Growth and development of the ovary and small follicle pool from mid fetal life to pre-puberty in the African elephant (Loxodonta africana)

Abstract

BackgroundFollicle numbers and developing ovarian morphology, particularly with reference to the presence of interstitial tissue, are intimately linked within the ovary of the African elephant during the period spanning mid-gestation to puberty. These have not been previously quantified in any studies. The collection of 7 sets of elephant fetal ovaries between 11.2 and 20.2 months of gestation, and 29 pairs of prepubertal calf ovaries between 2 months and 9 years of age during routine management off-takes of complete family groups in private conservancies in Zimbabwe provided an opportunity for a detailed study of this period.ResultsThe changing morphology of the ovary is described as the presumptive cortex and medulla components of the fetal ovary settled into their adult form. Interstitial tissue dominated the ovary in late fetal life and these cells stained strongly for 3β–hydroxysteroid dehydrogenase. This staining continued postnatally through to 4.5 years of age suggesting continued secretion of progestagens by the ovary during this period. The considerable growth of antral follicles peaked at 28% of ovarian volume at around 16.7 months of fetal age. The numbers of small follicles (primordial, early primary and true primary), counted in the cortex using stereological protocols, revealed fewer small follicles in the ovaries of animals aged 0 to 4.5 years of age than during either late fetal life or prepubertal life.ConclusionsThe small follicle populations of the late-fetal and prepubertal ovaries of the African elephant were described along with the changing morphology of these organs. The changes noted represent a series of events that have been recorded only in the elephant and the giraffe species to date. The expansion of the interstitial tissue of the fetal ovary and its continued presence in early post natal life may well contribute to the control of follicle development in these early years. Further research is required to determine the reasons behind the variation of numbers of small follicles in the ovaries of prepubertal calves.

Histology of 24 organs from Asian elephant calves (Elephas maximus)

“…The follicle reserve of the Asian elephant in this study was found to consist of early primary follicles (a single layer of cuboidal granulosa cells), true primary follicles (all cuboidal granulosa cells), and true primordial follicles (a single layer of squamous granulosa cells) grouped together as small follicles within the ovary. This is in agreement with previous studies on the African elephant, where the type of small follicles mostly found were early primary follicles and true primary follicles rather than primordial follicles ( Stansfield, Nöthling & Allen, 2012 ; Stansfield, Nothling & Ansari, 2011a ). Furthermore, the oocytes are larger in true primary follicles than in early primary follicles, suggesting activation of the follicle ( Picton, 2001 ) and also that true primary follicles do not belong to the ovarian reserve of the small follicle pool in the African elephant ( Stansfield, Nöthling & Allen, 2012 ) and possibly the Asian elephant as well.…”

“…This is in agreement with previous studies on the African elephant, where the type of small follicles mostly found were early primary follicles and true primary follicles rather than primordial follicles ( Stansfield, Nöthling & Allen, 2012 ; Stansfield, Nothling & Ansari, 2011a ). Furthermore, the oocytes are larger in true primary follicles than in early primary follicles, suggesting activation of the follicle ( Picton, 2001 ) and also that true primary follicles do not belong to the ovarian reserve of the small follicle pool in the African elephant ( Stansfield, Nöthling & Allen, 2012 ) and possibly the Asian elephant as well. It is necessary to determine the number of small follicles, including primordial, early primary and true primary follicles, in the ovaries of elephants, as the follicle reserve supplies oocytes throughout the reproductive cycle ( Stansfield, Nothling & Ansari, 2011a ).…”

“…The number of follicles in the ovary reserve of mammals is established during the development of the fetus and neonate. In Asian elephants, ovulation in each reproductive cycle is similar to that reported for African elephants ( Stansfield, Nöthling & Allen, 2012 ). A number of follicles in an Asian elephant calf are recruited each day and become atretic follicles, while very few develop into the dominant follicle.…”

“…The ovary of the African elephant has a lower density of small follicles per unit volume of ovarian cortex than other mammalian species ( Stansfield, Picton & Nöthling, 2011b ), including humans ( Faddy et al, 1992 ), suggesting that it is important to certify that a sufficiently large sample of ovarian specimens is used for the assessment of the number of small follicles in the Asian elephant ovary. The young Asian elephant ovary contained interstitial tissue within the medulla, similar to that reported in African elephants ( Stansfield, Nöthling & Allen, 2012 ), bovines ( Van Wezel & Rodgers, 1996 ) and other mammals ( Stansfield, Nöthling & Allen, 2012 ). There is a persistence of 3β-hydroxysteroid dehydrogenase (3βHSD)-positive nests of interstitial cells in the ovaries of female African elephant calves after birth ( Stansfield, Nöthling & Allen, 2012 ).…”

The Expression of Markers Related to Ovarian Germline Stem Cells in the Mouse Ovarian Surface Epithelium and the Correlation with Notch Signaling Pathway

“…In mouse ovaries, due to a large number of reproductive follicles that rupture at birth, the limited remaining germ cells are eventually wrapped in primitive granulosa cells and to form the primordial follicle pool [11,12]. As we known, the traditional view may suggest that the ovarian function gradually decrease with the female ages.…”