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.

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.

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.

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.

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.

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.

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.

Grandmothering life histories and human pair bonding.

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.

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.

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.

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.

Evolution of longevity, age at last birth and sexual conflict with grandmothering.

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. (2014) 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. (2014), 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.

The pyrophilic primate hypothesis.

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.

What's burning got to do with it? Primate foraging opportunities in fire-modified landscapes.

OBJECTIVES: 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. METHODS: 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. RESULTS: 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. CONCLUSIONS: 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.

Grandmothering drives the evolution of longevity in a probabilistic model.

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.

Fire and home range expansion: a behavioral response to burning among savanna dwelling vervet monkeys (Chlorocebus aethiops).

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 behavioral 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 unbothered 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 highlight the need for further investigation of these responses as they relate to foraging opportunities, migration, resource use, and especially fire-centric adaptations in our own genus.

Blood cell telomere lengths and shortening rates of chimpanzee and human females.

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.