Luteogenesis during the estrous cycle in Asian elephants (Elephas maximus)

Abstract

The occurrence of multiple corpora lutea (CLs) in the ovaries of the cycling and pregnant elephant, a monovulatory mammal, has driven scientific discussions during the past five decades. However, fundamental knowledge on luteogenesis is lacking. In this long-term study, CL formation and regression throughout the estrous cycle were monitored using transrectal 2D-and 3D ultrasonography in 33 captive Asian elephants. Serum or urinary progestagens (P m ) were measured to determine the reproductive cycle stage. In seven females, serum P m and LH concentrations were directly related to ovarian events. We have found two different modalities of luteal development: one for the accessory CL (acCL) and one for the ovulatory CL (ovCL). acCLs were derived from luteinization of larger, subordinate follicles after the first anovulatory LH peak. The dominant follicle produced the largest CL after the second (ovulatory) LH peak. The first luteal tissue formation became visible w10 days after the respective LH peak. After ovulation, it took 29.8G5.0 days for the acCLs to reach their maximum diameter, whereas the ovCL reached a significantly larger size (33.2G2.3 mm, P!0.0001) about 10-15 days later. All CLs were visible throughout the new follicular phase, with some of the larger ones still present in the subsequent luteal period. In this study, we have demonstrated that Asian elephants have evolved a novel method for luteal development and function, and by repeatedly forming two types of distinctly different CLs for every reproductive cycle, they have ensured that there will be sufficient luteal capacity for maintaining a 22-month pregnancy should conception occur.

The Secretory Pattern and Source of Immunoreactive Prolactin in Pregnant African (<i>Loxodonta africana</i>) and Asian (<i>Elephas maximus</i>) Elephants

“…Active secretion of PRL might play an important role for the maintenance of pregnancy in elephants [58]. Pregnant African and Asian elephants possess multiple corpora lutea in their ovaries throughout gestation [21,[59][60][61]. Allen et al demonstrated that the placenta of the elephant is steroidogenically inert [31].…”

Gestating for 22 months: luteal development and pregnancy maintenance in elephants

“…(b) Ultrasound A total of 336 transrectal ultrasound examinations were performed using previously reported approaches [13,25,26]. Five Asian elephants were ultrasonographically examined on random days during the entire pregnancy and in one case until day 459.…”

“…We showed previously that during the six-week-long follicular phase of the oestrous cycle, the acCLs are derived from luteinized unruptured follicles [26]. Luteinization of the first wave of follicles is induced by the first, anovulatory LH peak.…”

“…Luteinization of the first wave of follicles is induced by the first, anovulatory LH peak. Three weeks later, a second LH peak occurs which induces ovulation of a single-dominant follicle [26]. However, some intriguing questions remain unanswered: are there additional CLs forming during early pregnancy?…”

Luteal maintenance of pregnancy in the African elephant (Loxodonta africana)

“…In pregnant elephant, in contrast, mature follicles are rarely, if ever, seen in the maternal ovaries (Perry 1964, Short & Buss 1965, Laws 1969, Hodges 1998, Allen 2006 and it is now proposed that the accessory CLs of pregnancy first form as a result of luteinisation of small (0.8-1.2 cm) follicles that develop in response to the first of the two peaks in serum LH concentrations which characterise the 20-22 day inter-luteal period of the elephant oestrous cycle (Lueders et al 2010(Lueders et al , 2011. These accessory luteal structures, seen clearly by serial transrectal ultrasonographic examinations of the maternal ovaries (Lueders et al 2011), form predominantly, but not exclusively, on the ovary ipsilateral to the uterine horn that will contain the conceptus (Allen et al 2002), and they apparently remain dormant (and non-secretory) during the remainder of the inter-luteal phase, the release of the second ovulation-inducing LH peak (Kapustin et al 1996, Brown et al 1999) and early gestation.…”