Sequential ovulation and fertility of polyoestrus in American black bears (Ursus americanus)

Himelright, Brendan M.; Moore, Jenna M.; Gonzales, Ramona L.; Mendoza, Alejandra V.; Dye, Penny S.; Schuett, Randall J.; Durrant, Barbara S.; Read, Betsy; Spady, Thomas J.

doi:10.1093/conphys/cou051

Cited by 41 publications

(6 citation statements)

References 21 publications

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“…As noted above, seasonal factors such as light, rain and food availability are also controlling factors. One especially interesting strategy is that of the black bear, in which recurrent oestruses allow the relatively solitary bear to gain multiple paternity of her young via sequential ovulations and matings, so that the conceptuses of each mating enter diapause and later reactivate together (Himelright et al, 2014). Thus, the selective advantage of diapause allows species to synchronise their reproduction to benefit fitness and fecundity.…”

Section: Discussionmentioning

confidence: 99%

The enigma of embryonic diapause

2017

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Embryonic diapause - a period of embryonic suspension at the blastocyst stage - is a fascinating phenomenon that occurs in over 130 species of mammals, ranging from bears and badgers to mice and marsupials. It might even occur in humans. During diapause, there is minimal cell division and greatly reduced metabolism, and development is put on hold. Yet there are no ill effects for the pregnancy when it eventually continues. Multiple factors can induce diapause, including seasonal supplies of food, temperature, photoperiod and lactation. The successful reactivation and continuation of pregnancy then requires a viable embryo, a receptive uterus and effective molecular communication between the two. But how do the blastocysts survive and remain viable during this period of time, which can be up to a year in some cases? And what are the signals that bring it out of suspended animation? Here, we provide an overview of the process of diapause and address these questions, focussing on recent molecular data.

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Section: Discussionmentioning

confidence: 99%

The enigma of embryonic diapause

2017

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“…The peak of brown bear estrus is in early summer [31]. Body temperature and motion sensor data from free-ranging brown bears in Sweden, were used to calculate the mean date of implantation as December 1, with parturition approximately 56 days later [5], indicating a diapause of five month duration.…”

Section: Ursidsmentioning

confidence: 99%

“…This permits subsequent ovulations and matings and a litter derived from more than one sire. Superfetation is known to occur in black bears (Ursus americanus) [5] European badgers (Meles meles) [6,7] and American mink (Neovison vison) [8]. An advantage conferred by superfetation is introduction of genetic variation by polyandry [7].…”

Section: Introductionmentioning

confidence: 99%

Models of embryonic diapause in Carnivora

Murphy¹,

Fenelon²

2020

Proc

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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.

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“…While the giant panda is a monoestrous spontaneous ovulator, most of the other investigated bear species are polyoestrous (i.e. American black bear, polar bear, brown bear and sun bear) and may undergo induced ovulation, although the latter does not always seem to require coitus but merely presence of a male, as is the case for the polar bear and potentially the American black bear (American black bear [1][2][3][4][5][6][7], Asian black bear [4], Japanese black bear [8,9], Formosan black bear [10], polar bear [5,11,12], (Hokkaido) brown bear [13][14][15][16] and the sun bear [17][18][19]). Almost all bear species, including the giant panda, are thus seasonal breeders [14], except for certain (sub)tropical bear (sub)species of which the sun bear is probably the best studied one.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary survival strategies of the female giant panda: optimizing energy resources and expenditure prior to pregnancy by postponing corpus luteum reactivation

Wauters

Wilson

Bouts³

et al. 2022

Preprint

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The giant panda reproductive physiology shows important similarities with at least six of the eight existing bear species: the occurrence of diapause and/or pseudopregnancy is commonly described in bears. Nevertheless, significant differences including the earlier breeding season with - in general - a single estrus, a shorter delay of implantation and a more variable birth season, indicate an evolutionary adaptation from the seasonal reproductive traits described in hibernating bear species. In this study we aimed to determine true pregnancy length for giant pandas and to open the discussion on the peculiarities of giant panda reproductive biology, more specifically focusing on the rationale behind their short-seasoned reproductive cycle compared to the other bear species. For this purpose, metabolic (body weight and fecal output) profiles were matched with endocrine changes, mainly urinary progesterone metabolites, in 5 pregnant, 8 non-birth and 6 pseudopregnant cycles of 6 female giant pandas. Pregnancy in giant pandas lasts only 42 days from early reactivation of the corpora lutea (CLs) until birth. In addition, our findings urged the need to redefine the generally accepted biphasic progesterone profile into a triphasic primary progesterone rise (corpus luteum dormancy (CLD) I, II and III) prior to entering the active luteal phase (= secondary progesterone rise). Two episodes of progesterone increase (CLDII: 81.20 ± 5.85 days versus CLDIII: 60.80 ± 3.83 days prior to birth for pregnant cycles) were identified, respectively corresponding to CL reactivation (74-88 days prior to birth) and implantation ( ± 60 days prior to birth) in other bear species. The progesterone concentration during CLDIII was higher in pregnant cycles, indicating a potential communication between maternal tissues and blastocyst(s) enhancing progesterone concentrations and thus allowing optimal priming of uterine tissues to better prepare for blastocyst reactivation/development. Compared with other bear species, giant pandas seem to shorten the active luteal phase, and thus pregnancy, by approximately 30 days by actively postponing CL reactivation. Potential mechanisms in play overruling and suppressing the evolutionary conserved photoperiodical triggers of CL reactivation are discussed while a parallel study will further elaborate on the CL dynamics during giant panda gestation.

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Sequential ovulation and fertility of polyoestrus in American black bears (Ursus americanus)

Cited by 41 publications

References 21 publications

The enigma of embryonic diapause

The enigma of embryonic diapause

Models of embryonic diapause in Carnivora

Evolutionary survival strategies of the female giant panda: optimizing energy resources and expenditure prior to pregnancy by postponing corpus luteum reactivation

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