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Ovarian Dynamics and Follicle Development in Aves

Maintained by the Johnson Laboratory at the Center for Reproductive Biology and Health Health (CRBH), The Pennsylvania State University

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Background


The avian ovary represents a truly dynamic organ system capable of fostering the annual development of one or more broods of viable eggs, then undergoing nearly complete regression followed by eventual recrudescence. A unique morphological and functional aspect of the reproductively active avian ovary, as compared to the mammalian counterpart, is that follicles at all stages of development, from resting primordial and primary follicles to the fully differentiated preovulatory stage, exist simultaneously during egg-laying. As a consequence, the sequential selection of one undifferentiated follicle into the final rapid growth stage of development provides for ovulation of an oocyte from a fully differentiated follicle on an approximate daily basis (the interval between ovulations being species-dependent). The ovarian follicular hierarchy is a reflection of oviparity and is a feature held in common with avian predecessors, the reptiles and apparently some dinosaurs (Sato et al., Science 308(5720): 375, 2005).

Whereas all modern crocodilians have two functional ovaries, avian fossils from two species of an extinct lineage (enantiornithine birds of the Early Cretaceous period) have revealed that these ancestors possessed a single, functional left ovary (Zheng et al., Nature. 2013 Mar 28;495(7442):507-11). This is consistent with the hypothesis that the loss of one ovary to reduce body weight preceded the capacity for true flight. Interestingly, viviparity has evolved nearly 100 times within the lineage that includes lizards and snakes; thus, it is unclear why there is no incidence of viviparity within the avian lineage. One line of reasoning is that because extant birds are endothermic and can precisely control the process of egg incubation and embryo development, there may be no thermoregulatory advantage to viviparity in birds.

 

 ovary

In the mature hen, the four to six largest preovulatory follicles (9-35+mm diameter; F6 to F1) represent those that have already undergone the process of follicle selection in preparation for ovulation. The most recently selected follicle (F6, 9-12 mm) is selected each day from a cohort (predictably numbering 8 to 12) of prehierarchal follicles (arrows) measuring 6-8 mm. The follicle reserve is represented by slow growing (0.5-5 mm) and resting (<.5 mm) follicles. Among avian species, the number of preovulatory follicles developed and eggs produced within a clutch is species-specific.

While there are some excellent field studies documenting seasonal changes in reproductive hormones and comparing ovarian dynamics among free ranging species (e.g., see Wingfield and Farner, 1993, The endocrinology of wild species. In: Avian Biology, D. S. Farner, J. R. King, and K. C. Parkes, eds., vol 9, pp. 163-327, Academic Press, New York), the majority of information pertaining to cellular and molecular mechanisms regulating follicle growth and differentiation has been derived primarily from domesticated birds. This is largely due to the quantity and ready availability of tissues required for detailed studies, but nevertheless leaves open the question as to what extent models of ovarian organization and function developed from genetically-manipulated avian models maintained under well-controlled environmental and nutritional conditions directly pertain to wild birds.

This website represents an effort to collate data from previously published plus ongoing genomic, cellular and physiologic studies and make these avian data readily accessible to all comparative reproductive physiologists and endocrinologists for further analyses. It is envisioned that ultimately this resource will highlight the advantages of applying molecular and cellular techniques to address physiological and organismal questions in non-traditional animal model systems. A second objective is to highlight some of the many unresolved questions that can assist both field and bench biologists in developing more refined working models of ovarian function to better understand the remarkably diverse and successful reproductive strategies attributed to avian species.

The following links provide summaries of published and unpublished data related to avian follicle growth, follicle selection, the differentiation of granulosa cells during follicle development, and apoptotic pathways that contribute to avian follicle atresia:

This material is based upon work supported by the National Science Foundation

 NSF Logo NSF IBN-9419613
NSF IBN-0131185
NSF IOB-0445949
NSF IOS-0968784

Any opinions, findings, and conclusions
or recommendations expressed in this
material are those of the author(s) and do
not necessarily reflect the views of the National
Science Foundation.
 Csrees logo  USDA NRICGP 92-37203-8337
 USDA NRICGP 95-37203-1998
 USDA NRICGP 99-35203-7736
 NIH Logo  NIH HD36095
 DOD Logo  DOD DAMD17-03-1-0206

For additional information contact:

A.L. Johnson, Ph.D.
Department of Animal Science
The Pennsylvania State University
213 Henning Building
University Park, PA 16802 U.S.A.
email: alj14@psu.edu