Laurent Keller

The evolution of cooperation and altruism – a general framework and a classification of models

One of the enduring puzzles in biology and the social sciences is the origin and persistence of intraspecific cooperation and altruism in humans and other species. Hundreds of theoretical models have been proposed and there is much confusion about the relationship between these models. To clarify the situation, we developed a synthetic conceptual framework that delineates the conditions necessary for the evolution of altruism and cooperation. We show that at least one of the four following conditions needs to be fulfilled: direct benefits to the focal individual performing a cooperative act; direct or indirect information allowing a better than random guess about whether a given individual will behave cooperatively in repeated reciprocal interactions; preferential interactions between related individuals; and genetic correlation between genes coding for altruism and phenotypic traits that can be identified. When one or more of these conditions are met, altruism or cooperation can evolve if the cost‐to‐benefit ratio of altruistic and cooperative acts is greater than a threshold value. The cost‐to‐benefit ratio can be altered by coercion, punishment and policing which therefore act as mechanisms facilitating the evolution of altruism and cooperation. All the models proposed so far are explicitly or implicitly built on these general principles, allowing us to classify them into four general categories.

Communication in bacteria: an ecological and evolutionary perspective

Individual bacteria can alter their behaviour through chemical interactions between organisms in microbial communities ? this is generally referred to as quorum sensing. Frequently, these interactions are interpreted in terms of communication to mediate coordinated, multicellular behaviour. We show that the nature of interactions through quorum-sensing chemicals does not simply involve cooperative signals, but entails other interactions such as cues and chemical manipulations. These signals might have a role in conflicts within and between species. The nature of the chemical interaction is important to take into account when studying why and how bacteria react to the chemical substances that are produced by other bacteria.

Pleiotropy in the melanocortin system, coloration and behavioural syndromes.

In vertebrates, melanin-based coloration is often associated with variation in physiological and behavioural traits. We propose that this association stems from pleiotropic effects of the genes regulating the synthesis of brown to black eumelanin. The most important regulators are the melanocortin 1 receptor and its ligands, the melanocortin agonists and the agouti-signalling protein antagonist. On the basis of the physiological and behavioural functions of the melanocortins, we predict five categories of traits correlated with melanin-based coloration. A review of the literature indeed reveals that, as predicted, darker wild vertebrates are more aggressive, sexually active and resistant to stress than lighter individuals. Pleiotropic effects of the melanocortins might thus account for the widespread covariance between melanin-based coloration and other phenotypic traits in vertebrates.

Partitioning of reproduction in animal societies.

A key feature differentiating cooperative animal societies Is the apportionment of reproduction among individuals. Only recently have studies started to focus on intraspecific variability in the distribution of reproduction within animal societies, and the available data suggest that this variability might be greater than previously suspected. How can one account for intra-and interspecific variability in partitioning of reproduction? This Is one of the most intriguing problems in the study of social behaviour, and understanding the factors underlying this variability is one of the keys to understanding the properties of complex animal societies.

Evolution of supercolonies: The Argentine ants of southern Europe

Some ants have an extraordinary social organization, called unicoloniality, whereby individuals mix freely among physically separated nests. This type of social organization is not only a key attribute responsible for the ecological domination of these ants, but also an evolutionary paradox and a potential problem for kin selection theory because relatedness between nest mates is effectively zero. The introduction of the Argentine ant in Europe was apparently accompanied by a dramatic loss of inter-nest aggression and the formation of two immense supercolonies (which effectively are two unicolonial populations). Introduced populations experienced only limited loss of genetic diversity at neutral markers, indicating that the breakdown of recognition ability is unlikely to be merely due to a genetic bottleneck. Rather, we suggest that a “genetic cleansing” of recognition cues occurred after introduction. Indeed workers of the same supercolony are never aggressive to each other despite the large geographical distance and considerable genetic differentiation between sampling sites. By contrast, aggression is invariably extremely high between the two supercolonies, indicating that they have become fixed for different recognition alleles. The main supercolony, which ranges over 6,000 km from Italy to the Spanish Atlantic coast, effectively forms the largest cooperative unit ever recorded.

Extraordinary lifespans in ants: a test of evolutionary theories of ageing

Senescence presents not only a medical problem, but also an evolutionary paradox because it should be opposed by natural selection. Evolutionary hypotheses propose that ageing evolves as the necessary cost of processes increasing early reproductive success, or because of weaker selection against late-acting mutations. A prediction of these hypotheses is that the rate of ageing should increase and the average lifespan decrease as therate of extrinsic mortality increases. Alternatively, non-adaptive, purely mechanistic hypotheses invoke damage to DNA, cells, tissues and organs as being the unique cause of senescence and ineluctable death of organisms. Here we show that the evolution of eusociality is associated with a 100-fold increase in insect lifespan. Such an increase is predicted by evolutionary theories because termite, bee and ant queens live in colonies that are sheltered and heavily defended against predators. Moreover, a comparison of ants with contrasting life histories also reveals an association between lifespan and extrinsic rate of mortality. Theseresults provide strong support for evolutionary theories of ageing, as purely mechanistic hypotheses of senescence do not propose any association between the rate of extrinsic mortality and lifespans.

Selfish genes: a green beard in the red fire ant

A ‘green-beard’ gene is defined as a gene that causes a phenotypic effect (such as the presence of a green beard or any other conspicuous feature), allows the bearer of this feature to recognize it in other individuals, and causes the bearer to behave differently towards other individuals depending on whether or not they possess the feature. Such genes have been proposed on theoretical grounds to be agents mediating both altruism and intragenomic conflicts,, but until now few, if any, of these genes have been identified,. Here we provide evidence of a green-beard gene in the red imported fire ant, Solenopsis invicta. In polygyne (multiple-queen) colonies, all egg-laying queens are Bb heterozygotes at the locus Gp-9 (ref. 6). Previous studies suggested that bb females die prematurely from intrinsic causes; we now show that BB queens initiating reproduction are killed by workers, and that it is primarily Bb rather than BB workers that are responsible for these executions. This implies that allele Gp-9b is linked to a green-beard allele that preferentially induces workers bearing the allele to kill all queens that do not bear it. Workers appear to distinguish BB from Bb queens on the basis of a transferable odour cue.

Ant-like task allocation and recruitment in cooperative robots

One of the greatest challenges in robotics is to create machines that are able to interact with unpredictable environments in real time. A possible solution may be to use swarms of robots behaving in a self-organized manner, similar to workers in an ant colony. Efficient mechanisms of division of labour, in particular series–parallel operation and transfer of information among group members, are key components of the tremendous ecological success of ants. Here we show that the general principles regulating division of labour in ant colonies indeed allow the design of flexible, robust and effective robotic systems. Groups of robots using ant-inspired algorithms of decentralized control techniques foraged more efficiently and maintained higher levels of group energy than single robots. But the benefits of group living decreased in larger groups, most probably because of interference during foraging. Intriguingly, a similar relationship between group size and efficiency has been documented in social insects. Moreover, when food items were clustered, groups where robots could recruit other robots in an ant-like manner were more efficient than groups without information transfer, suggesting that group dynamics of swarms of robots may follow rules similar to those governing social insects.

The genome of the fire ant Solenopsis invicta

Ants have evolved very complex societies and are key ecosystem members. Some ants, such as the fire ant Solenopsis invicta, are also major pests. Here, we present a draft genome of S. invicta, assembled from Roche 454 and Illumina sequencing reads obtained from a focal haploid male and his brothers. We used comparative genomic methods to obtain insight into the unique features of the S. invicta genome. For example, we found that this genome harbors four adjacent copies of vitellogenin. A phylogenetic analysis revealed that an ancestral vitellogenin gene first underwent a duplication that was followed by possibly independent duplications of each of the daughter vitellogenins. The vitellogenin genes have undergone subfunctionalization with queen- and worker-specific expression, possibly reflecting differential selection acting on the queen and worker castes. Additionally, we identified more than 400 putative olfactory receptors of which at least 297 are intact. This represents the largest repertoire reported so far in insects. S. invicta also harbors an expansion of a specific family of lipid-processing genes, two putative orthologs to the transformer/feminizer sex differentiation gene, a functional DNA methylation system, and a single putative telomerase ortholog. EST data indicate that this S. invicta telomerase ortholog has at least four spliceforms that differ in their use of two sets of mutually exclusive exons. Some of these and other unique aspects of the fire ant genome are likely linked to the complex social behavior of this species.

Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig–wasp mutualism, sex allocation, and precision of adaptation

Fig-pollinating wasps have provided model systems for developing and testing theories of the evolution of mutualism, sex allocation, and precision of adaptation. With few exceptions, previous studies have assumed one species of pollinator wasp per host fig species. Here we report genetic data demonstrating the coexistence of previously undetected cryptic fig wasp species in at least half of the host fig species surveyed. The substantial mitochondrial sequence differences (4.2–6.1%) imply old divergences (≈1.5–5.1 million years ago) among these species. Furthermore, some cryptic species pairs seem to be sister taxa, whereas others clearly are not, indicating both long-term coexistence on shared hosts and the colonization of novel fig species. These findings undermine the prevalent notion of strict one-to-one specificity between cospeciating figs and their pollinators, thereby challenging existing theory concerning the evolution and stability of mutualisms. Moreover, the incorporation of the genetic information significantly improves the fit of the observed sex ratios to predictions of local mate-competition theory, further strengthening support for sex allocation theory and the precision of adaptation.