Inclusive fitness,asymmetric competition and kin selection in plants

The findings that some plants alter their competitive phenotype in response to genetic relatedness of its conspecific neighbour (and presumed competitor) has spurred an increasing interest in plant kin‐interactions. This phenotypic response suggests the ability to assess the genetic relatedness of conspecific competitors, proposing kin selection as a process that can influence plant competitive interactions. Kin selection can favour restrained competitive growth towards kin, if the fitness loss from reducing own growth is compensated by increased fitness in the related neighbour. This may lead to positive frequency dependency among related conspecifics with important ecological consequences for species assemblage and coexistence. However, kin selection in plants is still controversial. First, many studies documenting a plastic response to neighbour relatedness do not estimate fitness consequences of the individual that responds, and when estimated, fitness of individuals grown in competition with kin did not necessarily exceed that of individuals grown in non‐kin groups. Although higher fitness in kin groups could be consistent with kin selection, this could also arise from mechanisms like asymmetric competition in the non‐kin groups. Here we outline the main challenges for studying kin selection in plants taking genetic variation for competitive ability into account. We emphasize the need to measure inclusive fitness in order to assess whether kin selection occurs, and show under which circumstances kin selected responses can be expected. We also illustrate why direct fitness estimates of a focal plant, and group fitness estimates are not suitable for documenting kin selection. Importantly, natural selection occurs at the individual level and it is the inclusive fitness of an individual plant – not the mean fitness of the group – that can capture if a differential response to neighbour relatedness is favoured by kin selection.     

Kin selection in Columbian ground squirrels: direct and indirect fitness benefits

Empirical and theoretical studies have supported kin selection by demonstrating nepotism or modelling its conditions and consequences. As an alternative, we previously found that female Columbian ground squirrels had greater direct fitness when more close kin were present. Extending those results, we used population matrix methods to calculate minimum estimates of individual fitness, estimated direct and indirect components of fitness, estimated inclusive fitness by adding the direct fitness (stripped of estimated influences of the social environment) and indirect fitness components together, and finally looked for inclusive fitness benefits of associations with close kin who seem to be 'genial neighbours'. We examined the estimated fitness of a sample of 35 females for which complete lifetimes were known for themselves, their mothers and their littermate sisters. Six of these females had no cosurviving adult close kin, and their direct fitness was significantly lower than 29 females with such kin (λ = 0.66 vs. λ = 1.23). The net fitness benefit of the presence of close kin was thus 0.57. The estimated indirect component of fitness through benefits to the direct fitness of close kin was 0.43. Thus, estimated inclusive fitness for females with cosurviving close kin (λ = 1.09) was significantly greater than that for females without surviving close kin (viz., λ = 0.66). The presence of closely related and philopatric female kin appeared to result in considerable fitness benefits for female ground squirrels, perhaps through the behavioural mechanisms of lowered aggression and other forms of behavioural cooperation.     

ON MULTILEVEL SELECTION AND KIN SELECTION: CONTEXTUAL ANALYSIS MEETS DIRECT FITNESS

When Hamilton defined the concept of inclusive fitness, he specifically was looking to define the fitness of an individual in terms of that individual's behavior, and the effects of its’ behavior on other related individuals. Although an intuitively attractive concept, issues of accounting for fitness, and correctly assigning it to the appropriate individual make this approach difficult to implement. The direct fitness approach has been suggested as a means of modeling kin selection while avoiding these issues. Whereas Hamilton's inclusive fitness approach assigns to the focal individual the fitness effects of its behavior on other related individuals, the direct fitness approach assigns the fitness effects of other actors to the focal individual. Contextual analysis was independently developed as a quantitative genetic approach for measuring multilevel selection in natural populations. Although the direct fitness approach and contextual analysis come from very different traditions, both methods rely on the same underlying equation, with the primary difference between the two approaches being that the direct fitness approach uses fitness optimization modeling, whereas with contextual analysis, the same equation is used to solve for the change in fitness associated with a change in phenotype when the population is away from the optimal phenotype.     

Growing with siblings: a common ground for cooperation or for fiercer competition among plants?

Recent work has shown that certain plants can identify their kin in competitive settings through root recognition, and react by decreasing root growth when competing with relatives. Although this may be a necessary step in kin selection, no clear associated improvement in individual or group fitness has been reported to qualify as such. We designed an experiment to address whether genetic relatedness between neighbouring plants affects individual or group fitness in artificial populations. Seeds of Lupinus angustifolius were sown in groups of siblings, groups of different genotypes from the same population and groups of genotypes from different populations. Both plants surrounded by siblings and by genotypes from the same population had lower individual fitness and produced fewer flowers and less vegetative biomass as a group. We conclude that genetic relatedness entails decreased individual and group fitness in L. angustifolius. This, together with earlier work, precludes the generalization that kin recognition may act as a widespread, major microevolutionary mechanism in plants.     

Reduced plant competition among kin can be explained by Jensen's inequality

Plants often compete with closely related individuals due to limited dispersal, leading to two commonly invoked predictions on competitive outcomes. Kin selection, from evolutionary theory, predicts that competition between relatives will likely be weaker. The niche partitioning hypothesis, from ecological theory, predicts that competition between close relatives will likely be stronger. We tested for evidence consistent with either of these predictions by growing an annual legume in kin and nonkin groups in the greenhouse. We grew plant groups in treatments of symbiotic nitrogen fixing bacteria differing in strain identity and composition to determine if differences in the microbial environment can facilitate or obscure plant competition patterns consistent with kin selection or niche partitioning. Nonkin groups had lower fitness than expected, based on fitness estimates of the same genotypes grown among kin. Higher fitness among kin groups was observed in mixtures of N‐fixing bacteria strains compared to single inoculations of bacteria strains present in the soil, which increased fitness differences between kin and nonkin groups. Lower fitness in nonkin groups was likely caused by increased competitive asymmetry in nonkin groups due to genetic differences in plant size combined with saturating relationships with plant size and fitness‐ i.e. Jensen's inequality. Our study suggests that microbial soil symbionts alter competitive dynamics among kin and nonkin. Our study also suggests that kin groups can have higher fitness, as predicted by kin selection theory, through a commonly heritable trait (plant size), without requiring kin recognition mechanisms.     

Why do Hymenopteran workers drift to non-natal groups? Generalized reciprocity and the maximization of group and parental success

Eusocial Hymenoptera are often characterized by having facultatively or obligately sterile worker castes. However, findings across an increasing number of species are that some workers are non-natal—they have ‘drifted’ away from where they were born and raised. Moreover, drifters are often indistinguishable from natal workers in the work and benefits provided to joined groups. This seems an evolutionary paradox of providing benefits to potentially unrelated individuals over close kin. Rather than being mistakes, drifting is proposed to be adaptive if joiners either gain inclusive fitness by preferentially moving to other kin groups or through generalized reciprocity in which exchanging workers across groups raises group-level genetic diversity and creates social heterosis. It is unclear, however, if reciprocity is unlikely because of a susceptibility to cheating. In resolving this question, a series of evolutionary simulations show: (1) Reciprocity can persist under a range of genetic assumptions and scenarios of cheating, (2) cheating almost always evolves, but can be expressed in a variety of ways that are not always predictable, (3) the inclusive fitness hypothesis is equally or more susceptible to cheating. Moreover, existing data in Hymenoptera (although not extensive) are more consistent with generalized reciprocity. This supports a hypothesis that drifting, as a phenomenon, may more often reflect maximization of group and parental fitness rather than fitness gains for the individual drifters.     

Partitioning of covariance as a method for studying kin selection

Covariance models of selection predict gene frequency change in terms of the relationship between the fitness of an individual and its phenotype, and therefore provide a convenient method for studying evolution in natural systems. When these models are partitioned into effects acting within and between hierarchical levels of selection, they can be directly applied to questions of kin selection. In many cases, the partitioning of covariance approach to the study of kin selection is a more useful alternative to the traditional hamiltonian or inclusive fitness approach.     

The fitness consequences of kin-biased dispersal in a cooperatively breeding bird

Cooperative alliances among kin may not only lead to indirect fitness benefits for group-living species, but can also provide direct benefits through access to mates or higher social rank. However, the immigrant sex in most species loses any potential benefits of living with kin unless immigrants disperse together or recruit relatives into the group in subsequent years. To look for evidence of small subgroups of related immigrants within social groups (kin substructure), we used microsatellites to assess relatedness between immigrant females of the cooperatively breeding superb starling, Lamprotornis superbus. We determined how timing of immigration led to kin subgroup formation and if being part of one influenced female fitness. Although mean relatedness in groups was higher for males than females, 26% of immigrant females were part of a kin subgroup with a sister. These immigrant sibships formed through kin recruitment across years more often than through coalitions immigrating together in the same year. Furthermore, females were more likely to breed when part of a kin subgroup than when alone, suggesting that female siblings form alliances that may positively influence their fitness. Ultimately, kin substructure should be considered when determining the role of relatedness in the evolution of animal societies.     

Female Bechstein's Bats Share Foraging Sites with Maternal Kin but do not Forage Together with them – Results from a Long‐Term Study

In many social animals, group members exchange information about where to feed. Thereby, they may gain direct benefits, for example, if social hunting enhances individual foraging success. Alternatively, individuals may receive indirect fitness benefits by preferentially sharing information about suitable feeding sites with kin. Indeed, in some species, a positive correlation between the degree of relatedness among individuals and the overlap among their foraging areas was found. However, sharing foraging sites with kin can also have costs if it increases food competition, which is not compensated by direct benefits. The goal of this study was to investigate whether sharing of individual foraging areas in female Bechstein's bats is best explained by kin selection or by direct benefits through social foraging. To assess their individual foraging behaviour, we analysed radio‐tracking data of 22 members of one maternity colony, including nine mother–daughter pairs, seven pairs of less closely related individuals and six pairs of unrelated bats. We examined the bats' fidelity to specific foraging areas during several years and quantified the influence of kinship on the overlap among individual foraging areas. By measuring how close to each other the bats foraged, we assessed whether individuals with overlapping areas are likely to forage together. Our study confirms previous findings that Bechstein's bats show high fidelity to foraging areas across years. Moreover, we found that relatives share foraging areas significantly more often compared with unrelated colony members. Finally, our data reveal for the first time that most colony members that share foraging areas are unlikely to forage together. This suggests that female Bechstein's bats gain no direct benefits from sharing foraging areas with members of the same maternal lineage. Our findings also have implications for conservation as habitat loss within a colony's home range might expose entire matrilines to high risks.     

The role of kin recognition in the evolution of conspecific brood parasitism

Conspecific brood parasitism (CBP) is a common strategy in several species of birds. Currently, some studies suggest that relatedness between host and parasite enhances CBP, since indirect fitness benefits could select for acceptance of related eggs by hosts. Conversely, parasites should avoid laying eggs in nests of relatives if this is costly for the host. Based on the latter argument, kinship should not promote brood parasitism. A recent model clarified this relationship, and showed that kinship can promote brood parasitism, assuming kin recognition. However, in that model kin recognition was assumed perfect. Here we present a model that addresses the role of relatedness and kin selection in CBP, when kin recognition is not perfect and hosts do not always detect parasitism. We consider both the indirect fitness of the parasite and the possible responses of the host. Our results indicate that the existence and accuracy of a kin recognition system is crucial to the final outcome. When CBP represents a cost to the host, a parasitic female that has the choice should avoid parasitizing relatives, unless (1) the costs are not too high and (2) hosts can accurately enough recognize eggs laid by relatives, rejecting them less often than eggs laid by nonkin. But if ‘parasitism’ enhances the direct fitness of the host (which is possible in species with precocial young) parasites should choose relatives whenever possible, even if hosts do not recognize kin eggs. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Kinship reinforces cooperative predator inspection in a cichlid fish

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.     

Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines

Since Darwin ( 1859 ), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's ( 1964 ) theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, 2007 ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, 1998 ; Heinsohn, 2004 ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, 2012 ).     

Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin

Kin selection predicts that helpers in cooperative systems should preferentially aid relatives to maximize fitness. In family-based groups, this can be accomplished simply by assisting all group members. In more complex societies, where large numbers of kin and non-kin regularly interact, more sophisticated kin-recognition mechanisms are needed. Bell miners (Manorina melanophrys) are just such a system where individuals regularly interact with both kin and non-kin within large colonies. Despite this complexity, individual helpers of both sexes facultatively work harder when provisioning the young of closer genetic relatedness. We investigated the mechanism by which such adaptive discrimination occurs by assessing genetic kinship influences on the structure of more than 1900 provisioning vocalizations of 185 miners. These 'mew' calls showed a significant, positive linear increase in call similarity with increasing genetic relatedness, most especially in comparisons between male helpers and the breeding male. Furthermore, individual helping effort was more heavily influenced by call similarity to breeding males than to genetic relatedness, as predicted if call similarity is indeed the rule-of-thumb used to discriminate kin in this system. Individual mew call structure appeared to be inflexible and innate, providing an effective mechanism by which helpers can assess their relatedness to any individual. This provides, to our knowledge, the first example of a mechanism for fine-scale kin discrimination in a complex avian society.     

Kin discrimination in salmonids

Summary The data presented here suggest that significant selection pressures towards kin discrimination behaviour patterns result from kin-biased territorial defence behaviour patterns. Salmonids employ a phenotype matching recognition mechanism allowing individuals to discriminate unfamiliar kin. Kin discrimination abilities allow individuals to reduce the levels of aggression associated with territorial defence towards related conspecifics and to defend smaller territories near kin versus non-kin. This kin-biased territorial defence behaviour is observed in at least one species under a wide range of territorial quality conditions. Within kin groups, subordinate individuals obtain a greater number of foraging attempts, resulting in kin-biased foraging within the social group. As a result of this kin-bias, individuals within kin groups show significantly higher mean weight increases (increased direct fitness benefits) and reduced variance in these increases (increased indirect benefits). Since all individuals within the kin groups obtained higher, less variable weight increases, we can argue that individuals are increasing their inclusive fitness as a result of these kin-biased behaviour patterns.Based on these results, and on what is known about the life history of a variety of salmonid and non-salmonid species, we can formulate a number of testable predictions. By testing these predictions, we may be better able to understand both the proximate and ultimate causation of kin discrimination abilities in a variety of fishes.     

EVOLUTIONARY GAMES IN WRIGHT'S ISLAND MODEL: KIN SELECTION MEETS EVOLUTIONARY GAME THEORY

This article studies evolutionary game dynamics in Wright's infinite island model. I study a general n×n matrix game and derive a basic equation that describes the change in frequency of strategies. A close observation of this equation reveals that three distinct effects are at work: direct benefit to a focal individual, kin‐selected indirect benefit to the focal individual via its relatives, and the cost caused by increased kin competition in the focal individual's natal deme. Crucial parameters are the coefficient of relatedness between two individuals and its analogue for three individuals. I provide a number of examples and show when the traditional inclusive fitness measure is recovered and when not. Results demonstrate how evolutionary game theory fits into the framework of kin selection.     

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.     

Are flies kind to kin? The role of intra- and inter-sexual relatedness in mediating reproductive conflict

As individual success often comes at the expense of others, interactions between the members of a species are frequently antagonistic, especially in the context of reproduction. In theory, this conflict may be reduced in magnitude when kin interact, as cooperative behaviour between relatives can result in increased inclusive fitness. Recent tests of the potential role of cooperative behaviour between brothers in Drosophila melanogaster have proved to be both exciting and controversial. We set out to replicate these experiments, which have profound implications for the study of kin selection and sexual conflict, and to expand upon them by also examining the potential role of kinship between males and females in reproductive interactions. While we did observe reduced fighting and courtship effort between competing brothers, contrary to previous studies we did not detect any fitness benefit to females as a result of the modification of male antagonistic behaviours. Furthermore, we did not observe any differential treatment of females by their brothers, as would be expected if the intensity of sexual conflict was mediated by kin selection. In the light of these results, we propose an alternative explanation for observed differences in male–male conflict and provide preliminary empirical support for this hypothesis.     

Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius)

Parental care should evolve only if fitness benefits exceed fitness costs. In Cheirogaleus medius, a small nocturnal lemur of western Madagascar, we found the peculiar situation of considerable parental care by both sexes, combined with an extremely high rate of extra-pair young (EPY). In this paper, we try to elucidate the costs and benefits of parental care in C. medius, and we discuss hypotheses as to why males might actively participate in raising young, especially with regard to the high rate of EPY. The study was carried out in the dry deciduous forest of western Madagascar between 1996 and 2001. The most important components of parental care in C. medius are babysitting and guarding of the young. Observational data suggest that thermoregulatory demands during the first days after birth and defence from predators may be the driving factors selecting for this infant care behaviour. The reproducing individuals of both sexes incur considerable energetic costs by this behaviour, resulting in reduced fat stores and body condition in comparison to non-reproducing individuals. The reason why males also care for EPY remains elusive. We propose that males might not be able to detect individual relatedness and that they would jeopardise the survival of their own young if they gave no parental care. Alternatively, they might gain advantages other than direct fitness from raising EPY, for example if caring behaviour increases their chances in further reproduction, or if EPY are fathered by close kin.     

Dynamic-persistence of cooperation in public good games when group size is dynamic

The evolution of cooperation is possible with a simple model of a population of agents that can move between groups. The agents play public good games within their group. The relative fitness of individuals within the whole population affects their number of offspring. Groups of cooperators evolve but over time are invaded by defectors which eventually results in the group's extinction. However, for small levels of migration and mutation, high levels of cooperation evolve at the population level. Thus, evolution of cooperation based on individual fitness without kin selection, indirect or direct reciprocity is possible. We provide an analysis of the parameters that affect cooperation, and describe the dynamics and distribution of population sizes over time.