Ecological variation in wealth–fertility relationships in Mongolia: the ‘central theoretical problem of sociobiology’ not a problem after all?

The negative wealth–fertility relationship brought about by market integration remains a puzzle to classic evolutionary models. Evolutionary ecologists have argued that this phenomenon results from both stronger trade-offs between reproductive and socioeconomic success in the highest social classes and the comparison of groups rather than individuals. Indeed, studies in contemporary low fertility settings have typically used aggregated samples that may mask positive wealth–fertility relationships. Furthermore, while much evidence attests to trade-offs between reproductive and socioeconomic success, few studies have explicitly tested the idea that such constraints are intensified by market integration. Using data from Mongolia, a post-socialist nation that underwent mass privatization, we examine wealth–fertility relationships over time and across a rural–urban gradient. Among post-reproductive women, reproductive fitness is the lowest in urban areas, but increases with wealth in all regions. After liberalization, a demographic–economic paradox emerges in urban areas: while educational attainment negatively impacts female fertility in all regions, education uniquely provides socioeconomic benefits in urban contexts. As market integration progresses, socio-economic returns to education increase and women who limit their reproduction to pursue education get wealthier. The results support the view that selection favoured mechanisms that respond to opportunities for status enhancement rather than fertility maximization.     

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’.     

Interactions between genotype and sexual conflict environment influence transgenerational fitness in Drosophila melanogaster

Theory predicts that sexual conflict can fuel evolutionary change and generate substantial reproductive costs. This was tested here by measuring the fitness of focal individuals across multiple generations using an experimental framework. We manipulated sexual conflict through high versus low exposure of females to males across a four-generation pedigree of Drosophila melanogaster, and assessed fitness in 1062 females and 639 males. We used the animal model to estimate (1) genotype by sexual conflict environment interactions for female fitness and (2) indirect benefits gained through sons and daughters. Some female genotypes achieved higher fitness under low, in comparison to high, conflict and vice versa. We found a consistent 10% reduction in female fitness under high conflict, regardless of maternal history. Following high exposure, females produced sons with increased, but grandsons with decreased, fitness. This opposing effect suggests no consistent fitness gains through sons for females that mated multiply. We saw no indirect benefits through daughters. Our pedigree was based exclusively on maternal links; however, maternal effects are unlikely to contribute significantly unless expressed across multiple generations. In sum, we quantified a significant sexual conflict load and a female genotype by sexual conflict interaction that could slow the erosion of genetic variation.     

Demographic studies enhance the understanding of evolutionarily (mal)adaptive behaviors and phenomena in humans: a review on fertility decline and an integrated model

Recently, statistical analyses of demographic datasets have come to play an important role for studies into the evolution of human life history. In the first part of this paper, I highlight fertility decline, an evolutionarily paradoxical phenomenon in terms of fitness maximization. Then, I conduct a literature review regarding the effects of socioeconomic status on the number of offspring, especially in modern developed, (post-)industrial, and low-fertility societies. Although a non-positive relationship between them has often been recognized as a general feature of fertility decline, there actually exists a great deal of variation. Based on the review, I discuss the association between socioeconomic success and reproductive success, and tackle an evolutionary question as to why people seek higher socioeconomic success that would not directly lead to higher reproductive success. It has been suggested that, in modern competitive environments, parents should set a higher value on their investment in children, and aim to have a smaller number of high-quality children. Also, parents would maintain higher socioeconomic status for themselves so as to provide high-levels of investment in their children. In the second part, I broadly consider seemingly evolutionarily (mal)adaptive outcomes besides fertility decline, including child abuse, menopause, and suicide. The integration of the major three approaches to human behavioral and psychological research (behavioral ecology, evolutionary psychology, and cultural evolution) could lead to a deeper understanding. I provide a model for the integrated approach. Rich empirical evidence accumulated in demographic studies, especially longitudinal and cross-cultural resources, can assist to develop a theoretical framework.     

Life-history theory, fertility and reproductive success in humans

According to life-history theory, any organism that maximizes fitness will face a trade-off between female fertility and offspring survivorship. This trade-off has been demonstrated in a variety of species, but explicit tests in humans have found a positive linear relationship between fitness and fertility. The failure to demonstrate a maximum beyond which additional births cease to enhance fitness is potentially at odds with the view that human fertility behaviour is currently adaptive. Here we report, to our knowledge, the first clear evidence for the predicted nonlinear relationship between female fertility and reproductive success in a human population, the Dogon of Mali, West Africa. The predicted maximum reproductive success of 4.1+/-0.3 surviving offspring was attained at a fertility of 10.5 births. Eighty-three per cent of the women achieved a lifetime fertility level (7-13 births) for which the predicted mean reproductive success was within the confidence limits (3.4 to 4.8) for reproductive success at the optimal fertility level. Child mortality, rather than fertility, was the primary determinant of fitness. Since the Dogon people are farmers, our results do not support the assumptions that: (i) contemporary foragers behave more adaptively than agriculturalists, and (ii) that adaptive fertility behaviour ceased with the Neolithic revolution some 9000 years ago. We also present a new method that avoids common biases in measures of reproductive success.     

Contribution of maternal effects to dietary selection in Mediterranean fruit flies

Individual responses to dietary variation represent a fundamental component of fitness, and nutritional adaptation can occur over just a few generations. Maternal effects can show marked proximate responses to nutrition, but whether they contribute to longer term dietary adaptation is unclear. Here, we tested the hypotheses that maternal effects: (i) contribute to dietary adaptation, (ii) diminish when dietary conditions are constant between generations, (iii) are trait‐specific and (iv) interact with high‐ and low‐quality food. We used experimental evolution regimes in the medfly (Ceratitis capitata) to test these predictions by subjecting an outbred laboratory‐adapted population to replicated experimental evolution on either constant high calorie sugar (‘A’) or low‐calorie starch (‘S’) larval diets, with a standard adult diet across both regimes. We measured the contribution of maternal effects by comparing developmental and adult phenotypes of individuals reared on their own diet with those swapped onto the opposite diet for either one or two generations (high and low maternal effect conditions, respectively), both at the start and after 30 generations of selection. Initially, there were strong maternal effects on female body mass and male mating success but not larval survival. Interestingly, the initial maternal effects observed in female body mass and male mating success showed sex‐specific interactions when individuals from high calorie regimes were tested on low calorie diets. However, as populations responded to selection, the effects of maternal provisioning on all traits diminished. The results broadly supported the predictions. They show how the contribution of maternal effects to dietary responses evolves in a context‐dependent manner, with significant variation across different fitness‐related traits. We conclude that maternal effects can evolve during nutritional adaptation and hence may be an important life history trait to measure, rather than to routinely minimize.     

How do reproductive skew and founder group size affect genetic diversity in reintroduced populations?

Reduced genetic diversity can result in short-term decreases in fitness and reduced adaptive potential, which may lead to an increased extinction risk. Therefore, maintaining genetic variation is important for the short- and long-term success of reintroduced populations. Here, we evaluate how founder group size and variance in male reproductive success influence the long-term maintenance of genetic diversity after reintroduction. We used microsatellite data to quantify the loss of heterozygosity and allelic diversity in the founder groups from three reintroductions of tuatara ( Sphenodon ), the sole living representatives of the reptilian order Rhynchocephalia. We then estimated the maintenance of genetic diversity over 400 years (∼10 generations) using population viability analyses. Reproduction of tuatara is highly skewed, with as few as 30% of males mating across years. Predicted losses of heterozygosity over 10 generations were low (1–14%), and populations founded with more animals retained a greater proportion of the heterozygosity and allelic diversity of their source populations and founder groups. Greater male reproductive skew led to greater predicted losses of genetic diversity over 10 generations, but only accelerated the loss of genetic diversity at small population size (<250 animals). A reduction in reproductive skew at low density may facilitate the maintenance of genetic diversity in small reintroduced populations. If reproductive skew is high and density-independent, larger founder groups could be released to achieve genetic goals for management.     

Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation

The consequences of sexual interactions extend beyond the simple production of offspring. These interactions typically entail direct effects on female fitness, but may also impact the life histories of later generations. Evaluating the cross-generational effects of sexual interactions provides insights into the dynamics of sexual selection and conflict. Such studies can elucidate whether offspring fitness optima diverge across sexes upon heightened levels of sexual interaction among parents. Here, we found that, in Drosophila melanogaster, components of reproductive success in females, but not males, were contingent on the nature of sexual interactions experienced by their mothers. In particular, maternal sexual interactions with non-sires enhanced female fecundity in the following generation. This highlights the importance of non-sire influences of sexual interactions on the expression of offspring life histories.     

Retirement investment theory explains patterns in songbird nest-site choice

When opposing evolutionary selection pressures act on a behavioural trait, the result is often stabilizing selection for an intermediate optimal phenotype, with deviations from the predicted optimum attributed to tracking a moving target, development of behavioural syndromes or shifts in riskiness over an individual''s lifetime. We investigated nest-site choice by female golden-winged warblers, and the selection pressures acting on that choice by two fitness components, nest success and fledgling survival. We observed strong and consistent opposing selection pressures on nest-site choice for maximizing these two fitness components, and an abrupt, within-season switch in the fitness component birds prioritize via nest-site choice, dependent on the time remaining for additional nesting attempts. We found that females consistently deviated from the predicted optimal behaviour when choosing nest sites because they can make multiple attempts at one fitness component, nest success, but only one attempt at the subsequent component, fledgling survival. Our results demonstrate a unique natural strategy for balancing opposing selection pressures to maximize total fitness. This time-dependent switch from high to low risk tolerance in nest-site choice maximizes songbird fitness in the same way a well-timed switch in human investor risk tolerance can maximize one''s nest egg at retirement. Our results also provide strong evidence for the adaptive nature of songbird nest-site choice, which we suggest has been elusive primarily due to a lack of consideration for fledgling survival.     

Optimizing Modern Family Size

Modern industrialized populations lack the strong positive correlations between wealth and reproductive success that characterize most traditional societies. While modernization has brought about substantial increases in personal wealth, fertility in many developed countries has plummeted to the lowest levels in recorded human history. These phenomena contradict evolutionary and economic models of the family that assume increasing wealth reduces resource competition between offspring, favoring high fertility norms. Here, we review the hypothesis that cultural modernization may in fact establish unusually intense reproductive trade-offs in wealthy relative to impoverished strata, favoring low fertility. We test this premise with British longitudinal data (the Avon Longitudinal Study of Parents and Children), exploring maternal self-perceptions of economic hardship in relation to increasing family size and actual socioeconomic status. Low-income and low-education-level mothers perceived the greatest economic costs associated with raising two versus one offspring. However, for all further increases to family size, reproduction appears most expensive for relatively wealthy and well-educated mothers. We discuss our results and review current literature on the long-term consequences of resource dilution in modern families.     

EXTRA‐PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.     

The variance in inbreeding depression and the recovery of fitness in bottlenecked populations

Theoretical analyses of inbreeding suggest that following an increased degree of inbreeding there may be a temporary recovery of fitness, because of selection either within or among inbred lineages. This is possible because selection can act more efficiently to remove deleterious alleles given the greater homozygosity of such populations. If common, recovery of fitness following inbreeding may be important for understanding some evolutionary processes and for management strategies of remnant populations, yet empirical evidence for such recovery in animals is scant. Here we describe the effects of single-pair population bottlenecks on a measure of fitness in Drosophila melanogaster. We compared a large number of families from each of 52 inbred lines with many families from the outbred population from which the inbred lineages were derived. Measures were made at the third and the 20th generations after the bottleneck. In both generations there was, on average, substantial inbreeding depression together with a highly significant variance among the inbred lines in the amount of fitness reduction. The average fitness of inbred lines was correlated across generations. Our data provide evidence for the possibility of recovery of fitness at two levels, because (i) the average fitness reduction in the F20 generation was significantly less than in the F3 generation, which implies that selection within lines has occurred, and (ii) the large variance in inbreeding depression among inbred lines implies that selection among them is possible. The high variance in inbreeding depression among replicate lines implies that modes of evolution which require a low level of inbreeding depression can function at least in a fraction of inbred populations within a species and that results from studies with low levels of replication should be treated with caution.     

Low fertility in contemporary humans and the mate value of their children: sex-specific effects on social status indicators

Evolutionary explanations of low fertility in modern affluent societies commonly state that low fertility is the outcome of high parental investments in the quality of their children. Although the empirical evidence that modern parents do face a quantity–quality trade-off is strong, two issues that are relevant from an evolutionary perspective have not received much attention. First, sex differences in the proximate aspects of quality have been largely ignored. Second, the relationship between the quantity of children and their reproductive success in contemporary low-fertility societies remains unclear. In this article, we study the quantity–quality trade-off as a trade-off between the number of children and the mate value and reproductive success of those children. We examine the trade-off in two steps. First, a lower number of children is expected to increase the mate value of these children. Second, greater mate value is expected to lead to greater reproductive success. Using sex-specific indicators of mate value, we test these hypotheses in a representative sample of the Dutch population aged 55–85 in 1992 (n=3229). This sample contains information on three successive generations in which the middle generation has completed fertility. We find support for the first hypothesis, but only partial support for the second hypothesis. A higher number of children is traded off against the mate value of the children, but not against their reproductive success. We conclude that the conditions under which the quantity of children is traded off against their reproductive success depend on the social environment.     

Top-down and bottom-up control of life-history strategies in coho salmon (Oncorhynchus kisutch)

Sexual maturation profoundly affects population dynamics, but the degrees to which genetic, top-down, and bottom-up controls affect age at maturity are unclear. Salmonid fishes have plastic age at maturity, and we consider genetic and environmental effects on this trait by developing fitness functions for coho salmon (Oncorhynchus kisutch). The functions are based on size-specific survival and reproductive success, where reproductive success is the product of fecundity and ability to defend nests (females) or the product of sperm volume and ability to mate (males). We model genetic and bottom-up controls (e.g., food availability) with an environmentally explicit growth function and top-down control (predation mortality) with survival functions that consider both size-dependent and size-independent mortality. For females, we predict that early maturation rarely maximizes fitness, but males can maximize fitness by maturing early if they grow well in freshwater. We predict that early maturation is most affected by the bottom-up effects of resource distribution at sea, followed by bottom-up and genotypic effects in freshwater. Top-down processes are predicted to have strong effects on the likelihood of delayed maturation.     

The effect of school performance upon marriage and long-term reproductive success in 10,000 Swedish males and females born 1915–1929

Humans are an exceptionally intelligent species, and the selective pressures which may have shaped these advanced cognitive powers are therefore of interest. This study investigates the fitness consequences of pre-reproductive school performance in a Swedish population-based cohort of 5244 males and 4863 females born 1915-1929. School performance was measured at around age 10 using three variables: mean school marks, being promoted/held back in school, and recognised learning difficulties. Our primary outcomes were probability of ever marrying, total number of children and total number of grandchildren. In males (but not females), poorer school performance predicted fewer children and grandchildren. This was primarily mediated via probability of marriage; mortality and fertility within marriage were not important mediating pathways. The effect of school performance upon marriage in males was independent of early-life social and biological characteristics, including birth weight for gestational age, preterm birth, family composition, and family socioeconomic position. The effect of school performance upon the probability of marriage in males was, however, largely mediated by adult socioeconomic position. This suggests that in general sexual selection for cognitive abilities per se did not play a major role in either males or females in this cohort. Adult socioeconomic position did not, however, fully explain the marriage disadvantage in males or (at marginal significance) females with particularly poor school performance. We conclude that school performance can affect long-term reproductive success. In this population, however, the effect is confined to males and is largely mediated by the increased probability of marriage which comes with their greater socioeconomic success.     

Early and adult social environments have independent effects on individual fitness in a social vertebrate

Evidence that the social environment at critical stages of life-history shapes individual trajectories is accumulating. Previous studies have identified either current or delayed effects of social environments on fitness components, but no study has yet analysed fitness consequences of social environments at different life stages simultaneously. To fill the gap, we use an extensive dataset collected during a 24-year intensive monitoring of a population of Alpine marmots (Marmota marmota), a long-lived social rodent. We test whether the number of helpers in early life and over the dominance tenure length has an impact on litter size at weaning, juvenile survival, longevity and lifetime reproductive success (LRS) of dominant females. Dominant females, who were born into a group containing many helpers and experiencing a high number of accumulated helpers over dominance tenure length showed an increased LRS through an increased longevity. We provide evidence that in a wild vertebrate, both early and adult social environments influence individual fitness, acting additionally and independently. These findings demonstrate that helpers have both short- and long-term effects on dominant female Alpine marmots and that the social environment at the time of birth can play a key role in shaping individual fitness in social vertebrates.     

Effects of fragmentation of clones compound over vegetative generations in the floating plant Pistia stratiotes

Background and AimsClonal plants dominate many plant communities, especially in aquatic systems, and clonality appears to promote invasiveness and to affect how diversity changes in response to disturbance and resource availability. Understanding how the special physiological and morphological properties of clonal growth lead to these ecological effects depends upon studying the long-term consequences of clonal growth properties across vegetative generations, but this has rarely been done. This study aimed to show how a key clonal property, physiological integration between connected ramets within clones, affects the response of clones to disturbance and resources in an aquatic, invasive, dominant species across multiple generations.MethodsSingle, parental ramets of the floating stoloniferous plant Pistia stratiotes were grown for 3 weeks, during which they produced two or three generations of offspring; connections between new ramets were cut or left intact. Individual offspring were then used as parents in a second 3-week iteration that crossed fragmentation with previous fragmentation in the first iteration. A third iteration yielded eight treatment combinations, zero to three rounds of fragmentation at different times in the past. The experiment was run once at a high and once at a low level of nutrients.ResultsIn each iteration, fragmentation increased biomass of the parental ramet, decreased biomass of the offspring and increased number of offspring. These effects persisted and compounded from one iteration to another, though more recent fragmentation had stronger effects, and were stronger at the low than at the high nutrient level. Fragmentation did not affect net accumulation of mass by groups after one iteration but increased it after two iterations at low nutrients, and after three iterations at both nutrient levels.ConclusionsBoth the positive and negative effects of fragmentation on clonal performance can compound and persist over time and can be stronger when resource levels are lower. Even when fragmentation has no short-term net effect on clonal performance, it can have a longer-term effect. In some cases, fragmentation may increase total accumulation of mass by a clone. The results provide the first demonstration of how physiological integration in clonal plants can affect fitness across generations and suggest that increased disturbance may promote invasion of introduced clonal species via effects on integration, perhaps especially at lower nutrient levels.     

Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar)

Major histocompatibility complex (MHC)-dependent mating preferences have been observed across vertebrate taxa and these preferences are expected to promote offspring disease resistance and ultimately, viability. However, little empirical evidence linking MHC-dependent mate choice and fitness is available, particularly in wild populations. Here, we explore the adaptive potential of previously observed patterns of MHC-dependent mate choice in a wild population of Atlantic salmon (Salmo salar) in Québec, Canada, by examining the relationship between MHC genetic variation and adult reproductive success and offspring survival over 3 years of study. While Atlantic salmon choose their mates in order to increase MHC diversity in offspring, adult reproductive success was in fact maximized between pairs exhibiting an intermediate level of MHC dissimilarity. Moreover, patterns of offspring survival between years 0+ and 1+, and 1+ and 2+ and population genetic structure at the MHC locus relative to microsatellite loci indicate that strong temporal variation in selection is likely to be operating on the MHC. We interpret MHC-dependent mate choice for diversity as a likely bet-hedging strategy that maximizes parental fitness in the face of temporally variable and unpredictable natural selection pressures.     

A silver spoon for a golden future: long-term effects of natal origin on fitness prospects of oystercatchers (Haematopus ostralegus)

1. Long-term effects of conditions during early development on fitness are important for life history evolution and population ecology. Using multistrata mark-recapture models on 20 years of data, we quantified the relation between rearing conditions and lifetime fitness in a long-lived shorebird, the oystercatcher (Haematopus ostralegus). We addressed specifically the relative contribution of short- and long-term effects of rearing conditions to overall fitness consequences. 2. Rearing conditions were defined by differences in natal habitat quality, in which there is a clear dichotomy in our study population. In the first year of life, fledglings from high-quality natal origin had a 1.3 times higher juvenile survival. Later in life (age 3-11), individuals of high-quality natal origin had a 1.6 times higher adult prebreeder survival. The most striking effect of natal habitat quality was that birds that were reared on high-quality territories had a higher probability of settling in high-quality habitat (44% vs. 6%). Lifetime reproductive success of individuals born in high-quality habitat was 2.2 times higher than that of individuals born in low-quality habitat. This difference increased further when fitness was calculated over several generations, due to a correlation between the quality of rearing conditions of parents and their offspring. 3. Long-term effects of early conditions contributed more to overall fitness differences as short-term consequences, contrary to common conceptions on this issue. 4. This study illustrates that investigating only short-term effects of early conditions can lead to the large underestimation of fitness consequences. We discuss how long-term consequences of early conditions may affect settlement decisions and source-sink population interactions.     

Variation and change in fertility in West Central Nepal

This article employs temporal and intracultural frames of reference to examine patterns of variation in fertility among the caste-Hindus of West Central Nepal. Before the onset of major socioeconomic development in the region, three groups, the large-farm high castes, the small-farm high castes, and the low castes, exhibited distinct patterns of reproductive behavior which have been traced over the course of 25 years. Analysis of age-specific fertility rates suggests that one group, the small farm high-caste, maintained relatively low fertility before major development of the region occurred, and, over time, began using modern contraception in order to keep fertility low. Evidence from the low castes suggests that they are beginning deliberately to reduce fertility, but the large-farm high castes continue to have high fertility.