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Germ-cell cluster formation in the telotrophic meroistic ovary of Tribolium castaneum (Coleoptera, Polyphaga, Tenebrionidae) and its implication on insect phylogeny

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Abstract

Tribolium castaneum has telotrophic meroistic ovarioles of the Polyphaga type. During larval stages, germ cells multiply in a first mitotic cycle forming many small, irregularly branched germ-cell clusters which colonize between the anterior and posterior somatic tissues in each ovariole. Because germ-cell multiplication is accompanied by cluster splitting, we assume a very low number of germ cells per ovariole at the beginning of ovariole development. In the late larval and early pupal stages, we found programmed cell death of germ-cell clusters that are located in anterior and middle regions of the ovarioles. Only those clusters survive that rest on posterior somatic tissue. The germ cells that are in direct contact with posterior somatic cells transform into morphologically distinct pro-oocytes. Intercellular bridges interconnecting pro-oocytes are located posteriorly and are filled with fusomes that regularly fuse to form polyfusomes. Intercellular bridges connecting pro-oocytes to pro-nurse cells are always positioned anteriorly and contain small fusomal plugs. During pupal stages, a second wave of metasynchronous mitoses is initiated by the pro-oocytes, leading to linear subclusters with few bifurcations. We assume that the pro-oocytes together with posterior somatic cells build the center of determination and differentiation of germ cells throughout the larval, pupal, and adult stages. The early developmental pattern of germ-cell multiplication is highly similar to the events known from the telotrophic ovary of the Sialis type. We conclude that among the common ancestors of Neuropterida and Coleoptera, a telotrophic meroistic ovary of the Sialis type evolved, which still exists in Sialidae, Raphidioptera, and a myxophagan Coleoptera family, the Hydroscaphidae. Consequently, the telotrophic ovary of the Polyphaga type evolved from the Sialis type.

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Authors and Affiliations

  1. Department of Biology, Chair of Developmental Biology, Friedrich-Alexander-University of Erlangen-Nuremberg, Staudtstr. 5, 91058, Erlangen, Germany

    Jochen Trauner & Jürgen Büning

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  1. Jochen Trauner
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  2. Jürgen Büning
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Correspondence to Jürgen Büning.

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Communicated by S. Roth

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Supplementary Fig. S1

Pro-oocytes are connected by transverse bridges. a Part of section 97 showing that part of the germarial region in which pro-oocytes nest on the posterior somatic tissue (pS). Pro-oocytes are connected to each other by eccentrically localized intercellular bridges next to posterior somatic tissue. Huge areas of fusomal material stretch between neighboring bridges. All pro-oocytes are apparently larger than any other germ cell found in anterior regions. Lateral germ cells are bordered by inner sheath cells (iS), while germ cells of interior regions border each other or some rare somatic interstitial cells (not shown). b The drawing from the original section 97 shows pro-oocytes (numbered, magenta), and, in addition, the connections to pronurse cells (lighter magenta) depicted from other sections nearby. These bridges are shown in dark red as well as all fusomal regions (dark red stippling) of the nearby sections. b The drawing shows all germ cells of the posterior region of the germarium of section 97. Numbers written in pro-oocytes (magenta) refer to the numbers given in Fig. 5. Most of the pro-oocytes are directly connected to each other by intercellular bridges (thickened lines). Four pro-oocytes are connected to pronurse cells (lighter magenta) by intercellular bridges. Fusomal areas are shown by colored dots. A polyfusome stretches through most of the pro-oocyte–pro-oocyte intercellular bridges. The pro-oocyte–pronurse-cell intercellular bridges are filled with smaller fusomal areas. All intercellular bridges as well as those parts of the fusomes that can be seen on section 97 are drawn in lighter magenta, while all the intercellular bridges as well as those parts of the fusomes that can be seen on nearby sections are drawn in dark red (JPG 195 428 kb)

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Trauner, J., Büning, J. Germ-cell cluster formation in the telotrophic meroistic ovary of Tribolium castaneum (Coleoptera, Polyphaga, Tenebrionidae) and its implication on insect phylogeny. Dev Genes Evol 217, 13–27 (2007). https://doi.org/10.1007/s00427-006-0114-3

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