Extending the range of additivity in using inclusive fitness

Inclusive fitness is a concept widely utilized by social biologists as the quantity organisms appear designed to maximize. However, inclusive fitness theory has long been criticized on the (uncontested) grounds that other quantities, such as offspring number, predict gene frequency changes accurately in a wider range of mathematical models. Here, we articulate a set of modeling assumptions that extend the range of scenarios in which inclusive fitness can be applied. We reanalyze recent formal analyses that searched for, but did not find, inclusive fitness maximization. We show (a) that previous models have not used Hamilton''s definition of inclusive fitness, (b) a reinterpretation of Hamilton''s definition that makes it usable in this context, and (c) that under the assumption of probabilistic mixing of phenotypes, inclusive fitness is indeed maximized in these models. We also show how to understand mathematically, and at an individual level, the definition of inclusive fitness, in an explicit population genetic model in which exact additivity is not assumed. We hope that in articulating these modeling assumptions and providing formal support for inclusive fitness maximization, we help bridge the gap between empiricists and theoreticians, which in some ways has been widening, demonstrating to mathematicians why biologists are content to use inclusive fitness, and offering one way to utilize inclusive fitness in general models of social behavior.     

Evolution of helping and harming in heterogeneous populations

There has been much interest in understanding how demographic factors can mediate social evolution in viscous populations. Here, we examine the impact of heterogeneity in patch quality--that is, the availability of reproductive resources for each breeder--upon the evolution of helping and harming behaviors. We find that, owing to a cancellation of relatedness and kin competition effects, the evolution of obligate and facultative helping and harming is not influenced by the degree of viscosity in populations characterized by either spatial or temporal heterogeneity in patch quality. However, facultative helping and harming may be favored when there is both spatial and temporal heterogeneity in patch quality, with helping and harming being favored in both high-quality and low-quality patches. We highlight the prospect for using kin selection theory to explain within-population variation in social behavior, and point to the need for further theoretical and empirical investigation of this topic.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.     

Nice natives and mean migrants: the evolution of dispersal-dependent social behaviour in viscous populations

There has been much interest in the evolution of social behaviour in viscous populations. While low dispersal increases the relatedness of neighbours, which tends to promote the evolution of indiscriminate helping behaviour, it can also increase competition between neighbours, which tends to inhibit the evolution of helping and may even favour harming behaviour. In the simplest scenario, these two effects exactly cancel, so that dispersal rate has no impact on the evolution of helping or harming. Here, we show that dispersal rate does matter when individuals can adjust their social behaviour conditional on whether they have dispersed or whether they have remained close to their place of origin. We find that nondispersing individuals are weakly favoured to indiscriminately help their neighbours, whereas dispersing individuals are more readily favoured to indiscriminately harm their neighbours.     

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.     

Direct vs. inclusive fitness in the evolution of aphid cornicle length

By comparing the relative sizes of anatomical structures among phenotypes, selective pressures that shape species' morphologies can be evaluated. Aphids emit droplets containing an alarm pheromone/defensive secretion from unique anatomical structures called cornicles, upon being attacked. As aphids live in colonies of high relatedness, it is uncertain whether direct or inclusive fitness benefits have chiefly promoted cornicle evolution. Morphological measurements for apterous parthenogen, alate parthenogen, female sexual and male sexual morphs of 43 species (21 genera, one subfamily) were assessed to distinguish between the hypotheses that: (1) cornicles evolved for mechanical defence against natural enemies (direct fitness); (2) cornicles evolved for alarm signalling (inclusive fitness); or (3) cornicle length has been largely constrained by flight aerodynamics. Our results generally support the inclusive fitness hypothesis; cornicle length decreases as the relative number and relatedness of offspring decreases. As cornicle length is greatest in apterous parthenogenetic morphs, inclusive fitness benefits of protecting highly related kin may have been a key factor selecting for cornicles, and increased cornicle length, in aphids.     

Extrapair paternity, inclusive fitness, and within-group benefits of helping in western bluebirds

In central coastal California, USA, 3–16% of western bluebird ( Sialia mexicana ) pairs have adult male helpers at the nest. Demographic data on a colour-ringed population over a 13-year period indicate that helpers gain a small indirect fitness benefit through increases in the number of young fledged from nests of close kin. A small proportion of adult helpers (16%) that were able to breed and help simultaneously had higher annual inclusive fitness than males that only bred. These males comprised such a minor proportion of helpers that the mean fitness of helpers was still lower than the mean fitness of independent breeders. We used DNA fingerprinting to determine whether extrapair fertilizations alter within-group benefits enough to tip the balance in favour of helping behaviour. Overall, 19% of 207 offspring were sired by males other than their social father and extrapair fertilizations occurred in 45% of 51 nests. Intraspecific brood parasitism was rare so that mean mother-nestling relatedness approximated the expected value of 0.5. Extrapair paternity reduced putative father-offspring relatedness to 0.38. Mean helper-nestling relatedness was 0.41 for helpers assisting one or both parents and 0.28 for helpers aiding their brothers. Helpers rarely sired offspring in the nests at which they helped. Helping was not conditional on paternity and helpers were not significantly more closely related to offspring in their parents' nests than to offspring in their own nests. Although helpers may derive extracurricular benefits if helping increases their own or their father's opportunities for extrapair fertilizations, within-nest inclusive fitness benefits of helping do not compensate males for failing to breed. Breeding failure and constraints on breeding are the most likely explanations for why most helpers help.     

Fine‐scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal

The relatedness structure of animal populations is thought to be a critically important factor underlying the evolution of mating systems and social behaviours. While previous work has shown that population structure is shaped by many biological processes, few studies have investigated how these factors vary over time. Consequently, we explored the fine‐scale spatiotemporal genetic structure of an intensively studied population of cooperatively breeding banded mongooses (Mungos mungo) over a 10‐year period. Overall population structure was strong (average F_ST = 0.129) but groups with spatially overlapping territories were not more genetically similar to one another than noncontiguous groups. Instead, genetic differentiation was associated with historical group‐fission (budding) events, with new groups diverging from their parent groups over time. Within groups, relatedness was high within but not between the sexes, although the latter increased over time since group formation due to group founders being replaced by philopatric young. This trend was not mirrored by a decrease in average offspring heterozygosity over time, suggesting that close inbreeding may often be avoided, even when immigration into established groups is virtually absent and opportunities for extra‐group matings are rare. Fine‐scale spatiotemporal population structure could have important implications in social species, where relatedness between interacting individuals is a vital component in the evolution of patterns of inbreeding avoidance, reproductive skew and kin‐selected helping and harming.     

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.     

Population demography and the evolution of helping behaviors

Limited dispersal may favor the evolution of helping behaviors between relatives as it increases their relatedness, and it may inhibit such evolution as it increases local competition between these relatives. Here, we explore one way out of this dilemma: if the helping behavior allows groups to expand in size, then the kin-competition pressure opposing its evolution can be greatly reduced. We explore the effects of two kinds of stochasticity allowing for such deme expansion. First, we study the evolution of helping under environmental stochasticity that may induce complete patch extinction. Helping evolves if it results in a decrease in the probability of extinction or if it enhances the rate of patch recolonization through propagules formed by fission of nonextinct groups. This mode of dispersal is indeed commonly found in social species. Second, we consider the evolution of helping in the presence of demographic stochasticity. When fecundity is below its value maximizing deme size (undersaturation), helping evolves, but under stringent conditions unless positive density dependence (Allee effect) interferes with demographic stochasticity. When fecundity is above its value maximizing deme size (oversaturation), helping may also evolve, but only if it reduces negative density-dependent competition.     

Natural selection. VI. Partitioning the information in fitness and characters by path analysis

Three steps aid in the analysis of selection. First, describe phenotypes by their component causes. Components include genes, maternal effects, symbionts and any other predictors of phenotype that are of interest. Second, describe fitness by its component causes, such as an individual's phenotype, its neighbours’ phenotypes, resource availability and so on. Third, put the predictors of phenotype and fitness into an exact equation for evolutionary change, providing a complete expression of selection and other evolutionary processes. The complete expression separates the distinct causal roles of the various hypothesized components of phenotypes and fitness. Traditionally, those components are given by the covariance, variance and regression terms of evolutionary models. I show how to interpret those statistical expressions with respect to information theory. The resulting interpretation allows one to read the fundamental equations of selection and evolution as sentences that express how various causes lead to the accumulation of information by selection and the decay of information by other evolutionary processes. The interpretation in terms of information leads to a deeper understanding of selection and heritability, and a clearer sense of how to formulate causal hypotheses about evolutionary process. Kin selection appears as a particular type of causal analysis that partitions social effects into meaningful components.     

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.     

Investment in the public good through conditional phenotypes of large effect

We investigate the evolution of an individual's willingness to invest in a public good (what we call, helping) in a patch‐structured population with limited natal dispersal. We assume that an individual's decision to invest is informed by its dispersal status: an individual makes one decision given it is native to the patch on which it breeds, and is free to make a different decision given that it is not native to the patch on which it breeds. Unlike previous work, we assume that investment in the public good, and the public good, itself, both have a large effect on individual fecundity. Kin selection analysis reveals that only extreme investment decisions (i.e. ‘always invest’ or ‘never invest’) can be evolutionarily stable. Numerical results suggest that the evolutionary instability of the ‘never invest’ phenotype (what we call, complete nonhelping) implies the evolutionary stability of ‘always invest’ (what we call, complete helping). In addition, numerical results show that bistability of extreme phenotypes is possible, indicating that the adaptive significance of altruism, in this context, is greater than has been previously recognized. Numerical results are supported by computer simulation, and results, themselves, are briefly discussed in a concluding section.     

Discovery of a large clonal patch of a social amoeba: implications for social evolution

Studies of genetic population structures of clonally reproducing macro-organisms have revealed large areas where only one clone is found. These areas, referred to as clonal patches, have not been shown to occur in free-living microbes until now. In free-living microbes, high genetic diversity at local scales is usually maintained by high rates of dispersal. We report, however, a highly dense, 12-m clonal patch of the social amoeba Dictyostelium discoideum in a cattle pasture located in a Texas Gulf Coast prairie. We confirm the presence of only one clone by the analysis of 65 samples and amplification of 10 polymorphic microsatellite loci. Samplings of additional cattle pastures nearby showed higher clonal diversity, but with a density of D. discoideum isolates lower than in the clonal patch. These findings show that high rates of microbial dispersal do not always produce genetic diversity at local scales, contrary to the findings of previous studies. The existence of clonal patches may be particularly important for microbial social evolution.     

The evolution of altruism: Correlation,cost, and benefit

A simple and general criterion is derived for the evolution of altruism when individuals interact in pairs. It is argued that the treatment of this problem in kin selection theory and in game theory are special cases of this general criterion.My thanks to James Crow, Carter Denniston, Lee Dugarkin, David Wilson, and an anonymous referee of this journal for helpful discussion.     

Sex differences in dispersal and the evolution of helping and harming

In this article, we explore the impact of sex-biased dispersal on local relatedness and on selection for helping and harming behavior among males and females. We show that in a patch-structured population, when there is a marked sex bias in dispersal, selection will almost always favor harming behavior among individuals of the sex more prone to dispersal. This result holds regardless of the effects of mating skew or overlapping generations. Selection may well also favor helping behavior among individuals of the philopatric sex, particularly if there is generational overlap, but this is less likely to occur if individuals of the philopatric sex compete more intensely for fewer breeding opportunities. In this last case, if generational overlap is low and mating skew pronounced, the result may be selection for harming behavior among both males and females. In general, the rate of dispersal and the level of relatedness among individuals of one sex do not reliably predict their level of helping or harming behavior; selection on either males or females depends on the dispersal of both sexes.     

Distinguishing four fundamental approaches to the evolution of helping

The evolution and stability of helping behaviour has attracted great research efforts across disciplines. However, the field is also characterized by a great confusion over terminology and a number of disagreements, often between disciplines but also along taxonomic boundaries. In an attempt to clarify several issues, we identify four distinct research fields concerning the evolution of helping: (1) basic social evolution theory that studies helping within the framework of Hamilton's inclusive fitness concept, i.e. direct and indirect benefits, (2) an ecological approach that identifies settings that promote life histories or interaction patterns that favour unconditional cooperative and altruistic behaviour, e.g. conditions that lead to interdependency or interactions among kin, (3) the game theoretic approach that identifies strategies that provide feedback and control mechanisms (protecting from cheaters) favouring cooperative behaviour (e.g. pseudo-reciprocity, reciprocity), and (4) the social scientists' approach that particularly emphasizes the special cognitive requirements necessary for human cooperative strategies. The four fields differ with respect to the 'mechanisms' and the 'conditions' favouring helping they investigate. Other major differences concern a focus on either the life-time fitness consequences or the immediate payoff consequences of behaviour, and whether the behaviour of an individual or a whole interaction is considered. We suggest that distinguishing between these four separate fields and their complementary approaches will reduce misunderstandings, facilitating further integration of concepts within and across disciplines.