Energetics and reproductive effort

Natural selection favors the optimal allocation of energy and other limiting resources to reproduction. Human reproductive physiology displays characteristic patterns that can be viewed as mechanisms that help optimize reproductive effort in the face of environmental energetic constraints. Female ovarian function is particularly sensitive to energy balance and energy flux, resulting in a synchronization of conception with favorable energetic conditions. Reproductive effort during gestation is highly buffered from environmental energetic constraints, but the duration of gestation and final birthweight are both very sensitive to maternal energy availability. Milk production during lactation is relatively buffered from maternal energetic constraints as well, but the duration of lactational amenorrhea is sensitive to the relative metabolic load of lactation. Male gamete production is very insensitive to energetic constraints, but variation in testosterone production in response to both age and longer‐lasting energetic conditions contributes to the modulation of somatic and behavioral aspects of male reproductive effort, aspects that are more energetically costly for a male. There is also new evidence that testosterone may also help to modulate the trade‐off between male parenting and mating effort. Am. J. Hum. Biol. 15:342–351, 2003. © 2003 Wiley‐Liss, Inc.     

Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation

The purpose of this article is to compare the energetics of reproduction for human and other primates in order to evaluate the extent to which human reproductive energetics are distinct from other primates and other large‐bodied placental mammals. The article also evaluates the energetics of human and primate gestation and lactation using data from a variety of different populations living under different environmental circumstances. Energetics refers to energy intake and expenditure, and changes in body fat stores. Human and nonhuman primates have longer periods of gestation and lactation and slower prenatal and postnatal growth than other mammals of similar size. This reduces daily maternal energy costs. The development of sizable fat stores is not unique to humans, but fat stores are typically greater in human females and may play a greater role in reproduction. The strategies used to meet the energy costs of pregnancy vary among populations of humans and nonhuman primates and among humans interindividual variability is high. In pregnancy, some increase energy intake but others apparently do not. Increases in metabolic efficiency are evident in some human populations, whereas decreases in physical activity occur, but are not seen in all human or primate populations. Lactation is more energetically costly on a daily basis among humans and nonhuman primates, but has not been as well studied. It appears that both nonhuman and human primates tend to increase energy intake to meet in part the cost of lactation. They also use other strategies such as relying on body tissue stores, reductions in physical activity, and/or increases in metabolic efficiency to meet the remainder of the cost. It is also clear that human females in different populations and different women in the same population use a different combination of strategies to meet the cost of lactation. Am. J. Hum. Biol. 14:584–602, 2002. © 2002 Wiley‐Liss, Inc.     

A life history approach to prenatal supplementation: Building a bridge from biological anthropology to public health and nutrition

While prenatal supplementation with protein, lipids, carbohydrates, and micronutrients has been used to improve infant outcomes in undernourished populations since the 1960s with inconsistent results, a flourishing body of literature within biological anthropology has used life history theory to explain why supplemental resources are often allocated to maternal survival and future reproduction and not to the current offspring. To date, however, public health and nutrition researchers have not adopted evolutionary perspectives in designing or analyzing prenatal supplementation studies. The result is a long series of supplementation trials with unpredictable and often disappointing outcomes for women and children, as well as serious lacunae in the understanding of long‐term consequences of supplementation for women. The goal of this article is to open a tactical conversation about how to build a bridge between the evolutionary logic of biological anthropology and the evidentiary standards and methods of public health and nutrition with the aim of advancing knowledge about reproductive and metabolic physiology and improving women's health over the life course. The article reviews recent prenatal supplementation studies and proposes programmatic strategies by which biological anthropologists and public health and nutrition workers may collaborate to define different conditions of prenatal supplement resource allocation and to target more effective interventions.     

Impact of breastfeeding on anthropometric changes in peri‐urban Toba women (Argentina)

We present an analysis of the effect of lactation on average maternal anthropometric and body composition measures in a population of Toba women in Formosa, Argentina. This indigenous population is undergoing a continuing transition from a seminomadic hunter–gatherer lifestyle to a sedentary, peri‐urban one. Using a mixed‐longitudinal design, we measured monthly maternal body mass index (BMI), body fat percentage, and triceps and subscapular skinfold thickness between birth and the 18th month postpartum in 113 breastfeeding women. The pattern of change in postpartum body composition varied with maternal age. Adult women (20 years old and older) did not show significant changes in any of the anthropometric measures during the entire study. Older adult women (30 years old and older) consistently had the highest values in measures of BMI and percentage fat, and tended to retain weight postpartum. Adolescent subjects (19 years old and younger) tended to lose weight during the first 6 months postpartum but regain their prepregnancy weight by 12 months postpartum. The same patterns were observed for changes in body fat percentage and in skinfold thickness. We conclude that in this population the energetic stress of lactation does not pose a serious challenge to the maintenance of long‐term maternal energy balance or to short‐term energy balance in women over 20 years of age. From a public health perspective, postpartum weight retention in older women may represent a more serious health threat. The low level of energetic stress associated with lactation may also contribute to the relatively short duration of lactational amenorrhea in this population despite a cultural pattern of intensive breastfeeding. Am. J. Hum. Biol. 15:717–724, 2003. © 2003 Wiley‐Liss, Inc.     

Energetic consequences of being a Homo erectus female

Body size is one of the most important characteristics of any animal because it affects a range of behavioral, ecological, and physiological traits including energy requirements, choice of food, reproductive strategies, predation risk, range size, and locomotor style. This article focuses on the implications of being large bodied for Homo erectus females, estimated to have been over 50% heavier than average australopithecine females. The energy requirements of these hominins are modeled using data on activity patterns, body mass, and life history from living primates. Particular attention is given to the inferred energetic costs of reproduction for Homo erectus females based on chimpanzee and human reproductive scheduling. Daily energy requirements during gestation and lactation would have been significantly higher for Homo erectus females, as would total energetic cost per offspring if the australopithecines and Homo erectus had similar reproductive schedules (gestation and lactation lengths and interbirth intervals). Shortening the interbirth interval could considerably reduce the costs per offspring to Homo erectus and have the added advantage of increasing reproductive output. The mother would, however, incur additional daily costs of caring for the dependent offspring. If Homo erectus females adopted this reproductive strategy, it would necessarily imply a revolution in the way in which females obtained and utilized energy to support their increased energetic requirements. This transformation is likely to have occurred on several levels involving cooperative economic division of labor, locomotor energetics, menopause, organ size, and other physiological mechanisms for reducing the energetic load on females. Am. J. Hum. Biol. 14:551–565, 2002. © 2002 Wiley‐Liss, Inc.     

An evolutionary ecological perspective on demographic transitions: Modeling multiple currencies

Life history theory postulates tradeoffs of current versus future reproduction; today women face evolutionarily novel versions of these tradeoffs. Optimal age at first birth is the result of tradeoffs in fertility and mortality; ceteris paribus, early reproduction is advantageous. Yet modern women in developed nations experience relatively late first births; they appear to be trading off socioeconomic status and the paths to raised SES, education and work, against early fertility. Here, [1] using delineating parameter values drawn from data in the literature, we model these tradeoffs to determine how much socioeconomic advantage will compensate for delayed first births and lower lifetime fertility; and [2] we examine the effects of work and education on women's lifetime and age‐specific fertility using data from seven cohorts in the Panel Study of Income Dynamics (PSID). Am. J. Hum. Biol. 14:149–167, 2002. © 2002 Wiley‐Liss, Inc.     

Issues in evolutionary medicine.

This paper illustrates the utility of applying evolutionary thought to medical issues with three examples: selection arenas, aging, and tradeoffs. First, the human female reproductive tract functions as a selection arena at two levels: in the ovaries, where atresia reduces the number of oocytes by more than 99.99% before any are ovulated, and in the uterus, where early embryos homozygous for immune genes are spontaneously aborted. These selective filters early in life have implications both for eugenics and for the anti-abortion movement. Second, the evolutionary theory of aging predicts that intrinsic mortality should reflect extrinsic mortality: if life for adults is risky, then it does not pay to invest in maintenance at the expense of reproduction. This idea is well confirmed, at least in populations where density effects are not important. While only organisms that reproduce asymmetrically should age, even bacteria reproduce asymmetrically, and they do age, suggesting that all organisms reproduce asymmetrically and therefore age. Third, tradeoffs are central to theories of phenotypic design, but the mechanisms that cause them remain obscure. A method is suggested to get at the mechanisms of tradeoffs by examining conflicts among functions over gene expression. It could be applied in humans to the tradeoff between reproductive performance and disease resistance.     

Overlapping litters and reproductive performance in the domestic rabbit

Rabbits (Oryctolagus cuniculus), like many small mammals, have a marked postpartum estrus, and during the breeding season, are often both pregnant and lactating. We examined reproductive performance and allocation of resources by rabbit mothers with overlapping litters under presumably optimal conditions of unrestricted food, standardized litter size, and young reproductive age. Even under these conditions, females raising overlapping litters incurred higher costs in terms of greatly increased food intake and pup mortality than females raising nonoverlapping litters. Despite such costs, females with overlapping litters raised a larger total number of young to weaning than females without the load of simultaneous lactation and pregnancy. By more than doubling food intake during lactation, females maintained a stable baseline body weight throughout the study, suggesting that this, in a species with low fat reserves, might have priority over the short-term raising of a maximum number of young. Contrary to the expectation that females with overlapping litters would allocate more resources to their senior young, no appreciable difference in number, growth, or survival between pups of senior and junior litters was found either at birth or weaning. While this might reflect a strategy in this opportunistic breeder of distributing reproductive chances similarly between senior and junior litters, it is now necessary to investigate females' breeding strategy when resources are limited.     

Integration of proximate and evolutionary explanation of reproductive strategy: The case of callitrichid primates and implications for human biology

We offer examples of how proximate and evolutionary forms of argument may inform each other in better understanding reproductive strategy in callitrichid primates, the smallest of the anthropoid primates. In addition, we illustrate how comparative approaches, when applied judiciously, can aid in the formulation of hypotheses regarding even seemingly unique traits within a taxonomic group. In the first example, examination of the nature of genetics in cytokine systems that leads to altered ovulation number in sheep suggests some relatively simple changes could explain both the adaptation of increased ovulation number in marmosets and the subsequent decrease in ovulation number in the closely related species, callimico. In the second example, the role of body size and phylogeny in explaining the role of maternal energy constraints upon gestation and lactation is explored, leading to additional hypotheses regarding these relations in a species that is both small but also in a phylogenetic line selected for slow reproduction. Finally, the role of comparative data in the study of proximate and evolutionary explanations of “unique” human reproductive strategies is discussed. Am. J. Hum. Biol., 2009. © 2009 Wiley‐Liss, Inc.     

Demographic consequences of unpredictability in fertility outcomes

Child survival is probabilistic, but the unpredictability in family formation and completed family size has been neglected in the fertility literature. In many societies, ending the family cycle with too few or too many surviving offspring entails serious social, economic, or fitness consequences. A model of risk‐ (or variance‐) sensitive adaptive behavior that addresses long‐term fertility outcomes is presented. The model shows that under conditions likely to be common, optimal, risk‐sensitive reproductive strategies deviate systematically from the completed family size that would be expected if reproductive outcome is were predictable. This is termed the “variance compensation hypothesis.” Variance compensation may be either positive or negative, resulting in augmented or diminished fertility. Which outcome obtained is a function of identifiable social, economic, and environmental factors. Through its effect on fertility behavior, variance compensation has a direct bearing on birth spacing and completed fertility, and thereby on problems in demography and human population biology ranging from demographic transitions to maternal depletion and child health. Risk‐sensitive models will be a necessary component of a general theory of fertility. Am. J. Hum. Biol. 14:168–183, 2002. © 2002 Wiley‐Liss, Inc.     

Food restriction affects reproduction and survival of F1 and F2 offspring of Rat-like hamster (Cricetulus triton)

Food restriction in parent may have long-term consequence on the reproductive capabilities of the offspring, and these consequences may, in turn, play an important role in population regulation. In this paper, we systematically examined the effect of maternal food restriction on reproduction and survival of maternal individuals, and F1 and F2 offspring of Rat-like hamsters (Cricetulus triton). Food restriction to 75% of that eaten by ad libitum-fed hamsters (75% FR) did not affect the reproductive organs and hormone concentration of maternal females, but 50% FR significantly reduced the size of ovarian organ and estradiol concentration of maternal females. 75% FR significantly reduced the testosterone concentration of maternal males; 50% FR significantly reduced both the size of epididymides and concentration of testosterone of maternal males. 70% FR in maternal females significantly reduced the sizes of reproductive organs and hormone concentrations of both their male and female F1 offspring. FR maternal females also produced significantly more male than female F1 offspring. The sizes of reproductive organs or hormone concentration of F2 males of maternal FR continued to significantly decline, but no such effect was observed in F2 females. However, the number of F2 offspring per F1 female of FR maternal females at birth became significantly smaller and with significantly more males than females. Survival to weaning of F1 and F2 offspring of FR maternal females became significantly smaller during the period from birth to weaning. Thus, the effects of maternal food restriction could be an important mechanism to explain the prolonged low population density that is commonly observed after the population crash of this species.     

Maternal capital and the metabolic ghetto: An evolutionary perspective on the transgenerational basis of health inequalities

There is particular interest in understanding socioeconomic and ethnic variability in health status. The developmental origins of disease hypothesis emphasize the importance of growth patterns across the life‐course in relation to noncommunicable disease risk. The physiological components of cardiovascular risk, collectively termed the metabolic syndrome, derive in part from a disparity between the homeostatic “metabolic capacity” of vital organs and the “metabolic load” induced by large tissue masses, a rich diet and sedentary behavior. From an evolutionary perspective, the risk of such disparity is decreased by maternal physiology regulating offspring growth trajectory during gestation and lactation. Maternal capital, defined as phenotypic resources enabling investment in the offspring, allows effective buffering of the offspring from nutritional perturbations and represents the environmental niche initially occupied by the offspring. Offspring growth patterns are sensitive to the magnitude of maternal capital during early windows of plasticity. Offspring life‐history strategy can then respond adaptively to further factors across the life‐course, but only within the context of this initial maternal influence on growth. Maternal somatic capital is primarily gained or lost across generations, through variable rates of fetal and infant growth. I argue that the poor nutritional experience of populations subjected to colonialism resulted in a systematic loss of maternal capital, reflected in downward secular trends in stature. Accelerating the recovery of somatic capital within generations overloads metabolic capacity and exacerbates cardiovascular risk, reflected in increased disease rates in urbanizing and emigrant populations. Public health policies need to benefit metabolic capacity without exacerbating metabolic load. Am. J. Hum. Biol., 2010. © 2009 Wiley‐Liss, Inc.     

A hypothesis for the origin and evolution of menopause

Menopause is widely believed by biological anthropologists and life history theorists to have arisen early in human evolution. In this paper, I suggest that female reproductive senescence was the result of the escalating energetic cost of gestation, lactation and childcare that accompanied the continuing encephalization of early hominid offspring and the ensuing increase in infant altriciality, or helplessness, and the concomitant prolongation of juvenile dependence. Natural selection favored females who became prematurely infertile, as the escalating cost of raising each offspring led to maternal depletion and made it more profitable in terms of lifetime reproductive success to continue investing in existing offspring rather than attempting late pregnancies. Results of a mathematical model are presented which show that reproductive senescence can be advantageous even when maximum potential lifespan is only 50 years, if the premature cessation of reproduction allows females to moderately increase the survival and fertility of their existing subadult offspring. These findings suggest that menopause could have originated as much as 1.5 million years ago, and that if menopause is indeed such an old trait, it was more likely the result of selective pressure on females to invest more in their own children, as opposed to their grandchildren.     

Lactation in lean and obese rats: effect of cafeteria feeding and of dietary obesity on milk composition

Changes in milk composition associated with maternal dietary obesity and cafeteria feeding were investigated. Protein, lactose and fat contents, and the fat composition, were determined for lean and obese rats given a cafeteria diet at different stages of reproduction. Feeding the cafeteria diet during lactation resulted in an increase in long-chain fatty acids and a fall in the characteristic medium-chain fatty acids. This effect was modified by obesity and the diet during pregnancy. Feeding the cafeteria diet in lactation reduced the milk protein and increased the fat. The milk of obese rats contained more energy, with more fat but less protein than that of lean rats. Increases in fat and long-chain fatty acid content, and decreases in protein and medium-chain fatty acid content of the milk were correlated with increased maternal intake of energy, total fat and long-chain fatty acids. Thus, the greatest influence on milk composition is exerted by the maternal diet during lactation. However, these effects are modified by pre-existing maternal obesity and the diet during pregnancy.     

Evolutionary approach to below replacement fertility

The large human brain, the long period of juvenile dependence, long life span, and male support of reproduction are the co‐evolutionary result of the human niche based on skill‐intensive techniques of resource accrual. The regulation of fertility under traditional conditions is based upon a co‐evolved psychology and physiology where adjustments of investment in offspring depend upon the returns to skill and mortality hazards. When all wealth is somatic, the hormonal system controlling ovulation and implantation translates income into genetic descendants. In modern society the existence of extra‐somatic wealth is a critical condition to which our evolved proximate physiological mechanisms do not respond. However, psychological mechanisms regulating parental investment in offspring quality may lead to greater and greater investment in own and offspring education, a smaller desired family size, a delay in the onset of reproduction, and a reduction in the total numbers of offspring produced. This delay in reproduction can cause many individuals to produce fewer children than desired because fecundity falls during the reproductive part of the life course. As more individuals in a society follow this pattern, more will fail to reach their desired family size. At the same time the effective use of birth control decreases the numbers of families producing more children than desired. Below replacement fertility can result. Predictions from this model were tested using data from the National Survey of Families and Households and the Albuquerque Men study. Am. J. Hum. Biol. 14:233–256, 2002. © 2002 Wiley‐Liss, Inc.     

Energetics and evolution: An emerging research domain

The study of energetics is important to human biology because the availability and utilization of food energy influence health, survival, and reproduction. Over the last decade, human biologists, biological anthropologists, and other evolutionary scientists have increasingly come to recognize the importance of energy dynamics in shaping evolutionary processes. Thus far, different lines of energetics research have been conducted largely in isolation from one another. This thematic collection examines topics of evolutionary energetics from several different perspectives, drawing together research from human paleontology, comparative primate and mammalian biology, human population biology, and mathematical modeling. It represents a starting point for further integrative research on human evolutionary energetics. Am. J. Hum. Biol. 14: 547–550, 2002. © 2002 Wiley‐Liss, Inc.     

Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny

Recent studies demonstrate long-term programming of function of specific organ systems resulting from suboptimal environments during fetal life and development up to weaning. Nutrient restriction during pregnancy and lactation impairs overall fetal growth and development. We determined the effects of maternal protein restriction (MPR; 50% normal protein intake) during fetal development and/or lactation in rats on the function and ageing of the reproductive system of female progeny. Rats were fed either a control 20% casein diet (C) or a restricted diet (R) of 10% casein during pregnancy. After delivery mothers received either C or R diet until weaning to provide four groups, CC, RR, CR and RC. We report data on female offspring only. After weaning pups were fed the C diet. MPR increased maternal progesterone, corticosterone, oestradiol and testosterone concentrations at 19 days gestation. Reproductive and somatic phenotype was altered as pup birth weight was decreased, and ano-genital distance was increased by MPR. Pup corticosterone was decreased at 2 days postnatal (PN) life. Vaginal opening and timing of the first oestrus were delayed in RR and CR and these differences were not related to body weight. At 21 days PN oestradiol in RR and CR and progesterone in RR were reduced; at 70 days PN luteinizing hormone (LH) in all restricted groups was reduced in dioestrus while follicle stimulating hormone (FSH) was unchanged. Cycle length increased between 140 days and 1 year in RR and CR but remained unchanged in CC, providing evidence of premature ageing of reproductive function. Fertility rates declined over the same period in the three experimental groups but not CC. MPR in one of the two experimental periods, either pregnancy or lactation, resulted in decreased pup survival compared with CC and RR. These data show that MPR results in delayed sexual maturation and premature ageing of reproductive function.     

Caloric restriction: impact upon pituitary function and reproduction

Reduced energy intake, or caloric restriction (CR), is known to extend life span and to retard age-related health decline in a number of different species, including worms, flies, fish, mice and rats. CR has been shown to reduce oxidative stress, improve insulin sensitivity, and alter neuroendocrine responses and central nervous system (CNS) function in animals. CR has particularly profound and complex actions upon reproductive health. At the reductionist level the most crucial physiological function of any organism is its capacity to reproduce. For a successful species to thrive, the balance between available energy (food) and the energy expenditure required for reproduction must be tightly linked. An ability to coordinate energy balance and fecundity involves complex interactions of hormones from both the periphery and the CNS and primarily centers upon the master endocrine gland, the anterior pituitary. In this review article we review the effects of CR on pituitary gonadotrope function and on the male and female reproductive axes. A better understanding of how dietary energy intake affects reproductive axis function and endocrine pulsatility could provide novel strategies for the prevention and management of reproductive dysfunction and its associated comorbidities.     

Energy intake during reproduction in captive common marmosets (Callithrix jacchus)

Among haplorhine primates, the highly specialized Callitrichidae (marmosets and tamarins) are expected to have comparatively high reproductive costs, a feature that might be related to the evolution of a cooperative breeding system. Costs of reproduction in captivity were investigated on the basis of changes in energy intake and body weight during pregnancy and lactation in pair-living female and male common marmosets (Callithrix jacchus). The experimental design had little effect on carrying behavior, food intake, and body weight of adults, but a negative transitory effect of offspring body weight. Increased energetic requirements during pregnancy did not result in a higher energy intake in females. During lactation, females increased their energy intake up to 100% and gradually lost weight, suggesting even higher costs. Extensive carrying behavior by males, on the other hand, did not result in an increased energy intake in males, or in changes in male body weight. It is suggested that, at least in captivity, increased energetic demands during reproduction are reduced by behavior allocations towards energetically less expensive behaviors.     

Diet, energy expenditure, and body composition of lactating Ribeirinha women in the Brazilian Amazon.

Lactation is the most energetically demanding part of human reproduction; yet, compared with pregnancy, we know little about the strategies women in different settings employ to cope with these increased energy demands. This paper takes a biocultural approach and reports longitudinal data on the anthropometry, dietary intakes and energy expenditure of a sample of 23 rural, lactating Ribeirinha women living in subsistence-based communities in the eastern Amazon. The dietary intakes of these lactating women were insufficient to meet their lactating energy needs and were least sufficient during resguardo, a 40-day period in the immediate postpartum when the women observed a series of food taboos and work restrictions. Instead, the women in this study met the increased energy demands of lactation by drawing on their energy reserves and reducing their energy expenditure in physical activity. The women showed a significant reduction in weight (P<0.001), BMI (P<0.001) and in circumferences (hip, P=0.01; waist, P=0.03) and skinfolds (thigh, P=0.03) in the gluteal femoral region. Total daily energy expenditure (TDEE) was lowest during resguardo and increased as lactation progressed (P=0.01). While the practice of resguardo reduced maternal energy expenditure and allowed women more time to spend with their newborn infants, it came at a cost (low dietary intake), which appears to be related to the loss of the adult woman from subsistence activities. By taking a biocultural approach this study illustrates the role the social environment plays in shaping the experience of lactating women.