Effects of Exposure to Male Goat Hair Extracts on Luteinizing Hormone Secretion and Neuronal Activation in Seasonally Anestrous Ewes

Abstract

In sheep and goats, exposure of seasonally anestrous females to males or their fleece/hair activates the gonadotropin-releasing hormone (GnRH) pulse generator leading to pulsatile luteinizing hormone (LH) secretion. Pheromones emitted by sexually mature males are thought to play a prominent role in this male effect. In the present study, we first aimed to clarify whether the male goat pheromone is effective in ewes. Seasonally anestrous St. Croix ewes were exposed to hair extracts derived from either intact or castrated (control) male Shiba goats. The male goat-hair extract significantly increased LH secretion compared to the control, suggesting that an interspecies action of the male pheromone occurs between sheep and goats. Using the male goat-hair extract as the pheromone source, we then aimed to clarify the neural pathway involved in the signal transduction of the male pheromone. Ewes were exposed to either the goat-hair extract or the control and sacrificed 2 hr after the exposure. Expression of c-Fos, a marker of neuronal activation, was immunohistochemically examined. The male goat-hair extract significantly increased the c-Fos expression compared to the control in regions of the vomeronasal system, such as the accessory olfactory bulb and medial amygdala, and the arcuate nucleus. The main olfactory bulb did not exhibit any significant increase in the c-Fos expression by the male goat-hair extract. This result suggests that the neural signal of the male pheromone is conveyed to the GnRH pulse generator through the activated regions in ewes.

The comparison of reproductive hormone receptor expressions of the sheep ovary and hormone concentrations in two Chinese breeds

“…In temperate zones, climatic changes occur concomitantly with changes in seasons, and environmental factors such as temperature, day length and food supply are drastically altered. Some animals, such as hamsters (Weems, Goodman, & Lehman, 2015), deer (Barrell et al, 2016), buffalo (de Carvalho, Soares, & Baruselli, 2016), goats and sheep (Ohara et al, 2014), prefer to give birth in warm and food abundant seasons. Consequently, they exhibit physiological seasonal regulation in step with the changing seasons, known as seasonal reproduction.…”

The “ram effect”: new insights into neural modulation of the gonadotropic axis by male odors and socio-sexual interactions

“…In the accessory olfactory bulb on the other hand while Fos expression was higher after exposure to male odor than after the control situation it showed a similar response to female odor, indicating that the accessory olfactory system may respond more generally to social odors rather than in selective detection of those associated with males. These results are however challenged by a recent study which found Fos activation in the accessory but not the main olfactory system of St Croix ewes in response to extracts of hair from male goats that induce an increase in LH secretion (Ohara et al, 2014 ). However, the physiological relevance of these intriguing results remains to be established.…”

“…The olfactory stimuli which generate the “ram effect” are not strictly species specific since hair from male goats stimulates LH pulsatile secretion (Over et al, 1990 ) and induces ovulation in ewes (Birch et al, 1989 ). A recent study showed that an acidic fraction of male goat hair that stimulated multiunit activity of the mediobasal hypothalamus of ovariectomized Shiba goats also stimulated pulsatile LH secretion in St Croix ewes (Ohara et al, 2014 ). The same group has also used this approach to show that 4-ethyloctanol is of key importance for activating the GnRH pulse generator in goats (Murata et al, 2014 ).…”

“…This pulsatile secretion of GnRH is regulated by gonadal steroids at the level of the mediobasal hypothalamus (Knobil, 1981 ; Karsch, 1984 ; Maeda et al, 2010 ; MBH) by mechanisms that are not yet clear (Tsutsumi and Webster, 2009 ). Studies from a Japanese group have correlated, multiunit electrical activity of neurons in the MBH with the LH response to male goat odor in ovariectomized females (Mori et al, 1991 ; Hamada et al, 1996 ; Murata et al, 2014 ) and this area of the brain is also thought to be central to the male effect in sheep (De Bond et al, 2013 ; Ohara et al, 2014 ).…”

The olfactory secretome varies according to season in female sheep and goat

“…By contrast, exposing females to the odour of the male (wool, hair) strongly stimulates LH pulsatility in both sheep and goat (4,5) and therefore, the effect of the ram or the buck on the LH secretion of females can be mimicked by presentation of their odours (6,7). According to the definition of Karlson and Lüscher (8), ram and buck odours could thus be classified as primer pheromones, but several authors reported that goat "pheromones" could induce LH secretion in anoestrus ewes (9,10). This apparent lack of specificity is clearly not in favour of a pheromonal action.…”