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.     

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.     

Mortality rates among wild chimpanzees

In order to compare evolved human and chimpanzees' life histories we present a synthetic life table for free-living chimpanzees, derived from data collected in five study populations (Gombe, Ta?, Kibale, Mahale, Bossou). The combined data from all populations represent 3711 chimpanzee years at risk and 278 deaths. Males show higher mortality than females and data suggest some inter-site variation in mortality. Despite this variation, however, wild chimpanzees generally have a life expectancy at birth of less than 15 years and mean adult lifespan (after sexual maturity) is only about 15 years. This is considerably lower survival than that reported for chimpanzees in zoos or captive breeding colonies, or that measured among modern human hunter-gatherers. The low mortality rate of human foragers relative to chimpanzees in the early adult years may partially explain why humans have evolved to senesce later than chimpanzees, and have a longer juvenile period.     

The effect of socio-economic status and food availability on first birth interval in a pre-industrial human population

Individual variation in nutritional status has direct implications for fitness and thus is crucial in shaping patterns of life-history variation. Nevertheless, it is difficult to measure in natural populations, especially in humans. Here, we used longitudinal data on individual life-histories and annual crop yield variation collected from pre-industrial Finnish populations experiencing natural mortality and fertility to test the validity of first birth interval (FBI; time between marriage and first birth) as a surrogate measure of nutritional status. We evaluated whether women with different socio-economic groups differ in length of FBI, whether women of poorer socio-economic status and experiencing lower crop yields conceive slower following marriage, and whether shorter FBI is associated with higher lifetime breeding success. We found that poorer women had longer FBI and reduced probability of giving birth in months with low food availability, while the FBI of richer women was not affected by variation in food availability. Women with shorter FBI achieved higher lifetime breeding success and a faster reproductive rate. This is, to our knowledge, the first study to show a direct relationship between environmental conditions and speed of childbirth following marriage, highlighting the value of FBI as an indicator of nutritional status when direct data are lacking.     

Resource allocation,demography and the radiation of life histories in rough periwinkles (Gastopoda)

Applicability of life-history theory to higher levels of comparison (from populations, through ecotypes to sibling species) was investigated in rough periwinkles, whose life histories have diversified since colonization of the North Atlantic by an oviparous ancestor in the upper Pliocene. Comparisons were made among populations of the ovoviviparous Littorina saxatilis, between L. saxatilis and its ecotype, L. neglecta (with an annual life history) and between the sibling species L. saxatilis and L. arcana, the latter of which retains the ancestral oviparity. Resource-allocation priority, reproductive effort and related trade offs were compared between the ecotypes and the sibling species by measuring changes in flesh mass and reproductive output in snails subjected to different degrees of food deprivation, and by measuring mortality rate of snails stressed by desiccation, high temperature and low salinity. Body size had a marked effect on all parameters, but after statistically removing this effect there remained no significant differences in allocation among ecotypes or species. Published demographical data were reviewed for correlations between habitat, mortality regime and life-history characteristics. Populations of L. saxatilis varied principally in size at birth and in adult size. Theoretical premises based on density-dependent versus density-independent mortality regimes could not explain these trends. Instead, size at birth may have reflected the mechanical, physiological or biological nature of mortality risk rather than its density dependence or independence. Adult size reflected the available sizes of crevices used for shelter and perhaps also the quality of feeding conditions. Radiation of life histories within the rough periwinkles is interpreted as a series of adaptations to a progressively wider range of habitats. The transition from oviparity to ovoviviparity allows colonization of estuaries, saltmarshes and pebble beaches too hazardous for naked egg masses. The transition from a perennial to an annual life history in barnacle ecotypes follows from allometric re-scaling of morphological and physiological parameters, enabling reproduction and brooding to occur at the small body size necessary for life within empty barnacle tests. This suite of adaptations allows exploitation of a relatively benign microhabitat that occurs almost ubiquitously on exposed rocky shores of the temperate North Atlantic. The persistence of oviparous forms, presumably in the face of competition from sympatric ovoviviparous forms, remains unexplained.     

The influence of juvenile and adult environments on life-history trajectories

There is increasing evidence that the environment experienced early in life can strongly influence adult life histories. It is largely unknown, however, how past and present conditions influence suites of life-history traits regarding major life-history trade-offs. Especially in animals with indeterminate growth, we may expect that environmental conditions of juveniles and adults independently or interactively influence the life-history trade-off between growth and reproduction after maturation. Juvenile growth conditions may initiate a feedback loop determining adult allocation patterns, triggered by size-dependent mortality risk. I tested this possibility in a long-term growth experiment with mouthbrooding cichlids. Females were raised either on a high-food or low-food diet. After maturation half of them were switched to the opposite treatment, while the other half remained unchanged. Adult growth was determined by current resource availability, but key reproductive traits like reproductive rate and offspring size were only influenced by juvenile growth conditions, irrespective of the ration received as adults. Moreover, the allocation of resources to growth versus reproduction and to offspring number versus size were shaped by juvenile rather than adult ecology. These results indicate that early individual history must be considered when analysing causes of life-history variation in natural populations.     

Life-history evolution in guppies viii: the demographics of density regulation in guppies (poecilia reticulata)

In prior research, we found the way guppy life histories evolve in response to living in environments with a high or low risk of predation is consistent with life-history theory that assumes no density dependence. We later found that guppies from high-predation environments experience higher mortality rates than those from low-predation environments, but the increased risk was evenly distributed across all age/size classes. Life-history theory that assumes density-independent population growth predicts that life histories will not evolve under such circumstances, yet we have shown with field introduction experiments that they do evolve. However, theory that incorporates density regulation predicts this pattern of mortality can result in the patterns of life-history evolution we had observed. Here we report on density manipulation experiments performed in populations of guppies from low-predation environments to ask whether natural populations normally experience density regulation and, if so, to characterize the short-term demographic changes that underlie density regulation. Our experiments reveal that these populations are density regulated. Decreased density resulted in higher juvenile growth, decreased juvenile mortality rates, and increased reproductive investment by adult females. Increased density causes reduced offspring size, decreased fat storage by adult females, and increased adult mortality.     

A dynamic framework for the study of optimal birth intervals reveals the importance of sibling competition and mortality risks

Human reproductive patterns have been well studied, but the mechanisms by which physiology, ecology and existing kin interact to affect the life history need quantification. Here, we create a model to investigate how age‐specific interbirth intervals adapt to environmental and intrinsic mortality, and how birth patterns can be shaped by competition and help between siblings. The model provides a flexible framework for studying the processes underlying human reproductive scheduling. We developed a state‐based optimality model to determine age‐dependent and family‐dependent sets of reproductive strategies, including the state of the mother and her offspring. We parameterized the model with realistic mortality curves derived from five human populations. Overall, optimal birth intervals increase until the age of 30 after which they remain relatively constant until the end of the reproductive lifespan. Offspring helping each other does not have much effect on birth intervals. Increasing infant and senescent mortality in different populations decreases interbirth intervals. We show that sibling competition and infant mortality interact to lengthen interbirth intervals. In lower‐mortality populations, intense sibling competition pushes births further apart. Varying the adult risk of mortality alone has no effect on birth intervals between populations; competition between offspring drives the differences in birth intervals only when infant mortality is low. These results are relevant to understanding the demographic transition, because our model predicts that sibling competition becomes an important determinant of optimal interbirth intervals only when mortality is low, as in post‐transition societies. We do not predict that these effects alone can select for menopause.     

The Evolution of Senescence and Post-Reproductive Lifespan in Guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history. Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness. Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.     

Monitoring Change in Child Mortality through Household Surveys

Background

Most low- and middle-income countries lack fully functional civil registration systems. Measures of under-five mortality are typically derived from periodic household surveys collecting detailed information from women on births and child deaths. However, such surveys are expensive and are not appropriate for monitoring short-term changes in child mortality. We explored and tested the validity of two new analysis methods for less-expensive summary histories of births and child deaths for such monitoring in five African countries.

Methods and Findings

The first method we explored uses individual-level survey data on births and child deaths to impute full birth histories from an earlier survey onto summary histories from a more recent survey. The second method uses cohort changes between two surveys in the average number of children born and the number of children dead by single year of age to estimate under-five mortality for the inter-survey period. The first method produces acceptable annual estimates of under-five mortality for two out of six applications to available data sets; the second method produced an acceptable estimate in only one of five applications, though none of the applications used ideal data sets.

Conclusions

The methods we tested were not able to produce consistently good quality estimates of annual under-five mortality from summary birth history data. The key problem we identified was not with the methods themselves, but with the underlying quality of the summary birth histories. If summary birth histories are to be included in general household surveys, considerable emphasis must be placed on quality control.     

Can life history predict the effect of demographic stochasticity on extinction risk?

Demographic stochasticity is important in determining extinction risks of small populations, but it is largely unknown how its effect depends on the life histories of species. We modeled effects of demographic stochasticity on extinction risk in a broad range of generalized life histories, using matrix models and branching processes. Extinction risks of life histories varied greatly in their sensitivity to demographic stochasticity. Comparing life histories, extinction risk generally increased with increasing fecundity and decreased with higher ages of maturation. Effects of adult survival depended on age of maturation. At lower ages of maturation, extinction risk peaked at intermediate levels of adult survival, but it increased along with adult survival at higher ages of maturation. These differences were largely explained by differences in sensitivities of population growth to perturbations of life-history traits. Juvenile survival rate contributed most to total demographic variance in the majority of life histories. Our general results confirmed earlier findings, suggesting that empirical patterns can be explained by a relatively simple model. Thus, basic life-history information can be used to assign life-history-specific sensitivity to demographic stochasticity. This is of great value when assessing the vulnerability of small populations.     

Social and biological determinants of reproductive success in Swedish males and females born 1915–1929

Studying biological and social determinants of mortality and fertility provides insight into selective pressures in a population and the possibility of trade-offs between short- and long-term reproductive success. Limited data is available from post-demographic transition populations. We studied determinants of reproductive success using multi-generational data from a large, population-based cohort of 13,666 individuals born in Sweden between 1915 and 1929. We studied the effects of birthweight for gestational age, preterm birth, birth multiplicity, birth order, mother's age, mother's marital status and family socioeconomic position (SEP) upon reproductive success, measured as total number of children and grandchildren. We further tested the hypothesis that number of grandchildren would peak at intermediate family size, as predicted by some life history explanations for fertility limitation. Reproductive success was associated with both social and biological characteristics at birth. In both sexes, a higher birthweight for gestational age, a term birth and a younger mother were independently associated with a greater number of descendants. A married mother and higher family SEP were also associated with a greater number of descendants in males (but not in females), while higher birth order was associated with a greater number of descendents in females (but not males). These effects were mediated by sex-specific effects upon the probability of marriage. Marriage was also affected by other early life characteristics including birthweight, indicating how ‘biological’ characteristics may operate via social pathways. Number of grandchildren increased with increasing number of children in both sexes, providing no evidence for a trade-off between quantity of offspring and their subsequent reproductive ‘quality’.     

Does Absence Matter?

This paper examines the effects of three different types of father absence on the timing of life history events among women in rural Bangladesh. Age at marriage and age at first birth are compared across women who experienced different father presence/absence conditions as children. Survival analyses show that daughters of fathers who divorced their mothers or deserted their families have consistently younger ages at marriage and first birth than other women. In contrast, daughters whose fathers were labor migrants have consistently older ages at marriage and first birth. Daughters whose fathers died when they were children show older ages at marriage and first birth than women with divorced/deserted fathers and women with fathers present. These effects may be mediated by high socioeconomic status and high levels of parental investment among the children of labor migrants, and a combination of low investment, high psychosocial stress, and low alloparental investment among women with divorced/deserted fathers. Our findings are most consistent with the Child Development Theory model of female life history strategies, though the Paternal Investment and Psychosocial Acceleration models also help explain differences between women in low paternal investment situations (e.g., father divorced/abandoned vs. father dead). Father absence in and of itself seems to have little effect on the life history strategies of Bangladeshi women once key reasons for or correlates of absence are controlled, and none of the models is a good predictor of why women with deceased fathers have delayed life histories compared with women whose fathers are present.     

Fifty years of chimpanzee demography at Taronga Park Zoo

There has been a captive Pan troglodytes colony at Taronga Park Zoo in Sydney, Australia, since the mid-1930s. Demographic data on these animals were first analyzed in 1986; however, further information collected for 15 years since then is now available. The reproductive histories of 33 females in the colony have been recorded, and these data form the largest collection of captive chimpanzee data from a setting that has involved natural breeding conditions since the mid-1960s. These data were analyzed in conjunction with data from wild populations to establish the degree of variability present within chimpanzee reproductive parameters, and to identify which distinctive life history characteristics persist in well-provisioned, natural-fertility populations. The age at first birth for the chimpanzee females is 9.8 yr on average (n=16), which is 1-4.8 yr earlier than the average for wild populations. In line with this accelerated reproduction, birth intervals are also significantly shorter than those in noncaptive chimpanzee populations. The median birth interval for all surviving infants (based on a Kaplan-Meier survival analysis) is 49 months (n=43) compared to 62+ months for wild groups. At the same time, infant mortality remains high. The data confirm distinctive features of the life history of common chimpanzees, including later maturation, long birth intervals, a relatively invariant fertility schedule, and high juvenile mortality. However, aspects of both fertility and mortality are significantly related to social circumstances, indicating that in common chimpanzees, as in humans, life history characters may represent ecological and social adaptations rather than species-fixed characteristics.     

The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata)

The study of post-reproductive lifespan has been of interest primarily with regard to the extended post-menopausal lifespan seen in humans. This unusual feature of human demography has been hypothesized to have evolved because of the “grandmother” effect, or the contributions that post-reproductive females make to the fitness of their children and grandchildren. While some correlative analyses of human populations support this hypothesis, few formal, experimental studies have addressed the evolution of post-reproductive lifespan. As part of an ongoing study of life history evolution in guppies, we compared lifespans of individual guppies derived from populations that differ in their extrinsic mortality rates. Some of these populations co-occur with predators that increase mortality rate, whereas other nearby populations above barrier waterfalls are relatively free from predation. Theory predicts that such differences in extrinsic mortality will select for differences in the age at maturity, allocation of resources to reproduction, and patterns of senescence, including reproductive declines. As part of our evaluation of these predictions, we quantified differences among populations in post-reproductive lifespan. We present here the first formal, comparative study of the evolution of post-reproductive lifespan as a component of the evolution of the entire life history.

Guppies that evolved with predators and that experienced high extrinsic mortality mature at an earlier age but also have longer lifespans. We divided the lifespan into three non-overlapping components: birth to age at first reproduction, age at first reproduction to age at last reproduction (reproductive lifespan), and age at last reproduction to age at death (post-reproductive lifespan). Guppies from high-predation environments live longer because they have a longer reproductive lifespan, which is the component of the life history that can make a direct contribution to individual fitness. We found no differences among populations in post-reproductive lifespan, which is as predicted since there can be no contribution of this segment of the life history to an individual's fitness.

Prior work on the evolution of post-reproductive lifespan has been dominated by speculation and correlative analyses. We show here that this component of the life history is accessible to formal study as part of experiments that quantify the different segments of an individual's life history. Populations of guppies subject to different mortality pressures from predation evolved differences in total lifespan, but not in post-reproductive lifespan. Rather than showing the direct effects of selection characterizing other life-history traits, post-reproductive lifespan in these fish appears to be a random add-on at the end of the life history. These findings support the hypothesis that differences in lifespan evolving in response to selection are confined to the reproductive lifespan, or those segments of the life history that make a direct contribution to fitness. We also show, for the first time, that fish can have reproductive senescence and extended post-reproductive lifespans despite the general observation that they are capable of producing new primary oocytes throughout their lives.

     

Living fast and dying young: A comparative analysis of life-history variation among mammals

Recent comparative studies point to the importance of mortality schedules as determinants in the evolution of life-history characteristics. In this paper, we compare patterns of mortality from natural populations of mammals with a variety of life histories. We find that, after removing the effects of body weight, mortality is the best predictor of variation in life-history traits. Mammals with high levels of natural mortality tend to mature early and give birth to small offspring in large litters after a short gestation, before and after body size effects are factored out. We examine the way in which life-history traits relate to juvenile mortality versus adult mortality and find that juvenile mortality is more highly correlated with life-history traits than is adult mortality. We discuss the necessity of distinguishing between extrinsic sources of mortality (e.g. predation) and mortality caused by intrinsic sources (e.g. costs of reproduction), and the role that ecology might play in the evolution of patterns of mortality and fecundity. We conclude that these results must be explained not simply in the light of the demographic necessity of balancing mortality and fecundity, but as a result of age-specific costs and benefits of reproduction and parental investment. Detailed comparative studies of mortality patterns in natural populations of mammals offer a promising avenue towards understanding the evolution of life-history strategies.     

Effects of life history variation on vertical transfer of toxicants in marine mammals

Toxicant bioaccumulation poses a risk to many marine mammal populations. Although individual-level toxicology has been the subject of considerable research in several species, we lack a theoretical framework to generalize the results across environments and life histories. Here we formulate a dynamic energy budget model to predict the effects of intra- and interspecific life history variation on toxicant dynamics in marine mammals. Dynamic energy budget theory attempts to describe the most general processes of energy acquisition and utilization in heterotrophs. We tailor the basic model to represent the marine mammal reproductive cycle, and we add a model of toxicant uptake and partitioning to describe vertical transfer of toxicants from mother to offspring during gestation and lactation. We first show that the model predictions are consistent with qualitative patterns reported in empirical studies and previous species-specific modeling studies. Next, we use this model to examine the dependence of offspring toxicant load on birth order, food density, and interspecific life history variation.     

Phenotypic plasticity of life history traits in relation to reproductive strategies in <Emphasis Type="Italic">Boa constrictor occidentalis</Emphasis>

The close connection between reproductive ecology and life history in snakes leads to trade-offs between reproductive and other life-history traits. Optimal energy allocation to growth and reproduction is a key factor to determine life history structure. Therefore, elucidating the relationship between body size variations and reproductive characters is essential for a better understanding of life-history plasticity. The aim of this work was to determine to what extent life-history differs among populations of Boa constrictor occidentalis and to identify possible life-history trade-offs between morphological and reproductive traits. We compared two populations from areas that are separated latitudinally, with different climatic conditions and vegetation landscape structure. Reproductive and morphological data of specimens were recorded. Although populations had a similar mean length of mature snakes, the frequency of some size classes tended to be different. Size at sexual maturity differed between populations for females, generating variations in the proportion of mature individuals. Reproductive threshold and follicular size also varied, but female reproductive frequency was similar between populations. Reproductive frequency of males varied between populations although their body condition was similar. We discussed two major issues: (1) implications of size at sexual maturity for body size and fecundity; (2) trade-offs in reproductive characters.     

Famine-related mortality in early life and accelerated life histories in nineteenth-century Belgium

Density-dependent and extrinsic mortality are predicted to accelerate reproductive maturation. The first 5 years of life is a proposed sensitive period for life-history regulation. This study examines the ways in which local mortality during this sensitive period was related to subsequent marriage timing in nineteenth-century Belgium (n women = 11 892; n men = 14 140). Local mortality during the sensitive period was inversely associated with age at first marriage for men and women controlling for literacy, occupational status, population growth and migration. Cox regression indicated decreased time to marriage for women (HR = 1.661, 95% CI: 1.542–1.789) and men (HR = 1.327, 95% CI: 1.238–1.422) from high mortality municipalities. Rising population growth rates were associated with earlier marriage for men and women. Migration in general was associated with later marriage for men and women. Consistent with life-history predictions, harsh ecological conditions during early life such as famine coincided with earlier marriage.     

Extrinsic Mortality Effects on Reproductive Strategies in a Caribbean Community

Extrinsic mortality is a key influence on organisms’ life history strategies, especially on age at maturity. This historical longitudinal study of 125 women in rural Domenica examines effects of extrinsic mortality on human age at maturity and pace of reproduction. Extrinsic mortality is indicated by local population infant mortality rates during infancy and at maturity between the years 1925 and 2000. Extrinsic mortality shows effects on age at first birth and pace of reproduction among these women. Parish death records show huge historical variation in age-specific mortality rates. The infant mortality rate (IMR) in the early 1920s was low, increased dramatically beginning in 1929, and reached a maximum in the 1950s, at which point IMR declined steadily to its present low rate. The mortality rate early in life showed a quadratic association with age at first birth. Women who experienced conditions of low IMR early in life reproduced relatively late in life. Those born into moderately high levels of infant mortality tended to reproduce earlier than those born at low levels. At very high infant mortality levels early in life, women went on to delay reproduction until relatively late, possibly as a result of somatic depletion and energetic stress associated with the conditions that lead to high IMR. Population mortality rates at age of maturity also showed a quadratic association with age at first birth. The pace of reproduction, estimated as number of surviving offspring controlled for maternal age, showed a similar quadratic effect. There were complex interactions between population mortality rates in infancy and at maturity. When extrinsic mortality was high during infancy, extrinsic mortality later in life had little effect on timing of first birth. When extrinsic mortality was low to moderate in infancy, extrinsic mortality later in life had significant effects on adult reproduction. I speculate that these effects are mediated through development of personality facets associated with reproduction.