Many pathogens transmit horizontally through usual routes and vertically from parent to offspring. Co-evolution is predicted, under certain circumstances, to produce a positive relationship between host-pathogen antagonism and the rate of vertical transmission. We cannot disentangle the roles of host demographics and the costs of host immune function in establishing this pattern. On one hand, models that assume no density-dependent growth of host populations and limit the cost of immune function to infected hosts only predict that the positive relationship is possible. On the other hand, models that assume density-dependent growth of host populations and impose the cost of immune function on all hosts, regardless of infection status, suggest that the positive relationship is not possible. Here, we seek to resolve the confusion. We model the co-evolution of a host and its pathogen when the latter can transmit both vertically and horizontally. We assume host population growth is self-limiting, and we impose the cost of immune function only on infected hosts. We find that a positive relationship between host-pathogen antagonism and vertical transmission is possible under our assumptions. Our finding points to the critical role played by assumptions about when hosts pay the cost of immune function. We also find that the combination of density-dependent host population growth and the cost-free lifestyle of uninfected hosts raises the possibility of selection-driven pathogen extinction. We discuss our findings in relation to previous theory and empirical findings.

Individuals can be subject to brood failure for many reasons, e.g. egg predation. Some species have adopted a strategy to compensate for fitness loss due to brood failure. In some bird species, individuals that experience brood failure can help a related neighbor care for their offspring. This behavior is known as redirected helping and it compensates for the loss of fitness by improving inclusive fitness. However, inclusive fitness gains associated with redirected helping are counteracted in a 'viscous' population, where individuals remain close to their natal site, by increased competition among kin. In a previous model, we investigated how population viscosity affects the evolution of redirected help by building an infinite-island model that lacked explicit spatial structure and emphasized dispersal on a global scale. Here, we revisit the role of population viscosity in the evolution of redirected help with a spatially explicit stepping-stone dispersal model. The dispersal pattern in this new framework is much more constrained than in the infinite-island case, strengthening the population viscosity we are interested in. In contrast to previous work, we find that localized dispersal can prevent the evolution of redirected help and even lead to the evolution of spiteful behavior in some specific cases. Our predictions are sensitive to the scale of dispersal, survival rate and the benefits provided by helping. We discuss our findings with regard to the previous literature investigating the evolution of helping in a viscous population.

Kin selection theory predicts that individuals should evolve to help relatives, either by helping indiscriminately in a population where they do not move very far from their relatives, or by discriminating kin and conditionally helping them. It has been argued that, because kin discrimination enables individuals to reduce how helpful they are with some social partners as well increase how helpful they are with others, this could lead to an increase or a decrease in the overall level of helping. Specifically, it was argued that kin discrimination would increase the overall level of helping if the function relating the optimal level of help and genetic relatedness is convex, but kin discrimination would decrease the overall level of helping if the function relating the optimal level of help and genetic relatedness is concave. However, this prediction was based on a model in which individuals were not able to choose their social partners but only adjust how helpful they should be toward those social partners they have been allocated. Here, we perform a mathematical analysis showing that being able to choose social partners increases the overall level of helping. Consequently, if kin discriminators are allowed to choose whom they help, kin discrimination is more likely to increase the overall level of helping than previously anticipated. We obtained these results in two complementary theoretical settings: one more general, which makes few demographic assumptions, and the other more specific and concrete, which assumes a patch-structured population with complete dispersal.

Vertical transmission is widely predicted to select for reduced virulence of pathogens. Recent theory cast doubt on this prediction by showing that the evolutionary response of the host to vertical transmission can lead to severe disease outcomes. That theory, however, takes a simplified view of host population dynamics by assuming pathogen-induced mortality alone inhibits host population growth. The assumption limits our ability to uncover benign co-evolutionary outcomes characterized by low levels of pathogen-induced mortality. Here, we revisit the role of vertical transmission using a model that assumes host population growth is self-regulated. Our model tracks the co-evolution of pathogen-induced mortality and host recovery until both have reached an evolutionarily stable level. For any given set of model conditions, we could identify as many as two distinct pairs of stable mortality-recovery traits. Mortality and recovery were higher for one of the pairs (the 'escalated' one) and lower for the other of the pairs (the 'de-escalated' one). As the rate of vertical transmission rose, stable expression of the pathogen-induced mortality trait always decreased, while stable expression of the host-recovery trait increased for 'escalated' pairs and decreased for 'de-escalated' ones. In addition, (i) increasing the intrinsic rate of host population growth, (ii) increasing the cost of host recovery, and (iii) decreasing the efficiency of horizontal disease transmission all led to lower levels of stable trait expression for both pathogen and host. Factors (i)-(iii) also led to lower virulence, more frequent occurrence of the de-escalated (almost commensal) stable outcome, and greater disease prevalence. We conclude that (i)-(iii) promote the co-evolution of more benign interactions in keeping with previous findings. However, our new insight is that the benign nature of the host-pathogen interaction can now be understood as the more frequent occurrence of the de-escalated outcome. We discuss our findings in light of previous theory and experimental work.

When a brood fails, the failed parent can help a neighbor rear its offspring. This behavior is known as redirected helping and occurs in various species. The advantage of redirected helping may seem obvious, provided the individual whose brood fails helps a related neighbor: The helper at least gains indirect fitness by redirecting its parental effort. However, complications arise when considering a viscous population, where individuals remain on or close to their natal site. In such a population, individuals compete with relatives, which dilutes the advantage of helping and may counteract it altogether. This raises a question: when can we expect redirected helping to evolve in a viscous population? We address this question with inclusive fitness models. We find that redirected helping can always be favored in a viscous population, provided the cost is sufficiently low. We also identify life-history features-like survival, dispersal, and brood-failure rate-that promote redirected helping. The effect of these life-history features, in general, depends on which component of fitness (survival or fecundity) benefits from help and how brood failure varies among demes. Unlike previous authors, we find that helping can be more strongly promoted when it provides survival rather than fecundity benefits.

Individuals delay natal dispersal for many reasons. There may be no place to disperse to; immediate dispersal or reproduction may be too costly; immediate dispersal may mean that the individual and their relatives miss the benefits of group living. Understanding the factors that lead to the evolution of delayed dispersal is important because delayed dispersal sets the stage for complex social groups and social behavior. Here, we study the evolution of delayed dispersal when the quality of the local environment is improved by greater numbers of individuals (e.g., safety in numbers). We assume that individuals who delay natal dispersal also expect to delay personal reproduction. In addition, we assume that improved environmental quality benefits manifest as changes to fecundity and survival. We are interested in how do the changes in these life-history features affect delayed dispersal. We use a model that ties evolution to population dynamics. We also aim to understand the relationship between levels of delayed dispersal and the probability of establishing as an independent breeder (a population-level feature) in response to changes in life-history details. Our model emphasizes kin selection and considers a sexual organism, which allows us to study parent-offspring conflict over delayed dispersal. At evolutionary equilibrium, fecundity and survival benefits of group size or quality promote higher levels of delayed dispersal over a larger set of life histories with one exception. The exception is for benefits of increased group size or quality reaped by the individuals who delay dispersal. There, the increased benefit does not change the life histories supporting delay dispersal. Next, in contrast to previous predictions, we find that a low probability of establishing in a new location is not always associated with a higher incidence of delayed dispersal. Finally, we find that increased personal benefits of delayed dispersal exacerbate the conflict between parents and their offspring. We discuss our findings in relation to previous theoretical and empirical work, especially work related to cooperative breeding.

Understanding the capacity of pathogens to cause severe disease is of fundamental importance to human health and the preservation of biodiversity. Many of those pathogens are not only transmitted horizontally between unrelated hosts but also vertically between parents and their progeny. It is widely accepted that vertical transmission leads to the evolution of less virulent pathogens, but this idea stems from research that neglects the evolutionary response of hosts. Here, we use a game-theory model of coevolution between pathogen and host to show that vertical transmission does not always lead to more benign pathogens. We highlight scenarios in which vertical transmission results in pathogens exhibiting more virulence. However, we also predict that more benign outcomes are still possible (a) when generating new horizontal infections inflicts too much damage on hosts, (b) when clearing an infection is too costly for the host, and (c) when vertical transmission is promoted by a greater growth rate of the host population. Though our work offers a new perspective on the role of vertical transmission in pathogen-host systems, it does agree with previous experimental work.

Small numbers of fetal cells cross the placenta during pregnancy turning mothers into microchimeras. Fetal cells from all previous pregnancies accumulate forming the mother's fetal microchiome. What is significant about microchimeric cells is that they have been linked to health problems including reproductive and autoimmune diseases. Three decades after the discovery of fetal microchimerism, the function of these cells remains a mystery. Here, we contend that the role of microchimeric cells is to inform the fetus about the likelihood that its genes are present in future pregnancies. We argue that, when genes are more likely than average to be in future maternal siblings, fetuses will send a fixed number of cells that will not elicit a maternal immune response against them. However, when genes are less likely to be in future maternal siblings, fetuses will send an ever-increasing number of cells that will elicit an ever-stronger maternal immune response. Our work can explain the observed clinical association between microchimeric cells and pre-eclampsia. However, our work predicts that this association should be stronger in women with a genetically diverse microchiome. If supported by medical tests, our work would allow establishing the likelihood of pregnancy or autoimmune problems advising medical interventions.

Humans and other primates exhibit pro-social preferences for fairness. These preferences are thought to be reinforced by strong reciprocity, a policy that rewards fair actors and punishes unfair ones. Theories of fairness based on strong reciprocity have been criticized for overlooking the importance of individual differences in socially heterogeneous populations. Here, we explore the evolution of fairness in a heterogeneous population. We analyse the Ultimatum Game in cases where players' roles in the game are determined by their status. Importantly, our model allows for non-random pairing of players, and so we also explore the role played by kin selection in shaping fairness. Our kin-selection model shows that, when individuals condition their behaviour on their role in the game, fairness can be understood as either altruistic or spiteful. Altruistic fairness directs resources from less valuable members of a genetic lineage to more valuable members of the same lineage, whereas spiteful fairness keeps resources away from the competitors of the actor's high-value relatives. When individuals express fairness unconditionally it can be understood as altruistic or selfish. When it is altruistic, unconditional fairness again serves to direct resources to high-value members of genetic lineages. When it is selfish, unconditional fairness simply improves an individual's own standing. Overall, we expand kin-selection based explanations for fairness to include motivations other than spite. We show, therefore, that one need not invoke strong reciprocity to explain the advantage of fairness in heterogeneous populations.

I contributed a paper to volume 60 of the journal. The paper reported on my study of sex-ratio evolution when one sex (females) is helpful but the other sex (males) suffers less from kin competition. I had based my study on a kin-selection model, and so I was dismayed to discover an error in the relatedness calculations therein. Specifically, relatedness coefficients that should have been calculated using a sampling-without-replacement scheme were instead calculated using sampling with replacement. Here, I correct my error and show how it impacts my original findings. I argue that my main conclusions are unchanged. Furthermore, only two new findings contrast with those I presented earlier. First, changing those model details unrelated to the marginal fitness benefits of help does not, in turn, impact substantially the conflict that occurs between mates over the brood sex ratio (I had previously reported some noteworthy impact was possible). Second, help can reduce sex-ratio conflict between mates more effectively when breeders occur in smaller groups (previously, I had said this occurred in larger groups).

In multipartite viruses, the genome is split into multiple segments, each of which is transmitted via a separate capsid. The existence of multipartite viruses poses a problem, because replication is only possible when all segments are present within the same host. Given this clear cost, why is multipartitism so common in viruses? Most previous hypotheses try to explain how multipartitism could provide an advantage. In so doing, they require scenarios that are unrealistic and that cannot explain viruses with more than 2 multipartite segments. We show theoretically that selection for cheats, which avoid producing a shared gene product, but still benefit from gene products produced by other genomes, can drive the evolution of both multipartite and segmented viruses. We find that multipartitism can evolve via cheating under realistic conditions and does not require unreasonably high coinfection rates or any group-level benefit. Furthermore, the cheating hypothesis is consistent with empirical patterns of cheating and multipartitism across viruses. More broadly, our results show how evolutionary conflict can drive new patterns of genome organisation in viruses and elsewhere.

Cooperative societies can be threatened by cheats, who invest less in cooperation and exploit the contributions of others. The impact of cheats depends on the extent to which they are maintained in the population. However, different empirical studies, across organisms ranging from RNA replicators to bacteria, have shown diverse cheat-cooperator dynamics. These vary from approaching a stable equilibrium to dynamic cyclical oscillations. The reason for this variation remains unclear. Here, we develop a theoretical model to identify the factors that determine whether dynamics should tend toward stable equilibria or cyclical oscillations. Our analyses show that (1) a combination of both periodic population bottlenecks and density-dependent selection on cheating is required to produce cyclical oscillations and (2) the extent of frequency-dependent selection for cheating can influence the amplitude of these oscillations but does not lead to oscillations alone. Furthermore, we show that stochastic group formation (demographic stochasticity) can generate different forms of oscillation, over a longer time scale, across growth cycles. Our results provide experimentally testable hypotheses for the processes underlying cheat-cooperator dynamics.

Asexual reproduction is ancestral in prokaryotes; the switch to sexuality in eukaryotes is one of the major transitions in the history of life. The study of the maintenance of sex in eukaryotes has raised considerable interest for decades and is still one of evolutionary biology's most prominent question. The observation that many asexual species are of hybrid origin has led some to propose that asexuality in hybrids results from sexual processes being disturbed because of incompatibilities between the two parental species' genomes. However, in some cases, failure to produce asexual F1s in the lab may indicate that this mechanism is not the only road to asexuality in hybrid species. Here, we present a mathematical model and propose an alternative, adaptive route for the evolution of asexuality from previously sexual hybrids. Under some reproductive alterations, we show that asexuality can evolve to rescue hybrids' reproduction. Importantly, we highlight that when incompatibilities only affect the fusion of sperm and egg's genomes, the two traits that characterize asexuality, namely unreduced meiosis and the initiation of embryogenesis without the incorporation of the sperm's pronucleus, can evolve separately, greatly facilitating the overall evolutionary route. Taken together, our results provide an alternative, potentially complementary explanation for the link between asexuality and hybridization.

Humans and other primates exhibit pro-social preferences for fairness. These preferences are thought to be reinforced by strong reciprocity, a policy that rewards fair actors and punishes unfair ones. Theories of fairness based on strong reciprocity have been criticized for overlooking the importance of individual differences in socially heterogeneous populations. Here, we explore the evolution of fairness in a heterogeneous population. We analyse the Ultimatum Game in cases where players' roles in the game are determined by their status. Importantly, our model allows for incomplete mixing of players, and so we also explore the role played by kin selection in shaping fairness. Our kin-selection model shows that, when individuals condition their behaviour on their role in the game, fairness can be understood as either altruistic or spiteful. Altruistic fairness directs resources from less valuable members of a genetic lineage to more valuable members of the same lineage, whereas spiteful fairness keeps resources away from the competitors of the actor's high-value relatives. When individuals express fairness unconditionally it can be understood as altruistic or selfish. When it is altruistic, unconditional fairness again serves to direct resources to high-value members of genetic lineages. When it is selfish, unconditional fairness simply improves an individual's own standing. Overall, we expand kin-selection based explanations for fairness to include motivations other than spite. We show, therefore, that one need not invoke strong reciprocity to explain the advantage of fairness in heterogeneous populations.

Social behaviours are typically modelled using neighbour-modulated fitness, which focuses on individuals having their fitness altered by neighbours. However, these models are either interpreted using inclusive fitness, which focuses on individuals altering the fitness of neighbours, or not interpreted at all. This disconnect leads to interpretational mistakes and obscures the adaptive significance of behaviour. We bridge this gap by presenting a systematic methodology for constructing inclusive-fitness models. We find a behaviour's 'inclusive-fitness effect' by summing primary and secondary deviations in reproductive value. Primary deviations are the immediate result of a social interaction; for example, the cost and benefit of an altruistic act. Secondary deviations are compensatory effects that arise because the total reproductive value of the population is fixed; for example, the increased competition that follows an altruistic act. Compared to neighbour-modulated fitness methodologies, our approach is often simpler and reveals the model's inclusive-fitness narrative clearly. We implement our methodology first in a homogeneous population, with supplementary examples of help under synergy, help in a viscous population and Creel's paradox. We then implement our methodology in a class-structured population, where the advantages of our approach are most evident, with supplementary examples of altruism between age classes, and sex-ratio evolution.

It has been hypothesized that horizontal gene transfer on plasmids can facilitate the evolution of cooperation, by allowing genes to jump between bacteria, and hence increase genetic relatedness at the cooperative loci. However, we show theoretically that horizontal gene transfer only appreciably increases relatedness when plasmids are rare, where there are many plasmid-free cells available to infect (many opportunities for horizontal gene transfer). In contrast, when plasmids are common, there are few opportunities for horizontal gene transfer, meaning relatedness is not appreciably increased, and so cooperation is not favored. Plasmids, therefore, evolve to be rare and cooperative, or common and noncooperative, meaning plasmid frequency and cooperativeness are never simultaneously high. The overall level of plasmid-mediated cooperation, given by the product of plasmid frequency and cooperativeness, is therefore consistently negligible or low.

• I briefly summarize two classic papers by W. D. Hamilton, published in Volume 7 of the journal (in 1964). • In this work Hamilton introduced 'inclusive fitness' and I explain why the concept was transformative. • I identify three key developments in inclusive-fitness theory since 1964, and I suggest there is scope to develop the theory further.

Medical research reports that women often exhibit stronger immune responses than men, while pathogens tend to be more virulent in men. Current explanations cannot account for this pattern, creating an obstacle for our understanding of infectious-disease outcomes and the incidence of autoimmune diseases. We offer an alternative explanation that relies on a fundamental difference between the sexes: maternity and the opportunities it creates for transmission of pathogens from mother to child (vertical transmission). Our explanation relies on a mathematical model of the co-evolution of host immunocompetence and pathogen virulence. Here, we show that when there is sufficient vertical transmission co-evolution leads women to defend strongly against temperate pathogens and men to defend weakly against aggressive pathogens, in keeping with medical observations. From a more applied perspective, we argue that limiting vertical transmission of infections would alleviate the disproportionate incidence of autoimmune diseases in women over evolutionary time.

A social cheat is typically assumed to be an individual that does not perform a cooperative behaviour, or performs less of it, but can still exploit the cooperative behaviour of others. However, empirical data suggests that cheating can be more subtle, involving evolutionary arms races over the ability to both exploit and resist exploitation. These complications have not been captured by evolutionary theory, which lags behind empirical studies in this area. We bridge this gap with a mixture of game-theoretical models and individual-based simulations, examining what conditions favour more elaborate patterns of cheating. We found that as well as adjusting their own behaviour, individuals can be selected to manipulate the behaviour of others, which we term 'manipulative cheating'. Further, we found that manipulative cheating can lead to dynamic oscillations (arms races), between selfishness, manipulation, and suppression of manipulation. Our results can help explain both variation in the level of cheating, and genetic variation in the extent to which individuals can be exploited by cheats.