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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

Authors
  • Hartfelder, Klaus1
  • Tiberio, Gustavo Jacomini1
  • Lago, Denyse Cavalcante1
  • Dallacqua, Rodrigo Pires2
  • Bitondi, Marcia Maria Gentile3
  • 1 Universidade de São Paulo, Departamento de Biologia Celular e Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Av. Bandeirantes 3900, Ribeirão Preto, SP, 14049-900, Brazil , Ribeirão Preto (Brazil)
  • 2 Universidade Federal de Mato Grosso do Sul, Instituto de Biociências, Cidade Universitária, Campo Grande, MS, 14049-900, Brazil , Campo Grande (Brazil)
  • 3 Universidade de São Paulo, Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Av. Bandeirantes 3900, Ribeirão Preto, SP, 14040-901, Brazil , Ribeirão Preto (Brazil)
Type
Published Article
Journal
Apidologie
Publisher
Springer-Verlag
Publication Date
Oct 11, 2017
Volume
49
Issue
1
Pages
49–70
Identifiers
DOI: 10.1007/s13592-017-0548-9
Source
Springer Nature
Keywords
License
Yellow

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 developmental 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.

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