The Reproductive Ecology of Industrial Societies,Part II

Studies of the association between wealth and fertility in industrial populations have a rich history in the evolutionary literature, and they have been used to argue both for and against a behavioral ecological approach to explaining human variability. We consider that there are strong arguments in favor of measuring fertility (and proxies thereof) in industrial populations, not least because of the wide availability of large-scale secondary databases. Such data sources bring challenges as well as advantages, however. The purpose of this article is to illustrate these by examining the association between wealth and reproductive success in the United States, using the National Longitudinal Study of Youth 1979. We conduct a broad-based exploratory analysis of the relationship between wealth and fertility, employing both cross-sectional and longitudinal approaches, and multiple measures of both wealth (income and net worth) and fertility (lifetime reproductive success and transitions to first, second and third births). We highlight the kinds of decisions that have to be made regarding sample selection, along with the selection and construction of explanatory variables and control measures. Based on our analyses, we find a positive effect of both income and net worth on fertility for men, which is more pronounced for white men and for transitions to first and second births. Income tends to have a negative effect on fertility for women, while net worth is more likely to positively predict fertility. Different reproductive strategies among different groups within the same population highlight the complexity of the reproductive ecology of industrial societies. These results differ in a number of respects from other analyses using the same database. We suggest this reflects the impossibility of producing a definitive analysis, rather than a failure to identify the “correct” analytical strategy. Finally, we discuss how these findings inform us about (mal)adaptive decision-making.     

The spatial patterns of directional phenotypic selection

Local adaptation, adaptive population divergence and speciation are often expected to result from populations evolving in response to spatial variation in selection. Yet, we lack a comprehensive understanding of the major features that characterise the spatial patterns of selection, namely the extent of variation among populations in the strength and direction of selection. Here, we analyse a data set of spatially replicated studies of directional phenotypic selection from natural populations. The data set includes 60 studies, consisting of 3937 estimates of selection across an average of five populations. We performed meta‐analyses to explore features characterising spatial variation in directional selection. We found that selection tends to vary mainly in strength and less in direction among populations. Although differences in the direction of selection occur among populations they do so where selection is often weakest, which may limit the potential for ongoing adaptive population divergence. Overall, we also found that spatial variation in selection appears comparable to temporal (annual) variation in selection within populations; however, several deficiencies in available data currently complicate this comparison. We discuss future research needs to further advance our understanding of spatial variation in selection.     

Wealth,fertility and adaptive behaviour in industrial populations

The lack of association between wealth and fertility in contemporary industrialized populations has often been used to question the value of an evolutionary perspective on human behaviour. Here, we first present the history of this debate, and the evolutionary explanations for why wealth and fertility (the number of children) are decoupled in modern industrial settings. We suggest that the nature of the relationship between wealth and fertility remains an open question because of the multi-faceted nature of wealth, and because existing cross-sectional studies are ambiguous with respect to how material wealth and fertility are linked. A literature review of longitudinal studies on wealth and fertility shows that the majority of these report positive effects of wealth, although levels of fertility seem to fall below those that would maximize fitness. We emphasize that reproductive decision-making reflects a complex interplay between individual and societal factors that resists simple evolutionary interpretation, and highlight the role of economic insecurity in fertility decisions. We conclude by discussing whether the wealth–fertility relationship can inform us about the adaptiveness of modern fertility behaviour, and argue against simplistic claims regarding maladaptive behaviour in humans.     

Understanding the nature of wealth and its effects on human fitness

Studying fitness consequences of variable behavioural, physiological and cognitive traits in contemporary populations constitutes the specific contribution of human behavioural ecology to the study of human diversity. Yet, despite 30 years of evolutionary anthropological interest in the determinants of fitness, there exist few principled investigations of the diverse sources of wealth that might reveal selective forces during recent human history. To develop a more holistic understanding of how selection shapes human phenotypic traits, be these transmitted by genetic or cultural means, we expand the conventional focus on associations between socioeconomic status and fitness to three distinct types of wealth-embodied, material and relational. Using a model selection approach to the study of women's success in raising offspring in an African horticultural population (the Tanzanian Pimbwe), we find that the top performing models consistently include relational and material wealth, with embodied wealth as a less reliable predictor. Specifically, child mortality risk is increased with few household assets, parent nonresidency, child legitimacy, and one or more parents having been accused of witchcraft. The use of multiple models to test various hypotheses greatly facilitates systematic comparative analyses of human behavioural diversity in wealth accrual and investment across different kinds of societies.     

The Reproductive Ecology of Industrial Societies,Part I

Is fertility relevant to evolutionary analyses conducted in modern industrial societies? This question has been the subject of a highly contentious debate, beginning in the late 1980s and continuing to this day. Researchers in both evolutionary and social sciences have argued that the measurement of fitness-related traits (e.g., fertility) offers little insight into evolutionary processes, on the grounds that modern industrial environments differ so greatly from those of our ancestral past that our behavior can no longer be expected to be adaptive. In contrast, we argue that fertility measurements in industrial society are essential for a complete evolutionary analysis: in particular, such data can provide evidence for any putative adaptive mismatch between ancestral environments and those of the present day, and they can provide insight into the selection pressures currently operating on contemporary populations. Having made this positive case, we then go on to discuss some challenges of fertility-related analyses among industrialized populations, particularly those that involve large-scale databases. These include “researcher degrees of freedom” (i.e., the choices made about which variables to analyze and how) and the different biases that may exist in such data. Despite these concerns, large datasets from multiple populations represent an excellent opportunity to test evolutionary hypotheses in great detail, enriching the evolutionary understanding of human behavior.     

SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER,GERRIS ODONTOGASTER

Studies of phenotypic selection in natural populations are often concerned with simply detecting selection. In adopting a more mechanistic approach, this study compares the sexual selection regimes in natural populations of the water strider Gerris odontogaster with a priori predictions of selection, based on a number of previous field and laboratory studies of the behavioral mechanisms of selection. In this species, a general reluctance of females to mate allows for intersexual selection for ability to subdue reluctant females in males. Female reluctance to mate has been shown to decrease with increasing population density, suggesting that sexual selection should be weaker in high density populations. Three different populations with large differences in population density were studied. A number of traits including parasite load, body mass, body size and male abdominal process length were found to experience significant sexual selection. The investigated populations differed considerably with regard to the total strength of selection on the measured traits and the form of selection on single traits. In general, males in the population with the highest density experienced the weakest selection for grasping ability. This pattern is ascribed to density-related alterations of female mating behavior. Selection for male grasping ability, as reflected by selection on male abdominal process length, is reduced in high-density populations where reluctant females are more easily subdued. Further, the studied populations differed significantly in mean phenotype and phenotypic variance for male abdominal process length. It is suggested that interpopulational differences in selective regimes may generate local adaptations with respect to male abdominal process length, and that gene flow may contribute to the maintenance of the high genetic variation in this trait. It is further suggested that more empirical effort should be made in quantifying and understanding spatial and temporal variation in selection in natural populations, since this may provide information on the prevalence of local adaptations in metric traits and on the mechanisms of selection.     

The Strength of Selection against Neanderthal Introgression

Hybridization between humans and Neanderthals has resulted in a low level of Neanderthal ancestry scattered across the genomes of many modern-day humans. After hybridization, on average, selection appears to have removed Neanderthal alleles from the human population. Quantifying the strength and causes of this selection against Neanderthal ancestry is key to understanding our relationship to Neanderthals and, more broadly, how populations remain distinct after secondary contact. Here, we develop a novel method for estimating the genome-wide average strength of selection and the density of selected sites using estimates of Neanderthal allele frequency along the genomes of modern-day humans. We confirm that East Asians had somewhat higher initial levels of Neanderthal ancestry than Europeans even after accounting for selection. We find that the bulk of purifying selection against Neanderthal ancestry is best understood as acting on many weakly deleterious alleles. We propose that the majority of these alleles were effectively neutral—and segregating at high frequency—in Neanderthals, but became selected against after entering human populations of much larger effective size. While individually of small effect, these alleles potentially imposed a heavy genetic load on the early-generation human–Neanderthal hybrids. This work suggests that differences in effective population size may play a far more important role in shaping levels of introgression than previously thought.     

Will fatty worms help cure human obesity?

The incidence of obesity has reached epidemic proportions within industrial societies; however, research on human obesity has been hampered by our inability to control genetic and environmental factors. The control of energy homeostasis appears to be conserved among species. Recent creative research in Caenorhabditis elegans, including the application of a genome-wide RNA interference analysis, has provided insight into the genes involved in energy balance. In this article, we discuss the results of these studies and their potential importance to humans.     

The strength of phenotypic selection in natural populations

How strong is phenotypic selection on quantitative traits in the wild? We reviewed the literature from 1984 through 1997 for studies that estimated the strength of linear and quadratic selection in terms of standardized selection gradients or differentials on natural variation in quantitative traits for field populations. We tabulated 63 published studies of 62 species that reported over 2,500 estimates of linear or quadratic selection. More than 80% of the estimates were for morphological traits; there is very little data for behavioral or physiological traits. Most published selection studies were unreplicated and had sample sizes below 135 individuals, resulting in low statistical power to detect selection of the magnitude typically reported for natural populations. The absolute values of linear selection gradients |beta| were exponentially distributed with an overall median of 0.16, suggesting that strong directional selection was uncommon. The values of |beta| for selection on morphological and on life-history/phenological traits were significantly different: on average, selection on morphology was stronger than selection on phenology/life history. Similarly, the values of |beta| for selection via aspects of survival, fecundity, and mating success were significantly different: on average, selection on mating success was stronger than on survival. Comparisons of estimated linear selection gradients and differentials suggest that indirect components of phenotypic selection were usually modest relative to direct components. The absolute values of quadratic selection gradients |gamma| were exponentially distributed with an overall median of only 0.10, suggesting that quadratic selection is typically quite weak. The distribution of gamma values was symmetric about 0, providing no evidence that stabilizing selection is stronger or more common than disruptive selection in nature.     

Male Androphilia in the Ancestral Environment

The kin selection hypothesis posits that male androphilia (male sexual attraction to adult males) evolved because androphilic males invest more in kin, thereby enhancing inclusive fitness. Increased kin-directed altruism has been repeatedly documented among a population of transgendered androphilic males, but never among androphilic males in other cultures who adopt gender identities as men. Thus, the kin selection hypothesis may be viable if male androphilia was expressed in the transgendered form in the ancestral past. Using the Standard Cross-Cultural Sample (SCCS), we examined 46 societies in which male androphilia was expressed in the transgendered form (transgendered societies) and 146 comparison societies (non-transgendered societies). We analyzed SCCS variables pertaining to ancestral sociocultural conditions, access to kin, and societal reactions to homosexuality. Our results show that ancestral sociocultural conditions and bilateral and double descent systems were more common in transgendered than in non-transgendered societies. Across the entire sample, descent systems and residence patterns that would presumably facilitate increased access to kin were associated with the presence of ancestral sociocultural conditions. Among transgendered societies, negative societal attitudes toward homosexuality were unlikely. We conclude that the ancestral human sociocultural environment was likely conducive to the expression of the transgendered form of male androphilia. Descent systems, residence patterns, and societal reactions to homosexuality likely facilitated investments in kin by transgendered males. Given that contemporary transgendered male androphiles appear to exhibit elevated kin-directed altruism, these findings further indicate the viability of the kin selection hypothesis.     

Human marriage systems and sexual dimorphism in stature.

Contemporary populations of Homo sapiens are sexually dimorphic on a variety of traits. In terms of stature, men are reliably between 4% and 10% taller than women in well-sampled human populations. Are cross-cultural differences in the magnitude of sexual dimorphism consistent with expectations from sexual selection theory? Prior studies have provided conflicting answers to this question in part because they failed to agree on how the force of sexual selection should or could be operationalized. Here we offer a simple and unbiased method for operationalizing sexual selection and retest two separate predictions from earlier work (Alexander et al., 1979) about its expected impact on stature dimorphism in a sample of 155 societies. Neither prediction matches the observed cross-cultural distribution of dimorphism. However, this is not the consequence of a random distribution of dimorphism across societies. Instead, the data exhibit a robust and unexpected pattern.     

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.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata

The nature of male mating preferences, and how they differ from female mating preferences in species with conventional sex roles, has received little attention in sexual selection studies. We estimated the form and strength of sexual selection as a consequence of male and female mating preferences in a laboratory-based population of Drosophila serrata. The differences between sexual selection on male and female signal traits (cuticular hydrocarbons [CHCs]) were evaluated within a formal framework of linear and nonlinear selection gradients. Females tended to exert linear sexual selection on male CHCs, whereas males preferred intermediate female CHC phenotypes leading to convex (stabilizing) selection gradients. Possible mechanisms determining the nonlinear nature of sexual selection on female CHCs are proposed.     

Estimates of the average strength of natural selection are not inflated by sampling error or publication bias

Kingsolver et al.'s review of phenotypic selection gradients from natural populations provided a glimpse of the form and strength of selection in nature and how selection on different organisms and traits varies. Because this review's underlying database could be a key tool for answering fundamental questions concerning natural selection, it has spawned discussion of potential biases inherent in the review process. Here, we explicitly test for two commonly discussed sources of bias: sampling error and publication bias. We model the relationship between variance among selection gradients and sample size that sampling error produces by subsampling large empirical data sets containing measurements of traits and fitness. We find that this relationship was not mimicked by the review data set and therefore conclude that sampling error does not bias estimations of the average strength of selection. Using graphical tests, we find evidence for bias against publishing weak estimates of selection only among very small studies (N<38). However, this evidence is counteracted by excess weak estimates in larger studies. Thus, estimates of average strength of selection from the review are less biased than is often assumed. Devising and conducting straightforward tests for different biases allows concern to be focused on the most troublesome factors.     

Culturally transmitted paternity beliefs and the evolution of human mating behaviour

Recent anthropological findings document how certain lowland South American societies hold beliefs in 'partible paternity', which allow children to have more than one 'biological' father. This contrasts with Western beliefs in 'singular paternity', and biological reality, where children have just one father. Here, mathematical models are used to explore the coevolution of paternity beliefs and the genetic variation underlying human mating behaviour. A gene-culture coevolutionary model found that populations exposed to a range of selection regimes typically converge on one of two simultaneously stable equilibria; one where the population is monogamous and believes in singular paternity, and the other where the population is polygamous and believes in partible paternity. A second agent-based model, with alternative assumptions regarding the formation of mating consortships, broadly replicated this finding in populations with a strongly female-biased sex ratio, consistent with evidence for high adult male mortality in the region. This supports an evolutionary scenario in which ancestral South American populations with differing paternity beliefs were subject to divergent selection on genetically influenced mating behaviour, facilitated by a female-biased sex ratio, leading to the present-day associations of female control, partible paternity and polygamy in some societies, and male control, singular paternity and monogamy in others.     

Explaining marriage patterns in a globally representative sample through socio-ecology and population history: A Bayesian phylogenetic analysis using a new supertree

Comparative analyses have sought to explain variation in human marriage patterns, often using predictions derived from sexual selection theory. However, most previous studies have not controlled for non-independence of populations due to shared ancestry. Here we leverage a phylogenetic supertree of human populations that includes all 186 populations in the Standard Cross-Cultural Sample (SCCS), a globally representative and widely-used sample of human populations. This represents the most comprehensive human phylogeny to date, and allows us not only to control for non-independence, but also to quantify the role of population history in explaining behavioral variation, in addition to current socio-ecological conditions. We use multiple imputation to overcome missing data problems and build a comprehensive Bayesian phylogenetic model of marriage patterns with two correlated response variables and eleven minimally collinear predictors capturing various socio-ecological conditions. We show that ignoring phylogeny could lead to both false positives and false negatives, and that the phylogeny explained about twice as much variance as all the predictors combined. Pathogen stress and assault frequency emerged as the predictors most strongly associated with polygyny, which had been considered evidence for female choice of good genes and male intra-sexual competition or male coercion, respectively. Mixed support was found for a polygyny threshold based on variance in male wealth, which is discussed in light of recent theory. Barring caveats, these findings refine our understanding of the evolution of human marriage systems, and highlight the value of combining population history and current socio-ecology in explaining human behavioral variation. Future studies using the SCCS should do so using the present supertree.     

An analysis of continent-wide patterns of sexual selection in a passerine bird

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.     

Resources and the life course: Patterns through the demographic transition

In most mammals, and in the majority of traditional human societies for which data exist, status, power, or resource control correlates with lifetime reproductive success; male and female patterns differ. Because such correlations are often argued to have disappeared in human societies during the demographic transition of the nineteenth century, we analyzed wealth and lifetime reproductive success in a nineteenth-century Swedish population in four economically diverse parishes, subsuming geographic and temporal variation. Children of both sexes born to poorer parents were more likely than richer children to die or emigrate before reaching maturity. Poorer men, and women whose fathers were poorer, were less likely to marry in the parish than others, largely as a result of differential mortality and migration. Of all adults of both sexes who remained in their home parish and thus generated complete lifetime records, richer individuals had greater lifetime fertility and more children alive at age ten, than others. The age-specific fertility of richer women rises slightly sooner, and reaches a higher peak, than that of poorer women. These patterns persisted throughout the period of the sample (1824–1896). Thus, wealth appears, even during the demographic transition in an egalitarian society, to have influenced lifetime reproductive success positively.     

Low historical rates of cuckoldry in a Western European human population traced by Y-chromosome and genealogical data

Recent evidence suggests that seeking out extra-pair paternity (EPP) can be a viable alternative reproductive strategy for both males and females in many pair-bonded species, including humans. Accurate data on EPP rates in humans, however, are scant and mostly restricted to extant populations. Here, we provide the first large-scale, unbiased genetic study of historical EPP rates in a Western European human population based on combining Y-chromosomal data to infer genetic patrilineages with genealogical and surname data, which reflect known historical presumed paternity. Using two independent methods, we estimate that over the last few centuries, EPP rates in Flanders (Belgium) were only around 1–2% per generation. This figure is substantially lower than the 8–30% per generation reported in some behavioural studies on historical EPP rates, but comparable with the rates reported by other genetic studies of contemporary Western European populations. These results suggest that human EPP rates have not changed substantially during the last 400 years in Flanders and imply that legal genealogies rarely differ from the biological ones. This result has significant implications for a diverse set of fields, including human population genetics, historical demography, forensic science and human sociobiology.