Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

The evolution of group-beneficial traits potentially allows the survival of 'cheaters' that would otherwise be unfit. Here we describe experimental work on group-beneficial traits and the consequences of frequency-dependent selection in the context of bacterial antibiotic resistance. We constructed a 'self-limited antibiotic resistant' (SLAR) strain of Escherichia coli in which a TEM-1 beta-lactamase was anchored to the inner membrane. In pairwise competition experiments between the SLAR strain and ampicillin-sensitive strains, only the SLAR strain survived in the presence of ampicillin. We also constructed a 'shared antibiotic resistant' (SAR) strain in which TEM-1 beta-lactamase protected both the SAR strain and nearby sensitive cells, thus acting as a model for a genetically defined group-beneficial trait. In pairwise competition experiments of the SAR strain against two different sensitive strains of E. coli, we found that the sensitive strains maintained themselves at frequencies of 5-12% in the presence of ampicillin. When the relative cost of the SAR strain was lowered, its equilibrial frequency rose. Sensitive strains also arose from pure cultures of the SAR strain. In these cases, too, the sensitive 'cheaters' were maintained in ampicillin at frequencies comparable to those observed in the previous competitions. These results suggest that traits which benefit other group members can permit survival of genotypes that otherwise would be eliminated by natural selection, and allow the maintenance of greater genetic variation upon which evolution can operate.     

Internal and external constraints in the evolution of morphological allometries in a butterfly

Much diversity in animal morphology results from variation in the relative size of morphological traits. The scaling relationships, or allometries, that describe relative trait size can vary greatly in both intercept and slope among species or other animal groups. Yet within such groups, individuals typically exhibit low variation in relative trait size. This pattern of high intra- and low intergroup variation may result from natural selection for particular allometries, from developmental constraints restricting differential growth among traits, or both. Here we explore the relative roles of short-term developmental constraints and natural selection in the evolution of the intercept of the allometry between the forewing and hindwing of a butterfly. First, despite a strong genetic correlation between these two traits, we show that artificial selection perpendicular to the forewing-hindwing scaling relationship results in rapid evolution of the allometry intercept. This demonstrates an absence of developmental constraints limiting intercept evolution for this scaling relationship. Mating experiments in a natural environment revealed strong stabilizing selection favoring males with the wild-type allometry intercept over those with derived intercepts. Our results demonstrate that evolution of this component of the forewing-hindwing allometry is not limited by developmental constraints in the short term and that natural selection on allometry intercepts can be powerful.     

Multilevel and sex‐specific selection on competitive traits in North American red squirrels

Individuals often interact more closely with some members of the population (e.g., offspring, siblings, or group members) than they do with other individuals. This structuring of interactions can lead to multilevel natural selection, where traits expressed at the group‐level influence fitness alongside individual‐level traits. Such multilevel selection can alter evolutionary trajectories, yet is rarely quantified in the wild, especially for species that do not interact in clearly demarcated groups. We quantified multilevel natural selection on two traits, postnatal growth rate and birth date, in a population of North American red squirrels (Tamiasciurus hudsonicus). The strongest level of selection was typically within‐acoustic social neighborhoods (within 130 m of the nest), where growing faster and being born earlier than nearby litters was key, while selection on growth rate was also apparent both within‐litters and within‐study areas. Higher population densities increased the strength of selection for earlier breeding, but did not influence selection on growth rates. Females experienced especially strong selection on growth rate at the within‐litter level, possibly linked to the biased bequeathal of the maternal territory to daughters. Our results demonstrate the importance of considering multilevel and sex‐specific selection in wild species, including those that are territorial and sexually monomorphic.     

Levels of selection on threshold characters

Threshold models are useful for understanding the evolution of dimorphic traits with polygenic bases. Selection for threshold characters on individuals is expected to be frequency dependent because of the peculiar way that selection views underlying genetic and environmental factors. Selection among individuals is inefficient because individual phenotypes fall into only two discrete categories that map imperfectly to the underlying genes. Incidence, however, can be continuously distributed among groups, making among-group selection relatively more efficient. Differently put, the group-mean phenotype can be a better predictor of an individual's genotype than that individual's own phenotype. Because evolution in group-structured populations is governed by the balance of selection within and between groups, we can expect threshold traits to evolve in fundamentally different ways when group mean fitness is a function of morph frequency. We extend the theory of selection on threshold traits to include group selection using contextual analysis. For the simple case of linear group-fitness functions, we show that the group-level component of selection, like the individual-level component, is frequency dependent. However, the conditions that determine which component dominates when levels of selection are in conflict (as described by Hamilton's rule) are not frequency dependent. Thus, enhanced group selection is not an inherent property of threshold characters. Nevertheless, we show that predicting the effects of multiple levels of selection on dimorphic traits requires special considerations of the threshold model.     

The evolution of strong reciprocity: cooperation in heterogeneous populations

How do human groups maintain a high level of cooperation despite a low level of genetic relatedness among group members? We suggest that many humans have a predisposition to punish those who violate group-beneficial norms, even when this imposes a fitness cost on the punisher. Such altruistic punishment is widely observed to sustain high levels of cooperation in behavioral experiments and in natural settings. We offer a model of cooperation and punishment that we call STRONG RECIPROCITY: where members of a group benefit from mutual adherence to a social norm, strong reciprocators obey the norm and punish its violators, even though as a result they receive lower payoffs than other group members, such as selfish agents who violate the norm and do not punish, and pure cooperators who adhere to the norm but free-ride by never punishing. Our agent-based simulations show that, under assumptions approximating likely human environments over the 100000 years prior to the domestication of animals and plants, the proliferation of strong reciprocators when initially rare is highly likely, and that substantial frequencies of all three behavioral types can be sustained in a population. As a result, high levels of cooperation are sustained. Our results do not require that group members be related or that group extinctions occur.     

Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes

The relative contribution of sexual and natural selection to evolution of sexual ornaments has rarely been quantified under natural conditions. In this study we used a long-term dataset of house sparrows in which parents and offspring were matched genetically to estimate the within- and across-sex genetic basis for variation and covariation among morphological traits. By applying two-sex multivariate "animal models" to estimate genetic parameters, we estimated evolutionary changes in a male sexual ornament, badge size, from the contribution of direct and indirect selection on correlated traits within males and females, after accounting for overlapping generations and age-structure. Indirect natural selection on genetically correlated traits in males and females was the major force causing evolutionary change in the male ornament. Thus, natural selection on female morphology may cause indirect evolutionary changes in male ornaments. We observed however no directional phenotypic change in the ornament size of one-year-old males during the study period. On the other hand, changes were recorded in other morphological characters of both sexes. Our analyses of evolutionary dynamics in sexual characters require application of appropriate two-sex models to account for how selection on correlated traits in both sexes affects the evolutionary outcome of sexual selection.     

Group selection among alternative evolutionarily stable strategies

Many important models of the evolution of social behavior have more than one evolutionarily stable strategy (ESS). Examples include co-ordination games, contests, mutualism, reciprocity, and sexual selection. Here we show that when there are multiple evolutionarily stable strategies, selection among groups can cause the spread of the strategy that has the lowest extinction rate or highest probability of contributing to the colonization of empty habitats, and that this may occur even when groups are usually very large, migration rates are substantial, and "extinction" entails only the disruption of the group and the dispersal of its members. The main requirements are: (1) individuals drawn from a single surviving group make up a sufficiently large fraction newly formed groups, and (2) the processes increasing the frequency of successful strategies within groups are strong compared to rate of migration among groups. The latter condition suggests that this form of group selection will be particularly important when behavioral variation is culturally acquired.     

Genetic niche-hiking: an alternative explanation for the evolution of flammability

In fire-prone ecosystems, many plants possess traits that enhance their relative flammability and ecologists have suggested increased flammability could result from natural selection. To date, theoretical models addressing the evolution of flammable characteristics assume that flammable plants realize some direct fitness advantage. In this paper, we explore the idea that enhanced flammability can increase in frequency in a population without any direct fitness benefit to the flammable type. In our model, flammability evolves due to an association between an allele that promotes flammability and alleles at unlinked loci that give high fitness. In analogy to genetic hitchhiking, in which a deleterious allele can invade due to a genetic linkage, we call this process "genetic niche-hiking," because the association results from localized niche construction. Specifically, flammable plants sacrifice themselves and their neighbors to produce local fire-cleared gaps (the constructed niche) in which their offspring are able to continually track an ever-changing environment. Niche-hiking requires that mating, dispersal and niche construction all occur locally (i.e. the population is spatially structured), such that offspring are likely to experience the niches their parents construct. Using a spatially-explicit lattice-based simulation, we find that increased flammability can evolve despite the "self-killing" cost of such a trait. Genetic niche-hiking may also be applicable to the evolution of other traits in spatially structured ecological systems such as plant disease susceptibility and forest tree characteristics that influence gap production.     

Protection of Salmonella by ampicillin-resistant Escherichia coli in the presence of otherwise lethal drug concentrations

Microbial systems have become the preferred testing grounds for experimental work on the evolution of traits that benefit other group members. This work, based on conceptual and theoretical models of frequency-dependent selection within populations, has proven fruitful in terms of understanding the dynamics of group beneficial or ‘public goods’ traits within species. Here, we expand the scope of microbial work on the evolution of group-beneficial traits to the case of multi-species communities, particularly those that affect human health. We examined whether β-lactamase-producing Escherichia coli could protect ampicillin-sensitive cohorts of other species, particularly species that could cause human disease. Both β-lactamase-secreting E. coli and, surprisingly, those engineered to retain it, allowed for survival of a large number of ampicillin-sensitive cohorts of Salmonella enterica serovar Typhimurium, including both laboratory and clinical isolates. The Salmonella survivors, however, remained sensitive to ampicillin when re-plated onto solid medium and there was no evidence of gene transfer. Salmonella survival did not even require direct physical contact with the resistant E. coli. The observed phenomenon appears to involve increased release of β-lactamase from the E. coli when present with S. enterica. Significantly, these findings imply that resistant E. coli, that are not themselves pathogenic, may be exploited, even when they are normally selfish with respect to other E. coli. Thus, Salmonella can gain protection against antibiotics from E. coli without gene transfer, a phenomenon not previously known. As a consequence, antibiotic-resistant E. coli can play a decisive role in the survival of a species that causes disease and may thereby interfere with successful treatment.     

Asymmetry within social groups: division of labour and intergroup competition

Social animals vary in their ability to compete with group members over shared resources and also vary in their cooperative efforts to produce these resources. Competition among groups can promote within‐group cooperation, but many existing models of intergroup cooperation do not explicitly account for observations that group members invest differentially in cooperation and that there are often within‐group competitive or power asymmetries. We present a game theoretic model of intergroup competition that investigates how such asymmetries affect within‐group cooperation. In this model, group members adopt one of two roles, with relative competitive efficiency and the number of individuals varying between roles. Players in each role make simultaneous, coevolving decisions. The model predicts that although intergroup competition increases cooperative contributions to group resources by both roles, contributions are predominantly from individuals in the less competitively efficient role, whereas individuals in the more competitively efficient role generally gain the larger share of these resources. When asymmetry in relative competitive efficiency is greater, a group's per capita cooperation (averaged across both roles) is higher, due to increased cooperation from the competitively inferior individuals. For extreme asymmetry in relative competitive efficiency, per capita cooperation is highest in groups with a single competitively superior individual and many competitively inferior individuals, because the latter acquiesce and invest in cooperation rather than within‐group competition. These predictions are consistent with observed features of many societies, such as monogynous Hymenoptera with many workers and caste dimorphism.     

Revisiting santa rosalia to unfold a degeneracy of classic models of speciation

Abstract Many classic models of speciation incorporate assortative mating based on mating groups, such as plants with different flowering times, and they investigate whether an ecological trait under disruptive natural selection becomes genetically associated with the selectively neutral mating trait. It is well known that this genetic association is potently destroyed by recombination. In this note, we point out a more fundamental difficulty: if a "knife-edge" symmetry assumption of previous models is violated, then the mating trait is no longer neutral and sexual selection eliminates the polymorphism in the mating locus. This result strengthens the growing consensus that magic traits are the more likely route to nonallopatric speciation. We expand the model assuming also ecological selection on the mating trait and investigate the conditions for natural selection to overcome sexual selection and maintain mating polymorphism; we find that the combination of natural and sexual selection can cause also bistability of allele frequencies.     

Frequency-dependent selection and the evolution of assortative mating

A long-standing goal in evolutionary biology is to identify the conditions that promote the evolution of reproductive isolation and speciation. The factors promoting sympatric speciation have been of particular interest, both because it is notoriously difficult to prove empirically and because theoretical models have generated conflicting results, depending on the assumptions made. Here, we analyze the conditions under which selection favors the evolution of assortative mating, thereby reducing gene flow between sympatric groups, using a general model of selection, which allows fitness to be frequency dependent. Our analytical results are based on a two-locus diploid model, with one locus altering the trait under selection and the other locus controlling the strength of assortment (a "one-allele" model). Examining both equilibrium and nonequilibrium scenarios, we demonstrate that whenever heterozygotes are less fit, on average, than homozygotes at the trait locus, indirect selection for assortative mating is generated. While costs of assortative mating hinder the evolution of reproductive isolation, they do not prevent it unless they are sufficiently great. Assortative mating that arises because individuals mate within groups (formed in time or space) is most conducive to the evolution of complete assortative mating from random mating. Assortative mating based on female preferences is more restrictive, because the resulting sexual selection can lead to loss of the trait polymorphism and cause the relative fitness of heterozygotes to rise above homozygotes, eliminating the force favoring assortment. When assortative mating is already prevalent, however, sexual selection can itself cause low heterozygous fitness, promoting the evolution of complete reproductive isolation (akin to "reinforcement") regardless of the form of natural selection.     

An evolutionary quantitative genetics model for phenotypic (co)variances under limited dispersal,with an application to socially synergistic traits

Darwinian evolution consists of the gradual transformation of heritable traits due to natural selection and the input of random variation by mutation. Here, we use a quantitative genetics approach to investigate the coevolution of multiple quantitative traits under selection, mutation, and limited dispersal. We track the dynamics of trait means and of variance–covariances between traits that experience frequency‐dependent selection. Assuming a multivariate‐normal trait distribution, we recover classical dynamics of quantitative genetics, as well as stability and evolutionary branching conditions of invasion analyses, except that due to limited dispersal, selection depends on indirect fitness effects and relatedness. In particular, correlational selection that associates different traits within‐individuals depends on the fitness effects of such associations between‐individuals. We find that these kin selection effects can be as relevant as pleiotropy for the evolution of correlation between traits. We illustrate this with an example of the coevolution of two social traits whose association within‐individuals is costly but synergistically beneficial between‐individuals. As dispersal becomes limited and relatedness increases, associations between‐traits between‐individuals become increasingly targeted by correlational selection. Consequently, the trait distribution goes from being bimodal with a negative correlation under panmixia to unimodal with a positive correlation under limited dispersal.     

Group selection, individual selection, and the evolution of genetic drift.

In a subdivided population, genetic drift affects variation between groups, and thus it can have an important effect on the outcome of evolution (Wright, 1978). The rate of genetic drift is determined, in part, by the behaviour of population members. This paper presents three mathematical models in which behavioural traits that affect the rate of genetic drift are allowed to coevolve with traits that are under selection at the group and individual levels. The results show that if group selection is strong relative to individual selection, then behavioural traits that enhance the rate of genetic drift will tend to increase in frequency. The strength of this effect depends, in part, on the way in which vacant sites are colonized.     

Individuals in foraging groups may use vocal cues when assessing their need for anti-predator vigilance

Many studies of social species have reported variation in the anti-predator vigilance behaviour of foraging individuals depending on the presence and relative position of other group members. However, little attention has focused on how foragers assess these variables. It is commonly assumed that they do so visually, but many social species produce frequent calls while foraging, and these 'close' calls might provide valuable spatial information. Here, we show that foraging pied babblers (Turdoides bicolor) are less vigilant when in larger groups, in the centre of a group and in closer proximity to another group member. We then show that foragers are less vigilant during playbacks of close calling by more individuals and individuals on either side of them when compared with calls of fewer individuals and calls on one side of them. These results suggest that foragers can use vocal cues to gain information on group size and their spatial position within a group. Future studies of anti-predator vigilance should consider the relative importance of both visual and vocal monitoring of group members.     

Inducible defence and the social evolution of herd immunity.

Many organisms vary their level of investment in defensive characters. Protective traits may be induced upon exposure to predators or parasites. In a similar way, humans vaccinate in response to threatening epidemics. When most group members defend themselves, epidemics die out quickly because parasites cannot spread. A high level of group (herd) immunity is therefore beneficial to the group. There is, however, a well-known divergence between the optimum degree of induction for selfish individuals and the level of induction that maximizes group benefit. I develop two optimality models for the frequency of induction. The first model shows that higher relatedness favours more induction and a smaller difference between selfish and cooperative optima. The second model assumes variation in the vigour of individuals and therefore differences in the relative cost for induction. The model predicts that strong individuals induce more easily than weak individuals. Small differences in vigour cause a large divergence in the optimal levels of induction for strong and weak individuals. The concept of genetic relatedness in an evolutionary model is analogous to correlated interests and correlated strategies in an economic model of human behaviour. The evolutionary models presented here therefore provide a basis for further study of human vaccination.     

Neoproterozoic 'snowball Earth' glaciations and the evolution of altruism

We hypothesize that a demographic and ecological effect of Neoproterozoic ‘snowball Earth’ glaciations was to increase the fitness of group‐level traits and consequently the likelihood of the evolution of macroscopic form. Extreme and repeated founder effects raised genetic relatedness – and therefore the influence of kin selection on the individuals within a group. This was permissive for the evolution of some highly costly altruistic traits, including those for macroscopic differentiation. In some eukaryotic species, the harsh and fluctuating abiotic conditions made a macroscopic physiology advantageous, perhaps necessary, for collective survival. This caused population‐wide group viability selection, whereby non‐altruist ‘cheat’ genotypes killed the groups they were in, and therefore themselves, by reaching fixation. Furthermore, dispersal between refugia would reach zero under anything near a ‘hard snowball’, which would protect altruists at high local frequency from the influx of cheats from neighbouring groups. We illustrate our hypothesis analytically and with a simple spatial model. We show how removal of between‐group dispersal, in a population with initial between‐group variation in cheat frequency, causes the relative frequency of altruists to increase while the population as a whole decreases in size, as a result of group death caused by cheat invasion. This may be of particular relevance to animal multicellularity because irreversible differentiation (highly altruistic in that it imposes a high fitness cost on the individual cell) is more prevalent than in other multicellular eukaryotes. The relevance of our hypothesis should be scaled by any future consensus on the severity of snowball Earth, but it is theoretically plausible that global‐scale glaciations had a systematic influence on the level of selection during Earth history.     

Altruism and organism: disentangling the themes of multilevel selection theory

The evolution of groups into adaptive units, similar to single organisms in the coordination of their parts, is one major theme of multilevel selection theory. Another major theme is the evolution of altruistic behaviors that benefit others at the expense of self. These themes are often assumed to be strongly linked, such that altruism is required for group-level adaptation. Multilevel selection theory reveals a more complex relationship between the themes of altruism and organism. Adaptation at every level of the biological hierarchy requires a corresponding process of natural selection, which includes the fundamental ingredients of phenotypic variation, heritability, and fitness consequences. These ingredients can exist for many kinds of groups and do not require the extreme genetic variation among groups that is usually associated with the evolution of altruism. Thus, it is reasonable to expect higher-level units to evolve into adaptive units with respect to specific traits, even when their members are not genealogically related and do not behave in ways that are obviously altruistic. As one example, the concept of a group mind, which has been well documented in the social insects, may be applicable to other species.     

A new test for detecting ongoing selection

Much effort has been made to search for signatures of past natural selection in DNA sequences. However, currently acting selection is rarely detected in natural populations because of its rarity, low detection power of available methods, or both. Here, we develop a new test to detect viability selection over a single generation. In this test, one specific type of chromosomes is chosen as a reference, while all other chromosomes are designated as "focal". The test compares measures of variation between two groups of "focal" chromosomes: those found in reference/focal heterozygous individuals and those found in focal/focal homozygous individuals. In the absence of selection, we do not expect differences between these two groups as long as mating is random. On the other hand, currently acting selection can cause differences in some measures of variation. We applied this test to typing data for In(2L)t inversion polymorphism in a Drosophila melanogaster population, using "standard" (non-inverted) chromosomes as the focal class. Although the frequencies of In(2L)t and standard chromosomes did not deviate from the Hardy-Weinberg equilibrium, we found differences in allele frequency and the number of haplotypes between the two groups of standard chromosomes. This new test, in conjunction with the Hardy-Weinberg test, may shed light on how often strong selection is operating in extant populations.