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The evolution of social life and division of labour

Final Report Summary - SOCIAL LIFE (The evolution of social life and division of labour)

The first part of the project consisted in studying division of labor among ant workers. We used a tracking system to continuously monitor individually tagged workers in six colonies of the ant Camponotus fellah over 41 days. Network analyses of more than 9 million interactions revealed three distinct groups that differ in behavioral repertoires. Each group represents a functional behavioral unit with workers moving from one group to the next as they age. The rate of interactions was much higher within groups than between groups. The precise information on spatial and temporal distribution of all individuals allowed us to calculate the expected rates of within- and between-group interactions. These values suggest that the network of interaction within colonies is primarily mediated by age-induced changes in the spatial location of workers.

The second part of the project consisted in conducting quantitative test for kin selection theory which had not yet been possible due to the difficulty of quantifying the costs and benefits of helping acts. In this study we conduct simulations with the help of a simulated system of foraging robots to manipulate the costs and benefits of altruism and determine the conditions under which altruism evolves. By conducting experimental evolution over hundreds of generations of selection in populations with different costs and benefits of altruistic behavior, we show that kin selection theory always accurately predicts the minimum relatedness necessary for altruism to evolve. This high accuracy is remarkable given the presence of pleiotropic and epistatic effects as well as mutations with strong effects on behavior and fitness. In addition to providing the first quantitative test of kin selection theory in a system with a complex mapping between genotype and phenotype, this study reveals that a fundamental principle of natural selection also applies to synthetic organisms when these have heritable properties.

The third part of the project consisted in studying the genetic basis of social organization. In the fire ant Solenopsis invicta, the existence of two divergent forms of social organization is under the control of a single Mendelian genomic element marked by two variants of an odorant-binding protein gene. We characterized the genomic region responsible for this important social polymorphism, and showed that it is part of a pair of hetero- morphic chromosomes that have many of the key properties of sex chromosomes. The two variant, (the social B and social b (SB and Sb) chromosomes) are characterized by a large region of approximately 13 megabases (55% of the chromosome) in which recombination is completely suppressed between SB and Sb. Recombination seems to occur normally between the SB chromo- somes but not between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differenti- ation between SB and Sb, and the vast majority of the 616 genes identified in the non-recombining region are present in the two variants. The lack of recombination over more than half of the two heteromorphic social chromosomes can be explained by at least one large inversion of around 9 megabases, and this absence of recombination has led to the accumulation of deleterious mutations, including repetitive elements in the non-recombining region of Sb compared with the homologous region of SB. Importantly, most of the genes with demonstrated expression differences between indi- viduals of the two social forms reside in the non-recombining region. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting together by locally limiting recombination.