Jay M. Biernaskie

Evidence for competition and cooperation among climbing plants

A plants 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 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.

Multicoloured greenbeards, bacteriocin diversity and the rock-paper-scissors game.

Greenbeard genes identify copies of themselves in other individuals and cause their bearer to behave nepotistically towards those individuals. Bacterial toxins (bacteriocins) exemplify the greenbeard effect because producer strains carry closely linked genes for immunity, such that toxicity is limited to nonproducer strains. Bacteriocin producers can be maintained in a dynamic polymorphism, known as rock‐paper‐scissors (RPS) dynamics, with immune and susceptible strains. However, it is unclear whether and how such dynamics will be maintained in the presence of multiple toxin types (multiple beard ‘colours’). Here, we analyse strain dynamics using models of recurrent patch colonization and population growth. We find that (i) polymorphism is promoted by a small number of founding lineages per patch, strong local resource competition and the occurrence of mutations; (ii) polymorphism can be static or dynamic, depending on the intensity of local interactions and the costs of toxins and immunity; (iii) the occurrence of multiple toxins can promote RPS dynamics; and (iv) strain diversity can be maintained even when toxins differ in toxicity or lineages can exhibit multitoxicity/multi‐immunity. Overall, the factors that maintain simple RPS dynamics can also promote the coexistence of multiple toxin types (multiple beard colours), thus helping to explain the remarkable levels of bacteriocin diversity in nature. More generally, we contrast these results with the maintenance of marker diversity in genetic kin recognition.

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 individuals 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.

Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities

Cooperation and diversity abound in nature despite cooperators risking exploitation from defectors and superior competitors displacing weaker ones. Understanding the persistence of cooperation and diversity is therefore a major problem for evolutionary ecology, especially in the context of well-mixed populations, where the potential for exploitation and displacement is greatest. Here, we demonstrate that a ‘loner effect’, described by economic game theorists, can maintain cooperation and diversity in real-world biological settings. We use mathematical models of public-good-producing bacteria to show that the presence of a loner strain, which produces an independent but relatively inefficient good, can lead to rock–paper–scissor dynamics, whereby cooperators outcompete loners, defectors outcompete cooperators and loners outcompete defectors. These model predictions are supported by our observations of evolutionary dynamics in well-mixed experimental communities of the bacterium Pseudomonas aeruginosa. We find that the coexistence of cooperators and defectors that produce and exploit, respectively, the iron-scavenging siderophore pyoverdine, is stabilized by the presence of loners with an independent iron-uptake mechanism. Our results establish the loner effect as a simple and general driver of cooperation and diversity in environments that would otherwise favour defection and the erosion of diversity.

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.

Ecology and multilevel selection explain aggression in spider colonies

Abstract 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 outcome—from 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.

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.

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.