Genetic variation in tolerance of competition and neighbour suppression in Arabidopsis thaliana

Intraspecific competitive interactions can profoundly influence phenotypic evolution. However, prior studies have rarely evaluated the evolutionary potential of the two components of competitive ability, tolerance of competition and suppression of neighbours. Here, we grow a set of 20 Arabidopsis thaliana recombinant inbred lines in three competitive treatments (noncompetitive, intra‐genotypic competition and inter‐genotypic competition) to examine if there is genetic variation for the components of competitive ability and whether neighbour relatedness has an effect on fitness. We find evidence for genetic variation in tolerance of competition and neighbour suppression and that these two competitive strategies are correlated, such that genotypes that tolerate competition will also strongly suppress neighbours. We further observe that the effect of neighbour relatedness on fitness of target individuals depends on neighbour identity, i.e. whether target individuals perform better when competing against self vs. nonself individuals depends on the genotypic identity of the nonself neighbour. The results are particularly relevant to evolutionary responses under multi‐level selection.     

Neighbour tolerance,not suppression,provides competitive advantage to non‐native plants

High competitive ability has often been invoked as a key determinant of invasion success and ecological impacts of non‐native plants. Yet our understanding of the strategies that non‐natives use to gain competitive dominance remains limited. Particularly, it remains unknown whether the two non‐mutually exclusive competitive strategies, neighbour suppression and neighbour tolerance, are equally important for the competitive advantage of non‐native plants. Here, we analyse data from 192 peer‐reviewed studies on pairwise plant competition within a Bayesian multilevel meta‐analytic framework and show that non‐native plants outperform their native counterparts due to high tolerance of competition, as opposed to strong suppressive ability. Competitive tolerance ability of non‐native plants was driven by neighbour's origin and was expressed in response to a heterospecific native but not heterospecific non‐native neighbour. In contrast to natives, non‐native species were not more suppressed by hetero‐ vs. conspecific neighbours, which was partially due to higher intensity of intraspecific competition among non‐natives. Heterogeneity in the data was primarily associated with methodological differences among studies and not with phylogenetic relatedness among species. Altogether, our synthesis demonstrates that non‐native plants are competitively distinct from native plants and challenges the common notion that neighbour suppression is the primary strategy for plant invasion success.     

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.     

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.     

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.     

Inclusive fitness in agriculture

Trade-offs between individual fitness and the collective performance of crop and below-ground symbiont communities are common in agriculture. Plant competitiveness for light and soil resources is key to individual fitness, but higher investments in stems and roots by a plant community to compete for those resources ultimately reduce crop yields. Similarly, rhizobia and mycorrhizal fungi may increase their individual fitness by diverting resources to their own reproduction, even if they could have benefited collectively by providing their shared crop host with more nitrogen and phosphorus, respectively. Past selection for inclusive fitness (benefits to others, weighted by their relatedness) is unlikely to have favoured community performance over individual fitness. The limited evidence for kin recognition in plants and microbes changes this conclusion only slightly. We therefore argue that there is still ample opportunity for human-imposed selection to improve cooperation among crop plants and their symbionts so that they use limited resources more efficiently. This evolutionarily informed approach will require a better understanding of how interactions among crops, and interactions with their symbionts, affected their inclusive fitness in the past and what that implies for current interactions.     

Detecting kin selection at work using inclusive fitness

A recent model shows that altruism can evolve with limited migration and variable group sizes, and the authors claim that kin selection cannot provide a sufficient explanation of their results. It is demonstrated, using a recent reformulation of Hamilton's original arguments, that the model falls squarely within the scope of inclusive fitness theory, which furthermore shows how to calculate inclusive fitness and the relevant relatedness. A distinction is drawn between inclusive fitness, which is a method of analysing social behaviour; and kin selection, a process that operates through genetic similarity brought about by common ancestry, but not by assortation by genotype or by direct assessment of genetic similarity. The recent model is analysed, and it turns out that kin selection provides a sufficient explanation to considerable quantitative accuracy, contrary to the authors' claims. A parallel analysis is possible and would be illuminating for all models of social behaviour in which individuals' effects on each other's offspring numbers combine additively.     

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.     

Measures of Relatedness

Measures of genetic relatedness are essential to models of evolution by kin selection and determinations of inclusive fitness. Under a kin selection paradigm, individuals are expected to distribute actions influencing the fitness of relatives based on the relatedness of these relatives. In addition, it is necessary to have an accurate measure of relatedness to estimate heritability (h²) of phenotypic characters and to predict the efficacy of selection. Relatedness is often defined as the genotypic correlation between individuals. Assessed on the basis of common ancestry, relatedness can only be determined sensu strictu from pedigree analysis. Recent methodological and statistical advances allow the estimation of relatedness from allele frequency data. Many coefficients of relatedness can be found in the literature; I review and evaluate these, with emphasis on situations for which each is appropriate.     

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. III. SOCIAL EVOLUTION

Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamilton's rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.     

No evidence that within‐group male relatedness reduces harm to females in Drosophila

Conflict between males and females over whether, when, and how often to mate often leads to the evolution of sexually antagonistic interactions that reduce female reproductive success. Because the offspring of relatives contribute to inclusive fitness, high relatedness between rival males might be expected to reduce competition and result in the evolution of reduced harm to females. A recent study investigated this possibility in Drosophila melanogaster and concluded that groups of brothers cause less harm to females than groups of unrelated males, attributing the effect to kin selection. That study did not control for the rearing environment of males, rendering the results impossible to interpret in the context of kin selection. Here, we conducted a similar experiment while manipulating whether males developed with kin prior to being placed with females. We found no difference between related and unrelated males in the harm caused to females when males were reared separately. In contrast, when related males developed and emerged together before the experiment, female reproductive output was higher. Our results show that relatedness among males is insufficient to reduce harm to females, while a shared rearing environment – resulting in males similar to or familiar with one another – is necessary to generate this pattern.     

Relatedness,Conflict, and the Evolution of Eusociality

The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.     

Inclusive Fitness from Multitype Branching Processes

I use multitype branching processes to study genetic models for the evolution of social behaviour, i.e. behaviours that, when acted out, affect the success of the actor’s neighbours. Here, I suppose an individual bearing a mutant copy of a gene influences the reproductive success of a neighbour by altering its own competitive ability. Approximations based on assumptions about the rareness of the mutant allele and the strength of selection allow me to formulate statements concerning the probability of mutant extinction in terms of inclusive fitness. Inclusive fitness is an idea well known to biologists and can be thought of as a sum of an individual’s fitness and the fitness of each of its relatives, weighted by some measure of genetic relatedness. Previous work has led to some confusion surrounding the definition of the inclusive-fitness effect of a mutant allele when individuals carrying that allele experience demographic conditions that fluctuate randomly. In this paper, I emphasise the link between inclusive fitness and the probability of mutant extinction. I recover standard results for populations of constant size, and I show that inclusive fitness can be used to determine the short-term fate of mutants in the face of stochastic demographic fluctuations. Overall, then, I provide a connection between certain inclusive-fitness-based approaches routinely applied in theoretical studies of social evolution.     

The past,present and future of reproductive skew theory and experiments

A major evolutionary question is how reproductive sharing arises in cooperatively breeding species despite the inherent reproductive conflicts in social groups. Reproductive skew theory offers one potential solution: each group member gains or is allotted inclusive fitness equal to or exceeding their expectation from reproducing on their own. Unfortunately, a multitude of skew models with conflicting predictions has led to confusion in both testing and evaluating skew theory. The confusion arises partly because one set of models (the ‘transactional’ type) answer the ultimate evolutionary question of what ranges of reproductive skew can yield fitness‐enhancing solutions for all group members. The second set of models (‘compromise’) give an evolutionarily proximate, game‐theoretic evolutionarily stable state (ESS) solution that determines reproductive shares based on relative competitive abilities. However, several predictions arising from compromise models require a linear payoff to increased competition and do not hold with non‐linear payoffs. Given that for most species it may be very difficult or impossible to determine the true relationship between effort devoted to competition and reproductive share gained, compromise models are much less predictive than previously appreciated. Almost all skew models make one quantitative prediction (e.g. realized skew must fall within ranges predicted by transactional models), and two qualitative predictions (e.g. variation in relatedness or competitive ability across groups affects skew). A thorough review of the data finds that these three predictions are relatively rarely supported. As a general rule, therefore, the evolution of cooperative breeding appears not to be dependent on the ability of group members to monitor relatedness or competitive ability in order to adjust their behaviour dynamically to gain reproductive share. Although reproductive skew theory fails to predict within‐group dynamics consistently, it does better at predicting quantitative differences in skew across populations or species. This suggests that kin selection can play a significant role in the evolution of sociality. To advance our understanding of reproductive skew will require focusing on a broader array of factors, such as the frequency of mistaken identity, delayed fitness payoffs, and selection pressures arising from across‐group competition. We furthermore suggest a novel approach to investigate the sharing of reproduction that focuses on the underlying genetics of skew. A quantitative genetics approach allows the partitioning of variance in reproductive share itself or that of traits closely associated with skew into genetic and non‐genetic sources. Thus, we can determine the heritability of reproductive share and infer whether it actually is the focus of natural selection. We view the ‘animal model’ as the most promising empirical method where the genetics of reproductive share can be directly analyzed in wild populations. In the quest to assess whether skew theory can provide a framework for understanding the evolution of sociality, quantitative genetics will be a central tool in future research.     

A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal

The analysis of kin selection in subdivided populations has been hampered by the lack of well‐defined measures of genealogical relatedness in the presence of localized dispersal. Furthermore, the usual arguments underlying the definition of game‐theoretical measures of inclusive fitness are not exact under localized dispersal. We define such measures to give the first‐order effects of selection on the probability of fixation of an allele. The derived measures of kin selection and relatedness are valid in finite populations and under localized dispersal. For the infinite island model, the resulting measure of kin selection is equivalent to a previously used measure. In other cases its definition is based on definitions of relatedness which are different from the usual ones. To illustrate the approach, we reanalyse a model with localized dispersal. We consider sex ratio evolution under sex‐specific dispersal behaviour, and the results confirm the earlier conclusion that the sex ratio is biased towards the sex with the dispersal rate closer to the optimal dispersal rate in the absence of sex‐specific dispersal behaviour.     

PATTERNS OF PATERNITY SKEW AMONG POLYANDROUS SOCIAL INSECTS: WHAT CAN THEY TELL US ABOUT THE POTENTIAL FOR SEXUAL SELECTION?

Monogamy results in high genetic relatedness among offspring and thus it is generally assumed to be favored by kin selection. Female multiple mating (polyandry) has nevertheless evolved several times in the social Hymenoptera (ants, bees, and wasps), and a substantial amount of work has been conducted to understand its costs and benefits. Relatedness and inclusive fitness benefits are, however, not only influenced by queen mating frequency but also by paternity skew, which is a quantitative measure of paternity biases among the offspring of polyandrous females. We performed a large‐scale phylogenetic analysis of paternity skew across polyandrous social Hymenoptera. We found a general and significant negative association between paternity frequency and paternity skew. High paternity skew, which increases relatedness among colony members and thus maximizes inclusive fitness gains, characterized species with low paternity frequency. However, species with highly polyandrous queens had low paternity skew, with paternity equalized among potential sires. Equal paternity shares among fathers are expected to maximize fitness benefits derived from genetic diversity among offspring. We discuss the potential for postcopulatory sexual selection to influence patterns of paternity in social insects, and suggest that sexual selection may have played a key, yet overlooked role in social evolution.     

Reproductive Systems and Sibling Competition in Plants

Abstract Competition among relatives can modify the genetic structure of plant populations; in turn, competitive outcomes can depend on the genetic relatedness of the individuals competing. The offspring from individual parents exhibit a continuum of genetic relatedness, depending on parental reproductive systems. Competition among relatives may have evolutionary significance as a selection pressure; sibling competition, for example, has been invoked to explain the evolution of sexual systems, seed packaging within fruits, seed dispersal dimorphisms, and germination behavior.
Density-dependent fitness consequences of sibling competition have been documented in a population of the annual grass Sporobolus vaginiflorus . This species produces seeds matured in cleistogamous spikelets within leaf sheaths along tillers in autumn: when seeds along the tillers of a maternal parent (i.e. a sibship) germinate in situ the following spring in close proximity to one another, sibling competition results in a high-density zone centered around the original senescent parent. Both intra- and intersibship interactions can occur within a population. Although fitness is much reduced for siblings inside the zone of competition, potential seed rain and net primary productivity per unit area are significantly higher relative to outside the zone. This annual is functionally analogous to a perennial ramet producer with a phalanx growth strategy and the unit of selection may be the sibling group. It is not yet known whether sibling competition is a significant selection pressure in other species, but indirect evidence suggests it may be relatively widespread.     

Revising traditional theory on the link between plant body size and fitness under competition: evidence from old‐field vegetation

The selection consequences of competition in plants have been traditionally interpreted based on a “size‐advantage” hypothesis – that is, under intense crowding/competition from neighbors, natural selection generally favors capacity for a relatively large plant body size. However, this conflicts with abundant data, showing that resident species body size distributions are usually strongly right‐skewed at virtually all scales within vegetation. Using surveys within sample plots and a neighbor‐removal experiment, we tested: (1) whether resident species that have a larger maximum potential body size (MAX) generally have more successful local individual recruitment, and thus greater local abundance/density (as predicted by the traditional size‐advantage hypothesis); and (2) whether there is a general between‐species trade‐off relationship between MAX and capacity to produce offspring when body size is severely suppressed by crowding/competition – that is, whether resident species with a larger MAX generally also need to reach a larger minimum reproductive threshold size (MIN) before they can reproduce at all. The results showed that MIN had a positive relationship with MAX across resident species, and local density – as well as local density of just reproductive individuals – was generally greater for species with smaller MIN (and hence smaller MAX). In addition, the cleared neighborhoods of larger target species (which had relatively large MIN) generally had – in the following growing season – a lower ratio of conspecific recruitment within these neighborhoods relative to recruitment of other (i.e., smaller) species (which had generally smaller MIN). These data are consistent with an alternative hypothesis based on a ‘reproductive‐economy‐advantage’ – that is, superior fitness under competition in plants generally requires not larger potential body size, but rather superior capacity to recruit offspring that are in turn capable of producing grand‐offspring – and hence transmitting genes to future generations – despite intense and persistent (cross‐generational) crowding/competition from near neighbors. Selection for the latter is expected to favor relatively small minimum reproductive threshold size and hence – as a tradeoff – relatively small (not large) potential body size.