Kin selection,kin avoidance and correlated strategies

Summary Kin selection of correlated strategies is examined for both weak and strong altruism under simple haploid inheritance. While kin assortment enhances the range of evolutionary stability for (strongly altruistic) correlated strategies (defined herein), kin avoidance is possible under a weakly altruistic correlated strategy. When social competition induces role assignments of variable fitness, group mates may prefer association with non-relatives. Even when group life is mandatory, an individual may accept the risk of abandonment (and reproductive death) rather then associate with kin: a competitive superior may behave altruistically by permitting competitively inferior kin to emigrate. Thus, kin selection and social competition are not necessarily mutually supportive processes within groups. I conclude by interpreting dominance as a strongly altruistic correlated strategy in two social hymenopteran contexts.     

Kinship,parental manipulation and evolutionary origins of eusociality

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.     

Direct fitness for dynamic kin selection

The direct-fitness approach to modelling the evolution of social traits is an alternative to the classical inclusive-fitness-based approach. Despite both its utility and popularity, the direct-fitness approach has not yet been extended to include the analysis of dynamic traits, i.e. traits whose level of expression may vary over time. In this article, I apply the direct-fitness approach to cope with the evolution of a dynamic resource-allocation behaviour when this behaviour influences the fitness of relatives. I am able to implement the direct-fitness approach using components (reproductive value, fitness changes and measures of relatedness) found in standard, social-evolutionary models. I illustrate the modified direct-fitness model with an example studied by previous authors, and I show how the direct-fitness perspective can aid the validation of analytical results by means of a genetic algorithm.     

The joint effects of kin, multilevel selection and indirect genetic effects on response to genetic selection

Kin and levels-of-selection models are common approaches for modelling social evolution. Indirect genetic effect (IGE) models represent a different approach, specifying social effects on trait values rather than fitness. We investigate the joint effect of relatedness, multilevel selection and IGEs on response to selection. We present a measure for the degree of multilevel selection, which is the natural partner of relatedness in expressions for response. Response depends on both relatedness and the degree of multilevel selection, rather than only one or the other factor. Moreover, response is symmetric in relatedness and the degree of multilevel selection, indicating that both factors have exactly the same effect. Without IGEs, the key parameter is the product of relatedness and the degree of multilevel selection. With IGEs, however, multilevel selection without relatedness can explain evolution of social traits. Thus, next to relatedness and multilevel selection, IGEs are a key element in the genetical theory of social evolution.     

Lifetime monogamy and the evolution of eusociality

All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton''s rule (br_s > r_oc), but implies that relatedness cancels out of the equation because average relatedness to siblings (r_s) and offspring (r_o) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton''s rule.     

Implicit frequency dependence and kin selection in fluctuating environments

Summary I consider a general model of a fluctuating environment in which the environmental state each year is drawn at random from some given distribution. Each year organisms must choose what action to perform before the environmental state for that year is known. There is no interaction with kin. In this scenario, natural selection will tend to produce organisms which maximize their geometric mean fitness. In this paper I introduce the idea of the profile of a strategy. This function quantifies how the strategy peforms for each environmental state. I show that there is a unique profile such that a strategy is optimal if and only if it has this profile. I then give a characterization of the optimal profile which generalizes previous work by others in this area. The characterization of the optimal profile has a game theoretical interpretation. Motivated by this I introduce a game in which individuals play the field in a constant environment. This game may be interpreted as a cooperative game between kin. The key result of this paper shows that a strategy maximizes geometric mean fitness in the original fluctuating environment problem if and only if it is an evolutionarily stable strategy of the deterministic environment game. It is well known that an optimal strategy in a fluctuating environment may be mixed, involving adaptive coin-flipping. Others have previously noted that this may result in some individuals sacrificing individual reproductive success for the good of the genotype. My analysis shows that one may regain the concept of individual optimization if the quantity maximized is suitably defined. Under an optimal strategy every action taken maximizes the expected number of offspring produced, where this expectation is not calculated using the true distribution of environmental states, but a distribution modified to take account of the actions of kin.     

Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies

It is difficult to imagine how warning colours evolve in unpalatable prey. Firstly, novel warningly coloured variants gain no protection from their colours, since predators have not previously encountered and learnt their colour patterns. This leads to a frequency-dependent disadvantage of a rare variant within a species. Secondly, novel warningly coloured variants may be more conspicuous than non-aposematic prey.
Nevertheless, it is obvious that many palatable butterflies have bright colours used in intraspecific communication and in duping predators. Other palatable butterflies are already warningly coloured. Should such butterflies evolve unpalatability, perhaps because of a host-plant shift, these bright colours would be preadapted to a warning role. Warning colours could then continue to evolve by enhancement of memorable characteristics of these patterns, or by mimicry.
Even within lineages of warningly coloured, unpalatable butterflies, colour patterns have continued to evolve rapidly. This diversity of warning colour patterns could have evolved in a number of ways, including individual and kin selection, and by the shifting balance. Evidence for these mechanisms is discussed, as are the similarities between the evolution of warning colours and more general evolutionary processes, including sexual selection and speciation.     

Indirect genetic effects and kin recognition: estimating IGEs when interactions differ between kin and strangers

Social interactions among individuals are widespread, both in natural and domestic populations. As a result, trait values of individuals may be affected by genes in other individuals, a phenomenon known as indirect genetic effects (IGEs). IGEs can be estimated using linear mixed models. The traditional IGE model assumes that an individual interacts equally with all its partners, whether kin or strangers. There is abundant evidence, however, that individuals behave differently towards kin as compared with strangers, which agrees with predictions from kin-selection theory. With a mix of kin and strangers, therefore, IGEs estimated from a traditional model may be incorrect, and selection based on those estimates will be suboptimal. Here we investigate whether genetic parameters for IGEs are statistically identifiable in group-structured populations when IGEs differ between kin and strangers, and develop models to estimate such parameters. First, we extend the definition of total breeding value and total heritable variance to cases where IGEs depend on relatedness. Next, we show that the full set of genetic parameters is not identifiable when IGEs differ between kin and strangers. Subsequently, we present a reduced model that yields estimates of the total heritable effects on kin, on non-kin and on all social partners of an individual, as well as the total heritable variance for response to selection. Finally we discuss the consequences of analysing data in which IGEs depend on relatedness using a traditional IGE model, and investigate group structures that may allow estimation of the full set of genetic parameters when IGEs depend on kin.     

Fitness consequences of plants growing with siblings: reconciling kin selection, niche partitioning and competitive ability

Plant studies that have investigated the fitness consequences of growing with siblings have found conflicting evidence that can support different theoretical frameworks. Depending on whether siblings or strangers have higher fitness in competition, kin selection, niche partitioning and competitive ability have been invoked. Here, we bring together these processes in a conceptual synthesis and argue that they can be co-occurring. We propose that these processes can be reconciled and argue for a trait-based approach of measuring natural selection instead of the fitness-based approach to the study of sibling competition. This review will improve the understanding of how plants interact socially under competitive situations, and provide a framework for future studies.     

Social semantics: toward a genuine pluralism in the study of social behaviour

Pluralism is the coexistence of equivalent theoretical frameworks, either because they are historically entrenched or because they achieve separate insights by viewing the same process in different ways. A recent article by West et al. [Journal of Evolutionary Biology (2007) vol. 20, 415-432] attempts to classify the many equivalent frameworks that have been developed to study the evolution of social behaviour. This article addresses shortcomings in the West et al.'s article, especially with respect to multilevel selection, in a common effort to maximize the benefits of pluralism while minimizing the semantic costs.     

Natural selection. III. Selection versus transmission and the levels of selection

George Williams defined an evolutionary unit as hereditary information for which the selection bias between competing units dominates the informational decay caused by imperfect transmission. In this article, I extend Williams' approach to show that the ratio of selection bias to transmission bias provides a unifying framework for diverse biological problems. Specific examples include Haldane and Lande's mutation-selection balance, Eigen's error threshold and quasispecies, Van Valen's clade selection, Price's multilevel formulation of group selection, Szathmáry and Demeter's evolutionary origin of primitive cells, Levin and Bull's short-sighted evolution of HIV virulence, Frank's timescale analysis of microbial metabolism and Maynard Smith and Szathmáry's major transitions in evolution. The insights from these diverse applications lead to a deeper understanding of kin selection, group selection, multilevel evolutionary analysis and the philosophical problems of evolutionary units and individuality.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Group stability and homing behavior but no kin group structures in a coral reef fish

Understanding the reasons behind stable group formations hasreceived considerable theoretical and empirical attention. Stablegroups displaying homing behavior have been suggested to formas a result of, for instance, benefits from knowledge of thesocial or physical environment or through kin selection andthe forming of kin groups. However, no one has disentangledpreference for grouping in a familiar location from preferencefor grouping with familiar or related individuals. To investigatethis, we conducted a series of field experiments and a groupgenetic analysis on the group-living Banggai cardinalfish (Pterapogonkauderni). We found homing behavior but no evidence for recognitionof familiar group members. Instead, homing was based on theoriginal location of their group rather than the individualsin that group. Moreover, we found no evidence for kin structureswithin these groups. We suggest that benefits from living ina known social environment drive homing behavior in this speciesand that homing behavior is not enough for the formation ofkin group structures. Instead, our results suggest that kinrecognition may be a prerequisite for the forming of kin groups.     

Selective pressures for accurate altruism targeting: evidence from digital evolution for difficult-to-test aspects of inclusive fitness theory

Inclusive fitness theory predicts that natural selection will favour altruist genes that are more accurate in targeting altruism only to copies of themselves. In this paper, we provide evidence from digital evolution in support of this prediction by competing multiple altruist-targeting mechanisms that vary in their accuracy in determining whether a potential target for altruism carries a copy of the altruist gene. We compete altruism-targeting mechanisms based on (i) kinship (kin targeting), (ii) genetic similarity at a level greater than that expected of kin (similarity targeting), and (iii) perfect knowledge of the presence of an altruist gene (green beard targeting). Natural selection always favoured the most accurate targeting mechanism available. Our investigations also revealed that evolution did not increase the altruism level when all green beard altruists used the same phenotypic marker. The green beard altruism levels stably increased only when mutations that changed the altruism level also changed the marker (e.g. beard colour), such that beard colour reliably indicated the altruism level. For kin- and similarity-targeting mechanisms, we found that evolution was able to stably adjust altruism levels. Our results confirm that natural selection favours altruist genes that are increasingly accurate in targeting altruism to only their copies. Our work also emphasizes that the concept of targeting accuracy must include both the presence of an altruist gene and the level of altruism it produces.     

Why male butterflies are non-mimetic: natural selection,sexual selection,group selection,modification and sieving*

Thomas Belt suggested that the frequent limitation of mimicry in butterflies to the female resulted from sexual selection. Because female butterflies store sperm they can be fully fertile after only one mating; the reproductive success of a male is proportional to the number of times he mates. Sexual selection is therefore much stronger in males than females, with selection coefficients being greater by a small multiple of the number of times a female is courted during her life (long-lived species) or of the reciprocal of the female mortality rate between courtships (short-lived species). As butterflies of both sexes respond to colour when courting, sexual selection resists colour changes especially strongly in males. As a result, genes conferring new mimetic colour patterns can often become established in a butterfly population much more readily if their expression is initially limited to females; when the population size of a Batesian mimic, its model, and its predator fluctuates, such sex-limited genes have an enhanced probability of ultimate fixation in the population, and a reduced chance of loss; this effect is accentuated by the selection of modifiers which improve the mimicry. When the establishment of unimodal mimicry (expressed in both sexes) is favoured in a Batesian mimic, the gene tends to rise to an equilibrium frequency at which modifiers suppressing the expression of the mimicry only in males and'modifiers enhancing the mimicry only in females are favoured. The outcome is female-limited mimicry, or unimodal mimicry with better mimicry in the females, the males either retaining some of their sexual colour or the selective behaviour of the females becoming altered. In a Muellerian mimic there is no such equilibrium and selection ultimately favours expression of mimicry in both sexes and an appropriate alteration in the courtship responses. Hence Muellerian mimicry is seldom female-limited. Exceptional cases appear to result from the sexes flying in separate habitats. The genetical evidence in Papilio and Heliconius favours initial limitation of expression over subsequent modification as the usual basis for female-limited mimicry. Other explanations of female-limited mimicry can be found wanting in various ways; a higher predation rate on females could produce sex-limitation, but is probably not a strong factor. But the greater variability of the female in Lepidoptera may indicate lesser developmental stability, which could result in greater penetrance of mutants in the female, and hence account for the initial female-limitation. At very high densities of a mimetic species which has no non-mimetic form, mimicry tends to deteriorate more rapidly in a unimodal than in an otherwise identical sex-limited species. Although by itself this would equally favour male-limitation, and hence cannot explain the predominance of female-limitation, this effect may over evolutionary time be causing a slight increase in the proportion of sex-limited species among mimics. The stability of some mimetic polymorphisms is investigated by linear approximation: in some instances a stable equilibrium can be changed into an oscillating equilibrium by changes in the population size.     

Sex ratios, local fitness enhancement and eusociality in the allodapine bee Exoneura richardsoni

Previous studies of a facultatively eusocial allodapine bee, Exoneura richardsoni Rayment, indicated that high levels of cooperative nesting among close relatives seem to be maintained by benefits that lead to increases in per capita brood production. These traits could lead to local fitness enhancement, which in turn could select for female-biased sex ratios. We show here that sex investment ratios in this species are female-biased in small colony sizes, becoming progressively male-biased in larger colonies, consistent with expectations for local fitness enhancement, but not explainable by alternative models. Our results support previous suggestions that local fitness enhancement can lead to sex ratio bias in primitively social Hymenoptera, but differ from previous studies by suggesting that patterns of bias could lower selective thresholds for sib-directed altruism in small colonies, but have an opposing effect in large colonies.     

Benefits of foundress associations in the paper wasp Polistes dominulus: increased productivity and survival, but no assurance of fitness returns

Successful Polistes dominulus nests can be started by one ormore nest founding queens (foundresses). Consequently, thereis much interest in the specific benefits that induce cooperationamong foundresses. Here, we experimentally demonstrate one majorbenefit of cooperation, namely that multiple foundresses increasecolony productivity. This increase is close to the value predictedby subtracting the productivity of undisturbed single-foundresscolonies from the productivity of undisturbed multiple-foundresscolonies. However, we found no evidence that an associatingfoundress' contribution to colony growth is preserved if shedisappears (assured fitness returns). Our correlational datasuggest that cooperation provides survival benefits, multiple-foundresscolonies are more likely to survive to produce offspring thanare single-foundress colonies, and individual foundresses inmultiple-foundress groups are less likely to disappear beforeworker emergence than foundresses nesting alone. Therefore,association provides substantial productivity and survival benefitsfor cooperating foundresses.     

Demography and the tragedy of the commons

Individual success in group‐structured populations has two components. First, an individual gains by outcompeting its neighbours for local resources. Second, an individual's share of group success must be weighted by the total productivity of the group. The essence of sociality arises from the tension between selfish gains against neighbours and the associated loss that selfishness imposes by degrading the efficiency of the group. Without some force to modulate selfishness, the natural tendencies of self interest typically degrade group performance to the detriment of all. This is the tragedy of the commons. Kin selection provides the most widely discussed way in which the tragedy is overcome in biology. Kin selection arises from behavioural associations within groups caused either by genetical kinship or by other processes that correlate the behaviours of group members. Here, I emphasize demography as a second factor that may also modulate the tragedy of the commons and favour cooperative integration of groups. Each act of selfishness or cooperation in a group often influences group survival and fecundity over many subsequent generations. For example, a cooperative act early in the growth cycle of a colony may enhance the future size and survival of the colony. This time‐dependent benefit can greatly increase the degree of cooperation favoured by natural selection, providing another way in which to overcome the tragedy of the commons and enhance the integration of group behaviour. I conclude that analyses of sociality must account for both the behavioural associations of kin selection theory and the demographic consequences of life history theory.