Evolution of delayed dispersal with group size effect and population dynamics.

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.

How to make an inclusive-fitness model.

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.

Vertical transmission does not always lead to benign pathogen-host associations.

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.

Equilibria and oscillations in cheat-cooperator dynamics.

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.

Microchimerism as a source of information on future pregnancies.

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.

Why do hybrids turn down sex?

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.

Is cooperation favored by horizontal gene transfer?

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.

Cheating leads to the evolution of multipartite viruses.

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.

A kin-selection model of fairness in heterogeneous populations.

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.

Technical comment on "sex ratios when helpers stay at the nest".

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).

The evolution of manipulative cheating.

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.

On maternity and the stronger immune response in women.

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.

Plasmids do not consistently stabilize cooperation across bacteria but may promote broad pathogen host-range.

Horizontal gene transfer via plasmids could favour cooperation in bacteria, because transfer of a cooperative gene turns non-cooperative cheats into cooperators. This hypothesis has received support from theoretical, genomic and experimental analyses. By contrast, we show here, with a comparative analysis across 51 diverse species, that genes for extracellular proteins, which are likely to act as cooperative 'public goods', were not more likely to be carried on either: (1) plasmids compared to chromosomes; or (2) plasmids that transfer at higher rates. Our results were supported by theoretical modelling which showed that, while horizontal gene transfer can help cooperative genes initially invade a population, it has less influence on the longer-term maintenance of cooperation. Instead, we found that genes for extracellular proteins were more likely to be on plasmids when they coded for pathogenic virulence traits, in pathogenic bacteria with a broad host-range.

Epigenetic memories and the evolution of infectious diseases.

Genes with identical DNA sequence may show differential expression because of epigenetic marks. Where epigenetic marks respond to past conditions, they represent a form of "memory". Despite their medical relevance, the impact of memories on the evolution of infectious diseases has rarely been considered. Here we explore the evolution of virulence in pathogens that carry memories of the sex of their previous host. We show that this form of memory provides information about the sex of present and future hosts when the sexes differ in their pathogen's transmission pattern. Memories of past hosts enable the evolution of greater virulence in infections originating from one sex and infections transmitted across sexes. Thus, our results account for patterns of virulence that have, to date, defied medical explanation. In particular, it has been observed that girls infected by boys (or boys infected by girls) are more likely to die from measles, chickenpox and polio than girls infected by girls (or boys infected by boys). We also evaluate epigenetic therapies that tamper with the memories of infecting pathogens. More broadly, our findings imply that pathogens can be selected to carry memories of past environments other than sex. This identifies new directions in personalised medicine.

Prophylactic host behaviour discourages pathogen exploitation.

Much work has considered the evolution of pathogens, but little is known about how they respond to changes in host behaviour. We build a model of sublethal disease effects where hosts are able to choose to engage in prophylactic measures that reduce the likelihood of disease transmission. This choice is mediated by utility costs and benefits associated with prophylaxis, and the fraction of hosts engaged in prophylaxis is also affected by population dynamics. When prophylactic host behaviour occurs, we find that the level of pathogen host exploitation is reduced, by the action of selection, relative to the level that would otherwise be predicted in the absence of prophylaxis. Our work emphasizes the significance of the transmission-recovery trade-off faced by the pathogen and the ability of the pathogen to influence host prophylactic behaviour.

Dispersal altering local states has a limited effect on persistence of a metapopulation.

Metapopulations are collections of local populations connected by dispersal. Metapopulation models often assume would-be colonists affect the states of local populations they disperse from and those they disperse to. Here, we build a new framework to include that effect and to assess the impact of dispersal. Our model predicts that a metapopulation will, in general, be found either in the state of global extinction or in the state of persistence. Our key finding is that dispersal, and the state changes associated with dispersal, have significant qualitative and quantitative effects on long-term dynamics only in a narrow range of parameter space. We conclude that life history features other than dispersal (e.g. mortality rate) have a greater influence over metapopulation persistence. We discuss the implications of our results for conservation biology, the future application of our model to the study of cooperative breeding, as well as our model's limitations.

Evolution of delayed dispersal and subsequent emergence of helping, with implications for cooperative breeding.

Cooperative breeding occurs when individuals help raise the offspring of others. It is widely accepted that help displayed by cooperative breeders emerged only after individuals' tendency to delay dispersal had become established. We use this idea as a basis for two inclusive-fitness models: one for the evolution of delayed dispersal, and a second for the subsequent emergence of helpful behavior exhibited by non-breeding individuals. We focus on a territorial species in a saturated environment, and allow territories to be inherited by non-breeding individuals who have delayed dispersal. Our first model predicts that increased survivorship and increased fecundity both provide an incentive to non-breeding individuals to delay dispersal, and stay near their natal territory for some period of time. Predictions from the first model can be well understood by ignoring complications arising from competition among relatives. Our second model shows that effects on relatives play a primary role in the advantage of helping. In addition, the second model predicts that increased survivorship and fecundity promote the emergence of help. Together, our models lead us to conclude that the emergence of cooperative-breeding systems is made easier by life-history features associated with high survivorship and fecundity. We discuss the implications of our conclusions for life-history-based hypotheses of cooperative breeding and social evolution.

Fast-killing parasites can be favoured in spatially structured populations.

It is becoming increasingly clear that the evolution of infectious disease is influenced by host population structure. Theory predicts that parasites should be more 'prudent'-less transmissible-in spatially structured host populations. However, here we (i) highlight how low transmission, the phenotype being selected for in this in context, may also be achieved by rapacious host exploitation, if fast host exploitation confers a local, within-host competitive advantage and (ii) test this novel concept in a bacteria-virus system. We found that limited host availability and, to a lesser extent, low relatedness favour faster-killing parasites with reduced transmission. By contrast, high host availability and high relatedness favour slower-killing, more transmissible parasites. Our results suggest high, rather than low, virulence may be selected in spatially structured host-parasite communities where local competition and hence selection for a within-host fitness advantage is high.This article is part of the themed issue 'Opening the black box: re-examining the ecology and evolution of parasite transmission'.

Sex allocation and the emergence of helping in cooperatively breeding species.

In cooperative breeding systems individuals invest in the reproductive success of others. In this paper, we study the emergence of cooperative breeding systems in which reproductively active breeders receive investment from reproductively non-active helpers. Our goal is to understand how the division of an investment between male and female components of breeder fitness (i.e. the helper sex-allocation strategy) influences the emergence of cooperative breeding itself. Using mathematical models, we arrive at expressions for the inclusive-fitness advantage of helpful behaviour that generalize previous work. These expressions assume an ecologically stable environment, and that breeders make evolutionarily stable sex-allocation decisions. We find that, when breeders are extremely resource limited, the sex-allocation strategy used by a helper can be a key determinant in the success of helpful alleles. This finding, however, is restricted to cases in which helpers have access to intermediate levels of resources. Surprisingly, when helpers can make only a small investment in a recipient the division of the investment matters only very little to advantage of help. By contrast when resources are extremely abundant, we obtain the unsurprising result that the manner in which resources are allocated has little influence on the emergence of help. When breeders have access to intermediate levels of resources we find increasing relatedness can, in certain cases, inhibit the emergence of help. We also find that increasing the amount of resources available to a breeder can impede help as well. Both of these counter-intuitive results are mediated by evolutionary responses in breeder sex allocation.