Models of embryonic diapause in Carnivora

Abstract

The phenomenon of obligate embryonic diapause, comprising developmental arrest at the blastocyst stage, has been recognized to occur in more than 60 species in three families in the Order Carnivora. The evolutionary advantage believed to be conferred by this trait is that it permits mating and parturition to occur at the most favorable times of year for reproductive success and offspring survival. The carnivore blastocyst in diapause consists of hundreds of cells, configured in the classic mammalian compartments of inner cell mass and trophoblast. It is encapsulated in a glycoprotein coat, derived, at least in part, from the zona pellucida of the parent oocyte. The temporal uncoupling of mating from parturition is regulated by changes in the annual photoperiod, mediated through the pineal gland, pars tuberalis a pars distalis of the pituitary and thyroid glands. In the best-studied species, the pituitary signal that awakes the embryo from arrest is prolactin, acting on the ovary and on the uterus. Ovarian signals, other than progesterone are not well understood, but it appears that there is an ovarian peptide essential for the reactivation of the embryo in mink. New studies have identified the uterine signals in the mink, and it has been shown that the synthesis and secretion of polyamines activates the mink embryo from diapause. While extensive progress has been made, it is not clear whether the regulatory mechanisms that have been identified in the better-known species are universal to carnivore diapause. As many of the carnivore species are endangered, further research on diapause is essential to their survival.

Extrinsic and intrinsic factors drive the timing of gestation and reproductive success of Scandinavian brown bears

“…Although photoperiod is recognized as the main driver of the termination of embryonic diapause in non-hibernating carnivore species (Murphy and Fenelon, 2020), neither day length at den entry (the last day the female had potentially full access to this cue) nor the date of den entry itself (which is associated with a sharp decrease in perceived light) had a significant effect on CL reactivation (Supplementary Table 1). Furthermore, if photoperiod was the main cue synchronizing the end of embryonic diapause in ursids, implantation and parturition dates should occur in a narrow time range.…”

“…The embryonic diapause terminates with the reactivation of the CL causing a surge in progesterone (Tsubota et al, 1987;Tsubota and Kanagawa, 1993), and is followed by embryos' implantation in November-December after the female has entered her den (Wimsatt, 1963;Kordek and Lindzey, 1980). In other carnivores with a delayed implantation, there is a time span of several days between the CL reactivation and the implantation of the blastocysts, referred to as secretory phase, and during which the uterus lining prepares itself to receive the fertilized eggs by producing a hospitable environment (6-10 days in the American mink Neovison vison, Murphy et al, 1981;Murphy and Fenelon, 2020). To our knowledge, the duration of the secretory phase remains unknown in ursids which precludes the exact determination of the active gestation length.…”

“…But to our knowledge, no study has so far investigated the impact of these factors on the brown bear reproduction, with the exception of Friebe et al (2014) who found that favorable environmental conditions (formulated as a yearling body condition index as a proxy for food abundance) were correlated with a later parturition in Scandinavian brown bears in the southern range of their distribution. In contrast, the annual variation in daily lightdark cycles offers a highly predictive signal and is believed to be the main cue that synchronizes seasonal reproductive events in mammals, including the termination of embryonic diapause in non-hibernating carnivores (reviewed in Murphy and Fenelon, 2020). However, it is still unclear if this parameter plays a crucial role in the Scandinavian brown bear, as most females use underground den sites (Manchi and Swenson, 2005) that are snow covered from October to April (Swedish Meteorological and Hydrological Institute), which could reduce the perception of sun light in the den (Evernden and Fuller, 1972).…”

Multiple types of genomic variation contribute to adaptive traits in the mustelid subfamily Guloninae

“…Regulation of pineal melatonin secretion is influenced by a neural pathway that includes the circadian oscillators (Goldman 1999). Moreover, seasonal diapause is observed to be predominant among carnivores (Renfree and Fenelon 2017), and maintaining elevated melatonin in mink and spotted skunks has been shown to prolong embryonic diapause (Murphy and Fenelon 2020). FBXL3, associated with maintenance of circadian clock oscillation in mammals (Siepka et al 2007;Shi et al 2013;Fenelon et al 2017) is duplicated and rapidly evolving in sable, indicating an important role in regulating both daily and seasonal activity and possibly onset of diapause.…”

“…Maintaining elevated melatonin in mink and spotted skunks has been shown to prolong embryonic diapause (Murphy & Fenelon, 2020). FBXL3, associated with maintenance of circadian clock oscillation in mammals (Fenelon et al, 2017;Shi et al, 2013) is duplicated in sable, indicating its possible relation to diapause regulation.…”