Early sexual maturity among Pumé foragers of Venezuela: fitness implications of teen motherhood

Because humans have slow life histories, discussions of the optimal age at first birth have stressed the benefits of delayed reproduction. However, given the diversity of ecological, fertility, and mortality environments in which humans live, reproductive maturity is expected to be highly variable. This article uses reproductive histories to examine a pattern of early menarche and first birth among the Pume, a group of South American foragers. Age at menarche and first birth are constructed using both retrospective and cross‐sectional data for females over the age of 10 (n = 83). The objectives are first to define these patterns and then discuss their reproductive consequences. On average, Pume girls reach menarche at age 12.9, and give birth to their first child at age 15.3–15.5 (retrospective and cross‐sectional data, respectively). This populational average falls several years prior to what often is considered the human norm. Two questions are then considered. What are the infant mortality costs across a mother's reproductive career? How does surviving fertility vary with age at first birth? Results indicate that the youngest of first‐time mothers (<14) are four times more likely to loose their firstborns than older first‐time mothers (≥17). Given parity‐specific mortality rates, the optimal strategy to minimize infant mortality and maximize reproductive span is to initiate childbearing in the midteens. Women gain no additional advantage in surviving fertility by delaying childbearing until their late teens. Am J Phys Anthropol, 2008. © 2008 Wiley‐Liss, Inc.     

A tradeoff between reproduction and growth in contemporary Finnish women

Women have been suggested to trade growth in height for reproduction, as an earlier age at menarche and first birth seem to be related to shorter adult stature. Although women likely accrue fitness benefits by maturing and starting reproduction at young age, short adult stature may be selected against by natural and sexual selection later in their life. We studied how age at menarche and first reproduction affected adult height and whether adult height in turn was related to lifetime reproductive success in Finnish women born 1946–1958. Our results show that a delay of 1 year in age at menarche and first reproduction was related to a 0.43- and 0.20-cm increase in adult height, respectively. The sex of the first-born offspring was not related to adult height. Moreover, women gained fitness benefits by starting reproduction early but not by growing tall. These findings among Finnish women are thus compatible with tradeoffs between reproduction and growth, by showing a compromised adult height at the cost of early age at menarche and first birth. However, in these women, natural selection favored those women who traded their stature for young motherhood.     

Age at first birth and family size: Evidence from a longitudinal study

Abstract

This paper examines the correlates of the relationship of age at first birth to completed parity, using data from a fifteen‐year longitudinal study. Particular emphasis is given to measures of orientation toward family roles which have been singled out in previous studies as a likely causal factor not yet examined. Women who had an early first birth went on to have larger families than women who postponed childbearing longer. Demographic factors, including premarital pregnancies, unwanted births, and fecundity differentials, did not appear to account for the observed relationship. The hypothesis that early socialization toward traditional female roles might account for the higher fertility of women who began childbearing early was not confirmed. Women with a first birth at a young age were not characterized by more traditional sex‐role behavior or attitudes nor did they express higher initial fertility preferences. They did more often increase their fertility preferences over the inter‐survey period.     

A delay in age at first mating results in the loss of future reproductive potential via apoptosis

Summary Women who delay childbearing risk subfertility. However, this loss of fertility is not a simple function of aging. Women who have had children early in life tend to maintain fertility longer, measured as a later age at menopause. But why should otherwise healthy women lose reproductive capacity? Loss of fertility independent of senescence, menopause, has been approached from two perspectives: evolution and development. Evolutionary biologists focus on how natural selection favors survival after reproductive ability has ceased, whereas reproductive biologists examine mechanisms by which women lose fertility with age and factors that influence the rate of reproductive aging. Combining mechanistic studies with evolutionary theory should allow us to define principles of the evolution of postembryonic development of ovaries, including the role of reproductive timing relative to sexual maturation. Achieving this will require identifying appropriate, and more experimentally tractable, taxa in which to study how early reproductive events influence lifetime fertility. We work with an invertebrate species, the cockroach Nauphoeta cinerea, with a complex reproductive biology in which females experience reproductive cycles, give live birth, and show age‐related decline in fertility. Thus, N. cinerea provides an opportunity to use an experimental approach to examine mechanisms by which females lose reproductive potential as they delay reproduction. Our results demonstrate that the loss of both oocytes ready for fertilization and future oocytes in females that delay mating is because of apoptosis. We suggest that loss of fertility because of delayed mating may originate in a nonadaptive response in control of apoptosis through mistiming of reproduction.     

Why do women stop reproducing before menopause? A life-history approach to age at last birth

Evolutionary biologists have long considered menopause to be a fundamental puzzle in understanding human fertility behaviour, as post-menopausal women are no longer physiologically capable of direct reproduction. Menopause typically occurs between 45 and 55 years of age, but across cultures and history, women often stop reproducing many years before menopause. Unlike age at first reproduction or even birth spacing, a woman nearing the end of her reproductive cycle is able to reflect upon the offspring she already has—their numbers and phenotypic qualities, including sexes. This paper reviews demographic data on age at last birth both across and within societies, and also presents a case study of age at last birth in rural Bangladeshi women. In this Bangladeshi sample, age at last birth preceded age at menopause by an average of 11 years, with marked variation around that mean, even during a period of high fertility. Moreover, age at last birth was not strongly related to age at menopause. Our literature review and case study provide evidence that stopping behaviour needs to be more closely examined as an important part of human reproductive strategies and life-history theory. Menopause may be a final marker of permanent reproductive cessation, but it is only one piece of the evolutionary puzzle.     

Juvenile Subsistence Effort,Activity Levels,and Growth Patterns

Attention has been given to cross-cultural differences in adolescent growth, but far less is known about developmental variability during juvenility (ages 3–10). Previous research among the Pumé, a group of South American foragers, found that girls achieve a greater proportion of their adult stature during juvenility compared with normative growth expectations. To explain rapid juvenile growth, in this paper we consider girls’ activity levels and energy expended in subsistence effort. Results show that Pumé girls spend far less time in subsistence tasks in proportion to their body size compared with adults, and they have lower physical activity levels compared with many juveniles cross-culturally. Low activity levels help to explain where the extra energy comes from to support rapid growth in a challenging environment. We suggest that activity levels are important to account for the variation of resource and labor transfers in mediating energy availability.     

An evolutionary model of stature, age at first birth and reproductive success in Gambian women

We have built a model to predict optimal age at first birth for women in a natural fertility population. The only existing fully evolutionary model, based on Ache hunter-gatherers, argues that as women gain weight, their fertility (rate of giving birth) increases-thus age at first birth represents a trade-off between time allocated to weight gain and greater fertility when mature. We identify the life-history implications of female age at first birth in a Gambian population, using uniquely detailed longitudinal data collected from 1950 to date. We use height rather than weight as an indicator of growth as it is more strongly correlated with age at first birth. Stature does not greatly influence fertility in this population but has a significant effect on offspring mortality. We model age at first reproduction as a trade-off between the time spent growing and reduced infant mortality after maturation. Parameters derived from this population are fitted to show that the predicted optimal mean age of first birth, which maximizes reproductive success, is 18 years, very close to that observed. The reaction norm associated with variation in growth rate during childhood also satisfactorily predicts the variation in age at first birth.     

Is bigger better? The relationship between size and reproduction in female Asian elephants

The limited availability of resources is predicted to impose trade‐offs between growth, reproduction and self‐maintenance in animals. However, although some studies have shown that early reproduction suppresses growth, reproduction positively correlates with size in others. We use detailed records from a large population of semi‐captive elephants in Myanmar to assess the relationships between size (height and weight), reproduction and survival in female Asian elephants, a species characterized by slow, costly life history. Although female height gain during the growth period overlapped little with reproductive onset in the population, there was large variation in age at first reproduction and only 81% of final weight had been reached by peak age of reproduction at the population level (19 years). Those females beginning reproduction early tended to be taller and lighter later in life, although these trends were not significant. We found that taller females were more likely to have reproduced by a given age, but such effects diminished with age, suggesting there may be a size threshold to reproduction which is especially important in young females. Because size was not linked with female survival during reproductive ages, the diminishing effect of height on reproduction with age is unlikely to be due to biased survival of larger females. We conclude that although reproduction may not always impose significant costs on growth, height may be a limiting factor to reproduction in young female Asian elephants, which could have important implications considering their birth rates are low and peak reproduction is young – 19 years in this population.     

Reproduction in high altitude Aymara: physiological stress and fertility planning?

Reproductive characteristics at high altitude are described based on the reproductive histories of 720 Aymara women, collected in 1998 and 1999 in a group of twelve peasant communities at a mean altitude of 4000 m in the Bolivian Altiplano. The reproductive pattern is shaped by a late onset of childbearing, associated with a rather short reproductive span and large birth intervals. Environmental conditions could explain the particularly late age at menarche of rural girls compared with their urban counterparts, whereas the age at first birth is likely to be under cultural control. The short reproductive span appears to result from a large mean interval between last birth and menopause, which is essentially determined by cultural decisions. The birth intervals, which are longer than in many traditional societies, could be the result of a slower restoration of postpartum fecundability induced by the hard way of life inherent in the Altiplano (including poor sanitary and nutritional conditions and high workload), perhaps aggravated by hypoxia. However, a secular trend in fertility is perceptible, towards earlier menarche, earlier age at first birth, increasing reproductive span and a slight increase in live births and surviving offspring, which is probably the result of a slow improvement in living conditions. The existence of birth control on the one hand, and a total fertility rate averaging six live births among the couples who do not practise contraception on the other, are other arguments against the hypothesis of a low natural fecundity in these Aymara groups.     

The evolution of human phenotypic plasticity: age and nutritional status at maturity

Several evolutionary optimal models of human plasticity in age and nutritional status at reproductive maturation are proposed and their dynamics examined. These models differ from previously published models because fertility is not assumed to be a function of body size or nutritional status. Further, the models are based on explicitly human demographic patterns, that is, model human life-tables, model human fertility tables, and, a nutrient flow-based model of maternal nutritional status. Infant survival (instead of fertility as in previous models) is assumed to be a function of maternal nutritional status. Two basic models are examined. In the first the cost of reproduction is assumed to be a constant proportion of total nutrient flow. In the second the cost of reproduction is constant for each birth. The constant proportion model predicts a negative slope of age and nutritional status at maturation. The constant cost per birth model predicts a positive slope of age and nutritional status at maturation. Either model can account for the secular decline in menarche observed over the last several centuries in Europe. A search of the growth literature failed to find definitive empirical documentation of human phenotypic plasticity in age and nutritional status at maturation. Most research strategies confound genetics with phenotypic plasticity. The one study that reports secular trends suggests a marginally insignificant, but positive slope. This view tends to support the constant cost per birth model.     

Maternal risk of breeding failure remained low throughout the demographic transitions in fertility and age at first reproduction in Finland

Radical declines in fertility and postponement of first reproduction during the recent human demographic transitions have posed a challenge to interpreting human behaviour in evolutionary terms. This challenge has stemmed from insufficient evolutionary insight into individual reproductive decision-making and the rarity of datasets recording individual long-term reproductive success throughout the transitions. We use such data from about 2,000 Finnish mothers (first births: 1880s to 1970s) to show that changes in the maternal risk of breeding failure (no offspring raised to adulthood) underlay shifts in both fertility and first reproduction. With steady improvements in offspring survival, the expected fertility required to satisfy a low risk of breeding failure became lower and observed maternal fertility subsequently declined through an earlier age at last reproduction. Postponement of the age at first reproduction began when this risk approximated zero-even for mothers starting reproduction late. Interestingly, despite vastly differing fertility rates at different stages of the transitions, the number of offspring successfully raised to breeding per mother remained relatively constant over the period. Our results stress the importance of assessing the long-term success of reproductive strategies by including measures of offspring quality and suggest that avoidance of breeding failure may explain several key features of recent life-history shifts in industrialized societies.     

Rhesus macaques compensate for reproductive delay following ecological adversity early in life

Adversity early in life can shape the reproductive potential of individuals through negative effects on health and life span. However, long‐lived populations with multiple reproductive events may present alternative life history strategies to optimize reproductive schedules and compensate for shorter life spans. Here, we quantify the effects of major hurricanes and density dependence as sources of early‐life ecological adversity on Cayo Santiago rhesus macaque female reproduction and decompose their effects onto the mean age‐specific fertility, reproductive pace, and lifetime reproductive success (LRS). Females experiencing major hurricanes exhibit a delayed reproductive debut but maintain the pace of reproduction past debut and show a higher mean fertility during prime reproductive ages, relative to unaffected females. Increasing density at birth is associated to a decrease in mean fertility and reproductive pace, but such association is absent at intermediate densities. When combined, our study reveals that hurricanes early in life predict a delay‐overshoot pattern in mean age‐specific fertility that supports the maintenance of LRS. In contrast to predictive adaptive response models of accelerated reproduction, this long‐lived population presents a novel reproductive strategy where females who experience major natural disasters early in life ultimately overcome their initial reproductive penalty with no major negative fitness outcomes. Density presents a more complex relation with reproduction that suggests females experiencing a population regulated at intermediate densities early in life will escape density dependence and show optimized reproductive schedules. Our results support hypotheses about life history trade‐offs in which adversity‐affected females ensure their future reproductive potential by allocating more energy to growth or maintenance processes at younger adult ages.     

Primate life histories

An animal's life history can be summarized by key variables that account for its life course from conception to death. Biological parameters that are of interest relate to reproductive effort and developmental rates (e.g., gestation length, neonatal weight, prenatal and postnatal growth rates, weaning age, and weaning weight) and the rate of reproduction (e.g., age at first and last reproduction, interbirth interval, the number of offspring per litter, birth rate, and the intrinsic rate of natural increase [r_max]). The rather obvious fact that such variables differ from species to species and from individual to individual has been the subject of much interest since the late 1960s, following the observation that species seem to be arranged in a spectrum that ranges from small animals that breed rapidly and develop early, have many young per litter, and have short lives, to large animals that breed slowly and develop late, have few young per litter, and have long lives. © 1998 Wiley-Liss, Inc.     

Father's death does not affect growth and maturation but hinders reproduction: evidence from adolescent girls in post-war Estonia

The popular concept of predictive–adaptive responses poses that girls growing up without a father present in the family mature and start reproduction earlier because the father''s absence is a cue for environmental harshness and uncertainty that favours switching to a precocious life-history strategy. Most studies supporting this concept have been performed in situations where the father''s absence is caused by divorce or abandonment. Using a dataset of Estonian adolescent girls who had lost their fathers over the period of World War II, we show that father''s death did not affect the rate of pubertal maturation (assessed on the basis of development of breasts and axillary hair) or growth. Father''s death did not affect the age of first birth but, contrary to predictions, reduced lifetime reproductive success. Our findings thus do not support the concept of predictive–adaptive responses and suggest that alternative explanations for covariation between fatherlessness and early maturation are required.     

Condition, growth and reproduction in female red lechwe (Kobus leche leche Gray 1850)

Information on condition, growth and reproduction was collected from a sample of 155 female lechwe in the Linyanti Swamp, northern Botswana. Condition varied significantly with age, reproductive state and season and indications were found of relationships between body mass and the attainment of puberty in young females and body mass and the fertility of adult females. There were also indications that the population was under nutritional stress because of high water levels and that this had caused reductions in the growth rate and fertility of young females. It is suggested that the sensitivity of young females to adverse environmental conditions could be exploited to optimize population monitoring for conservation purposes by using them as an indicator class, rather than monitoring the entire population. Because of relationships between condition, growth and reproduction, it is also suggested that long-term monitoring of condition should form part of any effort to understand population dynamics.     

Demographic and endocrinological aspects of low natural fertility in Highland New Guinea

The Gainj of highland Papua New Guinea do not use contraception but have a total fertility rate of only 4.3 live births/woman, 1 of the lowest ever recorded in a natural fertility setting. Reproductive and marital histories were obtained from 305 females and 206 males aged 10+. Each subject was asked about: number of live born offspring ever produced; number of stillbirths ever produced; number and names of offspring currently being nursed; number of current and past spouses; and the cause of dissolution of all past marriages. Blood samples were drawn from 172 volunteer female subjects aged 10-60 years and ovarian function was classified by concentration of progesterone. From an analysis of these cross-sectional demographic and endocrinological data, the causes of low reproductive output have been identified in women of this population as: late menarche and marriage, a long interval between marriage and 1st birth, a high probability of widowhood at later reproductive ages, low effective fecundability and prolonged lactational amenorrhea. These are combined with near-universal marriage, and a low prevalence of primary sterility similar to that found in other populations. Of all the factors limiting fertility, by far the most important are those involved in birth spacing, especially lactational amenorrhea. The effects of widowhood on Gainj fertility are negligible. Factors acting to lower fertility fall into 2 categories: those that determine the age of onset of reproduction and those that act to space births. Given the observed pattern of birth spacing, however, the delay in commencement of reproduction represents on average no more than 1 or 2 live births averted/woman. In contrast, were age at 1st reproduction held constant while reducing birth intervals to a mean of 2.0-2.5 years, total fertility would increase to about 7 or 8. Future research on natural fertility should focus on specific behavioral and physiological mechanisms governing the reproductive process.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

Biological and behavioral determinants of fertility in Tierra del Fuego

The reproductive history of 182 women in postreproductive life or near menopause from the Chilean part of Tierra del Fuego was traced back by means of familial interviews. These postmenopausal women represent the population since almost the beginning of the settlement, and their reproductive years were spent on the island. Path analysis was applied to analyze fertility determinants of these women and to propose a complex model of interconnections among factors. The reproductive history of these women is characterized by a long fertile span, a short childbearing period, and low fertility. Age at menarche is relatively late, and the age of the women at first birth is mainly determined by their late age at marriage. The use of contraception is related to both spacing and stopping behaviors. The late age of women at marriage, the rhythm of conception, and practices of contraception are proposed as the main determinants of fertility in Tierra del Fuego.     

Father Absence and Reproduction-Related Outcomes in Malaysia,a Transitional Fertility Population

Father absence is consistently associated with children’s reproductive outcomes in industrialized countries. It has been suggested that father absence acts as a cue to particular environmental conditions that influence life history strategies. Much less is known, however, about the effects of father absence on such outcomes in lower-income countries. Using data from the 1988 Malaysian Family Life Survey (n?=?567), we tested the effect of father absence on daughters’ age at menarche, first marriage, and first birth; parity progression rates; and desired completed family size in Malaysia, a country undergoing an economic and fertility transition. Father absence during later childhood (ages 8 to 15), although not during earlier childhood, was associated with earlier progressions to first marriage and first birth, after controlling for other confounders. Father absence does not affect age at menarche, desired family size, or progression from first to second birth. The patterns found in this transitional population partly mirror those in developed societies, where father absence accelerates reproductive events. There is, however, a notable contrast between the acceleration in menarche for father-absent girls consistently found in developed societies and the lack of any association in our findings. The mechanisms through which father absence affects reproduction may differ in different ecological contexts. In lower-income contexts, direct paternal investment or influence may be of more importance in determining reproductive behavior than whether fathers act as a cue to environmental conditions.     

Effects of early horn growth on reproduction and hunting mortality in female chamois

1.?Environmental conditions during early development can affect the growth patterns of vertebrates, influencing future survival and reproduction. In long-lived mammals, females that experience poor environmental conditions early in life may delay primiparity. In female bovids, annual horn growth increments may provide a record of age-specific reproduction and body growth. Horn length, however, may also be a criterion used by hunters in selecting animals to harvest, possibly leading to artificial selection. 2.?We studied three populations of chamois (Rupicapra rupicapra) in the western Alps to explore the relationships between female horn length and early growth, age of primiparity and age-specific reproduction. We also compared the risk of harvest to reproductive status and horn length. 3.?Early horn growth was positively correlated with body mass in pre-reproductive females and with reproduction in very young and senescent adults. Females with strong early horn growth attained primiparity at an earlier age than those with weak early growth. Horn length did not affect hunter selection, but we found a strong hunter preference for nonlactating females. 4.?Our research highlights the persistent effects of early development on reproductive performance in mammals. Moderate sport harvests are unlikely to affect the evolution of phenotypic traits and reproductive strategies in female chamois. A policy of penalizing hunters that harvest lactating females, however, may increase the harvest of 2-year-old females, which have high reproductive potential.