The robustness of the weak selection approximation for the evolution of altruism against strong selection.

The weak selection approximation of population genetics has made possible the analysis of social evolution under a considerable variety of biological scenarios. Despite its extensive usage, the accuracy of weak selection in predicting the emergence of altruism under limited dispersal when selection intensity increases remains unclear. Here, we derive the condition for the spread of an altruistic mutant in the infinite island model of dispersal under a Moran reproductive process and arbitrary strength of selection. The simplicity of the model allows us to compare weak and strong selection regimes analytically. Our results demonstrate that the weak selection approximation is robust to moderate increases in selection intensity and therefore provides a good approximation to understand the invasion of altruism in spatially structured population. In particular, we find that the weak selection approximation is excellent even if selection is very strong, when either migration is much stronger than selection or when patches are large. Importantly, we emphasize that the weak selection approximation provides the ideal condition for the invasion of altruism, and increasing selection intensity will impede the emergence of altruism. We discuss that this should also hold for more complicated life cycles and for culturally transmitted altruism. Using the weak selection approximation is therefore unlikely to miss out on any demographic scenario that lead to the evolution of altruism under limited dispersal

The evolution of environmentally mediated social interactions and posthumous spite under isolation by distance.

Many social interactions happen indirectly via modifications of the environment, e.g. through the secretion of functional compounds or the depletion of renewable resources. Here, we derive the selection gradient on a quantitative trait affecting dynamical environmental variables that feed back on reproduction and survival in a finite patch-structured population subject to isolation by distance. Our analysis shows that the selection gradient depends on how a focal individual influences the fitness of all future individuals in the population through modifications of the environmental variables they experience, weighted by the neutral relatedness between recipients and the focal. The evolutionarily relevant trait-driven environmental modifications are formalized as the extended phenotypic effects of an individual, quantifying how a trait change in an individual in the present affects the environmental variables in all patches at all future times. When the trait affects reproduction and survival through a payoff function, the selection gradient can be expressed in terms of extended phenotypic effects weighted by scaled relatedness. We show how to compute extended phenotypic effects, relatedness, and scaled relatedness using Fourier analysis, which allow us to investigate a broad class of environmentally mediated social interactions in a tractable way. We use our approach to study the evolution of a trait controlling the costly production of some lasting commons (e.g. a common-pool resource or a toxic compound) that can diffuse in space and persist in time. We show that indiscriminate posthumous spite readily evolves in this scenario. More generally, whether selection favours environmentally mediated altruism or spite is determined by the spatial correlation between an individual's lineage and the commons originating from its patch. The sign of this correlation depends on interactions between dispersal patterns and the commons' renewal dynamics. More broadly, we suggest that selection can favour a wide range of social behaviours when these have carry-over effects in space and time

The evolution and consequences of sex-specific reproductive variance.

Natural selection favors alleles that increase the number of offspring produced by their carriers. But in a world that is inherently uncertain within generations, selection also favors alleles that reduce the variance in the number of offspring produced. If previous studies have established this principle, they have largely ignored fundamental aspects of sexual reproduction and therefore how selection on sex-specific reproductive variance operates. To study the evolution and consequences of sex-specific reproductive variance, we present a population-genetic model of phenotypic evolution in a dioecious population that incorporates previously neglected components of reproductive variance. First, we derive the probability of fixation for mutations that affect male and/or female reproductive phenotypes under sex-specific selection. We find that even in the simplest scenarios, the direction of selection is altered when reproductive variance is taken into account. In particular, previously unaccounted for covariances between the reproductive outputs of different individuals are expected to play a significant role in determining the direction of selection. Then, the probability of fixation is used to develop a stochastic model of joint male and female phenotypic evolution. We find that sex-specific reproductive variance can be responsible for changes in the course of long-term evolution. Finally, the model is applied to an example of parental-care evolution. Overall, our model allows for the evolutionary analysis of social traits in finite and dioecious populations, where interactions can occur within and between sexes under a realistic scenario of reproduction

Evolutionary Stability of Jointly Evolving Traits in Subdivided Populations.

The evolutionary stability of quantitative traits depends on whether a population can resist invasion by any mutant. While uninvadability is well understood in well-mixed populations, it is much less so in subdivided populations when multiple traits evolve jointly. Here, we investigate whether a spatially subdivided population at a monomorphic equilibrium for multiple traits can withstand invasion by any mutant or is subject to diversifying selection. Our model also explores the correlations among traits arising from diversifying selection and how they depend on relatedness due to limited dispersal. We find that selection tends to favor a positive (negative) correlation between two traits when the selective effects of one trait on relatedness is positively (negatively) correlated to the indirect fitness effects of the other trait. We study the evolution of traits for which this matters: dispersal that decreases relatedness and helping that has positive indirect fitness effects. We find that when dispersal cost is low and the benefits of helping accelerate faster than its costs, selection leads to the coexistence of mobile defectors and sessile helpers. Otherwise, the population evolves to a monomorphic state with intermediate helping and dispersal. Overall, our results highlight the effects of population subdivision for evolutionary stability and correlations among traits

Invasion fitness for gene-culture co-evolution in family-structured populations and an application to cumulative culture under vertical transmission.

Human evolution depends on the co-evolution between genetically determined behaviors and socially transmitted information. Although vertical transmission of cultural information from parent to offspring is common in hominins, its effects on cumulative cultural evolution are not fully understood. Here, we investigate gene-culture co-evolution in a family-structured population by studying the invasion fitness of a mutant allele that influences a deterministic level of cultural information (e.g., amount of knowledge or skill) to which diploid carriers of the mutant are exposed in subsequent generations. We show that the selection gradient on such a mutant, and the concomitant level of cultural information it generates, can be evaluated analytically under the assumption that the cultural dynamic has a single attractor point, thereby making gene-culture co-evolution in family-structured populations with multigenerational effects mathematically tractable. We apply our result to study how genetically determined phenotypes of individual and social learning co-evolve with the level of adaptive information they generate under vertical transmission. We find that vertical transmission increases adaptive information due to kin selection effects, but when information is transmitted as efficiently between family members as between unrelated individuals, this increase is moderate in diploids. By contrast, we show that the way resource allocation into learning trades off with allocation into reproduction (the "learning-reproduction trade-off") significantly influences levels of adaptive information. We also show that vertical transmission prevents evolutionary branching and may therefore play a qualitative role in gene-culture co-evolutionary dynamics. More generally, our analysis of selection suggests that vertical transmission can significantly increase levels of adaptive information under the biologically plausible condition that information transmission between relatives is more efficient than between unrelated individuals

Eco-Evolutionary Dynamics in Metacommunities: Ecological Inheritance, Helping within Species, and Harming between Species.

Understanding selection on intra- and interspecific interactions that take place in dispersal-limited communities is a challenge for ecology and evolutionary biology. The problem is that local demographic stochasticity generates eco-evolutionary dynamics that are generally too complicated to make tractable analytical investigations. Here we circumvent this problem by approximating the selection gradient on a quantitative trait that influences local community dynamics, assuming that such dynamics are deterministic with a stable fixed point. The model nonetheless captures unavoidable kin selection effects arising from demographic stochasticity. Our approximation reveals that selection depends on how an individual expressing a trait change influences (1) its own fitness and the fitness of its current relatives and (2) the fitness of its downstream relatives through modifications of local ecological conditions (i.e., through ecological inheritance). Mathematically, the effects of ecological inheritance on selection are captured by dispersal-limited versions of press perturbations of community ecology. We use our approximation to investigate the evolution of helping within species and harming between species when these behaviors influence demography. We find that altruistic helping evolves more readily when intraspecific competition is for material resources rather than for space, because in this case the costs of kin competition tend to be paid by downstream relatives. Similarly, altruistic harming between species evolves when it alleviates downstream relatives from interspecific competition. Beyond these examples, our approximation can help better understand the influence of ecological inheritance on a variety of eco-evolutionary dynamics in metacommunities, from consumer-resource and predator-prey coevolution to selection on mating systems with demographic feedbacks

The influence of the few: a stable 'oligarchy' controls information flow in house-hunting ants

Animals that live together in groups often face difficult choices, such as which food resource to exploit, or which direction to flee in response to a predator. When there are costs associated with deadlock or group fragmentation, it is essential that the group achieves a consensus decision. Here, we study consensus formation in emigrating ant colonies faced with a binary choice between two identical nest-sites. By individually tagging each ant with a unique radio-frequency identification microchip, and then recording all ant-to-ant ‘tandem runs’—stereotyped physical interactions that communicate information about potential nest-sites—we assembled the networks that trace the spread of consensus throughout the colony. Through repeated emigrations, we show that both the order in which these networks are assembled and the position of each individual within them are consistent from emigration to emigration. We demonstrate that the formation of the consensus is delegated to an influential but exclusive minority of highly active individuals—an ‘oligarchy’— which is further divided into two subgroups, each specialized upon a different tandem running role. Finally, we show that communication primarily occurs between subgroups not within them, and further, that such between-group communication is more efficient than within-group communication

Evolution of dosage compensation under sexual selection differs between X and Z chromosomes.

Complete sex chromosome dosage compensation has more often been observed in XY than ZW species. In this study, using a population genetic model and the chicken transcriptome, we assess whether sexual conflict can account for this difference. Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex. Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation. Using expression variance as a measure of selection strength, we find that, as predicted by the model, dosage compensation in the chicken is most pronounced in genes that are under strong selection biased towards females. Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation

Molecular evolution of Drosophila Sex-lethal and related sex determining genes.

Sex determining mechanisms are evolutionarily labile and related species often use different primary signals and gene regulatory networks. This is well illustrated by the sex determining cascade of Drosophila fruitflies, which have recruited Sex-lethal as the master switch and cellular memory of sexual identity, a role performed in other insects by the gene transformer. Here we investigate the evolutionary change in the coding sequences of sex determining genes associated with the recruitment of Sex-lethal. We analyze sequences of Sex-lethal itself, its Drosophila paralogue sister-or-Sex-lethal and downstream targets transformer and doublesex

Social polymorphism is favoured by the co-evolution of dispersal with social behaviour.

Dispersal determines gene flow among groups in a population and so plays a major role in many ecological and evolutionary processes. As gene flow shapes kin structure, dispersal is important to the evolution of social behaviours that influence reproduction within groups. Conversely, dispersal depends on kin structure and social behaviour. Dispersal and social behaviour therefore co-evolve, but the nature and consequences of this interplay are not well understood. Here, we show that it readily leads to the emergence of two social morphs: a sessile, benevolent morph expressed by individuals who tend to increase the reproduction of others within their group relative to their own; and a dispersive, self-serving morph expressed by individuals who tend to increase their own reproduction. This social polymorphism arises due to a positive linkage between the loci responsible for dispersal and social behaviour, leading to benevolent individuals preferentially interacting with relatives and self-serving individuals with non-relatives. We find that this linkage is favoured under a large spectrum of conditions, suggesting that associations between dispersal and other social traits should be common in nature. In line with this prediction, dispersers across a wide range of organisms have been reported to differ in their social tendencies from non-dispersers