Ovarioles (Insects)

Ovarioles are egg-producing tubules that are the fundamental units of ovaries in female insects. The number of ovarioles in each ovary is typically 4-8, but varies widely depending on the particular insect and its ecology.

GENERAL ARRANGEMENT AND STRUCTURE

Each ovariole is a tube in which oocytes form at one end and complete development as they reach the other. The terminal filament and the germarium, which contains germ cells, are at the distal end. Ovarioles may have one of several topological arrangements within an ovary. In some species ovarioles join the end of an oviduct radially around a central point. In others, ovarioles arise in single file off the oviduct, like teeth on a comb.

NUMBER

The number of ovarioles per ovary varies with taxon, size, and life history. All Lepidopteran females have four ovarioles, but many groups tend to be more variable, both within and across species. Variability in ovariole number is particularly spectacular in social insects. Obligately sterile workers in ants can lack ovarioles entirely, and the most fecund queens in ants and termites have about 1200 ovarioles per ovary.

DEVELOPMENTAL ORIGIN

The period during which ovarioles form varies widely in insects, ranging from embryonic development in aphids to the pupal stage in flies. In some taxa, the number of ovarioles can be adjusted based on environmental factors. In Drosophila, for example, ovarioles form during the pupal period. This timing provides the opportunity for the number of ovarioles constructed to be adjusted based on previous diet and temperature. In honey bees, however, ovarioles form in early larval development. The number of ovarioles formed is at first the same in future queens and workers. In workers, however, most ovarioles undergo cell death, whereas those in developing queens persist.


SOMATIC TISSUE AROUND DEVELOPING OOCYTES

Each ovariole is made up of both somatic and germ cells. The somatic tissue includes a tubular sheath surrounding all the developing eggs as well as follicle cells around each oocyte. The sheath consists of inner and outer layers. The outer sheath is an open network of cells, sometimes containing muscle. The tissue is rich in lipids and glycogen and is metabolically active. Even so, there is no evidence of direct involvement in oocyte development. Tracheoles form part of the outer sheath but do not penetrate below it. The outer sheath can be important in sequestering bacterial symbionts that will be passed on to offspring. The inner sheath is a layer of extracellular matrix. In addition to physical support, the inner sheath can function as a sieve.
A layer of follicle cells surrounds each developing oocyte. Follicle cells are very active metabolically, contributing a variety of materials essential to developing eggs. During yolk uptake, follicle cells can separate slightly, allowing vitellogenin-laden hemolymph to contact the oocyte surface directly. The oocyte then can take up vitellogenin and other nutrients. As egg development nears completion, follicle cells secrete the eggshell, which consists of vitelline envelope and layers of chorion.

PATTERNS OF OOCYTE DEVELOPMENT

Ovarioles can be categorized based on how oocytes are produced from stem germ cells (Fig. 1). A stem germ cell produces two daughter cells when it divides; one remains a stem cell and the other becomes a cystoblast. Most commonly, cystoblasts undergo rounds of division but remain connected by intercellular bridges. This process is called cluster formation. Generally, only one of the daughter cells in a cluster becomes an oocyte, while the remainder degenerate or become nurse cells. The type of oocyte development in which an oocyte is connected to sister cells that contribute to the contents of the egg is termed meroistic.
Patterns of oocyte development. (A) Panoistic ovary of an apterygote insect, Leppisma saccharina. G, germarium; FC, follicle cell. (Reprinted from R. C. King and J. Buning, 1985. The origin and functioning of insect oocytes and nurse cells. In "Comprehensive Insect Physiology, Biochemistry, and Pharmacology," Vol. 1, pp. 37-82, with permission from Elsevier Science.) (B) Teletrophic ovary of a heteropteran insect, Dysdercus intermedius. The nutritive cords (NC) extending from the nurse cells to the oocyte are clearly visible. (C) Polytrophic ovary of a carabid beetle, Nebria brevicollis.
FIGURE 1 Patterns of oocyte development. (A) Panoistic ovary of an apterygote insect, Leppisma saccharina. G, germarium; FC, follicle cell. (Reprinted from R. C. King and J. Buning, 1985. The origin and functioning of insect oocytes and nurse cells. In “Comprehensive Insect Physiology, Biochemistry, and Pharmacology,” Vol. 1, pp. 37-82, with permission from Elsevier Science.) (B) Teletrophic ovary of a heteropteran insect, Dysdercus intermedius. The nutritive cords (NC) extending from the nurse cells to the oocyte are clearly visible. (C) Polytrophic ovary of a carabid beetle, Nebria brevicollis.
Stem cells in ovarioles of the most primitive insects do not undergo cluster formation. Instead, each cystoblast develops into an oocyte. Such ovarioles are called panoistic. Insect orders that have primitively panoistic ovaries are Archeognatha, Thysanura, Odonata, Embioptera, and most of the orthopteroid orders. Plecoptera shows an interesting intermediate condition, in which cluster formation occurs, but all the daughter cells become oocytes. Panoistic ovaries are also found in more recently derived insect groups, in which the design has evolved secondarily, and these taxa include Siphonaptera, Strepsiptera, and Thysanoptera.
Meroistic ovaries can be subdivided into two types based on the location of accessory germ cells relative to the oocyte. In polytrophic ovaries, accessory germ cells maintain short connections and accompany the oocyte as it moves down the ovariole. In telotrophic ovaries, accessory tissue remains at the distal end of the ovariole.
In polytrophic ovaries, follicle cells encapsulate both the nurse cells and the oocyte. Nurse cells generally are polyploid and express genes whose products are transported to the growing egg. Trichoptera, Lepidoptera, Hymenoptera, Diptera, adephagan Coleoptera, Mecoptera, and Neuroptera all have polytrophic ovaries.
In telotrophic ovarioles, accessory nurse cells remain in the anterior part of the ovariole and so, as an oocyte moves away, cords of oocyte tissue lengthen to maintain the connection. Teletrophic ovaries have apparently evolved independently several times. In Heteroptera, Coleoptera (Polyphaga), Raphidioptera, and Megaloptera, they evolved from polytrophic ovaries. Telotrophic Ephemeroptera evolved directly from panoistic ancestors.
An army ant queen (Eciton burchelli) shows extreme development of ovarioles in both number and length.
FIGURE 2 An army ant queen (Eciton burchelli) shows extreme development of ovarioles in both number and length.
Ovariole architecture is related to both phylogeny and life history. Both panoistic and meroistic ovarioles can support very rapid egg production as illustrated by the more than 40,000 eggs/day produced by both the panoistic ovarioles of the most fecund termite queens and the polytrophic ovarioles of the most fecund ants (Fig. 2). An important consequence of panoistic vs meroistic eggs is duration of embryonic development. The design of meroistic ovarioles facilitates the production of eggs well-stocked with ribosomes, mRNA, tRNA, and other macromolecules. Such eggs generally develop rapidly, as exemplified by Drosophila melanogaster. In contrast, autonomous oocytes produced by panoistic ovaries require longer periods to complete embryogenesis.

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