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.

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.

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.

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.

Natural selection favours genes that increase an organism's 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.

Our understanding of the social lives of microbes has been revolutionized over the past 20 years. It used to be assumed that bacteria and other microorganisms lived relatively independent unicellular lives, without the cooperative behaviors that have provoked so much interest in mammals, birds, and insects. However, a rapidly expanding body of research has completely overturned this idea, showing that microbes indulge in a variety of social behaviors involving complex systems of cooperation, communication, and synchronization. Work in this area has already provided some elegant experimental tests of social evolutionary theory, demonstrating the importance of factors such as relatedness, kin discrimination, competition between relatives, and enforcement of cooperation. Our aim here is to review these social behaviors, emphasizing the unique opportunities they offer for testing existing evolutionary theory as well as highlighting the novel theoretical problems that they pose.

Individuals are predicted to behave more altruistically and less competitively toward their relatives, because they share a relatively high proportion of their genes (e.g., one-half for siblings and one-eighth for cousins). Consequently, by helping a relative reproduce, an individual passes its genes to the next generation, increasing their Darwinian fitness. This idea, termed kin selection, has been applied to a wide range of phenomena in systems ranging from replicating molecules to humans. Nevertheless, competition between relatives can reduce, and even totally negate, the kin-selected benefits of altruism toward relatives. Recent theoretical work has clarified the processes and selective forces underlying this effect and has demonstrated the generality of the effect of competition between relatives.

In many cooperatively breeding vertebrates, a dominant breeding pair is assisted in offspring care by nonbreeding helpers. A leading explanation for this altruistic behavior is Hamilton's idea that helpers gain indirect fitness benefits by rearing relatives (kin selection). Many studies have shown that helpers typically provide care for relatives, but relatively few have shown that helpers provide closer kin with preferential care (kin discrimination), fueling the suggestion that kin selection only poorly accounts for the evolution of cooperative breeding in vertebrates. We used meta-analysis to show that (i) individuals consistently discriminate between kin, and (ii) stronger discrimination occurs in species where the benefits of helping are greater. These results suggest a general role for kin selection and that the relative importance of kin selection varies across species, as predicted by Hamilton's rule.In cooperatively breeding vertebrates, a dominant pair usually produces the majority of the offspring, whereas the cost of caring for offspring is shared by nonbreeding subordinates (1-5). Explaining how this and other altruistic helping behavior by nonbreeders is maintained by natural selection is a major problem for evolutionary biology. Hamilton's hugely influential kin selection theory provides a possible solution to this problem by pointing out that subordinates can gain indirect fitness benefits by helping relatives (6, 7). However, although kin selection appears to play a crucial role in understanding social insects (8, 9), its potential importance in vertebrates has been much debated (1-4, 9, 10). Groups in cooperatively breeding species are typically made up of extended families, suggesting that subordinates will often be helping relatives (11). However, these associations between relatives can result from limited dispersal of individuals, and the relatedness among group members is not necessarily lower in species that live in stable groups but do not breed cooperatively (1, 10). Furthermore, it is increasingly realized that there are a number of ways in which subordinates may gain direct fitness benefits by helping to raise offspring, such as the survival benefits of increasing group size (1,2,10,(12)(13)(14).The most fundamental way to test for a role of kin selection is to test whether the probability or amount of helping covaries with genetic relatedness between potential helpers and beneficiaries. Relatedness between group members varies within groups because of immigration and changes in the identity of the breeding dominants. Helpers can potentially assess their relatedness to other group members through a variety of direct or indirect mechanisms (15,16). Kin selection theory predicts that there will be a positive correlation between the probability or amount of help and relatedness, with helpers preferentially aiding closer relatives (kin discrimination). Although many long-term studies on vertebrates have addressed this problem, there is no clear pattern, with some finding that individuals ...