Energy economy in the evolution of menstruation

Compared with other aspects of mammalian reproductive physiology, we know surprisingly little about menstruation. Medical research has illuminated many of the proximate mechanisms that bring menstruation about, but has left us in the dark as to why menstruation evolved. Evolutionary anthropology provides the expertise in primatology and evolutionary biology needed to shift the emphasis in this field from How to Why.     

The Link Between Human Menstruation and Placental Delivery: A Novel Evolutionary Interpretation

A new interpretation of human menstruation is presented, resulting from a cross‐disciplinary investigation of evolution, developmental biology, and physiology. A process evolutionarily associated with childbirth expresses itself as menstruation in women for whom frequent and continual failure to conceive has become the default situation. In humans and Old World primates, contractile uterine spiral arterioles evolved as the complement of the highly invasive hemochorionic placenta and is the selected phenotype. Placental progesterone withdrawal during the last stage of birth leads to arrested blood flow through maternal spiral arterioles, allowing detachment of the deciduous placenta with minimal maternal hemorrhage. In nonpregnant females, progesterone withdrawal from a degenerating corpus luteum initiates menstruation and stops blood flow through uterine spiral arterioles. Both events share similar physiological mechanisms and sequences. This explanation may improve our understanding of a recurrent event experienced by half of the human population and for a quarter of their adult reproductive life.     

Annual reproductive strategy of the squirrel monkey (Saimiri sciureus).

The physiological and behavioral factors underlying the annual reproductive cycle of the squirrel monkey were evaluated under controlled laboratory conditions. Mating activity following the formation of two social groups served to synchronize the reproductive phases during the subsequent year of observation. Changes in male and female reproductive status were assessed during four designated phases: breeding, pregnancy, lactation and fatting. Behavioral and somatic changes in gonadectomized subjects, living in the social groups, were also evaluated. The variations in behavior and physiology across the year were considered in terms of factors constraining the timing of the natural reproductive pattern.     

Optical coherence tomography for dynamic investigation of mammalian reproductive processes

The biological events associated with mammalian reproductive processes are highly dynamic and tightly regulated by molecular, genetic, and biomechanical factors. Implementation of live imaging in reproductive research is vital for the advancement of our understanding of normal reproductive physiology and for improving the management of reproductive disorders. Optical coherence tomography (OCT) is emerging as a promising tool for dynamic volumetric imaging of various reproductive processes in mice and other animal models. In this review, we summarize recent studies employing OCT-based approaches toward the investigation of reproductive processes in both, males and females. We describe how OCT can be applied to study structural features of the male reproductive system and sperm transport through the male reproductive tract. We review OCT applications for in vitro and dynamic in vivo imaging of the female reproductive system, staging and tracking of oocytes and embryos, and investigations of the oocyte/embryo transport through the oviduct. We describe how the functional OCT approach can be applied to the analysis of cilia dynamics within the male and female reproductive systems. We also discuss the areas of research, where OCT could find potential applications to progress our understanding of normal reproductive physiology and reproductive disorders.     

Is lactation nature's contraceptive? Data from Samoa.

Data from a Samoan menstruation study suggest that lactation, even intensive on-demand lactation, does not inhibit menstruation or conception. This paper explores the applied and theoretical implications of continuing to accept lactation as a universally effective fertility control mechanism. Such thinking can have disastrous implications for family planning programs, and it keeps us from challenging long-held assumptions about lactation's role in population growth in early populations.     

Association between Reproductive Factors and Age-Related Macular Degeneration in Postmenopausal Women: The Korea National Health and Nutrition Examination Survey 2010-2012

Purpose

To examine the association between female reproductive factors and age-related macular degeneration (AMD) in postmenopausal women.

Design

Nationwide population-based cross-sectional study.

Methods

A nationally representative dataset acquired from the 2010–2012 Korea National Health and Nutrition Examination Survey was analyzed. The dataset involved information for 4,377 postmenopausal women aged ≥50 years with a fundus photograph evaluable for AMD in either eye. All participants were interviewed using standardized questionnaires to determine reproductive factors including menstruation, pregnancy, parity, lactation, and hormonal use. The association between reproductive factors and each type of AMD was investigated.

Results

The mean age of the study participants was 63.1±0.2 years. Mean ages at menarche and menopause were 16.1±0.0 and 49.2±0.1 years, respectively. The overall prevalence rates of early and late AMD were 11.2% (95% confidence interval [CI], 10.1–12.5) and 0.8% (95% CI, 0.5–1.2), respectively. When adjusted for age, neither smoking nor alcohol use was associated with the presence of any AMD or late AMD. Multivariate logistic regression analysis revealed age (OR, 1.12 per 1 year), duration of lactation (OR, 0.91 per 6 months), and duration of use of oral contraceptive pills (OCP) (OR, 1.10 per 6 months) as associated factors for late AMD. The other variables did not yield a significant correlation with the risk of any AMD or late AMD.

Conclusion

After controlling for confounders, a longer duration of lactation appeared to protect against the development of late AMD. A longer duration of OCP use was associated with a higher risk of late AMD.     

Son preference and the sex ratio at birth in China: A provincial level analysis

Abstract

Data from a Samoan menstruation study suggest that lactation, even intensive on‐demand lactation, does not inhibit menstruation or conception. This paper explores the applied and theoretical implications of continuing to accept lactation as a universally effective fertility control mechanism. Such thinking can have disastrous implications for family planning programs, and it keeps us from challenging long‐held assumptions about lactation's role in population growth in early populations.     

The main factors affecting the reproductive performance of rabbit does: a review

This paper reviews the main factors affecting the reproductive performance of rabbit does. In the last 15 years the profitability of rabbit farms has increased mainly due to improvements in management and genetic selection but several problems related to animal welfare have also occurred. The replacement and the mortality rates of female per year are very high and the replaced does often show poor body condition and poor health status. The effect of kindling order, litter size, genetic strain, weaning age and reproductive rhythm on the reproductive performance and welfare of females and mechanisms implicated in these effects are discussed. The rabbit doe of modern strains produces a lot of milk with high energetic value, which leads to a mobilization of body fat resulting in a negative energy balance. In the current reproductive rhythms, there is an extensive overlap between lactation and gestation. The resulting energetic and hormonal antagonism reduces the fertility rate and lifespan of the doe. Strategies to optimize these parameters are discussed. An approach that combines various strategies seems to be required to meet these objectives. Since the factors involved in this system are predetermined (genetic strain, environment) the most powerful way to improve doe welfare is to choose a reproductive rhythm more adapted to the physiology of the does.     

Energy metabolism and the evolution of reproductive suppression in the human female

Reproduction places severe demands on the energy metabolism in human females. When physical work entails higher energy expenditure, not enough energy will be left for the support of the reproductive processes and temporal suppression of the reproductive function is expected. While energy needed for reproduction may be obtained by increases in energy intake, utilization of fat reserves, or reallocation of energy from basal metabolism, several environmental or physiological constraints render such solutions unlikely. For human ancestors increases in energy intake were limited by availability of food, by labor of food preparation and by metabolic ceilings to energy assimilation. Energy stored as fat may support only a fraction of the requirements for reproduction (especially lactation). Effects of intense physical activity on basal metabolism may also interfere with fat accumulation during pregnancy. Finally, the female physiology may experience demands on increasing the basal metabolism as a consequence of physical activity and, at the same time, on decreasing the basal metabolism, when energy to support the ongoing pregnancy or lactation is inadequate. The resulting metabolic dilemmas could constitute a plausible cause for the occurrence of reproductive suppression in response to physical activity. It is, therefore, likely that allocating enough energy to the reproductive processes during periods when energy expenditure rises may be difficult due to physiological and bioenergetic constraints. Females attempting pregnancy in such conditions may compromise their lifetime reproductive output. A reproductive suppression occurring in low energy availability situations may thus represent an adaptive rather then a pathological response.     

Observation of reproductive cycle of female yellow-margined box turtle (Cuora flavomarginata) using radiography and ultrasonography

This study presents a combination of radiography and ultrasonography to observe the reproductive cycle of 24 captive female yellow-margined box turtles in Taiwan. Radiography was mainly used to monitor clutch size, whereas ultrasonography was applied to detect changes in the follicles throughout the year. The observation of the 24 female turtles was performed from April 2007 to June 2008. Their average carapace length was 16.62 ± 1.66 cm and their average body weight was 812 ± 164.98 g. The mean clutch size was three (87 eggs/29 clutches) and the reproductive frequency was 95.83% (23/24). Double clutches were detected in 79.2%, and 20.8% had single clutches. Ovulation occurred from March through August, and the average follicular diameter was 2.16 ± 0.18 cm. Follicles entered the latent period in October (at 1.54 ± 0.26 cm), and vitellogenesis of the next reproductive cycle began in November. Using radiography, the eggshell could be detected on the ninth day after ovulation. The average period of the single clutch group was 6.9 weeks (range 5.1-8.5 weeks). In the double clutch group, the average period of the first clutch was 5.5 weeks (range 4-7.8 weeks) and that of the second clutch was 5.2 weeks (range 4-7.8 weeks). This study has advanced the understanding of reproductive physiology of yellow-margined box turtle and established a valuable and practical model for comparative study of the reproductive physiology of other chelonians.     

Management of pre-pubertal small ruminants: physiological basis and clinical approach

Puberty is a gradual process, during which animal reproductive competence is attained with respect to physiology, morphology and behaviour. Onset of puberty in small ruminants differs between sexes, due to early sexual differentiation in the control of steroid feedback systems and, thus, GnRH secretion. A number of puberty determinants have been identified, which include genetic factors, as well as endogenous signals, such as energy balance and environmental cues, whose dynamic interplay is responsible for the timing of puberty onset. Puberty timing affects reproduction through age at first lambing, which impacts on subsequent reproductive life and productivity of small ruminants. Thus, a greater knowledge of the mechanisms underlying puberty process would lead to optimisation of commonly applied strategies for selection of replacement animals. In addition, understanding reproductive responses of animals to exteroceptive factors, such as photoperiod, nutrition and socio-sexual signals, will enable development and improvement of those management tools that that will fulfil the requirements of a 'clean, green and ethical' production.     

Energetics during reproduction: a doubly labeled water study of lactating baboons

Understanding the costs and regulation of reproduction in primates requires understanding the separate but linked effects of energy availability and total energy expenditure (TEE). We compared variation in TEE and energy intake (EI) between two periods, early lactation and after the resumption of sexual cycling, for eight females from two groups of normally reproducing colony-living baboons (Papio h. anubis). Total energy expenditure was assessed using the doubly labeled water method. TEE was correlated with maternal mass both during early lactation and after the resumption of cycling. TEE after the resumption of cycling was positively related to infant growth rates; mothers with rapidly growing infants had higher energy expenditure. TEE was however unrelated to maternal rank and only weakly associated with reproductive parameters such as delay to conception. EI in early lactation was related to infant mass and interbirth intervals, but unrelated to infant growth or reproductive parameters once cycling had resumed. Energy availability (EA; the difference between intake and expenditure) differed significantly between subordinate and dominant females during early lactation, was highly variable among individuals as a function of body composition, and is suggested to follow a nonlinear relationship as a complex function of social status, lactation stage, infant growth, and female fertility. Thus, as a consequence of reduced energy availability, subordinate females in this captive context may experience reproductive delays even though the total energy expenditure after the return of cycling was similar between high and low ranking females.     

Effects of 12-hour rotating shifts on menstrual cycles of photoelectronic workers in Taiwan

12 h rotating shifts are common in high-tech industries in Taiwan. The aim of this longitudinal study was to evaluate the effect of the disruption of circadian rhythms by the shift schedule on menstrual cycle length (MCL) and regularity of female workers at an optoelectronic company in Taiwan. We recruited females who worked rotating shifts in a clean room environment as the shift-work group and female office workers who worked normal business hours as the comparison group. Every participant recorded their MCL for each menstruation cycle up to eight consecutive months prospectively and provided demographic characteristics, reproductive history, and menstrual characteristics. We collected data on 1,135 and 117 menstruation cycles in the shift-work (n = 280) and comparison groups (n = 49). Whereas the two groups had similar group means for MCL and number of menstrual bleeding days, the prevalence of menstrual cycle irregularity (cycles <25 or >35 days) was higher in the shift-work group ( p = 0.04). Univariate and multivariate logistic regression analyses demonstrated that rotating shift work was an independent predictor of menstrual cycle irregularity (odds ratio = 1.71, 95% confidence interval: 1.03-2.88) after adjusting for shift-work history, employment duration, coffee consumption,and pre-employment menstrual cycle irregularity. Although further study is required to confirm our findings plus to explore prevention and control measures, our data indicate rotating shift work can increase the risk of MCL irregularity.     

Fundulus heteroclitus: ovarian reproductive physiology and the impact of environmental contaminants

Fundulus heteroclitus, the mummichog or Atlantic killifish, is the dominant small-bodied fish species of the east coast estuaries and salt marshes of Canada and the USA, where it is present as two subspecies, the northern F. h. macrolepidotus and the southern F. h. heteroclitus. Recently identified as the premier teleost model in environmental biology, the species has long been of value in understanding evolved tolerance to toxicants and more lately in adding to our knowledge about reproductive effects of environmental endocrine disruptors. The body of literature on F. heteroclitus ovarian physiology and reproduction, from both field and laboratory studies, provides the foundation for present work focused on understanding the reproductive effects and modes of action of environmental toxicants. In this paper, we review the environmental and endocrine factors controlling ovarian and reproductive cycling in F. heteroclitus, noting specifics related to field and laboratory studies on the two subspecies as well as key research gaps compared to other fish species. We also summarize recent development of methodologies to study the effects of environmental contaminants on endocrine signalling and egg production in F. heteroclitus. Continued efforts to progress both our fundamental understanding of reproductive physiology in mummichog, coupled with studies focused on the modes of action of environmental contaminants, have high potential to further develop this teleost model. While the model may presently lag behind those based on other species of fish, the unique biochemical and physiological adaptations which allow F. heteroclitus to adapt to changing environmental and toxic conditions provide a valuable experimental system for comparative physiologists, ecotoxicologists and evolutionary biologists.     

Folliculogenesis in the domestic cat (Felis catus)

The dynamic regulation of mammalian folliculogenesis is a key component of the reproductive process. Traditionally, the rodent had been used as a model to study ovarian function and reproductive physiology due to the availability of animals, their relatively short cycle length, high rate of fecundity and short generation interval. We maintain that much basic information can be determined using domestic cat ovaries retrieved from local veterinary clinics following routine spaying, without having the expense of maintaining a colony of laboratory cats. Studies of normal feline reproductive physiology and advances in reproductive technology may be extrapolated for use in endangered non-domestic felids. Increased understanding of feline reproduction will be beneficial to veterinary medicine, and to groups working to control feral cat populations. It is important to examine reproductive mechanisms in alternative animal models as there are a vast number of threatened and endangered species in which we lack the critical reproductive information needed to assist in preserving their long-term survival.     

Regulation of VEGF in the reproductive tract by sex-steroid hormones

Vascular endothelial growth factor (VEGF) is a key regulator of angiogenesis. In adults, angiogenesis is an infrequent event in the normal tissue except in the female reproductive tract where angiogenesis occurs frequently during the cyclical repair and regeneration of the endometrium as well as in the ovary. Little is known about angiogenesis in the male reproductive tract. The role of VEGF in controlling reproductive tract physiology and the role of hormones in regulating this key regulator of angiogenesis is not well understood. Since reproductive tract physiology is largely under sex-steroid regulation, we have reviewed some recent studies describing the role of sex-steroid hormones in regulating VEGF. We have also included studies on the role of sex-steroids in regulating VEGF and angiogenesis in endometrial, breast and prostate pathologies. We have provided an extensive review of the classical VEGF and VEGF receptors with examples drawn from numerous studies in the literature using diverse biological systems to encourage similar studies in the area of reproductive tract physiology. It is speculated that such studies will provide insights into understanding the role of VEGF in reproductive tract development, causes of infertility, and cancer. Such knowledge would allow us to target VEGF for improving human reproductive tract abnormalities, for enhancing implantation and fertility, and for designing drugs for treatment of endocrine dependent cancers.     

Altered reproductive success in rat pairs after environmental-like exposure to xenoestrogen

Endocrine-disrupting compounds (EDCs) have the capacity of altering the normal function of the endocrine system. EDCs have shown dramatic effects on the reproductive biology of aquatic wildlife and may affect human reproduction as well. Studies on EDCs in mammalian species have often investigated the effects of short-term, high doses on male and female reproductive physiology. However, it is difficult to predict from such studies the effects of EDC on populations that are exposed to very low doses throughout their life via contaminated food and water. We studied the effects of EDC on mammalian reproduction with an environmental-like protocol where the endpoint is the reproductive success of exposed pairs. We focused on a subclass of EDC, the xenoestrogens, which mimic the action of natural oestrogen hormones. Male and female rats were exposed to low doses of the pure oestrogen, ethynyloestradiol, during development, by oral administration to their mothers during pregnancy and lactation, and to them until puberty. We evaluated the effects of the exposure on development and reproductive physiology of individuals, and on fertility and fecundity of pairs in which both members had been exposed to the same treatment. We found that low doses caused major reproductive deficits in the experimental animals. Very low, environmentally relevant doses did not have evident effects on exposed animals; however, the fecundity of exposed pairs was substantially altered. Environmentally relevant doses of xenoestrogens which have no evident physiological effects can alter the reproductive success of exposed pairs in natural populations.     

Reproductive resilience to food shortage in a small heterothermic primate

The massive energetic costs entailed by reproduction in most mammalian females may increase the vulnerability of reproductive success to food shortage. Unexpected events of unfavorable climatic conditions are expected to rise in frequency and intensity as climate changes. The extent to which physiological flexibility allows organisms to maintain reproductive output constant despite energetic bottlenecks has been poorly investigated. In mammals, reproductive resilience is predicted to be maximal during early stages of reproduction, due to the moderate energetic costs of ovulation and gestation relative to lactation. We experimentally tested the consequences of chronic-moderate and short-acute food shortages on the reproductive output of a small seasonally breeding primate, the grey mouse lemur (Microcebus murinus) under thermo-neutral conditions. These two food treatments were respectively designed to simulate the energetic constraints imposed by a lean year (40% caloric restriction over eight months) or by a sudden, severe climatic event occurring shortly before reproduction (80% caloric restriction over a month). Grey mouse lemurs evolved under the harsh, unpredictable climate of the dry forest of Madagascar and should thus display great potential for physiological adjustments to energetic bottlenecks. We assessed the resilience of the early stages of reproduction (mating success, fertility, and gestation) to these contrasted food treatments, and on the later stages (lactation and offspring growth) in response to the chronic food shortage only. Food deprived mouse lemurs managed to maintain constant most reproductive parameters, including oestrus timing, estrogenization level at oestrus, mating success, litter size, and litter mass as well as their overall number of surviving offspring at weaning. However, offspring growth was delayed in food restricted mothers. These results suggest that heterothermic, fattening-prone mammals display important reproductive resilience to energetic bottlenecks. More generally, species living in variable and unpredictable habitats may have evolved a flexible reproductive physiology that helps buffer environmental fluctuations.     

Factors influencing the postweaning reproductive performance of sows on commercial farms

The objective of this study was to investigate the effects of various factors, including lactational feed intake, on the reproductive performance of sows in commercial herds. The 4 measures of reproductive performance were weaning-to-first-service interval, weaning-to-conception interval, litter weight at weaning, and subsequent litter size. Parity, farrowing season, lactation length, farrowing-to-conception interval, litter size, and lactation feed intake were investigated as risk factors common to the 4 measures of post-weaning reproductive performance. Using 4 basic multiple regression models for each measure, the least-square means for sets of factors were compared using the GLM procedure of SAS. Parity 1 sows had the longest weaning-to-first-service interval and weaning-to-conception interval, and the lighter litter weight at weaning (P < 0.05) than mid-parity sows. Sows in Parities 2 to 5 had larger subsequent litter size (P < 0.05) than those in Parities 1 and >/= 7. Sows farrowing in summer and spring had the longest and second longest weaning-to-conception interval (P < 0.05), respectively, while sows farrowing in summer had longer weaning-to-first-service interval than those that farrowed in spring (P < 0.05). Sows farrowing in summer produced the lightest litter weight at weaning (P < 0.05). No differences in subsequent litter sizes were found due to farrowing season (P > 0.10). As lactation length increased, weaning-to-first-service interval and weaning-to-conception interval decreased, and litter weaning weight increased. Longer lactation length and farrowing-to-conception interval were associated with larger subsequent litter size (P < 0.05). Litter size did not affect weaning-to-first-service interval or weaning-to-conception interval. Larger litter sizes were associated with heavier litter weight at weaning. Greater lactation feed intake improved the 4 measures of reproductive performance.     

Dietary manipulations to improve embryonic survival in cattle

High-producing dairy cows are subfertile. Hormonal and metabolic responses associated with homeorrhetic and homeostatic regulatory responses to partition nutrients for lactation, coupled with management, contribute to the reduction in fertility. Systems of reproductive management partially restore herd reproductive performance and provide a basis to access the impact of targeted nutritional strategies to further improve postpartum health and reproduction. Increasing the number of days feeding prepartum diets with a negative dietary cation-anion difference (DCAD), combined with adequate energy, protein, amino acids, and trace/macrominerals, improves the subsequent pregnancy rate. Likewise, supplementation of organic Se in the transition period and lactation improves immune function, uterine health, and subsequent reproductive performance under conditions of Se insufficiency. A basic understanding of the regulatory processes between nutrient partitioning and reproduction has led to the development of dietary strategies that benefit both lactation and reproduction. Postpartum increases in dietary nonstructural carbohydrates (i.e., glucogenic diets) increases ovarian activity in either intensive or extensive systems. Furthermore, sequential feeding of glucogenic-lipogenic diets enhances the proportion of cows pregnant by 120 d of lactation. Fatty acids of the n-6 and n-3 families act as nutraceuticals, altering innate immune responses and subsequent gene expression within the uterus to complement the sequential processes of follicle and embryo development and survival of the embryo and fetus. Selective or sequential feeding of lipogenic diets can benefit reproductive and immunological responses of lactating dairy cows and extensively managed beef cows.