The Ovary and Its Genes-Developmental Processes Underlying the Establishment and Function of a Highly Divergent Reproductive
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The ovary and its genes-developmental processes underlying the establishment and function of a highly divergent reproductive system in the female castes of the honey bee, Apis mellifera Klaus Hartfelder, Gustavo Jacomini Tiberio, Denyse Cavalcante Lago, Rodrigo Pires Dallacqua, Marcia Maria Gentile Bitondi To cite this version: Klaus Hartfelder, Gustavo Jacomini Tiberio, Denyse Cavalcante Lago, Rodrigo Pires Dallacqua, Mar- cia Maria Gentile Bitondi. The ovary and its genes-developmental processes underlying the establish- ment and function of a highly divergent reproductive system in the female castes of the honey bee, Apis mellifera. Apidologie, 2018, 49 (1), pp.49-70. 10.1007/s13592-017-0548-9. hal-02973413 HAL Id: hal-02973413 https://hal.archives-ouvertes.fr/hal-02973413 Submitted on 21 Oct 2020 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 (2018) 49:49–70 Review article * INRA, DIB and Springer-Verlag France SAS, 2017 DOI: 10.1007/s13592-017-0548-9 The ovary and its genes—developmental processes underlying the establishment and function of a highly divergent reproductive system in the female castes of the honey bee, Apis mellifera 1 1 1 Klaus HARTFELDER , Gustavo Jacomini TIBERIO , Denyse Cavalcante LAGO , 2 3 Rodrigo Pires DALLACQUA , Marcia Maria Gentile BITONDI 1Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes 3900, Ribeirão Preto, SP 14049-900, Brazil 2Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Cidade Universitária, Campo Grande, MS 14049-900, Brazil 3Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes 3900, Ribeirão Preto, SP 14040-901, Brazil Received 18 May 2017 – Revised 4 September 2017 – Accepted 25 September 2017 Abstract – The strong dimorphism in ovary phenotype seen between honey bee queens and workers represents the anatomical fixation of reproductive division of labor. We review the developmental processes by which the divergent ovary phenotypes become established, mainly focusing on the massive programmed cell death (PCD) that destroys most of the ovariole primordia in the worker ovary during larval development. Ovary-specific transcriptome analyses revealed a set of differentially expressed genes associated with PCD, including two long noncoding RNAs. PCD also plays a major role regulating ovarian activity in adult honey bee workers, and a major effect candidate gene mediating this process is Anarchy, previously identified through classical genetics in a rebel worker strain. Finally, we ask how the strong ovary phenotype dimorphism in the genus Apis may have evolved, and we discuss this by contrasting honey bees with the equally eusocial stingless bees. Through a comparison of their mating systems (polyandry versus monandry), as well as comparative data on female and male gonad structure across several families of bees, we propose the hypothesis that the exceptional gonad structure in Apis queens and drones evolved via shared develop- mental pathways. Furthermore, we suggest that selection on massive sperm production in Apis drones may have been a driving force leading to this exaggerated gonad morphology. honeybee / gonad development / cell death / differential gene expression / meliponids Where does the spirit of the hive reside? At 1. INTRODUCTION least to some extent it is in the ovaries of a crowd of bees working in a dark hive With this answer, in response to the question (Robert E. Page Jr.) posed by Maurice Materlincks’ work The Life of the Bee , ends the remarkable book The Spirit of the Hive (Page 2013). The size of the ovaries, as well as their activity in terms of oogenesis pro- Corresponding author: K. Hartfelder, gression, is the main character that distinguishes [email protected] queens and workers of highly eusocial insects, Manuscript editor: David Tarpy and a large, active ovary essentially represents 50 K. Hartfelder et al. the fixation of the reproductive primacy of the body is the predominant tissue and of prime im- queen(s) against the thousands of subfertile portance for larval growth. (non-totipotent) or completely sterile workers liv- Questions concerning evolutionary aspects will ing in a colony. be addressed by including data on ovarian activity The honey bee, Apis mellifera ,isaprimeex- in stingless bees, the only other group of bees that ample for such structural and functional queen/ has reached the same level of a highly eusocial worker differences in the reproductive system, organization as the honey bees, and by drawing with very large ovaries, each typically consisting attention to parallels with the reproductive system of 120–200 serial units, the ovarioles, in the adult of male bees. Males are the neglected gender, not queen and small ovaries made up of 2–12 ovari- only among bees (Koeniger 2005) but also among oles each in the worker (Snodgrass 1956; social insects in general. Nevertheless, we be- Linksvayer et al. 2011). Furthermore, the sperm lieve that understanding gonad development storage organ, the spermatheca, is fully developed and the reproductive biology of males can shed in the queen, but only a remnant is present in the light on questions that may appear enigmatic, worker (Snodgrass 1956). In the adult females, such as the extraordinarily high number of ovar- these structural differences generated during ioles in Apis queens. preimaginal ovary development are also the basis for differences in ovary function or, in other 2. DEVELOPMENTAL BIOLOGY OF words, for worker sterility versus queen fertility. THE OVARY In this review, we will primarily focus on the question of ontogenetic mechanisms that govern 2.1. The embryonic gonad female gonad development. We start with the preimaginal stages, giving a brief overview on Except for studies investigating the embryonic gonad development, followed by an haplodiploid molecular mechanisms of the sex in-depth description on processes and mecha- determination pathway acting in early embryonic nisms that generate the divergence in gonadal stages (Beye et al. 2003;Hasselmannetal.2008), structure during the critical stages for caste differ- the embryonic development of honey bees has, entiation in the larval stages, when the adult ovar- until recently, not received nearly as much atten- iole number becomes determined. The subsequent tion as that of Drosophila . In fact, for thorough section is dedicated to the regulation of ovarian information, one must go back to studies done in activity in adult honey bees, especially the ques- the early twentieth century (Nelson 1915; tion of worker sterility. Throughout these sections, Schnetter 1935), followed later by detailed de- we will emphasize the importance of tissue or scriptions of embryonic stages (DuPraw 1967; organ-specific molecular studies, since global, Fleig and Sander 1986, 1988). Fortunately, this whole-body gene expression analyses unavoid- has somewhat changed once the fully sequenced ably merge the developmental dynamics of differ- honey bee genome became available, making pos- ent organs, making it difficult to arrive at insight- sible in-depth comparisons with Drosophila em- ful gene regulatory networks for a specific tissue. bryonic development (Cridge et al. 2017). Embry- This is especially the case for the reproductive onic development has since came under scrutiny system, which contains cellular elements of three primarily with respect to axial patterning, segmen- different embryonic origins, which, most likely, tation and Hox genes (Walldorf et al. 2000; also exhibit differences in their gene regulatory Dearden et al. 2006; Wilson et al. 2010), as well networks. These elements are the germ cells, the as microRNAs regulating such patterning genes mesoderm-derived (somatic) insect gonads and (Freitas et al. 2017). Another line of research ovarian ducts, and the ectoderm-derived genital addressed zygotic genome activation (Pires et al. imaginal discs. Furthermore, the transcriptomic 2016). All these studies were driven from the contribution of the reproductive system likely rep- perspective of comparative evolutionary develop- resents a very small percentage only in whole- mental biology. Nonetheless, compared to Dro- body analyses, especially in larvae, where the fat sophila melanogaster , very little is actually The honey bee ovary 51 known about the development of specific organs as elongated banana-shaped structures. In fact, for in A. mellifera. an embryologist, they do not look too different With respect to gonad development, a major from the elongated gonads of a day 10–11 mouse difference to Drosophila is apparent already at a embryo. The gonads are apically connected to very early step, namely the mode of germ cell each other over the dorsal midline, right beneath determination in the blastoderm stage. While the the dorsal vessel, and at their basal side emerges a prospective germ cells in Drosophila become string that bilaterally