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

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 Wlter 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.

Annelida

“…It is hypothesized that the ancestral state of larval annelid protonephridia was an organ composed of three cells: a terminal cell, a nephropore cell, and a duct cell (Bartolomaeus and Quast 2005 ). This simple construction has been modifi ed in adaptation to different developmental modes in several annelid lineages and especially in planktotrophic larvae, where the nephropore cell is often missing (Kato et al 2011(Kato et al , 2012.…”

Homology and Evolution of the Chaetae in Echiura (Annelida)

“…Traditionally Echiura was ranked as a phylum, but recent studies, especially molecular, have generated an increasing body of evidence that they actually are derived annelids [ 6 – 20 ] and mostly provide strong support for a sister group relationship between Echiura and Capitellidae. Loss of segmentation in the echiuran stem lineage was substantiated by studies showing serially repeated groups of neurons in the larval nervous system of certain echiuran species [ 6 – 8 ] as well as three subsequently formed pairs of nephridia [ 21 – 23 ] and confirmed with the recent molecular phylogenies [ 6 – 20 ].…”

Evolutionary Developmental Biology of Invertebrates 2

“…Head kidneys are present in some echiurans but are missing in sipunculid developmental stages. This simple construction has been modifi ed in adaptation to different developmental modes in several annelid lineages and especially in planktotrophic larvae, where the nephropore cell is often missing (Kato et al 2011(Kato et al , 2012. This simple construction has been modifi ed in adaptation to different developmental modes in several annelid lineages and especially in planktotrophic larvae, where the nephropore cell is often missing (Kato et al 2011(Kato et al , 2012.…”