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Ultrastructure and phylogenetic significance of the head kidneys in Thalassema thalassemum (Thalassematinae, Echiura)

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Abstract

Recent molecular analyses consistently resolve the “spoon worms” (Echiura) as a subgroup of the Annelida, but their closest relatives among annelids still remain unclear. Since the adult morphology of echiurans yields limited insight into their ancestry, we focused on characters of their larval anatomy to contribute to this discussion. Electron microscopical studies of the larval protonephridia (so-called head kidneys) of the echiuran species Thalassema thalassemum revealed distinct correspondences to character states in serpulid polychaetes, although a close relationship between Echiura and Serpulidae is not supported by any phylogenetic analysis. The larval head kidneys of T. thalassemum consist of only two cells, a terminal cell and a duct cell. The terminal cell forms a tuft of six cilia projecting into the lumen of the terminal cell. The cilia are devoid of circumciliary microvilli. A filter structure is formed by two to three layers of elongate microvilli that surround the lumen of the terminal cell in a tubular manner. A thin layer of extracellular matrix (ECM) encloses the outer microvilli of the tubular structure. The tips of the microvilli project into the lumen of the adjacent duct cell but are not directly connected to it. However, mechanic coupling is facilitated by the surrounding ECM and abundant hemidesmosomes. The distal end of the multiciliary duct cell forms the external opening of the nephridium; a specialized nephropore cell is absent. Apart from the multiciliarity of the duct cell, details of the head kidneys in T. thalassemum reveal no support for the current assumption that Echiura is closely related to Capitellida and/or Terebelliformia. Available data for other echiuran species, however, suggest that the head kidneys of T. thalassemum show a derived state within Echiura.

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Acknowledgments

We specially thank Markus Koch for valuable comments and discussions that improved the manuscript. We are also grateful to Thomas Bartolomaeus and Jörn von Döhren for support with rearing and fixation of T. thalassemum larvae. We also like to thank the Laboratoire de Biologie Marine (Concarneau, France) for hospitality and providing laboratory space during rearing the animals. Three anonymous reviewers are acknowledged for helpful comments on the manuscript.

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  1. Institut für Evolutionsbiologie und Ökologie, Rheinische Friedrich-Wilhelms-Universität Bonn, An der Immenburg 1, 53121, Bonn, Germany

    Chiharu Kato, Janina Lehrke & Björn Quast

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  1. Chiharu Kato
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  2. Janina Lehrke
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  3. Björn Quast
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Correspondence to Chiharu Kato.

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Communicated by T. Bartolomaeus.

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Kato, C., Lehrke, J. & Quast, B. Ultrastructure and phylogenetic significance of the head kidneys in Thalassema thalassemum (Thalassematinae, Echiura). Zoomorphology 130, 97–106 (2011). https://doi.org/10.1007/s00435-011-0124-1

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