Life history impacts on infancy and the evolution of human social cognition.

Greater longevity, slower maturation and shorter birth intervals are life history features that distinguish humans from the other living members of our hominid family, the great apes. Theory and evidence synthesized here suggest the evolution of those features can explain both our bigger brains and our cooperative sociality. I rely on Sarah Hrdy's hypothesis that survival challenges for ancestral infants propelled the evolution of distinctly human socioemotional appetites and Barbara Finlay and colleagues' findings that mammalian brain size is determined by developmental duration. Similar responsiveness to varying developmental contexts in chimpanzee and human one-year-olds suggests similar infant responsiveness in our nearest common ancestor. Those ancestral infants likely began to acquire solid food while still nursing and fed themselves at weaning as chimpanzees and other great apes do now. When human ancestors colonized habitats lacking foods that infants could handle, dependents' survival became contingent on subsidies. Competition to engage subsidizers selected for capacities and tendencies to enlist and maintain social connections during the early wiring of expanding infant brains with lifelong consequences that Hrdy labeled "emotionally modern" social cognition.

Somatic maintenance/reproduction tradeoffs and human evolution.

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.

Male mating choices: The drive behind menopause?

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.

Investigating foundations for hominin fire exploitation: Savanna-dwelling chimpanzees (Pan troglodytes verus) in fire-altered landscapes.

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.

Mate guarding in primates arises due to partner scarcity, even if the father provides no paternal care at all.

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.

Seasonality and distribution of cyanobacteria and microcystin toxin genes in an oligotrophic lake of Atlantic Canada.

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.

Why Males Compete Rather Than Care, with an Application to Supplying Collective Goods.

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.

Fire's impact on threat detection and risk perception among vervet monkeys: Implications for hominin 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.

It Takes Two to Tango: Including a Female Perspective in Reproductive Biology.

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.

Cognitive consequences of our grandmothering life history: cultural learning begins in infancy.

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'.

The Centrality of Ancestral Grandmothering in Human Evolution.

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.

Adult sex ratio as an index for male strategy in primates.

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.

Why does women's fertility end in mid-life? Grandmothering and age at last birth.

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.

Mammalian brain development and our grandmothering life history.

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.

Hunter-gatherer studies and human evolution: A very selective review.

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.

Evolution of male strategies with sex-ratio-dependent pay-offs: connecting pair bonds with grandmothering.

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'.

Modelling the Evolution of Traits in a Two-Sex Population, with an Application to Grandmothering.

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 trade-off 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 subsidise their daughter's fertility by provisioning grandchildren. Grandmothering can drive a shift towards increasingly male-biased mating sex ratios due to a post-fertile life stage in females, while male fertility continues to older 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.

Further Mathematical Modelling of Mating Sex Ratios & Male Strategies with Special Relevance to Human Life History.

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.

Paternal and grandpaternal ages at conception and descendant telomere lengths in chimpanzees and humans.

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.