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Ultrastructural and immunocytochemical investigation of acoel sperms with 9 + 1 axoneme structure: new sperm characters for unraveling phylogeny in Acoela

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Abstract

Acoel sperm characters proved useful in deciphering acoel taxonomy. The phylogenetic value of sperm characters in closely related sub-groups or in a monophyletic taxon has not yet been assessed. We have investigated sperm ultrastructure in seven members of the monophyletic taxon Childia sensu (Tekle et al. J Zool Sys Evol Res 43(1):72–90, 2005) and in their closest relatives, the Mecynostomidae (four taxa). All members of Childia examined show little variation in their sperm ultrastructure. The common characters of Childia taxa are: 9 + 1 axoneme structure, the presence of six distal cytoplasmic microtubules in the absence of axial or cortical ones, long nucleus and extensive nucleus–flagella overlap. We have identified a new set of cytoplasmic microtubules lying in the centriolar end of the sperm cell, distal microtubules. The origin and phylogenetic significance of this character is discussed. The types and arrangement of cytoplasmic granules could be used as phylogenetic characters at a low taxonomic level. A loose membrane amorphous core type of granule was found to be a synapomorphy for the following clade within the taxon Childia: C. crassum + C. groenlandica + C. vivipara + C. brachyposthium + C. macroposthium. Sausage shaped granules are plesiomorphic among the taxa examined. The rest of the granule characters were found to be homoplasious. Sperm ultrastructural characters have again proven their concordance with molecular phylogeny. The only morphological synapomorphies known for the sister taxa Childia–Mecynostomidae, in the molecular phylogeny, are characters derived from sperm ultrastructure: distal microtubules arranged in two groups of three microtubules each and a 9 + 1 axoneme structure. The spermatozoa of Childia and Mecynostomidae show 9 + 1 axoneme configuration, seemingly similar to the 9 + ‘1’ axoneme pattern of the Platyhelminthes—Trepaxonemata. Using electron-microscope immunocytochemistry, we have demonstrated that, unlike the central cylinder of trepaxonematans, the central cylinder of the 9 + 1 axonemal pattern in acoels is immunoreactive to tubulin and contains a single central microtubule. Therefore, the 9 + 1 patterns in acoels and trepaxonematans are homoplasious.

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Acknowledgments

We are grateful to Annete Axén, Stefan Gunnarsson, and Gary Wife for technical assistance. Thanks are extended to the staff of the marine biological stations at Kristineberg, Tjärnö (Sweden), and Cape Kartesh (Russia) for their help with collecting the material. This study was supported by the Asmara Program at ISP, Uppsala University and SIDA/SAREC (Y. Tekle). Additional financial support was received from the Swedish Research Council (U. Jondelius), the Royal Swedish Academy (U. Jondelius and O. Raikova), and the Russian Foundation for Basic Research grant 06-04-48053 (O. Raikova).

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Authors and Affiliations

  1. Department of Systematic Zoology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 75236, Uppsala, Sweden

    Yonas I. Tekle, Olga I. Raikova, Jan Hendelberg & Ulf Jondelius

  2. Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russia

    Olga I. Raikova

  3. Équipe Biogéographie Marine Tropicale, Unité Systématique, Adaptation, Évolution (CNRS, UPMC, MNHN, IRD), Institut de Recherche pour le Développement, BP A5, 98848, Nouméa Cedex, Nouvelle-Caledonia, New Caledonia

    Jean-Lou Justine

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  1. Yonas I. Tekle
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  2. Olga I. Raikova
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  3. Jean-Lou Justine
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  4. Jan Hendelberg
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  5. Ulf Jondelius
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Correspondence to Yonas I. Tekle.

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Tekle, Y.I., Raikova, O.I., Justine, JL. et al. Ultrastructural and immunocytochemical investigation of acoel sperms with 9 + 1 axoneme structure: new sperm characters for unraveling phylogeny in Acoela. Zoomorphology 126, 1–16 (2007). https://doi.org/10.1007/s00435-006-0023-z

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