Ashleigh S. Griffin

Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection

From an evolutionary perspective, social behaviours are those which have fitness consequences for both the individual that performs the behaviour, and another individual. Over the last 43 years, a huge theoretical and empirical literature has developed on this topic. However, progress is often hindered by poor communication between scientists, with different people using the same term to mean different things, or different terms to mean the same thing. This can obscure what is biologically important, and what is not. The potential for such semantic confusion is greatest with interdisciplinary research. Our aim here is to address issues of semantic confusion that have arisen with research on the problem of cooperation. In particular, we: (i) discuss confusion over the terms kin selection, mutualism, mutual benefit, cooperation, altruism, reciprocal altruism, weak altruism, altruistic punishment, strong reciprocity, group selection and direct fitness; (ii) emphasize the need to distinguish between proximate (mechanism) and ultimate (survival value) explanations of behaviours. We draw examples from all areas, but especially recent work on humans and microbes.

Social evolution theory for microorganisms

Microorganisms communicate and cooperate to perform a wide range of multicellular behaviours, such as dispersal, nutrient acquisition, biofilm formation and quorum sensing. Microbiologists are rapidly gaining a greater understanding of the molecular mechanisms involved in these behaviours, and the underlying genetic regulation. Such behaviours are also interesting from the perspective of social evolution ? why do microorganisms engage in these behaviours given that cooperative individuals can be exploited by selfish cheaters, who gain the benefit of cooperation without paying their share of the cost? There is great potential for interdisciplinary research in this fledgling field of sociomicrobiology, but a limiting factor is the lack of effective communication of social evolution theory to microbiologists. Here, we provide a conceptual overview of the different mechanisms through which cooperative behaviours can be stabilized, emphasizing the aspects most relevant to microorganisms, the novel problems that microorganisms pose and the new insights that can be gained from applying evolutionary theory to microorganisms.

Cooperation and competition in pathogenic bacteria

Explaining altruistic cooperation is one of the greatest challenges for evolutionary biology. One solution to this problem is if costly cooperative behaviours are directed towards relatives. This idea of kin selection has been hugely influential and applied widely from microorganisms to vertebrates. However, a problem arises if there is local competition for resources, because this leads to competition between relatives, reducing selection for cooperation. Here we use an experimental evolution approach to test the effect of the scale of competition, and how it interacts with relatedness. The cooperative trait that we examine is the production of siderophores, iron-scavenging agents, in the pathogenic bacterium Pseudomonas aeruginosa. As expected, our results show that higher levels of cooperative siderophore production evolve in the higher relatedness treatments. However, our results also show that more local competition selects for lower levels of siderophore production and that there is a significant interaction between relatedness and the scale of competition, with relatedness having less effect when the scale of competition is more local. More generally, the scale of competition is likely to be of particular importance for the evolution of cooperation in microorganisms, and also the virulence of pathogenic microorganisms, because cooperative traits such as siderophore production have an important role in determining virulence.

Evolutionary Explanations for Cooperation

Natural selection favours genes that increase an organisms ability to survive and reproduce. This would appear to lead to a world dominated by selfish behaviour. However, cooperation can be found at all levels of biological organisation: genes cooperate in genomes, organelles cooperate to form eukaryotic cells, cells cooperate to make multicellular organisms, bacterial parasites cooperate to overcome host defences, animals breed cooperatively, and humans and insects cooperate to build societies. Over the last 40 years, biologists have developed a theoretical framework that can explain cooperation at all these levels. Here, we summarise this theory, illustrate how it may be applied to real organisms and discuss future directions.

Cooperation and conflict in quorum-sensing bacterial populations.

It has been suggested that bacterial cells communicate by releasing and sensing small diffusible signal molecules in a process commonly known as quorum sensing (QS). It is generally assumed that QS is used to coordinate cooperative behaviours at the population level. However, evolutionary theory predicts that individuals who communicate and cooperate can be exploited. Here we examine the social evolution of QS experimentally in the opportunistic pathogen Pseudomonas aeruginosa, and show that although QS can provide a benefit at the group level, exploitative individuals can avoid the cost of producing the QS signal or of performing the cooperative behaviour that is coordinated by QS, and can therefore spread. We also show that a solution to the problem of exploitation is kin selection, if interacting bacterial cells tend to be close relatives. These results show that the problem of exploitation, which has been the focus of considerable attention in animal communication, also arises in bacteria.

Kin selection: fact and fiction

Abstract Hamiltons inclusive fitness theory represents one of the most important developments in evolutionary biology. In particular, the idea that individuals benefit from the reproduction of relatives (kin selection) has been extraordinarily successful in explaining a wide range of phenomena, especially cases of supposed altruism. However, recent work has emphasized how the importance of kin selection can be overestimated – an estimate of high relatedness between interacting individuals is not in itself sufficient evidence that kin selection is responsible for promoting altruism. In particular, supposedly altruistic traits can have direct fitness benefits, and competition between relatives can reduce the importance of indirect fitness benefits.

Testing Hamilton's rule with competition between relatives

Hamilton’s theory of kin selection suggests that individuals should show less aggression, and more altruism, towards closer kin. Recent theoretical work has, however, suggested that competition between relatives can counteract kin selection for altruism. Unfortunately, factors that tend to increase the average relatedness of interacting individuals—such as limited dispersal—also tend to increase the amount of competition between relatives. Therefore, in most natural systems, the conflicting influences of increased competition and increased relatedness are confounded, limiting attempts to test theory. Fig wasp taxa exhibit varying levels of aggression among non-dispersing males that show a range of average relatedness levels. Thus, across species, the effects of relatedness and competition between relatives can be separated. Here we report that—contrary to Hamiltons original prediction but in agreement with recent theory—the level of fighting between males shows no correlation with the estimated relatedness of interacting males, but is negatively correlated with future mating opportunities.

Promiscuity and the evolutionary transition to complex societies

Theory predicts that the evolution of cooperative behaviour is favoured by low levels of promiscuity leading to high within-group relatedness. However, in vertebrates, cooperation often occurs between non-relatives and promiscuity rates are among the highest recorded. Here we resolve this apparent inconsistency with a phylogenetic analysis of 267 bird species, demonstrating that cooperative breeding is associated with low promiscuity; that in cooperative species, helping is more common when promiscuity is low; and that intermediate levels of promiscuity favour kin discrimination. Overall, these results suggest that promiscuity is a unifying feature across taxa in explaining transitions to and from cooperative societies.

Quorum Sensing and the Social Evolution of Bacterial Virulence

The ability of pathogenic bacteria to exploit their hosts depends upon various virulence factors, released in response to the concentration of small autoinducer molecules that are also released by the bacteria [1-5]. In vitro experiments suggest that autoinducer molecules are signals used to coordinate cooperative behaviors and that this process of quorum sensing (QS) can be exploited by individual cells that avoid the cost of either producing or responding to signal [6, 7]. However, whether QS is an exploitable social trait in vivo, and the implications for the evolution of virulence [5, 8-10], remains untested. We show that in mixed infections of the bacterium Pseudomonas aeruginosa, containing quorum-sensing bacteria and mutants that do not respond to signal, virulence in an animal (mouse) model is reduced relative to that of an infection containing no mutants. We show that this is because mutants act as cheats, exploiting the cooperative production of signal and virulence factors by others, and hence increase in frequency. This supports the idea that the invasion of QS mutants in infections of humans [11-13] is due to their social fitness consequences [6, 7, 14] and predicts that increased strain diversity will select for lower virulence.

Evolutionary theory of bacterial quorum sensing: when is a signal not a signal?

The term quorum sensing (QS) is used to describe the communication between bacterial cells, whereby a coordinated population response is controlled by diffusible molecules produced by individuals. QS has not only been described between cells of the same species (intraspecies), but also between species (interspecies) and between bacteria and higher organisms (inter-kingdom). The fact that QS-based communication appears to be widespread among microbes is strange, considering that explaining both cooperation and communication are two of the greatest problems in evolutionary biology. From an evolutionary perspective, intraspecies signalling can be explained using models such as kin selection, but when communication is described between species, it is more difficult to explain. It is probable that in many cases this involves QS molecules being used as ‘cues’ by other species as a guide to future action or as manipulating molecules whereby one species will ‘coerce’ a response from another. In these cases, the usage of QS molecules cannot be described as signalling. This review seeks to integrate the evolutionary literature on animal signalling with the microbiological literature on QS, and asks whether QS within bacteria is true signalling or whether these molecules are also used as cues or for the coercion of other cells.