The dromedary camel displays annual variation in hypothalamic kisspeptin and Arg–Phe‐amide‐related peptide‐3 according to sex, season, and breeding activity

Abstract

The dromedary camel (Camelus dromedarius) is a desert mammal whose cycles in reproductive activity ensure that the offspring's birth and weaning coincide with periods of abundant food resources and favorable climate conditions. In this study, we assessed whether kisspeptin (Kp) and arginine–phenylalanine (RF)‐amide related peptide‐3 (RFRP‐3), two hypothalamic peptides known to regulate the mammalian hypothalamo‐pituitary gonadal axis, may be involved in the seasonal control of camel's reproduction. Using specific antibodies and riboprobes, we found that Kp neurons are present in the preoptic area (POA), suprachiasmatic (SCN), and arcuate (ARC) nuclei, and that RFRP‐3 neurons are present in the paraventricular (PVN), dorsomedial (DMH), and ventromedial (VMH) hypothalamic nuclei. Kp fibers are found in various hypothalamic areas, notably the POA, SCN, PVN, DMH, VMH, supraoptic nucleus, and the ventral and dorsal premammillary nucleus. RFRP‐3 fibers are found in the POA, SCN, PVN, DMH, VMH, and ARC. POA and ARC Kp neurons and DMH RFRP‐3 neurons display sexual dimorphism with more neurons in female than in male. Both neuronal populations display opposed seasonal variations with more Kp neurons and less RFRP‐3 neurons during the breeding (December–January) than the nonbreeding (July–August) season. This study is the first describing Kp and RFRP‐3 in the camel's brain with, during the winter period lower RFRP‐3 expression and higher Kp expression possibly responsible for the HPG axis activation. Altogether, our data indicate the involvement of both Kp and RFRP‐3 in the seasonal control of the dromedary camel's breeding activity.

Distribution of GnRH and Kisspeptin Immunoreactivity in the Female Llama Hypothalamus

“…In seasonal breeders, kisspeptin cells are reported to undergo variations in their product synthesis as a consequence of photoperiodic changes that affect both ARC and POA cell populations in a species-specific fashion (10). In line with this, dromedary camels (displaying reproductive seasonality between November and April in Morocco) exhibit twice the number of immunoreactive kisspeptin cells in both the POA and ARC during the breeding season than in the non-breeding season, and this increase is more marked in females (40). Conversely, female llamas-and other South American camelids-are not considered seasonal breeders, exhibiting ovarian cyclicity, conception, and labour all year round (41)(42)(43) similarly as observed in the llama herd involved in the present study; in their natural habitat, breeding seasonality is associated to management practices, as a short wet and warm season restricts the abundance of highquality forage between December and March in the high Andes (44).…”

GnRHand the photoperiodic control of seasonal reproduction: Delegating the task to kisspeptin andRFRP‐3

“…This is true not only for long-day breeders such as male and female Syrian and Siberian hamsters, 195,230,239,251,260 female Turkish hamsters, 206 male European hamsters, 114 male and female Jerboas, 197 female Brandt's voles, 200 male water voles 261 and male wild-derived mice, 202 but also for short-day breeders such as ewes, 231,232 female brushtail possums, 262 female goats, 263 and male and female dromedary camels. 201 Additionally, the number of RFRP-3 fibers contacting GnRH neurons in the Siberian hamster and ewe 232,239 and NpffR2 expression in the Syrian hamster 238 are lower in short-compared to long-day conditions. Altogether, these neuroanatomical data demonstrate that the high expression under long days and the short day/winter decrease in the RFRP-3/NPFFR2 system is the same among seasonal mammals, which points to conserved mechanisms for the seasonal regulation of Npvf expression, regardless of whether the animals are male or female, or long or short day breeders (Figure 2).…”

“…[226][227][228] In mammals, Npvf-expressing neurons are mainly located in the dorsomedial and ventromedial nuclei of the hypothalamus (DMH/VMH) in multiple species, including rodents, 225,[228][229][230] sheep, 231,232 humans, 233 non-human primates, 181,234 cattle, 235 horses 236 and camels. 201 RFRP-3 fibers project to various intraand extra-hypothalamic areas where the specific RFRP-3 receptor GPR147 (also known as NPFFR2) is also found, providing divergent neural pathways by which RFRP-3 might influence various biological functions. 228,237,238 Notably, RFRP-3 fibers project to the POA and form close contact with 20%-40% GnRH neurons, and approximately one-third of GnRH neurons expresses NPFFR2.…”

Seasonal morphology and immunoreactivity of cytokeratin and atrial natriuretic peptide in dromedary camel poll glands

“…Additionally, camels have mating‐induced ovulation (Marai et al., 2009) and long gestation period (13 months) which may be affected by conception date (Elias et al., 1991) and food availability (Yagil & Etzion, 1984). Thus, dromedary camel reproductive activities (mating, ovulation and parturition) occur at the same season of the year depending on its geographical distribution (Ainani et al., 2018, 2020). These reproductive activities are associated with rainy season which is characterised by low ambient temperature and food availability (Ainani et al., 2018, 2020; Ghazi, 2007; Hegazy et al., 2004; Tingari, et al., 1984).…”

“…Thus, dromedary camel reproductive activities (mating, ovulation and parturition) occur at the same season of the year depending on its geographical distribution (Ainani et al., 2018, 2020). These reproductive activities are associated with rainy season which is characterised by low ambient temperature and food availability (Ainani et al., 2018, 2020; Ghazi, 2007; Hegazy et al., 2004; Tingari, et al., 1984).…”