A simple genetic basis for complex social behaviour mediates widespread gene expression differences.

A remarkable social polymorphism is controlled by a single Mendelian factor in the fire ant Solenopsis invicta. A genomic element marked by the gene Gp-9 determines whether workers tolerate one or many fertile queens in their colony. Gp-9 was recently shown to be part of a supergene with two nonrecombining variants, SB and Sb. SB/SB and SB/Sb queens differ in how they initiate new colonies, and in many physiological traits, for example odour and maturation rate. To understand how a single genetic element can affect all these traits, we used a microarray to compare gene expression patterns between SB/SB and SB/Sb queens of three different age classes: 1-day-old unmated queens, 11-day-old unmated queens and mated, fully reproductive queens collected from mature field colonies. The number of genes that were differentially expressed between SB/SB and SB/Sb queens of the same age class was smallest in 1-day-old queens, maximal in 11-day-old queens and intermediate in reproductive queens. Gene ontology analysis showed that SB/SB queens upregulate reproductive genes faster than SB/Sb queens. For all age classes, genes inside the supergene were overrepresented among the differentially expressed genes. Consistent with the hypothesized greater number of transposons in the Sb supergene, 13 transposon genes were upregulated in SB/Sb queens. Viral genes were also upregulated in SB/Sb mature queens, consistent with the known greater parasite load in colonies headed by SB/Sb queens compared with colonies headed by SB/SB queens. Eighteen differentially expressed genes between reproductive queens were involved in chemical signalling. Our results suggest that many genes in the supergene are involved in regulating social organization and queen phenotypes in fire ants.

Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour.

In many gamma-proteobacteria, the conserved GacS/GacA (BarA/UvrY) two-component system positively controls the expression of one to five genes specifying small RNAs (sRNAs) that are characterized by repeated unpaired GGA motifs but otherwise appear to belong to several independent families. The GGA motifs are essential for binding small, dimeric RNA-binding proteins of a single conserved family designated RsmA (CsrA). These proteins, which also occur in bacterial species outside the gamma-proteobacteria, act as translational repressors of certain mRNAs when these contain an RsmA/CsrA binding site at or near the Shine-Dalgarno sequence plus additional binding sites located in the 5' untranslated leader mRNA. Recent structural data have established that the RsmA-like protein RsmE of Pseudomonas fluorescens makes specific contacts with an RNA consensus sequence 5'-(A)/(U)CANGGANG(U)/(A)-3' (where N is any nucleotide). Interaction with an RsmA/CsrA protein promotes the formation of a short stem supporting an ANGGAN loop. This conformation hinders access of 30S ribosomal subunits and hence translation initiation. The output of the Gac/Rsm cascade varies widely in different bacterial species and typically involves management of carbon storage and expression of virulence or biocontrol factors. Unidentified signal molecules co-ordinate the activity of the Gac/Rsm cascade in a cell population density-dependent manner.

Using robots to understand social behaviour.

A major challenge in studying social behaviour stems from the need to disentangle the behaviour of each individual from the resulting collective. One way to overcome this problem is to construct a model of the behaviour of an individual, and observe whether combining many such individuals leads to the predicted outcome. This can be achieved by using robots. In this review we discuss the strengths and weaknesses of such an approach for studies of social behaviour. We find that robots-whether studied in groups of simulated or physical robots, or used to infiltrate and manipulate groups of living organisms-have important advantages over conventional individual-based models and have contributed greatly to the study of social behaviour. In particular, robots have increased our understanding of self-organization and the evolution of cooperative behaviour and communication. However, the resulting findings have not had the desired impact on the biological community. We suggest reasons for why this may be the case, and how the benefits of using robots can be maximized in future research on social behaviour.

Adaptation and the genetics of social behaviour.

In recent years much progress has been made towards understanding the selective forces involved in the evolution of social behaviour including conflicts over reproduction among group members. Here, I argue that an important additional step necessary for advancing our understanding of the resolution of potential conflicts within insect societies is to consider the genetics of the behaviours involved. First, I discuss how epigenetic modifications of behaviour may affect conflict resolution within groups. Second, I review known natural polymorphisms of social organization to demonstrate that a lack of consideration of the genetic mechanisms involved may lead to erroneous explanations of the adaptive significance of behaviour. Third, I suggest that, on the basis of recent genetic studies of sexual conflict in Drosophila, it is necessary to reconsider the possibility of within-group manipulation by means of chemical substances (i.e. pheromones). Fourth, I address the issue of direct versus indirect genetic effects, which is of particular importance for the study of behaviour in social groups. Fifth, I discuss the issue of how a genetic influence on dominance hierarchies and reproductive division of labour can have secondary effects, for example in the evolution of promiscuity. Finally, because the same sets of genes (e.g. those implicated in chemical signalling and the responses that are triggered) may be used even in species as divergent as ants, cooperative breeding birds and primates, an integration of genetic mechanisms into the field of social evolution may also provide unifying ideas.

The genetical theory of social behaviour.

We survey the population genetic basis of social evolution, using a logically consistent set of arguments to cover a wide range of biological scenarios. We start by reconsidering Hamilton's (Hamilton 1964 J. Theoret. Biol. 7, 1-16 (doi:10.1016/0022-5193(64)90038-4)) results for selection on a social trait under the assumptions of additive gene action, weak selection and constant environment and demography. This yields a prediction for the direction of allele frequency change in terms of phenotypic costs and benefits and genealogical concepts of relatedness, which holds for any frequency of the trait in the population, and provides the foundation for further developments and extensions. We then allow for any type of gene interaction within and between individuals, strong selection and fluctuating environments and demography, which may depend on the evolving trait itself. We reach three conclusions pertaining to selection on social behaviours under broad conditions. (i) Selection can be understood by focusing on a one-generation change in mean allele frequency, a computation which underpins the utility of reproductive value weights; (ii) in large populations under the assumptions of additive gene action and weak selection, this change is of constant sign for any allele frequency and is predicted by a phenotypic selection gradient; (iii) under the assumptions of trait substitution sequences, such phenotypic selection gradients suffice to characterize long-term multi-dimensional stochastic evolution, with almost no knowledge about the genetic details underlying the coevolving traits. Having such simple results about the effect of selection regardless of population structure and type of social interactions can help to delineate the common features of distinct biological processes. Finally, we clarify some persistent divergences within social evolution theory, with respect to exactness, synergies, maximization, dynamic sufficiency and the role of genetic arguments.

Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution.

Eusociality is taxonomically rare, yet associated with great ecological success. Surprisingly, studies of environmental conditions favouring eusociality are often contradictory. Harsh conditions associated with increasing altitude and latitude seem to favour increased sociality in bumblebees and ants, but the reverse pattern is found in halictid bees and polistine wasps. Here, we compare the life histories and distributions of populations of 176 species of Hymenoptera from the Swiss Alps. We show that differences in altitudinal distributions and development times among social forms can explain these contrasting patterns: highly social taxa develop more quickly than intermediate social taxa, and are thus able to complete the reproductive cycle in shorter seasons at higher elevations. This dual impact of altitude and development time on sociality illustrates that ecological constraints can elicit dynamic shifts in behaviour, and helps explain the complex distribution of sociality across ecological gradients.

The evolution of social discounting in hierarchically clustered populations.

The expression of a social behaviour may affect the fitness of actors and recipients living in the present and in the future of the population. When there is a risk that a future reward will not be experienced in such a context, the value of that reward should be discounted; but by how much? Here, we evaluate social discount rates for delayed fitness rewards to group of recipients living at different positions in both space and time than the actor in a hierarchically clustered population. This is a population where individuals are grouped into families, families into villages, villages into clans, and so on, possibly ad infinitum. The group-wide fitness effects are assumed to either increase or decrease the fecundity or the survival of recipients and can be arbitrarily extended in space and time. We find that actions changing the survival of individuals living in the future are generally more strongly discounted than fecundity-changing actions for all future times and that the value of future rewards increases as individuals live longer. We also find that delayed fitness effects may not only be discounted by a constant factor per unit delay (exponential discounting), but that, as soon as there is localized dispersal in a population, discounting per unit delay is likely to fall rapidly for small delays and then slowly for longer delays (hyperbolic discounting). As dispersal tends to be localized in natural populations, our results suggest that evolution is likely to favour individuals that express present-biased behaviours and that may be time-inconsistent with respect to their group-wide effects.

Fitness correlates with the extent of cheating in a bacterium.

There is growing awareness of the importance of cooperative behaviours in microbial communities. Empirical support for this insight comes from experiments using mutant strains, termed 'cheats', which exploit the cooperative behaviour of wild-type strains. However, little detailed work has gone into characterising the competitive dynamics of cooperative and cheating strains. We test three specific predictions about the fitness consequences of cheating to different extents by examining the production of the iron-scavenging siderophore molecule, pyoverdin, in the bacterium Pseudomonas aeruginosa. We create a collection of mutants that differ in the amount of pyoverdin that they produce (from 1% to 96% of the production of paired wild types) and demonstrate that these production levels correlate with both gene activity and the ability to bind iron. Across these mutants, we found that (1) when grown in a mixed culture with a cooperative wild-type strain, the relative fitness of a mutant is negatively correlated with the amount of pyoverdin that it produces; (2) the absolute and relative fitness of the wild-type strain in the mixed culture is positively correlated with the amount of pyoverdin that the mutant produces; and (3) when grown in a monoculture, the absolute fitness of the mutant is positively correlated with the amount of pyoverdin that it produces. Overall, we demonstrate that cooperative pyoverdin production is exploitable and illustrate how variation in a social behaviour determines fitness differently, depending on the social environment.

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.

Co-evolution between sociality and dispersal: The role of synergistic cooperative benefits.

Explaining the evolution of sociality is challenging because social individuals face disadvantages that must be balanced by intrinsic benefits of living in a group. One potential route towards the evolution of sociality may emerge from the avoidance of dispersal, which can be risky in some environments. Although early studies found that local competition may cancel the benefits of cooperation in viscous populations, subsequent studies have identified conditions, such as the presence of kin recognition or specific demographic conditions, under which altruism will still spread. Most of these studies assume that the costs of cooperating outweigh the direct benefits (strong altruism). In nature, however, many organisms gain synergistic benefits from group living, which may counterbalance even costly altruistic behaviours. Here, we use an individual based model to investigate how dispersal and social behaviour co-evolve when social behaviours result in synergistic benefits that counterbalance the relative cost of altruism to a greater extent than assumed in previous models. When the cost of cooperation is high, selection for sociality responds strongly to the cost of dispersal. In particular, cooperation can begin to spread in a population when higher cooperation levels become correlated with lower dispersal tendencies within individuals. In contrast, less costly social behaviours are less sensitive to the cost of dispersal. In line with previous studies, we find that mechanisms of global population control also affect this relationship: when whole patches (groups) go extinct each generation, selection favours a relatively high dispersal propensity, and social behaviours evolve only when they are not very costly. If random individuals within groups experience mortality each generation to maintain a global carrying capacity, on the other hand, social behaviours spread and dispersal is reduced, even when the latter is not costly.

New perspective on the study of the authority relationship: Integrating individual and societal level research.

The concept of authority crosses many social sciences, but there is a lack of common taxonomy and definitions on this topic. The aims of this review are: (1) to define the basic characteristics of the authority relationship, reaching a definition suitable for the different domains of social psychology and social sciences; (2) to bridge the gap between individual and societal levels of explanation concerning the authority relationship, by proposing an interpretation within the framework of social representations. The authority relationship can be conceived as a negotiation of meanings and it is closely linked to shared value orientation and the attribution of meanings negotiated within a society. We assume that the authority relationship is socially constructed and represents both a shared representation of society and a normative principle of social life. A multidisciplinary approach is adopted, crossing definitions and studies provided in sociology, political science, law and social psychology.

The interplay between relatedness and horizontal gene transfer drives the evolution of plasmid-carried public goods.

Plasmids carry a wide range of genes that are often involved in bacterial social behaviour. The question of why such genes are frequently mobile has received increasing attention. Here, we use an explicit population genetic approach to model the evolution of plasmid-borne bacterial public goods production. Our findings highlight the importance of both transmission and relatedness as factors driving the evolution of plasmid-borne public goods production. We partition the effects of plasmid transfer of social traits into those of infectivity and the effect of increased relatedness. Our results demonstrate that, owing to its effect on relatedness, plasmid mobility increases the invasion and stability of public goods, in a way not seen in individually beneficial traits. In addition, we show that plasmid transfer increases relatedness when public goods production is rare but this effect declines when production is common, with both scenarios leading to an increase in the frequency of plasmid-borne public goods. Plasmids remain important vectors for the spread of social genes involved in bacterial virulence thus an understanding of their dynamics is highly relevant from a public health perspective.

Reciprocal preening and food sharing in colour-polymorphic nestling barn owls.

Barn owl (Tyto alba) siblings preen and offer food items to one another, behaviours that can be considered prosocial because they benefit a conspecific by relieving distress or need. In experimental broods, we analysed whether such behaviours were reciprocated, preferentially exchanged between specific phenotypes, performed to avoid harassment and food theft or signals of hierarchy status. Three of the results are consistent with the hypothesis of direct reciprocity. First, food sharing was reciprocated in three-chick broods but not in pairs of siblings, that is when nestlings could choose a partner with whom to develop a reciprocating interaction. Second, a nestling was more likely to give a prey item to its sibling if the latter individual had preened the former. Third, siblings matched their investment in preening each other. Manipulation of age hierarchy showed that food stealing was directed towards older siblings but was not performed to compensate for a low level of cooperation received. Social behaviours were related to melanin-based coloration, suggesting that animals may signal their propensity to interact socially. The most prosocial phenotype (darker reddish) was also the phenotype that stole more food, and the effect of coloration on prosocial behaviour depended upon rank and sex, suggesting that colour-related prosociality is state dependent.

Social structure emerges via the interaction between local ecology and individual behaviour.

1. The formation of groups is a fundamental aspect of social organization, but there are still many questions regarding how social structure emerges from individuals making non-random associations. 2. Although food distribution and individual phenotypic traits are known to separately influence social organization, this is the first study, to our knowledge, experimentally linking them to demonstrate the importance of their interaction in the emergence of social structure. 3. Using an experimental design in which food distribution was either clumped or dispersed, in combination with individuals that varied in exploratory behaviour, our results show that social structure can be induced in the otherwise non-social European shore crab (Carcinus maenas). 4. Regardless of food distribution, individuals with relatively high exploratory behaviour played an important role in connecting otherwise poorly connected individuals. In comparison, low exploratory individuals aggregated into cohesive, stable subgroups (moving together even when not foraging), but only in tanks where resources were clumped. No such non-foraging subgroups formed in environments where food was evenly dispersed. 5. Body size did not accurately explain an individual's role within the network for either type of food distribution. 6. Because of their synchronized movements and potential to gain social information, groups of low exploratory crabs were more effective than singletons at finding food. 7. Because social structure affects selection, and social structure is shown to be sensitive to the interaction between ecological and behavioural differences among individuals, local selective pressures are likely to reflect this interaction.