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Paternal care is unusual among primates; in most species males compete with one another for the acquisition of mates and leave the raising of offspring to the mothers. Callitrichids defy this trend with both fathers and older siblings contributing to the care of offspring. We extend a two-strategy population model (paternal care versus male-male competition) to account for various mechanisms that could possibly explain why male callitrichids invest in paternal care over male-male competition, and compare results from callitrichid, chimpanzee and hunter-gatherer life history parameters. The survival benefit to offspring due to care is an insufficient explanation of callitrichid paternal care, and the additional inclusion of differences in lactation-related biology similarly do not change that picture. Instead, paternal care may arise in parallel with, or even as a result of, mate guarding, which in turn is only beneficial when partners are scarce as modelled by the birth sex ratio in callitrichids and menopause in hunter-gatherers. In that situation, care need not even provide any benefit to the young (in the form of a survival bonus) for guarding to out-compete multiple mating competition.

Synopsis Like many scientific disciplines, the field of reproductive biology is subject to biases in terminology and research foci. For example, females are often described as coy and passive players in reproductive behaviors and are termed “promiscuous” if they engage in extra-pair copulations. Males on the other hand are viewed as actively holding territories and fighting with other males. Males are termed “multiply mating” if they mate with multiple females. Similarly, textbooks often illustrate meiosis as it occurs in males but not females. This edition of Integrative and Comparative Biology (ICB) includes a series of papers that focus on reproduction from the female perspective. These papers represent a subset of the work presented in our symposium and complementary sessions on female reproductive biology. In this round table discussion, we use a question and answer format to leverage the diverse perspectives and voices involved with the symposium in an exploration of theoretical, cultural, pedagogical, and scientific issues related to the study of female biology. We hope this dialog will provide a stepping-stone toward moving reproductive science and teaching to a more inclusive and objective framework.

When Fisher, Williams, and Hamilton laid the foundations of evolutionary life history theory, they recognized elements of what became a grandmother hypothesis to explain the evolution of human postmenopausal longevity. Subsequent study of modern hunter-gatherers, great apes, and the wider mammalian radiation has revealed strong regularities in development and behavior that show additional unexpected consequences that ancestral grandmothering likely had on human evolution, challenging the hypothesis that ancestral males propelled the evolution of our radiation by hunting to provision mates and offspring. Ancestral grandmothering has become a serious contender to explain not only the large fraction of post-fertile years women live and children’s prolonged maturation yet early weaning; it also promises to help account for the pair bonding that distinguishes humans from our closest living evolutionary cousins, the great apes (and most other mammals), the evolution of our big human brains, and our distinctive preoccupation with reputations, shared intentionality and persistent cultural learning that begins in infancy.

The authors propose that many morbidities higher in women than men are adaptations protecting survival, selected because survival has been especially crucial to mothers' reproductive success. Following their lead, I pursue variation in tradeoffs between reproduction and survival recognized by Darwin that were likely central to the evolution of many traits that distinguish us from our great ape cousins.

When we examine the life history of humans against our closest primate relatives, the other great apes, there is notably a greater longevity in humans which includes a distinctive postmenopausal life stage, leading to the question, "How did human females evolve to have old-age infertility?" In their paper "Mate choice and the origin of menopause" (Morton et al., 2013), Morton et al. developed an agent-based model (ABM) to investigate the novel hypothesis that ancestral male mating choices, particularly forgoing mating with older females, were the driving force behind the evolution of menopause. From their model, they concluded that indeed male preference for young female mates could have driven females to lose fertility at older ages through deleterious mutations, leading to menopause. In this work, we revisit their male-mate-choice hypothesis by formulating an analogous mathematical model using a system of ordinary differential equations (ODEs). We first show that our ODE model recreates the qualitative behaviour and hence conclusions of key scenarios in Morton et al. (2013). However, since our ODE system is less computationally demanding than their ABM, we also conduct a broader sensitivity analysis over a range of parameters and differing initial conditions to analyse the dependence on their conclusions to underlying assumptions. Our results challenge those of Morton et al. as we find that even the slightest deviation from an exclusive mating preference for younger females would counteract the evolution of menopause. Consequently, we propose that their male-mate-choice hypothesis is incomplete and needs further explanation of how a male strategy to exclusively mate with young females could have arisen in our common ancestors and remained evolutionarily stable for long enough to drive the evolution of old-age female infertility.

Cyanotoxins are an emerging threat to freshwater resources worldwide. The most frequently reported cyanotoxins are the microcystins, which threaten the health of humans, wildlife, and ecosystems. Determining the potential for microcystin production is hindered by a lack of morphological features that correlate with microcystin production. However, amplicon-based methods permit the detection of microcystin biosynthesis genes and were employed to assess the toxin potential in Lake Utopia, NB, Canada, an oligotrophic lake that occasionally experiences cyanobacteria blooms. Samples collected at 2 week intervals from June 27th to September 27th, 2016, were screened by polymerase chain reaction (PCR) for the microcystin synthetase E gene (mcyE). The mcyE gene was present in some samples every sampling day, despite microcystin not being detected via ELISA, and was most frequently associated with the larger pore size fractions of the serially filtered samples. Further PCR surveys using primer sets to amplify genus-specific (e.g., Microcystis, Anabaena/Dolichospermum, and Planktothrix) mcyE fragments identified Microcystis as the only taxa in Lake Utopia with toxigenic potential. Sequencing of the 16S rRNA V3-V4 region revealed a community dominated by members of the order Synechococcales (from 38 to 96% relative abundance), but with significant presence of taxa from Cyanobacteriales including Microcystaceae and Nostocaceae. A persistent Microcystis population was detected in samples both testing positive and negative for the mcyE gene, highlighting the importance of identifying cyanotoxin production potential by gene presence and not species identity. To our knowledge, this study represents the first application of amplicon-based approaches to studying toxic cyanobacteria in an understudied region-Atlantic Canada.

The question of why males invest more into competition than offspring care is an age-old problem in evolutionary biology. On the one hand, paternal care could increase the fraction of offspring surviving to maturity. On the other hand, competition could increase the likelihood of more paternities and thus the relative number of offspring produced. While drivers of these behaviours are often intertwined with a wide range of other constraints, here we present a simple dynamic model to investigate the benefits of these two alternative fitness-enhancing pathways. Using this framework, we evaluate the sensitivity of equilibrium dynamics to changes in payoffs for male allocation to mating versus parenting. Even with strong effects of care on offspring survivorship, small competitive benefits can outweigh benefits from care. We consider an application of the model that includes men's competition for hunting reputations where big game supplies a benefit to all and find a frequency-dependent parameter region within which, depending on initial population proportions, either strategy may outperform the other. Results demonstrate that allocation to competition gives males greater fitness than offspring care for a range of circumstances that are dependent on life-history parameters and, for the large-game hunting application, frequency dependent. The greater the collective benefit, the more individuals can be selected to supply it.

Postmenopausal longevity distinguishes humans from our closest living evolutionary cousins, the great apes, and may have evolved in our lineage when the economic productivity of grandmothers allowed mothers to wean earlier and overlap dependents. Since increased longevity retards development and expands brain size across the mammals, this hypothesis links our slower developing, bigger brains to ancestral grandmothering. If foraging interdependence favoured postmenopausal longevity because grandmothers' subsidies reduced weaning ages, then ancestral infants lost full maternal engagement while their slower developing brains were notably immature. With survival dependent on social relationships, sensitivity to reputations is wired very early in neural ontogeny, beginning our lifelong preoccupation with shared intentionality. This article is part of the theme issue ‘Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals’.

Humans' extensive use of fire is one behavior that sets us apart from all other animals. However, our ancestors' reliance on controlled forms of fire-i.e., for cooking-was likely preceded by a long familiarity with fire beginning with passive exploitation of naturally burned landscapes and followed by intermediate steps including active ecological modification via intentional burning. Here we explore our pyrophilic beginnings using observational data from savanna-dwelling chimpanzees. These data highlight the extent to which anthropogenic burning impacts the behavior and ecology of sympatric primates and provides an opportunity to study the ways in which apes living in a fire-altered world exploit opportunities presented by burning. Using monthly burn scar data and daily range use data we quantify the impact of burning episodes on chimpanzee habitat. Over the course of one dry season, approximately 74% of the total estimated range of the Fongoli community of savanna-dwelling chimpanzees (Pan troglodytes verus) was impacted by fire. We combine fire occurrences with behavioral data to test for relationships between burning and rate of encounter with food items and duration of subsequent patch residence time. Results show more frequent encounters and shorter patch residence times in burned areas. These data can be leveraged as a frame of reference for conceptualizing our extinct relatives' behavior around fire.

Among mammals, including humans, adult brain size and the relative size of brain components depend precisely on the duration of a highly regular process of neural development. Much wider variation is seen in rates of body growth and the state of neural maturation at life history events like birth and weaning. Large brains result from slow maturation, which in humans is accompanied by weaning early with respect to both neural maturation and longevity. The grandmother hypothesis proposes this distinctive combination of life history features evolved as ancestral populations began to depend on foods that just weaned juveniles couldn't handle. Here we trace possible reciprocal connections between brain development and life history, highlighting the resulting extended neural plasticity in a wider cognitive ecology of allomaternal care that distinguishes human ontogeny with consequences for other peculiarities of our lineage.

Influential models of male reproductive strategies have often ignored the importance of mate guarding, focusing instead on trade-offs between fitness gained through care for dependants in a pair bond versus fitness from continued competition for additional mates. Here we follow suggestions that mate guarding is a distinct alternative strategy that plays a crucial role, with special relevance to the evolution of our own lineage. Human pair bonding may have evolved in concert with the evolution of our grandmothering life history, which entails a shift to male-biased sex ratios in the fertile ages. As that sex ratio becomes more male biased, payoffs for mate-guarding increase due to partner scarcity. We present an ordinary differential equation model of mutually exclusive strategies (dependant care, multiple mating, and mate guarding), calculate steady-state frequencies and perform bifurcation analysis on parameters of care and guarding efficiency. Mate guarding triumphs over alternate strategies when populations are male biased, and guarding is fully efficient. When guarding does not ensure complete certainty of paternity, and multiple maters are able to gain some paternity from guarders, multiple mating can coexist with guarding. At female-biased sex ratios, multiple mating takes over, unless the benefit of care to the number of surviving offspring produced by the mates of carers is large.

Exploration and analyses of early archaeological sites and their faunal assemblages have grown increasingly sophisticated since the sites were first proposed to be home bases where ancestral hunters brought meat to share with their mates and offspring. Debates about that proposition motivated quantitative attention to hunting, scavenging, butchery and transport of big game among modern Hadza and the faunal assemblage characteristics and archaeological sites they create. Findings prompted a hypothesis about competitive scavenging that might explain the character and ecological context of the early sites, a hypothesis since strengthened by consensus among archaeologists working at Olduvai that the sites are not home bases. Hadza carcass procurement rates calibrate estimates for ancestral populations without similar technology, underscoring the likelihood that other food resources were especially important in human evolution.

The spatial behavior of primates is shaped by many factors including predation risk, the distribution of food sources, and access to water. In fire-prone settings, burning is a catalyst of change, altering the distribution of both plants and animals. Recent research has shown that primates alter their behavior in response to this change. Here, we study primates' perceived threat of predation in fire-modified landscapes. We focus on the predator-related behaviors of vervet monkeys (Chlorocebus pygerythrus) after controlled burning events. We compare the occurrence of vigilance and predator-deterrent behaviors, including alarm calls, scanning, and flight across different habitats and burn conditions to test the hypothesis that subjects exhibit fewer predator-specific vigilance and predator-deterrent behaviors in burned areas. The results demonstrate that predator-related behaviors occur less often in burned habitats, suggesting that predators are less common in these areas. These results provide foundations for examining hypotheses about the use of fire-altered landscapes among extinct hominins. We set these data in the context of increasing aridity, changes in burning regimes, and the emergence of pyrophilia in the human lineage.

We present a mathematical simplification for the evolutionary dynamics of a heritable trait within a two-sex population. This trait is assumed to control the timing of sex-specific life-history events, such as the age of sexual maturity and end of female fertility, and each sex has a distinct fitness tradeoff associated with the trait. We provide a formula for the fitness landscape of the population and show a natural extension of the result to an arbitrary number of heritable traits. Our method can be viewed as a dynamical systems generalisation of the Price Equation to include two sexes{, age structure} and multiple traits. We use this formula to examine the effect of grandmothering, whereby post-fertile females subsidize their daughter's fertility by provisioning grandchildren. Grandmothering can drive a shift towards higher sex ratios due to lengthening female post-fertile longevity, leading to changes in fitness for both sexes. For males, increased longevity is accompanied by a substantially longer fertile lifespan resulting in higher sex ratios in the fertile ages. Our fitness landscapes show a net increase in fitness for both males and females at longer lifespans, and as a result, we find that grandmothering alone provides an evolutionary trajectory to higher longevities., Comment: 12 pages, 3 figures

Great apes, the other living members of our hominid family, become decrepit before the age of forty and rarely outlive their fertile years. In contrast, women - even in high mortality hunter-gatherer populations - usually remain healthy and productive well beyond menopause. The grandmother hypothesis aims to account for the evolution of this distinctive feature of human life history. Our previous mathematical simulations of that hypothesis fixed the end of female fertility at the age of 45, based on the similarities among living hominids, and then modeled the evolution of human-like longevity from an ancestral state, like that of the great apes, due only to grandmother effects. A major modification here allows the age female fertility ends to vary as well, directly addressing a version of the question, influentially posed by GC Williams six decades ago: Why isn't menopause later in humans? Our model is an agent-based model (ABM) that accounts for the coevolution of both expected adult lifespan and end of female fertility as selection maximizes reproductive value. We find that grandmother effects not only drive the population from an equilibrium representing a great ape-like longevity to a new human-like longevity, they also maintain the observed termination of women's fertility before the age of 50., Comment: 32 pages, 5 figures

We use a two-sex partial differential equation (PDE) model based on the Grandmother Hypothesis. We build on an earlier model by Kim et al. [27] by allowing for evolution in both longevity and age at last birth, and also assuming that post-fertile females support only their daughters' fertility. Similarly to Kim et al. [27], we find that only two locally stable equilibria exist: one corresponding to great ape-like longevities and the other corresponding to hunter-gatherer longevities. Our results show that grandmothering enables the transition between these two equilibria, without extending the end of fertility. Moreover, sensitivity analyses of the model show that male competition, arising from a skew in the mating sex ratio towards males, plays a significant role in determining whether the transition from great ape-like longevities to higher longevities is possible and the equilibrium value of the average adult lifespan. Whereas grandmothering effects have a significant impact on the equilibrium value of the average age at last birth and enable the transition to higher longevities, they have an insignificant impact on the equilibrium value of the average adult lifespan., Comment: 22 pages, 20 figures

The century long publication of this journal overlapped major changes in the sciences it covers. We have been eyewitnesses to vast changes during the final third of the last century and beginning of this one, momentous enough to fundamentally alter our work separately and collectively. One (NBJ) from animal ethology, another from western North American archaeology (JOC), and a third (KH) from cultural anthropology came to longtime collaboration as evolutionary ecologists with shared focus on studying modern hunter-gatherers to guide hypotheses about human evolution. Our findings have radically revised hypotheses each of us took for granted when we began. Our (provisional) conclusions are not the consensus among hunter-gatherer specialists; but grateful that personal reflections are invited, we aim to explain how and why we continue to bet on them.

We differ from the great apes in so many ways. Yet they all belong to our hominid family, and some are even more closely related to us than they are to each other. One distinctive human feature is our much great longevity, a difference that the Grandmother Hypothesis might explain. Grandmothering not only helps account for our long life spans but also changes childrearing in ways that may explain why distinctly human capacities for social engagement and mutual understanding evolved in our lineage. We review the background to this Grandmother Hypothesis and summarize it and related findings from evolutionary modeling and empirical measurements of both grandmother effects and social capacities of human infants. Then, we point to questions arising for social development, discriminating grandmothers, future mathematical modeling, and social strategies of men, as well as the physiology of human aging. Keywords: human longevity; senescence; menopause; aging; cooperative child rearing; human evolution; life history evolution; shared intentionality

The adult sex ratio (ASR) is defined as the number of fertile males divided by the number of fertile females in a population. We build an ODE model with minimal age structure, in which males compete for paternities using either a multiple-mating or searching-then-guarding strategy, to investigate the value of ASR as an index for predicting which strategy males will adopt, with a focus in our investigation on the differences of strategy choice between chimpanzees Pan troglodytes and human hunter-gatherers Homo sapiens. Parameters in the model characterise aspects of life history and behaviour, and determine both dominant strategy and the ASR when the population is at or near equilibrium. Sensitivity analysis on the model parameters informs us that ASR is strongly influenced by parameters characterising life history, while dominant strategy is affected most strongly by the effectiveness of guarding (average length of time a guarded pair persists, and resistance to paternity theft) and moderately by some life history traits. For fixed effectiveness of guarding and other parameters, dominant strategy tends to change from multiple mating to guarding along a curve that aligns well with a contour of constant ASR, under variation of parameters such as longevity and age female fertility ends. This confirms the hypothesis that ASR may be a useful index for predicting the optimal male mating strategy, provided we have some limited information about ecology and behaviour., Comment: 22 pages, 9 figures

Bowlby recognized that studying other primates could help identify the needs of human infants; his evolutionary perspective has had a wide impact on understanding of human development. Much more is now known about evolutionary processes and variation, within and between species. This chapter reviews aspects of evolutionary theory and primatology relevant to Bowlby’s theory of attachment. Beginning with primate phylogeny, ecological and social forces that contribute to the varieties of primate sociality are considered and some reasons canvassed that explain why primatologists do not all agree on the choice of words to describe the relationships between animals, including use of the term “attachment.” Variations and commonalities are identified and used to explore how development in human infants can be understood in terms of social relationships and maturational state at birth and weaning compared to other primates. Infant experience has long-term effects in primates other than humans. Some of that evidence is summarized and special attention is given to interactions between particular chimpanzee mothers and infants in an unusual setting, where trusting relationships between mothers and human researchers reveal variations in mothering style that appear to result from early life events, recent experience, and social context.

This chapter begins with a brief discussion of the contrast between the phenomenon labeled "reciprocity" by ethnologists and "reciprocal altruism" by behavioral ecologists. It focuses especially on food sharing among ethnographically known hunter—gatherers and subsistence cultivators to illustrate some of the patterns, the explanatory problems they present, and some of the competing hypotheses that evolutionary ecologists pose to account for them. Three models used to explore problems of sharing and collective action are introduced. The models illustrate three kinds of explanation—delayed reciprocity, mutualism, and manipulation. The chapter reviews the effects of time lags, ancillary benefits, and resource "lumpiness" on collective action. Some applications to "the sexual division of labor" are briefly discussed. Finally, ethnographic examples in which variations in patterns of food sharing have been described are summarized and examined in light of issues. Evolutionary ecologists have thus found game theory to be a particularly useful analytical tool.

This chapter presents comparative data from hunting and gathering societies that argues against provisioning by males as a cause of pair bonding. Provisioning as paternal investment should vary with vulnerability of offspring and effectiveness of male care, and with male estimates of paternity. For instance, if male provisioning was important, and men stayed in a marriage because of the cost to their children from desertion, women with more small children should be less likely to get divorced. Pair bonding as a solution to male contests draws attention to the social nature of marriage more forcefully than paternal provisioning has done. Ideas about the evolution of human pair bonding have centered around the role of men as provisioners of wife and children. The many findings in the literature that cast doubt on the equally long assumed importance of paternal care in avian pair bonding.

This chapter summarizes the grandmother hypothesis and the life history patterns it may explain, note that it joins other challenges to the hunting hypothesis. It discusses alternative predictions about human evolution based on the idea that mother-child food sharing and the grandmothering it permits are among their most important behavioral characteristics. The grandmother hypothesis suggests a different model of human evolution than the conventional one that makes men's big game hunting and provisioning of mates and offspring the keystone human adaptation. The grandmother hypothesis implies that childbearing women produces babies faster than otherwise expected because of grandmothers' contribution to that production. The grandmother hypothesis should stimulate increased attention to the activities of older women and explicit examination of the spatial proximity of mothers and daughters. The grandmother hypothesis provides a rationale for the modeling needed to identify critical tests.

Men's provisioning of mates and offspring has been central to ideas about human evolution because paternal provisioning is absent in our closest evolutionary cousins, the great apes, and is widely assumed to result in pair bonding, which distinguishes us from them. Yet mathematical modelling has shown that paternal care does not readily spread in populations where competition for multiple mates is the common male strategy. Here we add to models that point to the mating sex ratio as an explanation for pairing as pay-offs to mate guarding rise with a male-biased sex ratio. This is of interest for human evolution because our grandmothering life history shifts the mating sex ratio from female- to male-biased. Using a difference equation model, we explore the relative pay-offs for three competing male strategies (dependant care, multiple mating, mate guarding) in response to changing adult sex ratios. When fertile females are abundant, multiple mating prevails. As they become scarce, mate guarding triumphs. The threshold for this shift depends on guarding efficiency. Combined with mating sex ratios of hunter–gatherer and chimpanzee populations, these results strengthen the hypothesis that the evolution of our grandmothering life history propelled the shift to pair bonding in the human lineage. This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.

Unlike other primate males, men invest substantial effort in producing food that is consumed by others. The Hunting Hypothesis proposes this pattern evolved in early Homo when ancestral mothers began relying on their mates' hunting to provision dependent offspring. Evidence for this idea comes from hunter-gatherer ethnography, but data we collected in the 1980s among East African Hadza do not support it. There, men targeted big game to the near exclusion of other prey even though they were rarely successful and most of the meat went to others, at significant opportunity cost to their own families. Based on Hadza data collected more recently, Wood and Marlowe contest our position, affirming the standard view of men's foraging as family provisioning. Here we compare the two studies, identify similarities, and show that emphasis on big game results in collective benefits that would not be supplied if men foraged mainly to provision their own households. Male status competition remains a likely explanation for Hadza focus on big game, with implications for hypotheses about the deeper past.

We present a mathematical model based on the Grandmother Hypothesis to simulate how human post-menopausal longevity could have evolved as ancestral grandmothers began to assist the reproductive success of younger females by provisioning grandchildren. Grandmothers׳ help would allow mothers to give birth to subsequent offspring sooner without risking the survival of existing offspring. Our model is an agent-based model (ABM), in which the population evolves according to probabilistic rules governing interactions among individuals. The model is formulated according to the Gillespie algorithm of determining the times to next events. Grandmother effects drive the population from an equilibrium representing a great-ape-like average adult lifespan in the lower twenties to a new equilibrium with a human-like average adult lifespan in the lower forties. The stochasticity of the ABM allows the possible coexistence of two locally-stable equilibria, corresponding to great-ape-like and human-like lifespans. Populations with grandmothering that escape the ancestral condition then shift to human-like lifespan, but the transition takes longer than previous models (Kim et al., 2012). Our simulations are consistent with the possibility that distinctive longevity is a feature of genus Homo that long antedated the appearance of our species.

The behavioral adaptations of primates to fire-modified landscapes are of considerable interest to anthropologists because fire is fundamental to life in the African savanna—the setting in which genus Homo evolved. Here we report the behavioral responses of a savanna-dwelling primate, vervet monkeys (Chlorocebus aethiops), to fire-induced ecological change. Using behav- ioral and spatial data to characterize ranging patterns prior to and postburn and between burn and nonburn years, we show that these primates inhabiting small, spatially bound, riverine habitats take advantage of newly burned savanna landscapes. When subjects encountered controlled fires, they did not flee but instead avoided the path of the fire seemingly unboth- ered by its approach. After fire, the primates' home range expanded into newly burned but previously unused areas. These results contribute to understanding the response of non-human primates to fire-modified landscapes and can shed light on the nature and scope of opportunities and constraints posed by the emergence of fire-affected landscapes in the past. Results also expose deficiencies in our knowledge of fire-related behavioral responses in the primate lineage and high- light the need for further investigation of these responses as they relate to foraging opportunities, migration, resource use, and especially fire-centric adap- tations in our own genus. Am J Phys Anthropol

Objectives Slower rates of aging distinguish humans from our nearest living cousins. Chimpanzees rarely survive their forties while large fractions of women are postmenopausal even in high-mortality hunter–gatherer populations. Cellular and molecular mechanisms for these somatic aging differences remain to be identified, though telomeres might play a role. To find out, we compared telomere lengths across age-matched samples of female chimpanzees and women. Methods We used a monochrome multiplex quantitative polymerase chain reaction to assay canonical telomere repeats in blood cells from captive female chimpanzees (65 individuals; age: 6.2–56.7 years) and compared them to the same measure in human females (43 individuals; age: 7.4–57.3 years). Results Our samples showed little difference in attrition rates between the species (∼0.022 T/S per year for chimpanzees and ∼0.012 T/S per year for humans with overlapping 95% confidence intervals), but telomeres were twice as long in chimpanzees as in humans (T/S ratios = 2.70 and 1.26, respectively). Conclusions Based on the longevity differences, we initially hypothesized that telomere shortening rates would be faster in chimpanzees than in humans. Instead, it is shorter telomere length that appears to be the derived state in humans. This comparison indicates that better characterization of physiological aging in our closest living relatives will be indispensable for understanding the evolution of distinctive human longevity. Am. J. Hum. Biol. 26:452–460, 2014. © 2014 Wiley Periodicals, Inc.

Women and female great apes both continue giving birth into their forties, but not beyond. However humans live much longer than other apes do.[1] Even in hunting and gathering societies, where the mortality rate is high, adult life spans average twice those of chimpanzees, which become decrepit during their fertile years and rarely survive them.[2, 3] Since women usually remain healthy through and beyond childbearing age, human communities include substantial proportions of economically productive postmenopausal women.[4-7] A grandmother hypothesis8–12 may explain why greater longevity evolved in our lineage while female fertility still ends at ancestral ages. This hypothesis has implications for the evolution of a wide array of human features. Here we review some history of the hypothesis, recent findings, and questions for ongoing research.

Ovarian cycling continues to similar ages in women and chimpanzees yet our nearest living cousins become decrepit during their fertile years and rarely outlive them. Given the importance of estrogen in maintaining physiological systems aside from fertility, similar ovarian aging in humans and chimpanzees combined with somatic aging differences indicates an important role for nonovarian estrogen. Consistent with this framework, researchers have nominated the adrenal androgen dehydroepiandrosterone (DHEA) and its sulfate (DHEAS), which can be peripherally converted to estrogen, as a biomarker of aging in humans and other primates. Faster decline in production of this steroid with age in chimpanzees could help explain somatic aging differences. Here, we report circulating levels of DHEAS in captive female chimpanzees and compare them with published levels in women. Instead of faster, the decline is slower in chimpanzees, but from a much lower peak. Levels reported for other great apes are lower still. These results point away from slowed decline but toward increased DHEAS production as one of the mechanisms underlying the evolution of human longevity.

The killing of Cecil the lion ( Panthera leo ) ignited enduring and increasingly global discussion about trophy hunting [[1][1]]. Yet, policy debate about its benefits and costs (e.g. [[2][2],[3][3]]) focuses only on the hunted species and biodiversity, not the unique behaviour of hunters. Some

Telomeres are repeating DNA at chromosome ends. Telomere length (TL) declines with age in most human tissues, and shorter TL is thought to accelerate senescence. In contrast, older men have sperm with longer TL; correspondingly, older paternal age at conception (PAC) predicts longer TL in offspring. This PAC-effect could be a unique form of transgenerational genetic plasticity that modifies somatic maintenance in response to cues of recent ancestral experience. The PAC-effect has not been examined in any non-human mammals. Objectives Here, we examine the PAC-effect in chimpanzees (Pan troglodytes). The PAC-effect on TL is thought to be driven by continual production of sperm—the same process that drives increased de novo mutations with PAC. As chimpanzees have both greater sperm production and greater sperm mutation rates with PAC than humans, we predict that the PAC-effect on TL will be more pronounced in chimpanzees. Additionally we examine whether PAC predicts TL of grandchildren. Materials and methods TL were measured using qPCR from DNA from blood samples from 40 captive chimpanzees and 144 humans. Results Analyses showed increasing TL with PAC in chimpanzees (p = .009) with a slope six times that in humans (p = .026). No associations between TL and grandpaternal ages were found in humans or chimpanzees—although statistical power was low. Discussion These results suggest that sperm production rates across species may be a determinant of the PAC-effect on offspring TL. This raises the possibility that sperm production rates within species may influence the TL passed on to offspring.

Members of genus Homo are the only animals known to create and control fire. The adaptive significance of this unique behavior is broadly recognized, but the steps by which our ancestors evolved pyrotechnic abilities remain unknown. Many hypotheses attempting to answer this question attribute hominin fire to serendipitous, even accidental, discovery. Using recent paleoenvironmental reconstructions, we present an alternative scenario in which, 2 to 3 million years ago in tropical Africa, human fire dependence was the result of adapting to progressively fire-prone environments. The extreme and rapid fluctuations between closed canopy forests, woodland, and grasslands that occurred in tropical Africa during that time, in conjunction with reductions in atmospheric carbon dioxide levels, changed the fire regime of the region, increasing the occurrence of natural fires. We use models from optimal foraging theory to hypothesize benefits that this fire-altered landscape provided to ancestral hominins and link these benefits to steps that transformed our ancestors into a genus of active pyrophiles whose dependence on fire for survival contributed to its rapid expansion out of Africa.

Postmenopausal longevity may have evolved in our lineage when ancestral grandmothers subsidized their daughters' fertility by provisioning grandchildren, but the verbal hypothesis has lacked mathematical support until now. Here, we present a formal simulation in which life spans similar to those of modern chimpanzees lengthen into the modern human range as a consequence of grandmother effects. Greater longevity raises the chance of living through the fertile years but is opposed by costs that differ for the sexes. Our grandmother assumptions are restrictive. Only females who are no longer fertile themselves are eligible, and female fertility extends to age 45 years. Initially, there are very few eligible grandmothers and effects are small. Grandmothers can support only one dependent at a time and do not care selectively for their daughters' offspring. They must take the oldest juveniles still relying on mothers; and infants under the age of 2 years are never eligible for subsidy. Our model includes no assumptions about brains, learning or pair bonds. Grandmother effects alone are sufficient to propel the doubling of life spans in less than sixty thousand years.

Many analyses of human populations have found that age-specific mortality rates increase faster across most of adulthood when overall mortality levels decline. This contradicts the relationship often expected from Williams' classic hypothesis about the effects of natural selection on the evolution of senescence. More likely, much of the within-species difference in actuarial aging is not due to variation in senescence, but to the strength of filters on the heterogeneity of frailty in older survivors. A challenge to this differential frailty hypothesis was recently posed by an analysis of life tables from historical European populations and traditional societies that reported variation in actuarial aging consistent with Williams' hypothesis after all. To investigate the challenge, we reconsidered those cases and aging measures. Here we show that the discrepancy depends on Ricklefs' aging rate measure, ω, which decreases as mortality levels drop because it is an index of mortality level itself, not the rate of increase in mortality with age. We also show unappreciated correspondence among the parameters of Gompertz-Makeham and Weibull survival models. Finally, we compare the relationships among mortality parameters of the traditional societies and the historical series, providing further suggestive evidence that differential heterogeneity has strong effects on actuarial aging.

Two kinds of evidence suggest that female fertility may end at an earlier age in modern people than in ancestral populations or in our closest living relatives, chimpanzees. We investigate both to see whether fertility schedules or ovarian follicle counts falsify the alternative hypothesis that the age of terminal fertility changed little in the human lineage while greater longevity evolved due to grandmother effects. We use 19th century Utah women to represent non-contracepting humans, and compare their fertility by age with published records for wild chimpanzees. Then we revisit published counts of ovarian follicular stocks in both species. Results show wide individual variation in age at last birth and oocyte stocks in both humans and chimpanzees. This heterogeneity, combined with interspecific differences in adult mortality, has large and opposing effects on fertility schedules. Neither realized fertility nor rates of follicular atresia stand as evidence against the hypothesis that ages at last birth changed little while greater longevity evolved in our lineage.

Gurven and Hill (2009) ask, “Why do men hunt?” As they say, “The observation that men hunt and women gather supported the simplistic view of marriage as a cooperative enterprise. Greater sophistication suggests that males may often be motivated by mating and status rather than offspring investment” (p. 60). We agree (e.g., Hawkes 1990, 1991; Hawkes et al. 1991, 2001a, 2001b). This is the revision we first proposed nearly 20 years ago (Hawkes 1990) and have elaborated several times since. Having endorsed our point, Gurven and Hill then reject it, expressing continuing confidence in the idea that “men’s food production efforts are mainly motivated by a concern for familial welfare” (p. 68). Their rejection of our argument and related reaffirmation of conventional wisdom stem from a misunderstanding of data from the Paraguayan Ache and Tanzanian Hadza and a failure to appreciate the importance of other sources of information. We elaborate this critique on four key points.

A long postreproductive lifespan may distinguish women from all other female primates. A long-held consensus among reproductive scientists has been that our closest living relative, the chimpanzee (Pan troglodytes), experiences menstrual cycles until death. However, a recent study of biannual assessments of gonadotropins, but lacking observations of menstruation, concluded that menopause occurs in chimpanzees between 35 and 40 yr of age. A separate report, but on wild chimpanzees, documented fertility through the 40-44 age range in all populations studied. These contradictory reports pose questions about differences between wild and captive populations and about assessments of menopause. The present study revisits this controversy by analyzing longitudinal records of anogenital swelling and menstruation in 89 female chimpanzees aged 6 to 59 yr (n = 2386 records on cycle length), monitored for most of their adult lives at the Yerkes National Primate Research Center. Twenty of these chimpanzees were observed past 39 yr of age; all 20 displayed menstrual cycles beyond this age, as confirmed by at least two observations of menses about 35 days apart. Three of these were older than 50 yr and still displayed menstrual cycles. Only the oldest female appeared menopausal, with cycles of anogenital swelling ceasing 2 yr prior to her death at age 59. Random-effects statistical modeling reveals a slight decrease in cycle length until 20 yr of age and a slight lengthening thereafter. Mean cycle length across the lifespan is 35.4 days. Our findings, based upon actual observations of menstrual cycles, suggest that menopause in the chimpanzee is rare, occurring near the end of the lifespan.

We retrieved ovarian sections taken from necropsies of 19 captive chimpanzees (Pan troglodytes) aged 0–47 yr, counted the number of primordial follicles in each, and compared the rate of decline in numbers to declines previously documented in humans. The follicular depletion rate in this sample was indistinguishable from that shown across the same ages in classic human data sets. This result supports earlier suggestions that ovarian senescence occurs at the same ages in chimpanzees and humans, implying that the influence of declining ovarian function on other physiologic systems may be distinctively buffered in humans. aging, chimpanzee, follicle, ovary

The evolution of distinctively human life history and social organization is generally attributed to paternal provisioning based on pair bonds. Here we develop an alternative argument that connects the evolution of human pair bonds to the male-biased mating sex ratios that accompanied the evolution of human life history. We simulate an agent-based model of the grandmother hypothesis, compare simulated sex ratios to data on great apes and human hunter–gatherers, and note associations between a preponderance of males and mate guarding across taxa. Then we explore a recent model that highlights the importance of mating sex ratios for differences between birds and mammals and conclude that lessons for human evolution cannot ignore mammalian reproductive constraints. In contradiction to our claim that male-biased sex ratios are characteristically human, female-biased ratios are reported in some populations. We consider the likelihood that fertile men are undercounted and conclude that the mate-guarding hypothesis for human pair bonds gains strength from explicit links with our grandmothering life history.

Anecdotal and formal evidence indicate that primates take advantage of burned landscapes. However, little work has been done to quantify the costs and benefits of this behavior. Using systematic behavioral observations from a population of South African vervet monkeys (Chlorocebus aethiops pygerythrus), we evaluate differences in food availability and energetics before and after controlled burns altered vegetation near their home range. We aim to determine whether burned habitats offer improved foraging opportunities.We collected feeding data from foraging individuals and analyzed common plant foods for their energetic content. We then used the feeding and energetic data to calculate postencounter profitabilities and encounter rates for food types. Using negative binomial and mixed linear regression models we compared data from burned and unburned habitats.Our results show significantly improved encounter rates in burned landscapes for two prey items, invertebrates and grasses. However, postencounter profitabilities in burned areas were not significantly different than those achieved in unburned areas.Results suggest that improved encounters alone can motivate changes in foraging behavior. These foraging benefits enable the exploitation of burned savanna habitats, likely driving postburn range expansions observed among populations of vervet monkeys. Thus quantified, these results may serve as a foundation for hypotheses regarding the evolution of fire-use in our own lineage.