Kin selection theory and the design of cooperative crops.

In agriculture and plant breeding, plant traits may be favoured because they benefit neighbouring plants and ultimately increase total crop yield. This idea of promoting cooperation among crop plants has existed almost as long as W.D. Hamilton's inclusive fitness (kin selection) theory, the leading framework for explaining cooperation in biology. However, kin selection thinking has not been adequately applied to the idea of cooperative crops. Here, I give an overview of modern kin selection theory and consider how it explains three key strategies for designing cooperative crops: (1) selection for a less-competitive plant type (a 'communal ideotype'); (2) group-level selection for yield; and (3) exploiting naturally selected cooperation. The first two strategies, using artificial selection, have been successful in the past but suffer from limitations that could hinder future progress. Instead, I propose an alternative strategy and a new 'colonial ideotype' that exploits past natural selection for cooperation among the modules (e.g., branches or stems) of individual plants. More generally, I suggest that Hamiltonian agriculture-a kin selection view of agriculture and plant breeding-transforms our understanding of how to improve crops of the future.

Kin discrimination, negative relatedness, and how to distinguish between selfishness and spite.

Spiteful behaviors occur when an actor harms its own fitness to inflict harm on the fitness of others. Several papers have predicted that spite can be favored in sufficiently small populations, even when the harming behavior is directed indiscriminately at others. However, it is not clear that truly spiteful behavior could be favored without the harm being directed at a subset of social partners with relatively low genetic similarity to the actor (kin discrimination, causing a negative relatedness between actor and harmed recipient). Using mathematical models, we show that (1) the evolution of spite requires kin discrimination; (2) previous models suggesting indiscriminate spite involve scenarios where the actor gains a direct feedback benefit from harming others, and so the harming is selfish rather than spiteful; (3) extreme selfishness can be favored in small populations (or, more generally, under local competition) because this is where the direct feedback benefit of harming is greatest.

A general model of biological signals, from cues to handicaps.

Organisms sometimes appear to use extravagant traits, or "handicaps", to signal their quality to an interested receiver. Before they were used as signals, many of these traits might have been selected to increase with individual quality for reasons apart from conveying information, allowing receivers to use the traits as "cues" of quality. However, current theory does not explain when and why cues of individual quality become exaggerated into costly handicaps. We address this here, using a game-theoretic model of adaptive signalling. Our model predicts that: (1) signals will honestly reflect signaler quality whenever there is a positive relationship between individual quality and the signalling trait's naturally selected, non-informational optimum; and (2) the slope of this relationship will determine the amount of costly signal exaggeration, with more exaggeration favored when the slope is more shallow. A shallow slope means that a lower quality male would pay only a small fitness cost to have the same trait value as a higher quality male, and this drives the exaggeration of signals as high-quality signalers are selected to distinguish themselves. Our model reveals a simple and potentially widespread mechanism for ensuring signal honesty and predicts a natural continuum of signalling strategies, from cost-free cues to costly handicaps.

Assortment and the analysis of natural selection on social traits.

A central problem in evolutionary biology is to determine whether and how social interactions contribute to natural selection. A key method for phenotypic data is social selection analysis, in which fitness effects from social partners contribute to selection only when there is a correlation between the traits of individuals and their social partners (nonrandom phenotypic assortment). However, there are inconsistencies in the use of social selection that center around the measurement of phenotypic assortment. Here, we use data analysis and simulations to resolve these inconsistencies, showing that: (i) not all measures of assortment are suitable for social selection analysis; and (ii) the interpretation of assortment, and how to detect nonrandom assortment, will depend on the scale at which it is measured. We discuss links to kin selection theory and provide a practical guide for the social selection approach.

Ecology and multilevel selection explain aggression in spider colonies.

Progress in sociobiology continues to be hindered by abstract debates over methodology and the relative importance of within-group vs. between-group selection. We need concrete biological examples to ground discussions in empirical data. Recent work argued that the levels of aggression in social spider colonies are explained by group-level adaptation. Here, we examine this conclusion using models that incorporate ecological detail while remaining consistent with kin- and multilevel selection frameworks. We show that although levels of aggression are driven, in part, by between-group selection, incorporating universal within-group competition provides a striking fit to the data that is inconsistent with pure group-level adaptation. Instead, our analyses suggest that aggression is favoured primarily as a selfish strategy to compete for resources, despite causing lower group foraging efficiency or higher risk of group extinction. We argue that sociobiology will benefit from a pluralistic approach and stronger links between ecologically informed models and data.

Cooperation, clumping and the evolution of multicellularity.

The evolution of multicellular organisms represents one of the major evolutionary transitions in the history of life. A potential advantage of forming multicellular clumps is that it provides an efficiency benefit to pre-existing cooperation, such as the production of extracellular 'public goods'. However, this is complicated by the fact that cooperation could jointly evolve with clumping, and clumping could have multiple consequences for the evolution of cooperation. We model the evolution of clumping and a cooperative public good, showing that (i) when considered separately, both clumping and public goods production gradually increase with increasing genetic relatedness; (ii) in contrast, when the traits evolve jointly, a small increase in relatedness can lead to a major shift in evolutionary outcome­from a non-clumping state with low public goods production to a cooperative clumping state with high values of both traits; (iii) high relatedness makes it easier to get to the cooperative clumping state and (iv) clumping can be inhibited when it increases the number of cells that the benefits of cooperation must be shared with, but promoted when it increases relatedness between those cells. Overall, our results suggest that public goods sharing can facilitate the formation of well-integrated cooperative clumps as a first step in the evolution of multicellularity.

Inclusive fitness and sexual conflict: how population structure can modulate the battle of the sexes.

Competition over reproductive opportunities among members of one sex often harms the opposite sex, creating a conflict of interest between individual males and females. Recently, this battle of the sexes has become a paradigm in the study of intersexual coevolution. Here, we review recent theoretical and empirical advances suggesting that - as in any scenario of intraspecific competition - selfishness (competitiveness) can be influenced by the genetic relatedness of competitors. When competitors are positively related (e.g. siblings), an individual may refrain from harming its competitor(s) and their mate(s) because this can improve the focal individual's inclusive fitness. These findings reveal that population genetic structure might be of paramount importance when studying the battle of the sexes. We conclude by identifying some new lines of research at the interface of sexual selection and social evolution.

The evolution of index signals to avoid the cost of dishonesty.

Animals often convey useful information, despite a conflict of interest between the signaller and receiver. There are two major explanations for such 'honest' signalling, particularly when the size or intensity of signals reliably indicates the underlying quality of the signaller. Costly signalling theory (including the handicap principle) predicts that dishonest signals are too costly to fake, whereas the index hypothesis predicts that dishonest signals cannot be faked. Recent evidence of a highly conserved causal link between individual quality and signal growth appears to bolster the index hypothesis. However, it is not clear that this also diminishes costly signalling theory, as is often suggested. Here, by incorporating a mechanism of signal growth into costly signalling theory, we show that index signals can actually be favoured owing to the cost of dishonesty. We conclude that costly signalling theory provides the ultimate, adaptive rationale for honest signalling, whereas the index hypothesis describes one proximate (and potentially very general) mechanism for achieving honesty.

Are greenbeards intragenomic outlaws?

Greenbeard genes identify copies of themselves in other individuals and cause their bearer to behave nepotistically toward those individuals. Hence, they can be favored by kin selection, irrespective of the degree of genealogical relationship between social partners. Although greenbeards were initially developed as a thought experiment, a number of recent discoveries of greenbeard alleles in real populations have led to a resurgence of interest in their evolutionary dynamics and consequences. One issue over which there has been disagreement is whether greenbeards lead to intragenomic conflict. Here, to clarify the "outlaw" status of greenbeards, we develop population genetic models that formally examine selection of greenbeard phenotypes under the control of different loci. We find that, in many cases, greenbeards are not outlaws because selection for or against the greenbeard phenotype is the same across all loci. In contrast, when social interactions are between genealogical kin, we find that greenbeards can be outlaws because different genes can be selected in different directions. Hence, the outlaw status of greenbeard genes crucially depends upon the particular biological details. We also clarify whether greenbeards are favored due to direct or indirect fitness effects and address the relationship of the greenbeard effect to sexual antagonism and reciprocity.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Evidence for competition and cooperation among climbing plants.

A plant's best strategy for acquiring resources may often depend on the identity of neighbours. Here, I ask whether plants adjust their strategy to local relatedness: individuals may cooperate (reduce competitiveness) with kin but compete relatively intensely with non-kin. In a greenhouse experiment with Ipomoea hederacea, neighbouring siblings from the same inbred line were relatively uniform in height; groups of mixed lines, however, were increasingly variable as their mean height increased. The reproductive yield of mixed and sibling groups was similar overall, but when adjusted to a common mean height and height inequality, the yield of mixed groups was significantly less. Where this difference in yield was most pronounced (among groups that varied most in height), mixed groups tended to allocate more mass to roots than comparable sibling groups, and overall, mixed groups produced significantly fewer seeds per unit mass of roots. These results suggest that, from the group perspective, non-kin may have wasted resources in below-ground competition at the expense of reproduction; kin groups, on the other hand, displayed the relative efficiency that is expected of reduced competitiveness.

The origin of gender dimorphism in animal-dispersed plants: disruptive selection in a model of social evolution.

Dioecy (separate sexes) in plants is associated with animal fruit dispersal, but hypotheses for a role of dispersal in the origin of gender dimorphism have received little support. Here, I present a patch-structured model to explore the conditions that favor dimorphism when dispersal is coupled with sex allocation. The model shows that if the proportion of fruits dispersed from a cosexual plant increases with its allocation to fruits (causing accelerating fitness returns from dispersed fruits), disruptive selection can arise when the cost of dispersal is minimal and the correlation among patchmates (i.e., relatedness) is high. In reality, however, the proportion of fruits dispersed from a plant's patch may decline with further allocation to fruits. Even in this case, novel contexts that lead to disruptive selection on sex allocation are discovered, occurring when dispersal costs are high and relatedness is low, which causes accelerating returns from nondispersed fruits. Hence, surprisingly, gender dimorphism can evolve because female specialists are better able to escape local competition or to succeed in it. Building on the few existing models of disruptive selection on social traits, the mechanisms here show that selection for relaxed local competition (cooperation) can sometimes facilitate diversification and sometimes prevent it.

Bumblebees learn to forage like Bayesians.

Bayesian foraging in patchy environments requires that foragers have information about the distribution of resources among patches (prior information), either set by natural selection or learned from past experience. We test the hypothesis that bumblebee foragers can rapidly learn prior information from past experience in two very different experimental environments. In the high-variance environment (patches of low and high quality), stochastic optimality models predicted that finding rewards should sometimes sharply increase an optimal forager's tendency to stay in a patch (an incremental response), whereas in the uniform environment, finding rewards should always decrease the tendency to stay (a decremental response). We use Cox regression models to show that, in a matter of hours, bees learned to match both predicted responses, resulting in a reward intake rate that averaged 80% of the predicted maximum. Following training in either environment, bees' adaptive behavior carried over to a common test environment, thus confirming the influence of memorized prior information. Although Bayesian foraging by learning is often presumed, this study is the first to clearly isolate the adaptive use of a learned prior expectation. More generally, it highlights the remarkable adaptive plasticity of an important generalist pollinator and agent of selection.

Habitat assessment ability of bumble-bees implies frequency-dependent selection on floral rewards and display size.

Foraging pollinators could visit hundreds of flowers in succession on mass-flowering plants, yet they often visit only a small number--potentially saving the plant from much self-pollination among its own flowers (geitonogamy). This study tests the hypothesis that bumble-bee (Bombus impatiens) residence on a particular plant depends on an assessment of that plant's reward value relative to the overall quality experienced in the habitat. In a controlled environment, naive bees were given experience in a particular habitat (all plants having equal nectar quality or number of rewarding flowers), and we tested whether they learn about and adaptively exploit a new habitat type. Bees' residence on a plant (number of flowers probed per visit) was eventually invariant to a doubling of absolute nectar quality and increased only slightly with a doubling of absolute flower number in the habitat. These results help to explain why pollinators are quick to leave highly rewarding plants and suggest that the fitness of rewarding plant traits will often be frequency dependent. One implication is that geitonogamy may be a less significant constraint on the evolution of rewarding traits than generally supposed.