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Ovariole Structure and Oogenesis in Queens And Ovariole structure and oogenesis in queens and workers of the stingless bee Melipona quadrifasciata (Hymenoptera: Apidae, Meliponini) kept under different social conditions Érica Donato Tanaka, Weyder Cristiano Santana, Klaus Hartfelder To cite this version: Érica Donato Tanaka, Weyder Cristiano Santana, Klaus Hartfelder. Ovariole structure and oogenesis in queens and workers of the stingless bee Melipona quadrifasciata (Hymenoptera: Apidae, Meliponini) kept under different social conditions. Apidologie, Springer Verlag, 2009, 40 (2), pp.163-177. hal- 00891990 HAL Id: hal-00891990 https://hal.archives-ouvertes.fr/hal-00891990 Submitted on 1 Jan 2009 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie 40 (2009)163–177 Available online at: c INRA/DIB-AGIB/ EDP Sciences, 2009 www.apidologie.org DOI: 10.1051/apido/2008071 Original article Ovariole structure and oogenesis in queens and workers of the stingless bee Melipona quadrifasciata (Hymenoptera: Apidae, Meliponini) kept under different social conditions* Érica Donato Tanaka1, Weyder Cristiano Santana1,KlausHartfelder2 1 Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Brazil 2 Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Brazil Received 4 June 2008 – Revised 5 November 2008 – Accepted 19 November 2008 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. worker reproduction / follicle development / actin cytoskeleton / ovary histology 1. INTRODUCTION tures within the corbiculate bees (such as ex- treme levels of polyandry, extreme differences Whether stingless bees (Meliponini) and in ovariole number between queens and work- honey bees (Apini) are sister taxa within the ers, progressive feeding of the larvae on a corbiculate bees is still a matter of debate (for diet of primarily glandular origin, and vertical an up-to-date overview of phylogenetic hy- combs and buzzing dances; Winston, 1987). pothesis see Kawakita et al., 2008). It is, how- ever, unquestionable that these two taxa have Comparative studies within stingless reached the apex in the evolution of sociality bees and with honey bees have a long his- in the Apidae. It is equally unquestionable that tory and are increasing in frequency (for the honey bee, Apis mellifera L., is one the best reviews see Michener, 1974; Sakagami, studied insect species, but there are difficul- 1982; Nogueira-Neto, 1997; Roubik, 2006; ties for understanding the evolution of social- Rasmussen and Camargo, 2008)Manyof ity in the Apini because this tribe (Michener, these studies are putting emphasis on the 2000) is composed of a single genus of ten reproductive process, especially the role of / species, all of which show many derived fea- the cell provisioning oviposition process (POP) in colony integration (Sakagami, 1982; Corresponding author: É.D. Tanaka, Zucchi et al., 1999; Cepeda, 2006) and on [email protected] differential reproductive activity of queens * Manuscript editor: Yves Le Conte and workers (Engels and Imperatriz-Fonseca, Article published by EDP Sciences 164 É.D. Tanaka et al. 1990; Hartfelder et al., 2006). Since dif- in each ovary (Cruz-Landim, 2000). In queens, ferential reproduction lies at the core of these ovarioles are more elongated than in insect sociality, understanding oogenesis workers. As they become active egg layers, and its intrinsic control mechanisms in the the ovarioles extend enormously in length un- castes becomes a crucial factor. Theoretically, der progressive oogenesis activity, causing the queens should either manipulate workers to abdomen to swell and the queen to become forego reproduction, or the workers should physogastric (Sakagami, 1982). Quite differ- accept the superior reproductive potential of ent from the honey bees, Melipona workers at the queen as a fact in their own interest and, a certain age are active egg layers in the pres- supposedly, such decisions should ultimately ence of the queen (Engels and Engels, 1977; be contingent on mating systems and genetic Engels and Imperatriz-Fonseca, 1990; Cepeda, relationships between colony members. Sur- 2006). prisingly, however, stingless bees are a bazaar In Meliponini, these workers can produce of diversity in worker reproductive options, two types of eggs: trophic eggs and reproduc- despite very minor differentiation in their tive eggs. This phenomenon is frequently ob- mating systems (Peters et al., 1999;Tothetal., served in various species of stingless bees, and 2004;Velthuisetal.,2005). This variability in the case of reproductive eggs, these may makes stingless bees, and especially their re- make a considerable contribution to a colony’s productive system biology, an ideal object for male production (Beig, 1972; Machado et al., comparative studies, including comparisons 1984; Peters et al., 1999; Drummond et al., with the “eccentric” honey bees. 2000; Paxton et al., 2003;Tothetal.,2004). In the genus Apis, the main morphological Workers laying reproductive eggs usually do difference between the queen and worker caste this right after the queen has laid her egg resides within the ovary. In queen ovaries, the and while sealing the brood cell (Engels number of serial functional units, the ovari- and Imperatriz-Fonseca, 1990; Koedam et al., oles, varies between 180 and 200 per ovary, 2007). Trophic eggs, in contrast, are laid as the whereas the standard number in workers is queen inspects provisioned brood cells right around 2–12 ovarioles per ovary (Snodgrass, before she lays her egg. They differ from re- 1956). The reduced number of ovarioles in productive eggs in size and shape (Koedam workers is the outcome of an autophagic et al., 1996) and they have been consid- cell-death process taking place during the ered as more immature than reproductive ones fifth larval instar (Hartfelder and Steinbrück, (Cruz-Landim and Cruz Höfling, 1971). 1997). Crucial endogenous components of this While worker reproduction – including al- caste divergence are the juvenile hormone most simultaneous production of trophic and titer (Schmidt Capella and Hartfelder, 1998), reproductive eggs – seems to be the most TOR signaling (Patel et al., 2007), and the commonly followed strategy in stingless bees, genome-methylation status (Kucharski et al., workers of some species do not oviposit in the 2008), superposed on or acting in concert presence of the queen even to supply trophic with genotype determinants for worker ovari- eggs to the queen (for review see Hartfelder ole number (Amdam et al., 2006; Makert et al., et al., 2006). In Frieseomelitta varia,worker 2006). Except for the anarchistic mutant phe- reproduction is even brought to a complete notype (Montague and Oldroyd, 1998), work- halt, as the ovary primordia in the worker caste ers are functionally sterile and activate their undergo complete degeneration during meta- ovaries only when a colony has lost its queen morphosis (Boleli et al., 1999). (Winston, 1987). Under such conditions, oo- How oogenesis becomes turned on in genesis in the worker ovary follows the same queens once they have mated (Melo et al., pathway as in queens (Tanaka and Hartfelder, 2001) and how it proceeds in egg-laying 2004). queens and reproductive workers is therefore In contrast to the honey bee, and as in a major issue in stingless bee sociobiology. most stingless bees, queens and workers of Using a comparative analysis with the dy- Melipona quadrifasciata have four ovarioles namics of the processes occurring in honey Oogenesis in Melipona quadrifasciata 165 bees, we attempt to shed light on the common 2.2. General histology principles and differences between the two major groups of highly eusocial bees. In this Ovaries were dissected in honey bee saline, and study, we start out with a general histologi- the ovarioles were individualized in honey bee cul- cal analysis of Melipona quadrifasciata ovar- ture medium (Rachinsky and Hartfelder, 1998)be- ioles dissected from virgin queens, egg-laying fore tracheae and the peritoneal sheath were man- queens, and workers
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