The Strategic Revolution.

On the 40(th) anniversary of the publication of Richard Dawkins's The Selfish Gene, we explore the origins of cynical, strategic thinking in evolutionary biology, investigate how this illuminated the sexual and social lives of animals, and assess Dawkins's suggestion that evolution is best understood by taking the gene's-eye view.

Author Correction: Inference of ecological and social drivers of human brain-size evolution.

In the Acknowledgements section of this Letter, the words "M.G.-F. was funded by a Marie Sklodowska-Curie Individual Fellowship (No 701464)" should have read "This project has received funding from the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 701464". This error has been corrected online.

A geometric approach to the evolution of altruism.

Fisher's geometric model provides a powerful tool for making predictions about key properties of Darwinian adaptation. Here, I apply the geometric model to predict differences between the evolution of altruistic versus nonsocial phenotypes. I recover Kimura's prediction that probability of fixation is greater for mutations of intermediate size, but I find that the effect size that maximises probability of fixation is relatively small in the context of altruism and relatively large in the context of nonsocial phenotypes, and that the overall probability of fixation is lower for altruism and is higher for nonsocial phenotypes. Accordingly, the first selective substitution is expected to be smaller, and to take longer, in the context of the evolution of altruism. These results strengthen the justification for employing streamlined social evolutionary methodologies that assume adaptations are underpinned by many genes of small effect.

Publisher Correction: Inference of ecological and social drivers of human brain-size evolution.

In the PDF version of this Letter, Andy Gardner was originally listed as a corresponding author, instead of Mauricio González-Forero. This has been corrected online.

Inference of ecological and social drivers of human brain-size evolution.

The human brain is unusually large. It has tripled in size from Australopithecines to modern humans 1 and has become almost six times larger than expected for a placental mammal of human size 2 . Brains incur high metabolic costs 3 and accordingly a long-standing question is why the large human brain has evolved 4 . The leading hypotheses propose benefits of improved cognition for overcoming ecological5-7, social8-10 or cultural11-14 challenges. However, these hypotheses are typically assessed using correlative analyses, and establishing causes for brain-size evolution remains difficult15,16. Here we introduce a metabolic approach that enables causal assessment of social hypotheses for brain-size evolution. Our approach yields quantitative predictions for brain and body size from formalized social hypotheses given empirical estimates of the metabolic costs of the brain. Our model predicts the evolution of adult Homo sapiens-sized brains and bodies when individuals face a combination of 60% ecological, 30% cooperative and 10% between-group competitive challenges, and suggests that between-individual competition has been unimportant for driving human brain-size evolution. Moreover, our model indicates that brain expansion in Homo was driven by ecological rather than social challenges, and was perhaps strongly promoted by culture. Our metabolic approach thus enables causal assessments that refine, refute and unify hypotheses of brain-size evolution.

The geometry of evolutionary conflict.

Conflicts of interest abound not only in human affairs but also in the biological realm. Evolutionary conflict occurs over multiple scales of biological organization, from genetic outlawry within genomes, to sibling rivalry within nuclear families, to collective-action disputes within societies. However, achieving a general understanding of the dynamics and consequences of evolutionary conflict remains an outstanding challenge. Here, we show that a development of R. A. Fisher's classic 'geometric model' of adaptation yields novel and surprising insights into the dynamics of evolutionary conflict and resulting maladaptation, including the discoveries that: (i) conflict can drive evolving traits arbitrarily far away from all parties' optima and, indeed, if all mutations are equally likely then contested traits are more often than not driven outwith the zone of actual conflict (hyper-maladaptation); (ii) evolutionary conflicts drive persistent maladaptation of orthogonal, non-contested traits (para-maladaptation); and (iii) modular design greatly ameliorates conflict-driven maladaptation, thereby facilitating major transitions in individuality.

Kin selection of time travel: the social evolutionary causes and consequences of dormancy.

A basic mechanism of kin selection is limited dispersal, whereby individuals remain close to their place of origin such that even indiscriminate social interaction tends to modify the fitness of genealogical kin. Accordingly, the causes and consequences of dispersal have received an enormous amount of attention in the social evolution literature. This work has focused on dispersal of individuals in space, yet similar logic should apply to dispersal of individuals in time (e.g. dormancy). We investigate how kin selection drives the evolution of dormancy and how dormancy modulates the evolution of altruism. We recover dormancy analogues of key results that have previously been given for dispersal, showing that: (1) kin selection favours dormancy as a means of relaxing competition between relatives; (2) when individuals may adjust their dormancy behaviour to local density, they are favoured to do so, resulting in greater dormancy in high-density neighbourhoods and a concomitant 'constant non-dormant principle'; (3) when dormancy is constrained to be independent of density, there is no relationship between the rate of dormancy and the evolutionary potential for altruism; and (4) when dormancy is able to evolve in a density-dependent manner, a greater potential for altruism is expected in populations with lower dormancy.

Transmission of social status drives cooperation and offspring philopatry.

The evolution of cooperation depends on two crucial overarching factors: relatedness, which describes the extent to which the recipient shares genes in common with the actor; and quality, which describes the recipient's basic capacity to transmit genes into the future. While most research has focused on relatedness, there is a growing interest in understanding how quality modulates the evolution of cooperation. However, the impact of inheritance of quality on the evolution of cooperation remains largely unexplored, especially in spatially structured populations. Here, we develop a mathematical model to understand how inheritance of quality, in the form of social status, influences the evolution of helping and harming within social groups in a viscous-population setting. We find that: (1) status-reversal transmission, whereby parental and offspring status are negatively correlated, strongly inhibits the evolution of cooperation, with low-status individuals investing less in cooperation and high-status individuals being more prone to harm; (2) transmission of high status promotes offspring philopatry, with more cooperation being directed towards the higher-dispersal social class; and (3) fertility inequality and inter-generational status inheritance reduce within-group conflict. Overall, our study highlights the importance of considering different mechanisms of phenotypic inheritance, including social support, and their potential interactions in shaping animal societies.

Sexual antagonism in sequential hermaphrodites.

Females and males may have distinct phenotypic optima, but share essentially the same complement of genes, potentially leading to trade-offs between attaining high fitness through female versus male reproductive success. Such sexual antagonism may be particularly acute in hermaphrodites, where both reproductive strategies are housed within a single individual. While previous models have focused on simultaneous hermaphroditism, we lack theory for how sexual antagonism may play out under sequential hermaphroditism, which has the additional complexities of age-structure. Here, we develop a formal theory of sexual antagonism in sequential hermaphrodites. First, we construct a general theoretical overview of the problem, then consider different types of sexually antagonistic and life-history trade-offs, under different modes of genetic inheritance (autosomal or cytoplasmic), and different forms of sequential hermaphroditism (protogynous, protoandrous or bidirectional). Finally, we provide a concrete illustration of these general patterns by developing a two-stage two-sex model, which yields conditions for both invasion of sexually antagonistic alleles and maintenance of sexually antagonistic polymorphisms.

W. D. Hamilton and the golden sex ratio.

In his famous two-part paper, published in Journal of Theoretical Biology in 1964, W. D. Hamilton predicted that natural selection acting in male-haploid populations favours a ratio of males to females that is in accordance with the golden ratio. This prediction has found its way into the pages of one of the best-selling books of all time, Dan Brown's 2003 novel The da Vinci Code, and is therefore in the running for the most widely known quantitative result in the history of evolutionary biology. Unfortunately, this golden-ratio result is wrong, and was later corrected by Hamilton, who showed that natural selection actually favours an unbiased sex ratio in this setting. But it has been unclear exactly how Hamilton arrived at the golden-ratio result in the first place. Here I show that the solution to this puzzle is found in unpublished work held in the British Library's W. D. Hamilton Archive. Specifically, in addition to employing a faulty method for calculating relatedness, Hamilton had also employed a faulty method for calculating reproductive value, considering only genetic contributions to the next generation rather than to the distant future. Repeating both mistakes recovers his erroneous golden-ratio result.

Population viscosity promotes altruism under density-dependent dispersal.

A basic mechanism of kin selection is population viscosity, whereby individuals do not move far from their place of birth and hence tend to be surrounded by relatives. In such circumstances, even indiscriminate altruism among neighbours will often involve interactions between kin, which has a promoting effect on the evolution of altruism. This has the potential to explain altruistic behaviour across the whole tree of life, including in taxa for which recognition of kin is implausible. However, population viscosity may also intensify resource competition among kin, which has an inhibitory effect on altruism. Indeed, in the simplest scenario, in which individuals disperse with a fixed probability, these two effects have been shown to exactly cancel such that there is no net impact of viscosity on altruism. Here, we show that if individuals are able to disperse conditionally upon local density, they are favoured to do so, with more altruistic neighbourhoods exhibiting a higher rate of dispersal and concomitant relaxation of kin competition. Comparing across different populations or species, this leads to a negative correlation between overall levels of dispersal and altruism. We demonstrate both analytically and using individual-based simulations that population viscosity promotes the evolution of altruism under density-dependent dispersal.

Density-dependent dispersal promotes female-biased sex allocation in viscous populations.

A surprising result emerging from the theory of sex allocation is that the optimal sex ratio is predicted to be completely independent of the rate of dispersal. This striking invariance result has stimulated a huge amount of theoretical and empirical attention in the social evolution literature. However, this sex-allocation invariant has been derived under the assumption that an individual's dispersal behaviour is not modulated by population density. Here, we investigate how density-dependent dispersal shapes patterns of sex allocation in a viscous-population setting. Specifically, we find that if individuals are able to adjust their dispersal behaviour according to local population density, then they are favoured to do so, and this drives the evolution of female-biased sex allocation. This result obtains because, whereas under density-independent dispersal, population viscosity is associated not only with higher relatedness-which promotes female bias-but also with higher kin competition-which inhibits female bias-under density-dependent dispersal, the kin-competition consequences of a female-biased sex ratio are entirely abolished. We derive analytical results for the full range of group sizes and costs of dispersal, under haploid, diploid and haplodiploid modes of inheritance. These results show that population viscosity promotes female-biased sex ratios in the context of density-dependent dispersal.

Sex-biased demography modulates male harm across the genome.

Recent years have seen an explosion of theoretical and empirical interest in the role that kin selection plays in shaping patterns of sexual conflict, with a particular focus on male harming traits. However, this work has focused solely on autosomal genes, and as such it remains unclear how demography modulates the evolution of male harm loci occurring in other portions of the genome, such as sex chromosomes and cytoplasmic elements. To investigate this, we extend existing models of sexual conflict for application to these different modes of inheritance. We first analyse the general case, revealing how sex-specific relatedness, reproductive value and the intensity of local competition combine to determine the potential for male harm. We then analyse a series of demographically explicit models, to assess how dispersal, overlapping generations, reproductive skew and the mechanism of population regulation affect sexual conflict across the genome, and drive conflict between nuclear and cytoplasmic genes. We then explore the effects of sex biases in these demographic parameters, showing how they may drive further conflicts between autosomes and sex chromosomes. Finally, we outline how different crossing schemes may be used to identify signatures of these intragenomic conflicts.

Genomic Imprinting As a Window into Human Language Evolution.

Humans spend large portions of their time and energy talking to one another, yet it remains unclear whether this activity is primarily selfish or altruistic. Here, it is shown how parent-of-origin specific gene expression-or "genomic imprinting"-may provide an answer to this question. First, it is shown why, regarding language, only altruistic or selfish scenarios are expected. Second, it is pointed out that an individual's maternal-origin and paternal-origin genes may have different evolutionary interests regarding investment into language, and that this intragenomic conflict may drive genomic imprinting which-as the direction of imprint depends upon whether investment into language is relatively selfish or altruistic-may be used to discriminate between these two possibilities. Third, predictions concerning the impact of various mutations and epimutations at imprinted loci on language pathologies are derived. In doing so, a framework is developed that highlights avenues for using intragenomic conflicts to investigate the evolutionary drivers of language.

A gene's-eye view of sexual antagonism.

Females and males may face different selection pressures. Accordingly, alleles that confer a benefit for one sex often incur a cost for the other. Classic evolutionary theory holds that the X chromosome, whose sex-biased transmission sees it spending more time in females, should value females more than males, whereas autosomes, whose transmission is unbiased, should value both sexes equally. However, recent mathematical and empirical studies indicate that male-beneficial alleles may be more favoured by the X chromosome than by autosomes. Here we develop a gene's-eye-view approach that reconciles the classic view with these recent discordant results, by separating a gene's valuation of female versus male fitness from its ability to induce fitness effects in either sex. We use this framework to generate new comparative predictions for sexually antagonistic evolution in relation to dosage compensation, sex-specific mortality and assortative mating, revealing how molecular mechanisms, ecology and demography drive variation in masculinization versus feminization across the genome.

Adjustment of sex allocation to co-foundress number and kinship under local mate competition: An inclusive-fitness analysis.

Hamilton's theory of local mate competition (LMC) describes how competition between male relatives for mating opportunities favours a female-biased parental investment. LMC theory has been extended in many ways to explore a range of genetic and life-history influences on sex allocation strategies, including showing that increasing genetic homogeneity within mating groups should favour greater female bias. However, there has been no quantitative theoretical prediction as to how females should facultatively adjust their sex allocation in response to co-foundress number and kinship. This shortfall has been highlighted recently by the finding that sex ratios produced by sub-social parasitoid wasps in the family Bethylidae are affected by the number of co-foundresses and by whether these are sisters or unrelated females. Here we close this gap in LMC theory by taking an inclusive-fitness approach to derive explicit theoretical predictions for this scenario. We find that, in line with the recent empirical results, females should adopt a more female-biased sex allocation when their co-foundresses are less numerous and are their sisters. Our model appears to predict somewhat more female bias than is observed empirically; we discuss a number of possible model extensions that would improve realism and that would be expected to result in a closer quantitative fit with experimental data.

Does kin discrimination promote cooperation?

Genetic relatedness is a key driver of the evolution of cooperation. One mechanism that may ensure social partners are genetically related is kin discrimination, in which individuals are able to distinguish kin from non-kin and adjust their behaviour accordingly. However, the impact of kin discrimination upon the overall level of cooperation remains obscure. Specifically, while kin discrimination allows an individual to help more-related social partners over less-related social partners, it is unclear whether and how the population average level of cooperation that is evolutionarily favoured should differ under kin discrimination versus indiscriminate social behaviour. Here, we perform a general mathematical analysis in order to assess whether, when and in which direction kin discrimination changes the average level of cooperation in an evolving population. We find that kin discrimination may increase, decrease or leave unchanged the average level of cooperation, depending upon whether the optimal level of cooperation is a convex, concave or linear function of genetic relatedness. We develop an extension of the classic 'tragedy of the commons' model of cooperation in order to provide an illustration of these results. Our analysis provides a method to guide future research on the evolutionary consequences of kin discrimination.

The social evolution of sleep: sex differences, intragenomic conflicts and clinical pathologies.

Sleep appears to be essential for most animals, including humans. Accordingly, individuals who sacrifice sleep are expected to incur costs and so should only be evolutionarily favoured to do this when these costs are offset by other benefits. For instance, a social group might benefit from having some level of wakefulness during the sleeping period if this guards against possible threats. Alternatively, individuals might sacrifice sleep in order to gain an advantage over mate competitors. Here, we perform a theoretical analysis of the social evolutionary pressures that drive investment into sleep versus wakefulness. Specifically, we: investigate how relatedness between social partners may modulate sleeping strategies, depending upon whether sleep sacrifice is selfish or altruistic; determine the conditions under which the sexes are favoured to adopt different sleeping strategies; identify the potential for intragenomic conflict between maternal-origin versus paternal-origin genes regarding an individual's sleeping behaviour; translate this conflict into novel and readily testable predictions concerning patterns of gene expression; and explore the concomitant effects of different kinds of mutations, epimutations, and uniparental disomies in relation to sleep disorders and other clinical pathologies. Our aim is to provide a theoretical framework for future empirical data and stimulate further research on this neglected topic.

Why war is a man's game.

Interest in the evolutionary origins and drivers of warfare in ancient and contemporary small-scale human societies has greatly increased in the last decade, and has been particularly spurred by exciting archaeological discoveries that suggest our ancestors led more violent lives than previously documented. However, the striking observation that warfare is an almost-exclusively male activity remains unexplained. Three general hypotheses have been proposed, concerning greater male effectiveness in warfare, lower male costs, and patrilocality. But while each of these factors might explain why warfare is more common in men, they do not convincingly explain why women almost never participate. Here, we develop a mathematical model to formally assess these hypotheses. Surprisingly, we find that exclusively male warfare may evolve even in the absence of any such sex differences, though sex biases in these parameters can make this evolutionary outcome more likely. The qualitative observation that participation in warfare is almost exclusive to one sex is ultimately explained by the fundamentally sex-specific nature of Darwinian competition-in fitness terms, men compete with men and women with women. These results reveal a potentially key role for ancestral conditions in shaping our species' patterns of sexual division of labour and violence-related adaptations and behavioural disorders.

Mother and offspring in conflict: why not?

A gene mediating interactions between mouse mothers and their pups has recently been claimed to support coadaptation rather than the kinship theory of genomic imprinting. This Formal Comment argues that this claim is unfounded.