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

Abstract

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.