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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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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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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.

Mentions: Sea urchins are characterized by a relatively complex haemal system [9,22,33,43]. The stomach is well integrated into this system and is supplied by an inner as well as outer marginal haemal duct. The inner marginal haemal duct ascends from the esophageal haemal ring along the esophagus and borders the adaxial edge of the anterior stomach (Figure 12A). The outer marginal haemal duct borders the abaxial edge of the anterior stomach and sends out branches towards the dorso-ventral mesentery which is connected to the axial complex and its haemal spaces. The outer marginal haemal duct is present in this form presumably in all "regular" sea urchins (Figure 12B). In the Spatangoida, the outer marginal haemal duct is located on the aboral side of the gastric caecum (Figure 12C). The inner marginal haemal duct, however, underwent considerable changes, although the precise timing of these events is difficult to trace based on the present data alone. These changes have led to the evolution of a side-branch of the inner marginal haemal duct which descends from the main branch in order to supply the adoral side of the gastric caecum. Such a novel side-branch can be found in the Clypeasteroida (Figure 6E, F) as well as the Spatangoida (Figure 12D). We were not able to identify this structure in the Echinoneoida, the Cassiduloida, or the Holasteroida and are therefore unsure about its origins. As indicated above, a number of authors elaborated on the complex anatomy of the sea urchin haemal system and so far the Cidaroida [33], the Echinothurioida [34], the Arbacioida [22], the Echinoida [22,23,43,48], the Temnopleuroida [41], the Clypeasteroida [40,55], and the Spatangoida [8,9,12,64,66,69] have been covered. Since the present study did not reveal any novel data on this subject, we will not consider the haemal system of the digestive tract any further.


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)

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

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

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.
Mentions: Sea urchins are characterized by a relatively complex haemal system [9,22,33,43]. The stomach is well integrated into this system and is supplied by an inner as well as outer marginal haemal duct. The inner marginal haemal duct ascends from the esophageal haemal ring along the esophagus and borders the adaxial edge of the anterior stomach (Figure 12A). The outer marginal haemal duct borders the abaxial edge of the anterior stomach and sends out branches towards the dorso-ventral mesentery which is connected to the axial complex and its haemal spaces. The outer marginal haemal duct is present in this form presumably in all "regular" sea urchins (Figure 12B). In the Spatangoida, the outer marginal haemal duct is located on the aboral side of the gastric caecum (Figure 12C). The inner marginal haemal duct, however, underwent considerable changes, although the precise timing of these events is difficult to trace based on the present data alone. These changes have led to the evolution of a side-branch of the inner marginal haemal duct which descends from the main branch in order to supply the adoral side of the gastric caecum. Such a novel side-branch can be found in the Clypeasteroida (Figure 6E, F) as well as the Spatangoida (Figure 12D). We were not able to identify this structure in the Echinoneoida, the Cassiduloida, or the Holasteroida and are therefore unsure about its origins. As indicated above, a number of authors elaborated on the complex anatomy of the sea urchin haemal system and so far the Cidaroida [33], the Echinothurioida [34], the Arbacioida [22], the Echinoida [22,23,43,48], the Temnopleuroida [41], the Clypeasteroida [40,55], and the Spatangoida [8,9,12,64,66,69] have been covered. Since the present study did not reveal any novel data on this subject, we will not consider the haemal system of the digestive tract any further.

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