Role of the Double Luteinizing Hormone Peak, Luteinizing Follicles, and the Secretion of Inhibin for Dominant Follicle Selection in Asian Elephants (Elephas maximus)1

Abstract

Elephants express two luteinizing hormone (LH) peaks timed 3 wk apart during the follicular phase. This is in marked contrast with the classic mammalian estrous cycle model with its single, ovulation-inducing LH peak. It is not clear why ovulation and a rise in progesterone only occur after the second LH peak in elephants. However, by combining ovarian ultrasound and hormone measurements in five Asian elephants (Elephas maximus), we have found a novel strategy for dominant follicle selection and luteal tissue accumulation. Two distinct waves of follicles develop during the follicular phase, each of which is terminated by an LH peak. At the first (anovulatory) LH surge, the largest follicles measure between 10 and 19.0 mm. At 7 ± 2.4 days before the second (ovulatory) LH surge, luteinization of these large follicles occurs. Simultaneously with luteinized follicle (LUF) formation, immunoreactive (ir) inhibin concentrations rise and stay elevated for 41.8 ± 5.8 days after ovulation and the subsequent rise in progesterone. We have found a significant relationship between LUF diameter and serum ir-inhibin level (r(2) = 0.82, P < 0.001). The results indicate that circulating ir-inhibin concentrations are derived from the luteinized granulosa cells of LUFs. Therefore, it appears that the development of LUFs is a precondition for inhibin secretion, which in turn impacts the selection of the ovulatory follicle. Only now, a single dominant follicle may deviate from the second follicular wave and ovulate after the second LH peak. Thus, elephants have evolved a different strategy for corpus luteum formation and selection of the ovulatory follicle as compared with other mammals.

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

“…However, the findings in the present study lend strong circumstantial support to the novel proposal by Lueders et al (2011) that these accessory luteal structures form initially by luteinisation of relatively small (5-15 mm diameter) follicles shortly after the first of the two pronounced serum LH peaks which characterise the 3-week inter-luteal period in the elephant, but with the notable exception that, clearly as shown by our demonstration of ovulation stigmata on many of the accessory CL, some of these follicles can actually ovulate before luteinisation commences. In others, particularly the smaller follicles situated deep in the ovarian stroma, luteinisation without ovulation occurs as proposed by Lueders et al (2011). It is not currently understood why, if ovulation occurs at the first LH peak and mating behaviour involving young bulls is observed (Moss 1983), that pregnancy does not ensue.…”

“…1h). Thus, it seemed reasonable to conclude that this animal had probably been in oestrus recently and the 'blood spot' represented the recent, possibly fertile, ovulation resulting from the second LH peak of the inter-luteal period while the nine luteal bodies, three of which had clear ovulation stigmata, represented the luteinised follicles described by Lueders et al (2011) as developing following the first LH rise of the inter-luteal period that had occurred 3 weeks previously.…”

“…Hodges 1998 and others), the more so since significant follicular growth is not seen at any stage of gestation in the elephant ovary (Allen 2006, Lueders et al 2011. However, the findings in the present study lend strong circumstantial support to the novel proposal by Lueders et al (2011) that these accessory luteal structures form initially by luteinisation of relatively small (5-15 mm diameter) follicles shortly after the first of the two pronounced serum LH peaks which characterise the 3-week inter-luteal period in the elephant, but with the notable exception that, clearly as shown by our demonstration of ovulation stigmata on many of the accessory CL, some of these follicles can actually ovulate before luteinisation commences.…”

“…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.…”

“…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. They then enlarge greatly to reach diameters of 10-38 mm (Hodges 1998, Lueders et al 2011) and begin to secrete appreciable quantities of 5a-dihydroprogesterone (5aDHP) and other 5a-pregnanes (Hodges et al 1994(Hodges et al , 1997, as evidenced by the sharp increase in maternal serum progestagen concentrations at this time (Meyer et al 2004). Whereas eCG secreted by the foetal endometrial cups (Allen & Moor 1972) is the stimulus for secondary luteal development in the pregnant mare (Allen 1975, Terqui & Palmer 1979, it now seems very likely that placental lactogen (elPL) secreted by the trophoblast from around the time of implantation and commencing development of the zonary endotheliochorial placenta is the essential luteotrophic stimulus in the pregnant elephant .…”