The life-history trade-off between fertility and child survival

Evolutionary models of human reproduction argue that variation in fertility can be understood as the local optimization of a life-history trade-off between offspring quantity and ‘quality’. Child survival is a fundamental dimension of quality in these models as early-life mortality represents a crucial selective bottleneck in human evolution. This perspective is well-rehearsed, but current literature presents mixed evidence for a trade-off between fertility and child survival, and little empirical ground to evaluate how socioecological and individual characteristics influence the benefits of fertility limitation. By compiling demographic survey data, we demonstrate robust negative relationships between fertility and child survival across 27 sub-Saharan African countries. Our analyses suggest this relationship is primarily accounted for by offspring competition for parental investment, rather than by reverse causal mechanisms. We also find that the trade-off increases in relative magnitude as national mortality declines and maternal somatic (height) and extrasomatic (education) capital increase. This supports the idea that socioeconomic development, and associated reductions in extrinsic child mortality, favour reduced fertility by increasing the relative returns to parental investment. Observed fertility, however, falls considerably short of predicted optima for maximizing total offspring survivorship, strongly suggesting that additional unmeasured costs of reproduction ultimately constrain the evolution of human family size.     

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.     

Fitness drivers in the threatened Dianthus guliae Janka (Caryophyllaceae): disentangling effects of growth context, maternal influence and inbreeding depression

We studied inbreeding depression, growth context and maternal influence as constraints to fitness in the self-compatible, protandrous Dianthus guliae Janka, a threatened Italian endemic. We performed hand-pollinations to verify outcomes of self- and cross-fertilisation over two generations, and grew inbred and outbred D.?guliae offspring under different conditions - in pots, a common garden and field conditions (with/without nutrient addition). The environment influenced juvenile growth and flowering likelihood/rate, but had little effect on inbreeding depression. Significant interactions among genetic and environmental factors influenced female fertility. Overall, genetic factors strongly affected both early (seed mass, seed germination, early survival) and late (seed/ovule ratio) life-history traits. After the first pollination experiment, we detected higher mortality in the selfed progeny, which is possibly a consequence of inbreeding depression caused by over-expression of early-acting deleterious alleles. The second pollination induced a strong loss of reproductive fitness (seed production, seed mass) in inbred D.?guliae offspring, regardless of the pollination treatment (selfing/crossing); hence, a strong (genetic) maternal influence constrained early life-history traits of the second generation. Based on current knowledge, we conclude that self-compatibility does not prevent the detrimental effects of inbreeding in D.?guliae populations, and may increase the severe extinction risk if out-crossing rates decrease.     

Senescence of reproduction may explain adaptive menopause in humans: a test of the "mother" hypothesis

The "mother" hypothesis is one of the main adaptive explanations of human menopause. It postulates that reproductive cessation constitutes a strategy that has been selected for during human evolution because mothers at older ages might maximize their fitness by investing resources in the survival and reproduction of their living children rather than by continuing to reproduce. This study provides a test of this hypothesis. Fertility functions that maximize fitness are built into a model incorporating the fact that the survival of females during the rearing period is a major determinant of their children's survival. Results are given according to different scenarios of increase with mothers' age of maternal mortality risk and risk of stillbirth and birth defects (on the assumption that these females do not experience menopause). Different estimates of the effect of a mother's death on her child's survival were also incorporated. Finally, a population genetics framework allows us to estimate selection on these optimal fertility functions. To determine whether or not these fertility functions show a menopause, three criteria are discussed: the rapidity of fertility decline, if any; the magnitude of selection on menopause compared with a nonmenopausal strategy; and the selection on survival during post-reproductive life. Our results show that menopause and subsequent post-reproductive life are significantly advantageous when two conditions are satisfied: a marked increase in stillbirth and risk of birth defects as well as in maternal mortality with mother's age.     

Maternal grandmothers improve nutritional status and survival of children in rural Gambia

Hypotheses for the evolution of human female life-history characteristics have often focused on the social nature of human societies, which allows women to share the burden of childcare and provisioning amongst other members of their kin group. We test the hypothesis that child health and survival probabilities will be improved by the presence of kin using a longitudinal database from rural Gambia. We find that the only kin to improve the nutritional status of children significantly (apart from mothers) are maternal grandmothers, and that this is reflected in higher survival probabilities for children with living maternal grandmothers. There is also evidence that the reproductive status of the maternal grandmother influences child nutrition, with young children being taller in the presence of non-reproductive grandmothers than grandmothers who are still reproductively active. Paternal grandmothers and male kin, including fathers, have negligible impacts on the nutritional status and survival of children.     

The force of selection on the human life cycle

In this article, I present evidence for a robust and quite general force of selection on the human life cycle. The force of selection acts in remarkably invariant ways on human life histories, despite a great abundance of demographic diversity. Human life histories are highly structured, with mortality and fertility changing substantially through the life cycle. This structure necessitates the use of structured population models to understand human life history evolution. Using such structured models, I find that the vital rates to which fitness is most sensitive are prereproductive survival probabilities, particularly the survival of children ages 0 to 4 years. The fact that the preponderance of selection falls on transitions related to recruitment combined with the late age at first reproduction characteristic of the human life cycle creates a fitness bottleneck out of recruitment. Because of this, antagonistic pleiotropy with any trait that detracts from the constituent transitions to recruitment is expected. I explore the predictors of variation in the force of selection on early survival. High fertility increases the selective premium placed on early survivorship, whereas high life expectancy at birth decreases it.     

Primates and the evolution of long, slow life histories

Primates are characterized by relatively late ages at first reproduction, long lives and low fertility. Together, these traits define a life-history of reduced reproductive effort. Understanding the optimal allocation of reproductive effort, and specifically reduced reproductive effort, has been one of the key problems motivating the development of life-history theory. Because of their unusual constellation of life-history traits, primates play an important role in the continued development of life-history theory. In this review, I present the evidence for the reduced reproductive effort life histories of primates and discuss the ways that such life-history tactics are understood in contemporary theory. Such tactics are particularly consistent with the predictions of stochastic demographic models, suggesting a key role for environmental variability in the evolution of primate life histories. The tendency for?primates to specialize in high-quality, high-variability food items may make them particularly susceptible to environmental variability and explains their?low reproductive-effort tactics. I discuss recent applications of life-history theory to human evolution and emphasize the continuity between models used to explain peculiarities of human reproduction and senescence with the long, slow life histories of primates more generally.     

Weaning behaviour in human evolution

Human life history incorporates early weaning, a prolonged period of post-weaning dependency and slow somatic growth, late onset of female reproduction, reduced birth spacing and a significant post-reproductive female lifespan, combined with rapid early brain growth. Weaned human offspring lack the cognitive skills and physical capacity required to locate, procure and prepare foods that are appropriate for their immature state and sufficient for their high energy requirements. During the weaning process and throughout childhood human offspring are supported by the provision of energy dense and easily digestible foods. Changes in weaning behaviour during human evolution imply a shift in the balance between maternal costs of lactation and the risk of poor offspring outcome, and may have been driven by an increase in infant nutritional and metabolic requirements, a reduction reproductive lifespan resulting in selection for reduced birth spacing or a change in other factors affecting offspring survival and fitness.     

Brain growth, life history, and cognition in primate and human evolution

This study investigates brain size ontogeny in a sample of seven anthropoid primate species (including humans) in order to evaluate longstanding ideas about the relations between brain size, brain ontogeny, life history, and cognition. First, this analysis tests the hypothesis that primate brain growth patterns vary across species. Second, the relations between the duration of the brain growth period and the duration of the pre-adult period are evaluated. Brain growth data, derived from a number of sources, are analyzed through parametric and nonparametric regressions. The results indicate that primates are characterized by significant variation in patterns of brain growth. In addition, the degree to which brain growth is allocated to either the pre- or the postnatal period varies substantially. Analyses of phylogenetically adjusted data show no correlation between the lengths of the brain growth period and the juvenile period, but there are correlations with other life-history variables. These results are explained in terms of maternal metabolic adaptations. Specifically, primates appear to present at least two major metabolic adaptations. In the first, brain growth occurs mainly during the prenatal period, reflecting heavy maternal investment. In the second, brain growth occupies large portions of the postnatal period. These differing patterns have important implications for maturation age, necessitating late maternal maturation in the first case and enabling relatively early maternal maturation in the second. Overall, these adaptations represent components of distinctive life-history adaptations, with potentially important implications for the evolution of primate cognition.     

Brief communication: Evaluating grandmother effects

Women who have outlived child‐bearing have long been described as postreproductive. But contributions they make to the survival or fertility of their descendants enhance the reproduction of their genes. Consequently, natural selection affects this characteristic stage of human life history. Grandmother effects can be measured in data sets that include births and deaths over several generations, but unmeasured covariates complicate the task. Here we focus on two complications: cohort shifts in mortality and fertility, and maternal age at death. We use the Utah Population Database to show that longevity of grandmothers may be associated with fewer grandchildren, as reported by Madrigal and Melendez‐Obando (Am J Phys Anthropol 136 (2008) 223–229) for a Costa Rican sample, even when grandmother effects are actually positive. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Where do all the maternal effects go? Variation in offspring body size through ontogeny in the live-bearing fish Poecilia parae

Maternal effects are an important source of adaptive variation, but little is known about how they vary throughout ontogeny. We estimate the contribution of maternal effects, sire genetic and environmental variation to offspring body size from birth until 1 year of age in the live-bearing fish Poecilia parae. In both the sexes, maternal effects on body size were initially high in juveniles, and then declined to zero at sexual maturity. In sons, this was accompanied by a sharp rise in sire genetic variance, consistent with the expression of Y-linked loci affecting male size. In daughters, all variance components decreased with time, consistent with compensatory growth. There were significant negative among-dam correlations between early body size and the timing of sexual maturity in both sons and daughters. However, there was no relationship between early life maternal effects and adult longevity, suggesting that maternal effects, although important early in life, may not always influence late life-history traits.     

Maternal telomere length inheritance in the king penguin

Telomeres are emerging as a biomarker for ageing and survival, and are likely important in shaping life-history trade-offs. In particular, telomere length with which one starts in life has been linked to lifelong survival, suggesting that early telomere dynamics are somehow related to life-history trajectories. This result highlights the importance of determining the extent to which telomere length is inherited, as a crucial factor determining early life telomere length. Given the scarcity of species for which telomere length inheritance has been studied, it is pressing to assess the generality of telomere length inheritance patterns. Further, information on how this pattern changes over the course of growth in individuals living under natural conditions should provide some insight on the extent to which environmental constraints also shape telomere dynamics. To fill this gap partly, we followed telomere inheritance in a population of king penguins (Aptenodytes patagonicus). We tested for paternal and maternal influence on chick initial telomere length (10 days old after hatching), and how these relationships changed with chick age (at 70, 200 and 300 days old). Based on a correlative approach, offspring telomere length was positively associated with maternal telomere length early in life (at 10 days old). However, this relationship was not significant at older ages. These data suggest that telomere length in birds is maternally inherited. Nonetheless, the influence of environmental conditions during growth remained an important factor shaping telomere length, as the maternal link disappeared with chicks'' age.     

Yellow-bellied marmots do not compensate for a late start: the role of maternal allocation in shaping life-history trajectories

Yellow-bellied marmots, Marmota flaviventris, are obligate hibernators with a relatively short active season. Animals born earlier in the season have higher chances of fulfilling the energetic requirements to survive the long winter. Therefore, the onset of breeding should have a profound impact on juvenile survival. However, there are different ways to compensate for a late start. Late breeders might allocate more resources to late born offspring, making up for the bad start, or juveniles might show compensatory growth. They are not exclusive hypotheses and both can lead to juveniles entering hibernation with a similar body condition. We used data from a long term study in and around the Rocky Mountain Biological Laboratory in Colorado to test these two hypotheses. Animals are individually marked and trapped regularly. We compared mass at weaning, mass at the end of the season, growth rates and survival between animals born earlier and later in the season. We found no evidence of increased maternal input: late breeders had lighter offspring at weaning than early breeders, and late born juveniles did not increase their growth rates. Therefore, late born individuals ended the season with lower body mass, and were thus, less likely to survive the winter. In conclusion, life-history trajectories of juvenile yellow-bellied marmots were determined by maternal allocation, whereas post-weaning decisions did not modify their fate.     

Ecology and energetics of encephalization in hominid evolution.

Hominid evolution is marked by very significant increase in relative brain size. Because relative brain size has been linked to energetic requirements it is possible to look at the pattern of encephalization as a factor in the evolution of human foraging and dietary strategies. Major expansion of the brain is associated with Homo rather than the Hominidae as a whole, and the energetic costs are likely to have forced a prolongation of growth rates and secondary altriciality. It is calculated here that modern human infants have energetic requirements approximately 9% greater than similar size apes due to their large brains. Consideration of energetic costs of brain allow the prediction of growth rates in hominid taxa and an examination of the implications for life-history strategy and foraging behaviour.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

Lifetime reproductive effort in humans

Lifetime reproductive effort (LRE) measures the total amount of metabolized energy diverted to reproduction during the lifespan. LRE captures key components of the life history and is particularly useful for describing and comparing the life histories of different organisms. Given a simple energetic production constraint, LRE is predicted to be similar in value for very different life histories. However, humans have some unique ecological characteristics that may alter LRE, such as the long post-reproductive lifespan, lengthy juvenile period and the cooperative nature of human foraging and reproduction. We calculate LRE for natural fertility human populations, compare the findings to other mammals and discuss the implications for human life-history evolution. We find that human life-history traits combine to yield the theoretically predicted value (approx. 1.4). Thus, even with the subsidized energy budget and uniqueness of the adult lifespan, human reproductive strategies converge on the same optimal value of LRE. This suggests that the fundamental demographic variables contained in LRE trade-off against one another in a predictable and highly constrained manner.     

TESTING LIFE-HISTORY PLEIOTROPY IN CAENORHABDITIS ELEGANS

Abstract Much life-history theory assumes that alleles segregating in natural populations pleiotropically affect life-history traits. This assumption, while plausible, has rarely been tested directly. Here we investigate the genetic relationship between two traits often suggested to be connected by pleiotropy: maternal body size and fertility. We carry out a quantitative trait locus (QTL) analysis on two isolates of the free-living nematode Caenorhabditis elegans , and identify two body size and three fertility QTLs. We find that one of the fertility QTLs colocalizes with the two body size QTLs on Chromosome IV. Further analysis, however, shows that these QTLs are genetically separable. Thus, none of the five body size or fertility QTLs identified here shows detectable pleiotropy for the assayed traits. The evolutionary origin of these QTLs, possible candidate loci, and the significance for life-history evolution are discussed.     

Kin influences on fertility in Thailand: Effects and mechanisms

It has been suggested that human mothers are cooperative breeders, as they need help from others to successfully raise offspring. Studies working under this framework have found correlations between the presence of kin and both child survival and female fertility rates. This study seeks to understand the proximate mechanisms by which kin influence fertility using data from the 1987 Thailand Demographic and Health Survey (DHS), a nationally representative sample of 6775 women. Kin influence is measured by the length of time couples live with the husband's or wife's parents after marriage. Event history analysis, multilevel modeling and structural equation modeling are used to investigate both fertility outcomes and potential pathways through which postnuptial residence may influence fertility outcomes, including employment status, maternal and child outcomes, contraceptive use, breastfeeding duration, and age at marriage. We show that living virilocally (with husband's kin after marriage) increases total fertility by shortening time from marriage to first birth, and increasing the likelihood of progression to each subsequent birth. These effects are mediated through correlations between virilocal residence and earlier age at marriage as well as delayed initiation of contraceptive use. We find no influence of husband's kin on maternal or child outcomes. Living uxorilocally (with wife's kin after marriage) also reduces age at marriage, shortens time from marriage to first birth and (marginally) improves child survivorship, but has no effect on other child and maternal outcomes or progression to subsequent births and results in a similar number of living children as women living neolocally.     

SELECTION ON MENOPAUSE IN TWO PREMODERN HUMAN POPULATIONS: NO EVIDENCE FOR THE MOTHER HYPOTHESIS

Evolutionary theory suggests that natural selection should synchronize senescence of reproductive and somatic systems. In some species, females show dramatic discordance in senescence rates in these systems, leading to a clear menopause coupled with prolonged postreproductive life span. The Mother Hypothesis proposes that menopause evolved to avoid higher reproductive‐mediated mortality risk in late‐life and ensure the survival of existing offspring. Despite substantial theoretical interest, the critical predictions of this hypothesis have never been fully tested in populations with natural fertility and mortality. Here, we provide an extensive test, investigating both short‐ and long‐term consequences of mother loss for offspring, using multigenerational demographic datasets of premodern Finns and Canadians. We found no support for the Mother Hypothesis. First, although the risk of maternal death from childbirth increased from middle age, the risk only reached 1–2% at age 50 and was predicted to range between 2% and 8% by 70. Second, offspring were adversely affected by maternal loss only in their first two years (i.e., preweaning), having reduced survival probability in early childhood as well as ultimate life span and fitness. Dependent offspring were not affected by maternal death following weaning, either in the short‐ or long‐term. We suggest that although mothers are required to ensure offspring survival preweaning in humans, maternal loss thereafter can be compensated by other family members. Our results indicate that maternal effects on dependent offspring are unlikely to explain the maintenance of menopause or prolonged postreproductive life span in women.     

Properties of ethylmethane sulfonate-induced mutations affecting life-history traits in Caenorhabditis elegans and inferences about bivariate distributions of mutation effects

The homozygous effects of ethylmethane sulfonate (EMS)-induced mutations in Caenorhabditis elegans are compared across life-history traits. Mutagenesis has a greater effect on early than late reproductive output, since EMS-induced mutations tend to cause delayed reproduction. Mutagenesis changes the mean and variance of longevity much less than reproductive output traits. Mutations that increase total or early productivity are not detected, but the net effect of mutations is to increase and decrease late productivity to approximately equal extents. Although most mutations decrease longevity, a mutant line with increased longevity was found. A flattening of mortality curves with age is noted, particularly in EMS lines. We infer that less than one-tenth of mutations that have fitness effects in natural conditions are detected in the laboratory, and such mutations have moderately large effects ( approximately 20% of the mean). Mutational correlations for life-history traits are strong and positive. Correlations between early or late productivity and longevity are of similar magnitude. We develop a maximum-likelihood procedure to infer bivariate distributions of mutation effects. We show that strong mutation-induced genetic correlations do not necessarily imply strong directional correlations between mutational effects, since correlation is also generated by lines carrying different numbers of mutations.