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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 - BMC Evol. Biol. (2010)

Bottom Line: 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.It is also undeveloped in certain spatangoid species.Its occurrence in "regular" euechinoids is linked to the presence of an additional festoon of the anterior stomach in ambulacrum III.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Immungenetik, Charité-Universitätsmedizin Berlin, Thielallee 73, 14195 Berlin, Germany. alexander.ziegler@charite.de

ABSTRACT

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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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.
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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.

Mentions: The topographic reference system for our descriptions is based upon Lovén's system [29] as depicted in Figure 1 A, B [ambulacra I-V (Amb I-V) and interambulacra 1-5 (IAmb 1-5)]. Furthermore, Figures 3, 4, 5, 6, 7, 8 denote whether the specimen is viewed aborally (AB), laterally (LA), or orally (OR). Figure 9 provides an overview of the general sea urchin digestive tract morphology - the models presented in this figure are entirely based on 3D MRI datasets [25,30]. Finally, Figure 10 provides three interactive 3D models of the digestive tracts of selected taxa. In all figures within the present article, except for a number of lateral views, Amb III is always facing upwards. The images taken from the literature have in some cases been modified slightly through removal of labels used by the original author(s). All images were chosen based on the quality and plausibility in the manner in which digestive tract structures in particular had been depicted.


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

Ziegler A, Mooi R, Rolet G, De Ridder C - BMC Evol. Biol. (2010)

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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2967547&req=5

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.
Mentions: The topographic reference system for our descriptions is based upon Lovén's system [29] as depicted in Figure 1 A, B [ambulacra I-V (Amb I-V) and interambulacra 1-5 (IAmb 1-5)]. Furthermore, Figures 3, 4, 5, 6, 7, 8 denote whether the specimen is viewed aborally (AB), laterally (LA), or orally (OR). Figure 9 provides an overview of the general sea urchin digestive tract morphology - the models presented in this figure are entirely based on 3D MRI datasets [25,30]. Finally, Figure 10 provides three interactive 3D models of the digestive tracts of selected taxa. In all figures within the present article, except for a number of lateral views, Amb III is always facing upwards. The images taken from the literature have in some cases been modified slightly through removal of labels used by the original author(s). All images were chosen based on the quality and plausibility in the manner in which digestive tract structures in particular had been depicted.

Bottom Line: 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.It is also undeveloped in certain spatangoid species.Its occurrence in "regular" euechinoids is linked to the presence of an additional festoon of the anterior stomach in ambulacrum III.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institut für Immungenetik, Charité-Universitätsmedizin Berlin, Thielallee 73, 14195 Berlin, Germany. alexander.ziegler@charite.de

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus