The initial fitness benefits of group living are considered to be the greatest hurdle to the evolution of sociality, and evolutionary theory predicts that these benefits need to arise at very small group sizes. Such benefits are thought to emerge partly from scaling effects that increase efficiency as group size increases. In social insects and other taxa, the benefits of group living have been proposed to stem from division of labour, which is characterized by between-individual variability and within-individual consistency (specialization) in task performance. However, at the onset of sociality groups were probably small and composed of similar individuals with potentially redundant-rather than complementary-function. Self-organization theory suggests that division of labour can emerge even in relatively small, simple groups. However, empirical data on the effects of group size on division of labour and on fitness remain equivocal. Here we use long-term automated behavioural tracking in clonal ant colonies, combined with mathematical modelling, to show that increases in the size of social groups can generate division of labour among extremely similar workers, in groups as small as six individuals. These early effects on behaviour were associated with large increases in homeostasis-the maintenance of stable conditions in the colony-and per capita fitness. Our model suggests that increases in homeostasis are primarily driven by increases in group size itself, and to a smaller extent by a higher division of labour. Our results indicate that division of labour, increased homeostasis and higher fitness can emerge naturally in social groups that are small and homogeneous, and that scaling effects associated with increasing group size can thus promote social cohesion at the incipient stages of group living.

We investigated sex-specific recombination rates in Hyla arborea, a species with nascent sex chromosomes and male heterogamety. Twenty microsatellites were clustered into six linkage groups, all showing suppressed or very low recombination in males. Seven markers were sex linked, none of them showing any sign of recombination in males (rZ0.00 versus 0.43 on average in females). This opposes classical models of sex chromosome evolution, which envision an initially small differential segment that progressively expands as structural changes accumulate on the Y chromosome. For autosomes, maps were more than 14 times longer in females than in males, which seems the highest ratio documented so far in vertebrates. These results support the pleiotropic model of Haldane and Huxley, according to which recombination is reduced in the heterogametic sex by general modifiers that affect recombination on the whole genome.

Mixed‐genotype infections have attracted considerable attention as drivers of pathogen evolution. However, experimental approaches often overlook essential features of natural host–parasite interactions, such as host heterogeneity, or the effects of between‐host selection during transmission. Here, following inoculation of a mixed infection, we analyse the success of different strains of a trypanosome parasite throughout the colony cycle of its bumblebee host. We find that most colonies efficiently filter the circulating infection before it reaches the new queens, the only offspring that carry infections to the next season. A few colonies with a poor filtering ability thus contributed disproportionately to the parasite population in the next season. High strain diversity but not high infection intensity within colony was associated with an increased probability of transmission of the infection to new queens. Interestingly, the representation of the different strains changed dramatically over time, so that long‐term parasite success could not be predicted from short‐term observations. These findings highlight the shaping of within‐colony parasite diversity through filtering as a crucial determinant of year‐to‐year pathogen transmission and emphasize the importance of host ecology and heterogeneity for disease dynamics.

The very diverse social systems of sweat bees make them interesting models to study social evolution. Here we focus on the dispersal behaviour and social organization of Halictus scabiosae, a common yet poorly known species of Europe. By combining field observations and genetic data, we show that females have multiple reproductive strategies, which generates a large diversity in the social structure of nests. A detailed microsatellite analysis of 60 nests revealed that 55% of the nests contained the offspring of a single female, whereas the rest had more complex social structures, with three clear cases of multiple females reproducing in the same nest and frequent occurrence of unrelated individuals. Drifting among nests was surprisingly common, as 16% of the 122 nests in the overall sample and 44% of the nests with complex social structure contained females that had genotypes consistent with being full-sisters of females sampled in other nests of the population. Drifters originated from nests with an above-average productivity and were unrelated to their nestmates, suggesting that drifting might be a strategy to avoid competition among related females. The sex-specific comparison of genetic differentiation indicated that dispersal was male-biased, which would reinforce local resource competition among females. The pattern of genetic differentiation among populations was consistent with a dynamic process of patch colonization and extinction, as expected from the unstable, anthropogenic habitat of this species. Overall, our data show that H. scabiosae varies greatly in dispersal behaviour and social organization. The surprisingly high frequency of drifters echoes recent findings in wasps and bees, calling for further investigation of the adaptive basis of drifting in the social insects.

The effects of heterogeneity in group composition remain a major hurdle to our understanding of collective behavior across disciplines. In social insects, division of labor (DOL) is an emergent, colony-level trait thought to depend on colony composition. Theoretically, behavioral response threshold models have most commonly been employed to investigate the impact of heterogeneity on DOL. However, empirical studies that systematically test their predictions are lacking because they require control over colony composition and the ability to monitor individual behavior in groups, both of which are challenging. Here, we employ automated behavioral tracking in 120 colonies of the clonal raider ant with unparalleled control over genetic, morphological, and demographic composition. We find that each of these sources of variation in colony composition generates a distinct pattern of behavioral organization, ranging from the amplification to the dampening of inherent behavioral differences in heterogeneous colonies. Furthermore, larvae modulate interactions between adults, exacerbating the apparent complexity. Models based on threshold variation alone only partially recapitulate these empirical patterns. However, by incorporating the potential for variability in task efficiency among adults and task demand among larvae, we account for all the observed phenomena. Our findings highlight the significance of previously overlooked parameters pertaining to both larvae and workers, allow the formulation of theoretical predictions for increasing colony complexity, and suggest new avenues of empirical study.

Parasite diversity is a constant challenge to host immune systems and has important clinical implications, but factors underpinning its emergence and maintenance are still poorly understood. Hosts typically harbour multiple parasite genotypes that share both host resources and immune responses. Parasite diversity is thus shaped not only by resource competition between co-infecting parasites but also by host-driven immune-mediated competition. We investigated these effects in an insect-trypanosome system, combining in vivo and in vitro single and double inoculations. In vivo, a non-pathogenic, general immune challenge was used to manipulate host immune condition and resulted in a reduced ability of hosts to defend against a subsequent exposure to the trypanosome parasites, illustrating the costs of immune activation. The associated increase in available host space benefited the weaker parasite strains of each pair as much as the otherwise more competitive strains, resulting in more frequent multiple infections in immune-challenged hosts. In vitro assays showed that in the absence of a host, overall parasite diversity was minimal because the outcome of competition was virtually fixed and resulted in strain extinction. Altogether, this shows that parasite competition is largely host-mediated and suggests a role for host immune condition in the maintenance of parasite diversity.

Division of labor in insect societies relies on simple behavioral rules, whereby individual colony members respond to dynamic signals indicating the need for certain tasks to be performed. This in turn gives rise to colony-level phenotypes. However, empirical studies quantifying colony-level signal-response dynamics are lacking. Here, we make use of the unusual biology and experimental amenability of the queenless clonal raider ant Cerapachys biroi, to jointly quantify the behavioral and physiological responses of workers to a social signal emitted by larvae. Using automated behavioral quantification and oocyte size measurements in colonies of different sizes and with different worker to larvae ratios, we show that the workers in a colony respond to larvae by increasing foraging activity and inhibiting ovarian activation in a progressive manner, and that these responses are stronger in smaller colonies. This work adds to our knowledge of the processes that link plastic individual behavioral/physiological responses to colony-level phenotypes in social insect colonies.

Social animals display a wide range of behavioural defences against infectious diseases, some of which increase social contacts with infectious individuals (e.g. mutual grooming), while others decrease them (e.g. social exclusion). These defences often rely on the detection of infectious individuals, but this can be achieved in several ways that are difficult to differentiate. Here, we combine non-pathogenic immune challenges with automated tracking in colonies of the clonal raider ant to ask whether ants can detect the immune status of their social partners and to quantify their behavioural responses to this perceived infection risk. We first show that a key behavioural response elicited by live pathogens (allogrooming) can be qualitatively recapitulated by immune challenges alone. Automated scoring of interactions between all colony members reveals that this behavioural response increases the network centrality of immune-challenged individuals through a general increase in physical contacts. These results show that ants can detect the immune status of their nest-mates and respond with a general ‘caring’ strategy, rather than avoidance, towards social partners that are perceived to be infectious. Finally, we find no evidence that changes in cuticular hydrocarbon profiles drive these behavioural effects.