Severe intergenerational reproductive conflict and the evolution of menopause

Human menopause is ubiquitous among women and is uninfluenced by modernity. In addition, it remains an evolutionary puzzle: studies have largely failed to account for diminishing selection on reproduction beyond 50 years. Using a 200‐year dataset on pre‐industrial Finns, we show that an important component is between‐generation reproductive conflict among unrelated women. Simultaneous reproduction by successive generations of in‐laws was associated with declines in offspring survivorship of up to 66%. An inclusive fitness model revealed that incorporation of the fitness consequences of simultaneous intergenerational reproduction between in‐laws, with those of grandmothering and risks of dying in childbirth, were sufficient to generate selection against continued reproduction beyond 51 years. Decomposition of model estimates suggested that the former two were most influential in generating selection against continued reproduction. We propose that menopause evolved, in part, because of age‐specific increases in opportunities for intergenerational cooperation and reproductive competition under ecological scarcity.     

Fitness,reproduction and longevity among European aristocratic and rural Finnish families in the 1700s and 1800s

The life histories of two socio-economically different groups of humans comprising birth cohorts from the 1700s and 1800s were investigated. It was discovered that fertility selection was greater among European aristocrats and mortality selection greater among rural Finns. The life history of the rural Finns involved shorter female life spans, a considerably longer period of reproduction, higher juvenile mortality, a greater total production of offspring and slightly higher individual fitness. In a comparison of parental cohorts, it was discovered that longevity and progeny survival improved significantly from the 1700s to the 1800s. Out of the three factors investigated, longevity was found to influence reproduction and fitness more than socio-economic group or birth cohort. The reproductive efficacy and fitness of women increased along with their life span. However, reproductive success and fitness were lower among women with the longest life span (over 80 years). Among men, reproductive success improved consistently along with the increase in longevity. When birth intervals were examined, it was discovered that the sex of previous offspring did not influence the interval between births.     

Evolutionary stability and the rarity of grandmothering

The provision of intergenerational care, via the Grandmother Hypothesis, has been implicated in the evolution of postfertile longevity, particularly in humans. However, if grandmothering does provide fitness benefits, a key question is why has it evolved so infrequently? We investigate this question with a combination of life‐history and evolutionary game theory. We derive simple eligibility and stability thresholds, both of which must be satisfied if intergenerational care is first to evolve and then to persist in a population. As one threshold becomes easier to fulfill, the other becomes more difficult, revealing a conflict between the two. As such, we suggest that, in fact, we should expect the evolution of grandmothering to be rare.     

Mating frequency and inclusive fitness in Drosophila melanogaster

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.     

Quantitative genetic versions of Hamilton's rule with empirical applications

Hamilton''s theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton''s perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton''s rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton''s rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton''s rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.     

Invasion fitness,inclusive fitness,and reproductive numbers in heterogeneous populations

How should fitness be measured to determine which phenotype or “strategy” is uninvadable when evolution occurs in a group‐structured population subject to local demographic and environmental heterogeneity? Several fitness measures, such as basic reproductive number, lifetime dispersal success of a local lineage, or inclusive fitness have been proposed to address this question, but the relationships between them and their generality remains unclear. Here, we ascertain uninvadability (all mutant strategies always go extinct) in terms of the asymptotic per capita number of mutant copies produced by a mutant lineage arising as a single copy in a resident population (“invasion fitness”). We show that from invasion fitness uninvadability is equivalently characterized by at least three conceptually distinct fitness measures: (i) lineage fitness, giving the average individual fitness of a randomly sampled mutant lineage member; (ii) inclusive fitness, giving a reproductive value weighted average of the direct fitness costs and relatedness weighted indirect fitness benefits accruing to a randomly sampled mutant lineage member; and (iii) basic reproductive number (and variations thereof) giving lifetime success of a lineage in a single group, and which is an invasion fitness proxy. Our analysis connects approaches that have been deemed different, generalizes the exact version of inclusive fitness to class‐structured populations, and provides a biological interpretation of natural selection on a mutant allele under arbitrary strength of selection.     

An inclusive fitness analysis of synergistic interactions in structured populations

We study the evolution of a pair of competing behavioural alleles in a structured population when there are non-additive or ‘synergistic’ fitness effects. Under a form of weak selection and with a simple symmetry condition between a pair of competing alleles, Tarnita et al. provide a surprisingly simple condition for one allele to dominate the other. Their condition can be obtained from an analysis of a corresponding simpler model in which fitness effects are additive. Their result uses an average measure of selective advantage where the average is taken over the long-term—that is, over all possible allele frequencies—and this precludes consideration of any frequency dependence the allelic fitness might exhibit. However, in a considerable body of work with non-additive fitness effects—for example, hawk–dove and prisoner''s dilemma games—frequency dependence plays an essential role in the establishment of conditions for a stable allele-frequency equilibrium. Here, we present a frequency-dependent generalization of their result that provides an expression for allelic fitness at any given allele frequency p. We use an inclusive fitness approach and provide two examples for an infinite structured population. We illustrate our results with an analysis of the hawk–dove game.     

The factors that favor adaptive habitat construction versus non‐adaptive environmental conditioning

Adaptive habitat construction is a process by which individuals alter their environment so as to increase their (inclusive) fitness. Such alterations are a subset of the myriad ways that individuals condition their environment. We present an individual‐based model of habitat construction to explore what factors might favor selection when the benefits of environmental alterations are shared by individuals of the same species. Our results confirm the predictions of inclusive fitness and group selection theory and expectations based on previous models that construction will be more favored when its benefits are more likely to be directed to self or near kin. We found that temporal variation had no effect on the evolution of construction. For spatial heterogeneity, construction was disfavored when the spatial pattern of movement did not match the spatial pattern of environmental heterogeneity, especially when there was spatial heterogeneity in the optimal amount of construction. Under those conditions, very strong selection was necessary to favor genetic differentiation of construction propensity among demes. We put forth a constitutive theory for the evolution of adaptive habitat construction that unifies our model with previous verbal and quantitative models into a formal conceptual framework.     

The evolution of non-maternal care in anthropoid primates: a test of the hypotheses

The amount of non-maternal care (allocare) found in primates varies greatly from species to species. Our paper examines this variation and focuses on possible reasons why mothers in some anthropoid primate species are prepared to relinquish their infants to other carers whereas others are not. We use data collected from the literature to test a number of hypotheses that attempt to explain the observed variation in non-maternal care. Analyses were carried out using comparative methods that control for the influence of both body size and phylogeny on life-history and ecological variation. The results support previous studies of both primates and other mammals in finding a clear link between the amount of allocare provided and female reproductive rates. Species with high allocare levels grow rapidly post-natally and wean their infants at a younger age (but at the same relative size) than species of the same body size with lower allocare levels. This early weaning allows high allocare species to support higher birth rates than low allocare species but does not result in earlier maturation. Our results, therefore, suggest that mothers allow non-maternal care of their infants in order to increase their own reproductive output. It is not clear whether such a strategy also benefits the infant, as we could find no link between the presence of allocare and early maturation (which would increase the infant's reproductive output) or between allocare levels and infant survival (as measured by vulnerability to infanticide). This suggests that mothers and infants might come into conflict over transfer to other carers, as the benefits to the mother may not be accompanied by benefits to the infant. However, although mothers may benefit from allocare in some circumstances, they will not be expected to allow allocare if the costs are high (e.g. if there is a high risk to the infant).     

Investment and relatedness: A cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis)

Helping at the nest in birds is often termed altruism. However, so far, no study has ever demonstrated high costs to a helper's own lifetime reproductive success (=direct fitness), nor its compensation through benefits from relatives other than its own offspring (=indirect fitness). In this paper on pied kingfishers (Ceryle rudis) the relationship between investment, relatedness and inclusive fitness (expressed in terms of genetic equivalents) is investigated for breeding males, and males that help either relatives (=primary helpers) or strangers (=secondary helpers). With respect to guarding nests against predators and feeding young, primary helpers invest as much as breeders, but secondary helpers contribute significantly less. These differences in status and investment (measured in energy expenditure) affect the birds' future to such an extent that primary helpers have a lower chance of surviving and mating than secondary helpers. However, their costs in direct fitness are compensated by pronounced benefits to indirect fitness, resulting from improved survival of siblings and parents. An attempt is made to calculate the inclusive fitness of birds following different strategies over a 2-year period. It is concluded that (a) breeding is superior to helping and helping superior to doing nothing and (b) that kin-selection must be invoked to explain why surplus males choose the more costly primary helper strategy instead of the cheaper secondary helper strategy. Alternative explanations, including group selection, parental manipulation and reciprocity, are discussed.     

Early‐life conditions impact juvenile telomere length,but do not predict later life‐history strategies or fitness in a wild vertebrate

Environmental conditions experienced during early life may have long‐lasting effects on later‐life phenotypes and fitness. Individuals experiencing poor early‐life conditions may suffer subsequent fitness constraints. Alternatively, individuals may use a strategic “Predictive Adaptive Response” (PAR), whereby they respond—in terms of physiology or life‐history strategy—to the conditions experienced in early life to maximize later‐life fitness. Particularly, the Future Lifespan Expectation (FLE) PAR hypothesis predicts that when poor early‐life conditions negatively impact an individual''s physiological state, it will accelerate its reproductive schedule to maximize fitness during its shorter predicted life span. We aimed to measure the impact of early‐life conditions and resulting fitness across individual lifetimes to test predictions of the FLE hypothesis in a wild, long‐lived model species. Using a long‐term individual‐based dataset, we investigated how early‐life conditions are linked with subsequent fitness in an isolated population of the Seychelles warbler Acrocephalus sechellensis. How individuals experience early‐life environmental conditions may vary greatly, so we also tested whether telomere length—shorter telomers are a biomarker of an individual''s exposure to stress—can provide an effective measure of the individual‐specific impact of early‐life conditions. Specifically, under the FLE hypothesis, we would expect shorter telomeres to be associated with accelerated reproduction. Contrary to expectations, shorter juvenile telomere length was not associated with poor early‐life conditions, but instead with better conditions, probably as a result of faster juvenile growth. Furthermore, neither juvenile telomere length, nor other measures of early‐life conditions, were associated with age of first reproduction or the number of offspring produced during early life in either sex. We found no support for the FLE hypothesis. However, for males, poor early‐life body condition was associated with lower first‐year survival and reduced longevity, indicating that poor early‐life conditions pose subsequent fitness constraints. Our results also showed that using juvenile telomere length as a measure of early‐life conditions requires caution, as it is likely to not only reflect environmental stress but also other processes such as growth.     

Fluctuating natural selection accounts for the evolution of diversification bet hedging

Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of ‘bet-hedging’ traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination—a model diversification bet-hedging trait—in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing—across 70 intervals throughout five seasons—to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.     

Evolutionary routes to non-kin cooperative breeding in birds

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.     

Mate choice for optimal (k)inbreeding

Mating between related individuals results in inbreeding depression, and this has been thought to select against incestuous matings. However, theory predicts that inbreeding can also be adaptive if it increases the representation of genes identical by descent in future generations. Here, I recapitulate the theory of inclusive fitness benefits of incest, and extend the existing theory by deriving the stable level of inbreeding in populations practicing mate choice for optimal inbreeding. The parsimonious assumptions of the model are that selection maximizes inclusive fitness, and that inbreeding depression is a linear function of homozygosity of offspring. The stable level of inbreeding that maximizes inclusive fitness, and is expected to evolve by natural selection, is shown to be less than previous theory suggests. For wide range of realistic inbreeding depression strengths, mating with intermediately related individuals maximizes inclusive fitness. The predicted preference for intermediately related individuals as reproductive partners is in qualitative agreement with empirical evidence from mate choice experiments and reproductive patterns in nature.     

A reconciliation of inclusive fitness and personal fitness approaches: a proposed correcting term for the inclusive fitness formula

Hamilton implicitly defined the inclusive fitness of an individual as the number of genomes, identical by descent to its own, but not in its own body, which owe their existence to expression of genes in said individual. Hamilton regarded inclusive fitness as the true metric of evolutionary success and the thin- maximized by selection. Williams, Stern and Orlove either claimed this property for mean reproductive success, or stated that expected reproductive success equals expected inclusive fitness. These statements are reconciled if a correcting term is added to Hamilton's inclusive fitness formula.This change completely accounts for inclusive fitness in personal fitness terminology. The use of ? in place of r renders the new formula exact. This has less numerical impact than the addition of the correcting term to begin with, but helps show inclusive fitness theory holds exactly.     

A tradeoff between reproduction and growth in contemporary Finnish women

Women have been suggested to trade growth in height for reproduction, as an earlier age at menarche and first birth seem to be related to shorter adult stature. Although women likely accrue fitness benefits by maturing and starting reproduction at young age, short adult stature may be selected against by natural and sexual selection later in their life. We studied how age at menarche and first reproduction affected adult height and whether adult height in turn was related to lifetime reproductive success in Finnish women born 1946–1958. Our results show that a delay of 1 year in age at menarche and first reproduction was related to a 0.43- and 0.20-cm increase in adult height, respectively. The sex of the first-born offspring was not related to adult height. Moreover, women gained fitness benefits by starting reproduction early but not by growing tall. These findings among Finnish women are thus compatible with tradeoffs between reproduction and growth, by showing a compromised adult height at the cost of early age at menarche and first birth. However, in these women, natural selection favored those women who traded their stature for young motherhood.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Lifetime reproductive success and longevity of queens in an annual social insect

Although central to understanding life‐history evolution, the relationship between lifetime reproductive success and longevity remains uncertain in many organisms. In social insects, no studies have reported estimates of queens’ lifetime reproductive success and longevity within populations, despite the importance of understanding how sociality and associated within‐group conflict affect life‐history traits. To address this issue, we studied two samples of colonies of the annual bumblebee, Bombus terrestris audax, reared from wild‐caught queens from a single population. In both samples, queens’ lifetime reproductive success, measured as either queens’ inclusive fitness or as total biomass of queen‐produced sexuals (new queens and males), was significantly positively associated with queen longevity, measured from the day the first worker was produced. We suggest that a positive relationship between reproductive success and longevity was inherited from nonsocial ancestors showing parental care and maintained, at least in part, because the presence of workers buffers queens against extrinsic mortality.     

Selection for long lifespan in men: benefits of grandfathering?

Life-history theory suggests that individuals should live until their reproductive potential declines, and the lifespan of human men is consistent with this idea. However, because women can live long after menopause and this prolonged post-reproductive life can be explained, in part, by the fitness enhancing effects of grandmothering, an alternative hypothesis is that male lifespan is influenced by the potential to gain fitness through grandfathering. Here we investigate whether men, who could not gain fitness through reproduction after their wife's menopause (i.e. married only once), enhanced their fitness through grandfathering in historical Finns. Father presence was associated with reductions in offspring age at first reproduction and birth intervals, but generally not increases in reproductive tenure lengths. Father presence had little influence on offspring lifetime fecundity and no influence on offspring lifetime reproductive success. Overall, in contrast to our results for women in the same population, men do not gain extra fitness (i.e. more grandchildren) through grandfathering. Our results suggest that if evidence for a 'grandfather' hypothesis is lacking in a monogamous society, then its general importance in shaping male lifespan during our more promiscuous evolutionary past is likely to be negligible.     

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.