More Status or More Children? Social Status,Fertility Reduction,and Long-Term Fitness

A model is presented that shows that reduced fertility in humans can be explained as part of an evolved strategy to maximize long-term fitness in the face of periodic calamities that result in demographic crashes. Three conditions must be met for this model to be plausible: (1) human population history has been characterized by local periods of growth punctuated by recurrent crashes caused by calamities such as climatically induced resource shortfalls; (2) a strategy is available to individuals that increases the probability of survival through a crash, but that, to implement, requires diverting resources away from producing more offspring; and (3) long-term fitness benefits to increased survivorship through a crisis must outweigh or equal the fitness benefits that would accrue to putting the same resources into higher fertility. We present a model that shows that increases in survivorship can outweigh the benefits of higher fertility even if crises are neither very frequent nor particularly severe.     

A DEMOGRAPHIC TRANSITION ALTERED THE STRENGTH OF SELECTION FOR FITNESS AND AGE‐SPECIFIC SURVIVAL AND FERTILITY IN A 19TH CENTURY AMERICAN POPULATION

Modernization has increased longevity and decreased fertility in many human populations, but it is not well understood how or to what extent these demographic transitions have altered patterns of natural selection. I integrate individual‐based multivariate phenotypic selection approaches with evolutionary demographic methods to demonstrate how a demographic transition in 19th century female populations of Utah altered relationships between fitness and age‐specific survival and fertility. Coincident with this demographic transition, natural selection for fitness, as measured by the opportunity for selection, increased by 13% to 20% over 65 years. Proportional contributions of age‐specific survival to total selection (the complement to age‐specific fertility) diminished from approximately one third to one seventh following a marked increase in infant survival. Despite dramatic reductions in age‐specific fertility variance at all ages, the absolute magnitude of selection for fitness explained by age‐specific fertility increased by approximately 45%. I show that increases in the adaptive potential of fertility traits followed directly from decreased population growth rates. These results suggest that this demographic transition has increased the adaptive potential of the Utah population, intensified selection for reproductive traits, and de‐emphasized selection for survival‐related traits.     

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.     

Optimal life histories and the age-specific costs of reproduction

Increases in reproduction at a given age may carry costs measured as reductions in subsequent survival and/or future fertility. Such costs generate constraints within which natural selection may mould life histories to maximize fitness. In this paper, I derive expressions predicting the age-specific costs of reproduction conditional on the maximization of fitness. Survival costs should, on this hypothesis, vary as the inverse of the reproductive value curve; fertility costs should vary as the ratio of successive terms in the stable age distribution. For many organisms, this means that survival costs should increase markedly with age, while fertility costs should be nearly age-invariant. Data on such age-specific costs is scarce, but that which is available (mainly for humans) agrees with these predictions.     

EFFECTS OF CROSS AND SELF-FERTILIZATION ON PROGENY FITNESS IN LOBELIA CARDINALIS AND L. SIPHILITICA

Inbreeding depression, or the decreased fitness of progeny derived from self-fertilization as compared to outcrossing, is thought to be the most general factor affecting the evolution of self-fertilization in plants. Nevertheless, data on inbreeding depression in fitness characters are almost nonexistent for perennials observed in their natural environments. In this study I measured inbreeding depression in both survival and fertility in two sympatric, short-lived, perennial herbs: hummingbird-pollinated Lobelia cardinalis (two populations) and bumblebee-pollinated L. siphilitica (one population). Crosses were performed by hand in the field, and seedlings germinated in the greenhouse. Levels of inbreeding depression were determined for one year in the greenhouse and for two to three years for seedlings transplanted back to the natural environment. Fertility was measured as flower number, which is highly correlated with seed production under natural conditions in these populations. Inbreeding depression was assessed in three ways: 1) survival and fertility within the different age intervals; 2) cumulative survival from the seed stage through each age interval; and 3) net fertility, or the expected fertility of a seed at different ages. Net fertility is a comprehensive measure of fitness combining survival and flower number. In all three populations, selfing had nonsignificant effects on the number and size of seeds. Lobelia siphilitica and one population of L. cardinalis exhibited significant levels of inbreeding depression between seed maturation and germination, excluding the consideration of possible differences in dormancy or longterm viability in the soil. There was no inbreeding depression in subsequent survival in the greenhouse in any population. In the field, significant survival differences between selfed and outcrossed progeny occurred only in two years and in only one population of L. cardinalis. For both survival and fertility there was little evidence for the expected differences among families in inbreeding depression. Compared to survival, inbreeding depression in fertility (flower number) tended to be much higher. By first-year flower production, the combined effects on survival and flower number caused inbreeding depression in net fertility to reach 54%, 34% and 71% for L. siphilitica and the two populations of L. cardinalis. By the end of the second year of flowering in the field, inbreeding depression in net fertility was 53% for L. siphilitica and 54% for one population of L. cardinalis. For the other population of L. cardinalis, these values were 76% through the second year of flowering and 83% through the third year. Such high levels of inbreeding depression should strongly influence selection on those characters affecting self-fertilization rates in these two species.     

Why do men seek status? Fitness payoffs to dominance and prestige

In many human societies, high male social status associates with higher fertility, but the means by which status increases lifetime fitness have not been systematically investigated. We analyse the pathways by which male status begets reproductive success in a small-scale, Amerindian society. Men who are more likely to win a dyadic physical confrontation, i.e. dominant men, have higher intra-marital fertility for their age, and men with more community-wide influence, i.e. prestigious men, exhibit both higher intra-marital fertility and lower offspring mortality. Both forms of status elicit support from allies and deference from competitors, but high status men are not provisioned more than their peers. Prestigious but not dominant men marry wives who first give birth at earlier ages, which multivariate analysis suggests is the strongest pathway between status and fitness in this population. Furthermore, men are motivated to pursue status because of fitness gains both within and outside of marital unions: dominant and prestigious men have more in-pair surviving offspring as well as more extra-marital affairs.     

The rank ordering of genotypic fitness values predicts genetic constraint on natural selection on landscapes lacking sign epistasis

Sewall Wright's genotypic fitness landscape makes explicit one mechanism by which epistasis for fitness can constrain evolution by natural selection. Wright distinguished between landscapes possessing multiple fitness peaks and those with only a single peak and emphasized that the former class imposes substantially greater constraint on natural selection. Here I present novel formalism that more finely partitions the universe of possible fitness landscapes on the basis of the rank ordering of their genotypic fitness values. In this report I focus on fitness landscapes lacking sign epistasis (i.e., landscapes that lack mutations the sign of whose fitness effect varies epistatically), which constitute a subset of Wright's single peaked landscapes. More than one fitness rank ordering lacking sign epistasis exists for L > 2 (where L is the number of interacting loci), and I find that a highly statistically significant effect exists between landscape membership in fitness rank-ordering partition and two different proxies for genetic constraint, even within this subset of landscapes. This statistical association is robust to population size, permitting general inferences about some of the characteristics of fitness rank orderings responsible for genetic constraint on natural selection.     

Effect of Body Weight on Reproductive Performance in Cnephasia jactatana (Lepidoptera: Tortricidae)

The larger-the-better theory predicts that fitness is positively linearly associated with body size or weight. We used the kiwifruit pest, Cnephasia jactatana Walker, to test whether larger insects perform better reproductively. We divided our insect population into three weight groups: light, average, and heavy, and assessed the reproductive performance of 9 breeding treatments (3 male weights × 3 female weights). Female fecundity is positively correlated with female body weight in low and average weight groups. There is no such correlation in the heavy weight group, suggesting that further weight increase has no fitness gain for females. The positive linear relationship between fertility and female weight in all weight groups may be attributed to the fact that permanently paired heavy females are more likely to remate, gaining more sperm and thus higher fertility. However, the previous study also indicates that mated females are less likely to be mated again when males have a choice. Therefore, in the natural environment the realized fertility may still follow an asymptotical pattern similar to the fecundity in relation to female weight. Males' beneficial effect on female reproductive outputs increases linearly with their body weight in all weight groups, indicating that male reproductive performance fits the larger-the-better theory. Fertility rate is not affected by the body weight of either sex. Heavy and average females lay eggs earlier and have higher daily fecundity and fertility than light females. Females of all weight groups have similar oviposition and postoviposition periods. Male weight and female–male weight interactions have no effect on oviposition parameters.     

Microsatellites reveal heterosis in red deer.

The fitness consequences of inbreeding and outbreeding are poorly understood in natural populations. We explore two microsatellite-based variables, individual heterozygosity (likely to correlate with recent inbreeding) and a new individual-specific internal distance measure, mean d2 (focusing on events deeper in the pedigree), in relation to two measures of fitness expressed early in life, birth weight and neonatal survival, in 670 red deer calves (Cervus elaphus) born on the Isle of Rum between 1982 and 1996. For comparison, we also analyse inbreeding coefficients derived from pedigrees in which paternity was inferred by molecular methods. Only 14 out of 231 calves (6.1%) had non-zero inbreeding coefficients, and neither inbreeding coefficient nor individual heterozygosity was consistently related to birth weight or neonatal survival. However, mean d2 was consistently related to both fitness measures. Low mean d2 was associated with low birth weight, especially following cold Aprils, in which foetal growth is reduced. Low mean d2 was also associated with low neonatal survival, but this effect was probably mediated by birth weight because fitting birth weight to the neonatal survival model displaced mean d2 as an explanatory variable. We conclude that in the deer population fitness measures expressed early in life do not show evidence of inbreeding depression, but they do show evidence of heterosis, possibly as a result of population mixing. We also demonstrate the practical problems of estimating inbreeding via pedigrees compared with a direct marker-based estimate of individual heterozygosity. We suggest that, together, individual heterozygosity and mean d2, estimated using microsatellites, are useful tools for exploring inbreeding and outbreeding in natural population.     

Natural selection on age-specific fertilities in human females: comparison of individual-level fitness measures.

Lifetime reproductive success and timing of reproduction are key components of life-history evolution. To understand the evolution of reproductive schedules, it is important to use a measure of fitness that is sensitive both to reproductive quantity and reproductive timing. There is a contradiction between the theory, which mainly focuses on the rate measures of fitness (r and lambda), and empirical studies, which mainly use lifetime reproductive success (LRS), or some of its correlates, as a fitness measure. We measured phenotypic selection on age-specific fertilities in three pre-modern human populations using individually estimated finite rate of increase, er (lambda). We found that lambda and lifetime reproductive success ranked individuals differently according to their fitness: for example, a female giving birth to four children at a young age may actually have a higher fitness than a female giving birth to six children at a greater age. Increase in fertility at the young age classes (15-19 years) was favoured by selection, but the intensity of selection on fertility was higher in the older age classes (20-30 years), where the variance in fertility was highest. Hence, variation in fertility in the older age classes (20-30) was actually responsible for most of the observed variation in fitness among the individuals. Additionally, more than 90% of variation in fitness (lambda) was attributable to individual differences in LRS, whereas only about 5% of all variation in fitness was due to differences in the reproductive schedule. The rate-sensitive fitness measure did not significantly challenge the importance of total fertility as a component of fitness in humans. However, the rate-sensitive measure clearly allowed more accurate estimation of individual fitness, which may be important for answering some more specific questions.     

The Heterozygote Superiority Hypothesis for Polymorphic Color Vision Is Not Supported by Long-Term Fitness Data from Wild Neotropical Monkeys

The leading explanatory model for the widespread occurrence of color vision polymorphism in Neotropical primates is the heterozygote superiority hypothesis, which postulates that trichromatic individuals have a fitness advantage over other phenotypes because redgreen chromatic discrimination is useful for foraging, social signaling, or predator detection. Alternative explanatory models predict that dichromatic and trichromatic phenotypes are each suited to distinct tasks. To conclusively evaluate these models, one must determine whether proposed visual advantages translate into differential fitness of trichromatic and dichromatic individuals. We tested whether color vision phenotype is a significant predictor of female fitness in a population of wild capuchins, using longterm 26 years survival and fertility data. We found no advantage to trichromats over dichromats for three fitness measures fertility rates, offspring survival and maternal survival. This finding suggests that a selective mechanism other than heterozygote advantage is operating to maintain the color vision polymorphism. We propose that attention be directed to field testing the alternative mechanisms of balancing selection proposed to explain opsin polymorphism nichedivergence, frequencydependence and mutual benefit of association. This is the first indepth, longterm study examining the effects of color vision variation on survival and reproductive success in a naturallyoccurring population of primates.     

Optimization of selection for growth in Menz Sheep while minimizing inbreeding depression in fitness traits

The genetic trends in fitness (inbreeding, fertility and survival) of a closed nucleus flock of Menz sheep under selection during ten years for increased body weight were investigated to evaluate the consequences of selection for body weight on fitness. A mate selection tool was used to optimize in retrospect the actual selection and matings conducted over the project period to assess if the observed genetic gains in body weight could have been achieved with a reduced level of inbreeding. In the actual selection, the genetic trends for yearling weight, fertility of ewes and survival of lambs were 0.81 kg, –0.00026% and 0.016% per generation. The average inbreeding coefficient remained zero for the first few generations and then tended to increase over generations. The genetic gains achieved with the optimized retrospective selection and matings were highly comparable with the observed values, the correlation between the average breeding values of lambs born from the actual and optimized matings over the years being 0.99. However, the level of inbreeding with the optimized mate selections remained zero until late in the years of selection. Our results suggest that an optimal selection strategy that considers both genetic merits and coancestry of mates should be adopted to sustain the Menz sheep breeding program.     

Assessment of possible ecological risks and hazards of transgenic fish with implications for other sexually reproducing organisms

Transgenic technology is developing rapidly; however, consumers and environmentalists remain wary of its safety for use in agriculture. Research is needed to ensure the safe use of transgenic technology and thus increase consumer confidence. This goal is best accomplished by using a thorough, unbiased examination of risks associated with agricultural biotechnology. In this paper, we review discussion on risk and extend our approach to predict risk. We also distinguish between the risk and hazard of transgenic organisms in natural environments. We define transgene risk as the probability a transgene will spread into natural conspecific populations and define hazard as the probability of species extinction, displacement, or ecosystem disruption given that the transgene has spread. Our methods primarily address risk relative to two types of hazards: extinction which has a high hazard, and invasion which has an unknown level of hazard, similar to that of an introduced exotic species. Our method of risk assessment is unique in that we concentrate on the six major fitness components of an organism's life cycle to determine if transgenic individuals differ in survival or reproductive capacity from wild type. Our approach then combines estimates of the net fitness parameters into a mathematical model to determine the fate of the transgene and the affected wild population. We also review aspects of fish ecology and behavior that contribute to risk and examine combinations of net fitness parameters which can lead to invasion and extinction hazards. We describe three new ways that a transgene could result in an extinction hazard: (1) when the transgene increases male mating success but reduces daily adult viability, (2) when the transgene increases adult viability but reduces male fertility, and (3) when the transgene increases both male mating success and adult viability but reduces male fertility. The last scenario is predicted to cause rapid extinction, thus it poses an extreme risk. Although we limit our discussion to aquacultural applications, our methods can easily be adapted to other sexually reproducing organisms with suitable adjustments of terminology.     

Superparasitism of larval hosts by the walnut fly, <Emphasis Type="Italic">Rhagoletis juglandis</Emphasis>, and its implications for female and offspring performance

The oviposition-preference–offspring-performance hypothesis predicts that female insects should prefer to deposit clutches on or in hosts that maximize offspring performance. An important assumption behind this prediction is that female fitness is tightly correlated with the fitness of any one offspring. In this study, we evaluate offspring performance in the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), in relation to a previously described oviposition preference for previously exploited host fruit. In particular, we examined how superparasitism of walnut hosts influences offspring survival and weight at pupation under field conditions. We found that superparasitism was common and that increases in larval densities within fruit were associated with reduced larval survival and weight at pupation. In a laboratory experiment, female size was correlated with lifetime fecundity. In this system, oviposition preference is therefore negatively, not positively, correlated with offspring performance. We argue that patterns of female preference in this system reflect direct benefits to females that are traded off against costs in terms of offspring fitness. Because female fitness is a product not only of offspring quality but also of the total number of offspring produced, female walnut flies may be optimizing their fitness by producing many less fecund offspring. Studies examining the preference-performance hypothesis should consider the reproductive conflicts between parents and offspring as potential factors that influence the congruence between parental preference and offspring performance.     

Fitness and fertility among Kalahari !Kung

In this paper we develop a model that examines fertility and childhood mortality patterns and their relationship to environmental variables. Interactions among environmental variables can account for different fertility patterns and different mixes of these variables can produce similar patterns of fertility. Our model attempts to quantify the idea that there is a trade-off between producing a few children likely to survive to reproductive age and producing a greater number of children with lower chances for survival. The optimum mix of these strategies depends on environmental characteristics. We use the model to make predictions about fertility and mortality patterns among two Bushmen populations of southern Africa--the Ghanzi and Ngamiland !Kung--using data collected by Harpending in 1967-1968. The results do not support explanations of the low fertilities observed among !Kung Bushmen women, in whom it is thought that fitness is maximized by limiting fertility, and show no relationship between mortality and family size in either !Kung population. Instead, the number of offspring reaching reproductive age in both populations increases as their completed family size increases. We examine the effects of sex, birth order, and paternal investment on mortality. No sex ratio differences and no differences in mortality by sex or birth order are present. Infant mortality among women who married more than once is significantly higher than among women who married once, suggesting that paternal care has a significant effect.     

Fitness and extra-group reproduction in male Verreaux's sifaka: An analysis of reproductive success from 1989-1999

Adult males in social groups often compete with other male group members for access to adult females. In some primate species, males also seek mating opportunities in neighboring social groups. Such extra-group fertilizations (EGFs) provide an additional source of variation in male fitness. This additional component of fitness provided by EGFs must be incorporated into analyses that investigate sources of variation in male lifetime reproductive success. In this study, a model is analyzed in which male fitness over a 10-year sample period is decomposed into additive and multiplicative variance and covariance components. The data come from an ongoing study of a wild population of Verreaux's sifaka (Propithecus verreauxi verreauxi) located at Beza Mahafaly Special Reserve, Southwest Madagascar. Paternity and demographic data for 134 males are used to decompose male fitness into the following three multiplicative components: reproductive lifespan during sample period, fertility, and offspring survival. These multiplicative components are estimated for males reproducing within their resident groups plus (i.e., the additive portion) for males reproducing in neighboring social groups. The analysis shows that variation in fertility makes the largest contribution to variation in total fitness, followed by variation in amount of time spent in sample period (which is a proxy of total reproductive lifespan) and variation in offspring survival. EGFs contribute an important source of variation to male fitness, and numerous factors enhance the opportunities for EGFs in male sifaka. These include female choice, a high degree of home range overlap, and a limited mating season.     

Genomic analysis reveals depression due to both individual and maternal inbreeding in a free‐living mammal population

There is ample evidence for inbreeding depression manifested as a reduction in fitness or fitness‐related traits in the focal individual. In many organisms, fitness is not only affected by genes carried by the individual, but also by genes carried by their parents, for example if receiving parental care. While maternal effects have been described in many systems, the extent to which inbreeding affects fitness directly through the focal individual, or indirectly through the inbreeding coefficients of its parents, has rarely been examined jointly. The Soay sheep study population is an excellent system in which to test for both effects, as lambs receive extended maternal care. Here, we tested for both maternal and individual inbreeding depression in three fitness‐related traits (birthweight and weight and hindleg length at 4 months of age) and three fitness components (first‐year survival, adult annual survival and annual breeding success), using either pedigree‐derived inbreeding or genomic estimators calculated using ~37 000 SNP markers. We found evidence for inbreeding depression in 4‐month hindleg and weight, first‐year survival in males, and annual survival and breeding success in adults. Maternal inbreeding was found to depress both birthweight and 4‐month weight. We detected more instances of significant inbreeding depression using genomic estimators than the pedigree, which is partly explained through the increased sample sizes available. In conclusion, our results highlight that cross‐generational inbreeding effects warrant further exploration in species with parental care and that modern genomic tools can be used successfully instead of, or alongside, pedigrees in natural populations.     

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.     

The fitness threshold model: Random environmental change alters adaptive landscapes

We used a probabilistic optimization model to explore the joint evolutionary effects of random phenotypic and environmental variation. Two forms of environmental noise were defined in which the optimal phenotype remained constant but all organisms experienced either the same proportionate or the same absolute fitness gains and losses. There was no evolutionary effect of proportionate fitness fluctuations. In contrast, the optimal genotype varied with absolute fitness fluctuations, despite the environmental effect being phenotype-independent. We refer to such phenotype-independent fluctuation in absolute fitness as the fitness threshold model, because shared fitness effects determine the zero-fitness points (i.e. the baseline) on an intrinsic fitness function. Thus, environmental effects that are unrelated to a focal trait can cause peak shifts in the genetic optimum for the trait. Changes in the fitness threshold not only changed peak locations, but also altered the slopes defining the peaks, and so should alter the rate of evolution towards optima. This model pertains to evolution in any system, unless there is no phenotypic or environmental variance, or the selection function and distribution of phenotypic error assume similar shapes. Our results have many basic and applied implications for topics such as the maintenance of genetic variation, the canalization of development and the management of natural populations.