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Ovariole structure and oogenesis in queens and workers of the stingless bee Melipona quadrifasciata (Hymenoptera: Apidae, Meliponini) kept under different social conditions

Structure des ovarioles et ovogenèse chez les reines et les ouvrières de l’abeille sans aiguillon, Melipona quadrifasciata (Hymenoptera, Apidae, Meliponini) en fonction des conditions sociales

Oogenese und Ovariolenstruktur bei Königinnen und Arbeiterinnen der Stachellosen Biene Melipona quadrifasciata (Hymenoptera: Apidae, Meliponini), die unter unterschiedlichen sozialen Bedingungen gehalten wurden

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Abstract

The high variability in the reproductive biology of stingless bees makes them very amenable for comparative studies with other eusocial bee taxa. We investigated the structural organization of the ovaries of Melipona quadrifasciata queens and workers kept under different social conditions by analyzing their general histology, mitotic activity, and microfilament organization. The overall dynamics of ovarian activity were similar in the two castes, and at emergence their ovarioles contained a previtellogenic follicle. Stingless bees and honey bees differ in the structural organization in the lower germarium, but they have in common synchronized mitotic activity and putative germ line stem cells in the terminal filament. Unlike honey bees, stingless bee workers lay trophic eggs in addition to reproductive eggs. The overall similarities in oogenesis between the two taxa suggest that the decision to form trophic eggs should only occur in the late stages of oogenesis.

Zusammenfassung

Die Tatsache, dass Stachellose Bienen nicht nur hocheusocial sind, sondern auch sehr variabel in ihrer Reproduktionsbiologie, macht sie zu interessanten Studienobjekten für vergleichende Untersuchungen, insbesondere mt der Honigbiene, Apis mellifera. In der vorliegenden Arbeit analysierten wir die strukturelle Organisation der Ovariolen und die Dynamik der Ovogenese bei der Stachellosen Biene Melipona quadrifasciata, in Königinnen und Arbeiterinnen unterschiedlichen Alters und unter verschiedenen sozialen Haltungsbedingungen.

Im Hinblick auf die generelle Histologie der Ovariolen (Abb. 1–3) fanden wir nur wenige Unterschiede zwischen Königinnen und Arbeiterinnen, ausser dass erstere ein wesenlich längeres Germarium aufweisen, in dem sich eine grössere Zahl an Follikeln sequentiell entwickelt. Ein zweiter Unterschied liegt in der Zahl der prävitellogenen Follikel, die bereits beim Schlupf aus der Brutzelle angelegt sind. Während die Ovariolen von Arbeiterinnen lediglich einen prävitellogenen Follikel aufweisen, sind dies bei Königinnen stets mehrere. Diese Befunde stehen in Einklang mit der Eiproduktion junger M. quadrifascata Arbeiterinnen, die neben Nähreiern auch funktionelle Eier ablegen können, aus denen sich Männchen entwickeln.

Auch im Hinblick auf die Dynamik der Mitoseprozesse, die durch BrdU-Inkubation und Detektion in Ovariolen sichtbar gemacht wurden (Abb. 4), unterschieden sich Königinnen und Arbeiterinnen nur wenig. Sowohl im Terminalfilum als auch im Germarium zeigte sich eine regionale Synchronie im Zellzyklus, die sich im weiteren Verlauf der Oogenese sukzessiv verliert. In diesem Punkt sind sich Stachellose Bienen und Honigbienen sehr ähnlich. F-Aktin wurde mittels TRITC-Palloidin-Markierung und Laserkonfokalmikroskopie sichbar gemacht (Abb. 5). Bereits die frühesten Oogenesestadien wiesen F-Aktin in den Fusomen auf, das mit der Auflösung der verzweigten Polyfusome im weiteren Verlauf der Oogenese in die Ringkanäle übergeht. Erst mit der Differenzierung von Oocyten und Nährzellen im unteren Bereich des Germariums und dann nach Abtrennung der Follikel aus dem Germarium weisen die Nährzellen und insbesondere die Oocyten ein stark markiertes corticales Aktin-Cytoskelet auf.

Eine interessante Parallele in der Ovariolenstruktur von Honigbienen und Stachellosen Bienen bildet das Vorkommen eines zweiten Zelltyps im Terminalfilum. Interkaliert zwischen den typischen abgeplatteten somatischen Zellen, die wie in einem Münzstapel angeordnet sind, fanden sich auch bei M. quadrifasciata abgerundete Zellen, die ein nur schwach färbbares Cytoplasma und kein ausgeprägtes Aktin-Cytoskelett aufwiesen. Es könnte sich hierbei wie auch bei Honigbienen um Stammzellen der Keimbahn handeln.

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Correspondence to Érica Donato Tanaka.

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Tanaka, É.D., Santana, W.C. & Hartfelder, K. Ovariole structure and oogenesis in queens and workers of the stingless bee Melipona quadrifasciata (Hymenoptera: Apidae, Meliponini) kept under different social conditions. Apidologie 40, 163–177 (2009). https://doi.org/10.1051/apido/2008071

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