from The Royal Society of New Zealand. AB = aboral view, OR = oral view. d = dilation, e = esophagus, f = festoon. Not to scale.
	Figure 6. Digestive tract anatomy of selected irregular sea urchin taxa (Echinoneidae - Arachnoididae). Echinoneidae (A), Apatopygidae (B), Cassidulidae (C), Neolampadidae (D), Clypeasteridae (E, F), and Arachnoididae (G = juvenile specimen, H = adult specimen). AB = aboral view, LA = lateral view, OR = oral view. e = esophagus, p = pouch. Not to scale.
	Figure 7. Digestive tract anatomy of selected irregular sea urchin taxa (Laganidae - Mellitidae). Laganidae (A, B), Fibulariidae (C), Rotulidae (D), Echinarachniidae (E, F), Dendrasteridae (G-I), Astriclypeidae (J), and Mellitidae (K, L). (H) from [57, Fig. 3] - reproduced in modified form with kind permission from the Marine Biological Laboratory, Woods Hole, MA, USA. AB = aboral view. e = esophagus, s = sacculated abaxial edge of the stomach. Not to scale.
	Figure 8. Digestive tract anatomy of selected irregular sea urchin taxa (Corystidae - Spatangidae). Corystidae (A), Urechinidae (B-D), Pourtalesiidae (E, F), Aeropsidae (G), Hemiasteridae (H), Schizasteridae (I), Brissidae (J, K), Brissopsidae (L), Loveniidae (M), Spatangidae (N, O), and Asterostomatidae (P). (K) from [67, Fig. 11] - reproduced in modified form with kind permission from the Rosenstiel School of Marine and Atmospheric Science. AB = aboral view, LA = lateral view, OR = oral view. e = esophagus, p = pouch. Not to scale.
	Figure 9. Comparative anatomy of the sea urchin digestive tract. (A-T) Aboral views of 3D models that were produced based on magnetic resonance imaging scans of 20 sea urchin species. Cidaridae (A), Micropygidae (B), Diadematidae (C), Stomopneustidae (D), Arbaciidae (E), Saleniidae (F), Temnopleuridae (G), Trigonocidaridae (H), Parechinidae (I), Echinometridae (J), Strongylocentrotidae (K), Echinoneidae (L), Cassidulidae (M), Echinolampadidae (N), Clypeasteridae (O), Laganidae (P), Rotulidae (Q), Echinarachniidae (R), Pourtalesiidae (S), Schizasteridae (T). Dark blue = main digestive tract (comprising the lateral dilation in "regular" euechinoid species (B-K)); cyan = thin-walled pouch(es) in irregular sea urchin species. Not to scale.
	Figure 10. Homology of the sea urchin gastric caecum based on its location as a primary criterion. (A-C) Interactive 3D PDF models of the digestive tract of two "regular" [Eucidaris metularia (A), Diadema savignyi (B)] and one irregular [Echinoneus cyclostomus (C)] sea urchin species. Left-click onto each of the three images in order to activate the embedded 3D models. Labeling designates the structures we consider homologous. Note that the 3D model of Diadema savignyi (B) depicts a modelling artefact due to the close proximity of esophagus and rectum: both structures seem to be fused, although they are clearly not in reality. Please refer to [88-90] for an in-depth explanation of how to manipulate and generate publication-embedded 3D PDF models. This interactive 3D figure requires Adobe Reader 8.0 or higher to operate. Not to scale.
	Figure 11. Homology of the sea urchin gastric caecum based on its integration into the mesenterial system, in particularl the dorso-ventral mesentery, as a primary criterion. Virtual horizontal sections based on MRI scans of Cidaridae (A), Aspidodiadematidae (B), Stomopneustidae (C), Temnopleuridae (D), Parasaleniidae (E), Parechinidae (F), Strongylocentrotidae (G), Echinoneidae (H), Cassidulidae (I), Schizasteridae (J), Loveniidae (K), and Spatangidae (L). The gastric caecum - where present - is attached to esophagus, axial complex, and the test through the dorso-ventral mesentery (arrows). In the Cidaroida (A), the dorso-ventral mesentery attaches to the single festoon present in ambulacrum III. In the more derived spatangoid and certain holasteroid taxa, this mesentery is shifted away from its original insertion near ambulacrum III towards interambulacrum 3, resulting in an oblique position of the gastric caecum (K, L). Note that the gastric caecum, in contrast to the rest of the digestive tract, is always free of sediment grains in the burrowing irregular taxa (H-L). Not to scale.
	Figure 12. Homology of the sea urchin gastric caecum based on its integration into the haemal system of the digestive tract as a primary criterion. Schematic representations of the digestive tract haemal system in Cidaridae (A), Echinidae (B), and Spatangidae (C, D). The sea urchin stomach is accompanied by an inner (im) as well as an outer (om) marginal haemal duct. The outer marginal haemal duct sends out branches towards the dorso-ventral mesentery (dm) which is connected to the axial complex (ac) (A). The gastric caecum (gc) - if present (B-D) - is well-integrated into the haemal system. The black arrow in (D) depicts the conspicuous side branch of the inner marginal haemal duct present in presumably all spatangoids and potentially further irregular sea urchin taxa. AB = aboral view, LA = lateral view. Not to scale.

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