A supergene-controlling social structure in Alpine ants also affects the dispersal ability and fecundity of each sex.

Social organization, dispersal and fecundity coevolve, but whether they are genetically linked remains little known. Supergenes are prime candidates for coupling adaptive traits and mediating sex-specific trade-offs. Here, we test whether a supergene that controls social structure in Formica selysi also influences dispersal-related traits and fecundity within each sex. In this ant species, single-queen colonies contain only the ancestral supergene haplotype M and produce MM queens and M males, while multi-queen colonies contain the derived haplotype P and produce MP queens, PP queens and P males. By combining multiple experiments, we show that the M haplotype induces phenotypes with higher dispersal potential and higher fecundity in both sexes. Specifically, MM queens, MP queens and M males are more aerodynamic and more fecund than PP queens and P males, respectively. Differences between MP and PP queens from the same colonies reveal a direct genetic effect of the supergene on dispersal-related traits and fecundity. The derived haplotype P, associated with multi-queen colonies, produces queens and males with reduced dispersal abilities and lower fecundity. More broadly, similarities between the Formica and Solenopsis systems reveal that supergenes play a major role in linking behavioural, morphological and physiological traits associated with intraspecific social polymorphisms.

Trail pheromone identification in the ant Crematogaster scutellaris.

In this work, we identified the trail pheromone of the ant Crematogaster scutellaris. We combined gas chromatography-mass spectrometry analysis of extracts from the hind tibia, the location of the respective glands, with automated trail following assays. The study found tridecan-2-ol to be the strongest discriminator between hind tibia and other body part extracts. Tridecan-2-ol elicited trail-following behaviour at concentrations of 1 ng/µL. A separation of the enantiomers showed responses to (R)-tridecan-2-ol already at 0.001 ng/µL and only at a 1000-fold higher concentration for (S)-tridecan-2-ol, suggesting that only the R enantiomer is used by C. scutellaris in its natural environment. We also found strong behavioural responses to 2-dodecanol, a substance that was not detectable in the hind tibia extract of C. scutellaris, but which has been reported to be the trail pheromone of the related species C. castanea. We discuss the contribution of these results to the 'dissection and reconstruction' of strategies and mechanisms underlying the social organization of ants.

Nutritional inequalities structure worker division of labor in social insects.

Eusocial insect societies are fundamentally non-egalitarian. The reproductive caste 'wins' in terms of resource accumulation, whereas non-reproductive workers 'lose'. Here, we argue that the division of labor among workers is also organized by nutritional inequalities. Across vastly different social systems and a variety of hymenopteran species, there is a recurrent pattern of lean foragers and corpulent nest workers. Experimental manipulations confirm causal associations between nutritional differences, associated molecular pathways, and behavioral roles in insect societies. The comparative and functional genomic data suggest that a conserved toolkit of core metabolic, nutrient storage, and signaling genes has evolved to regulate the social insect division of labor. Thus, the unequal distribution of food resources can be considered a fundamental organizing factor in the social insect division of labor.

Dissecting the costs of a facultative symbiosis in an isopod living with ants.

The balance between costs and benefits is expected to drive associations between species. While these balances are well understood for strict associations, we have no insights to which extent they determine facultative associations between species. Here, we quantified the costs of living in a facultative association, by studying the effects of red wood ants on the facultatively associated isopod Porcellio scaber. Porcellio scaber frequently occurred in and near hostile red wood ant nests and might outnumber obligate nest associates. The facultative association involved different costs for the isopod. We found that the density of the isopod decreases near the nest with higher ant traffic. Individuals in and near the nest were smaller than individuals further away from the nest. Smaller individuals were also found at sites with higher ant traffic. A higher proportion of wounded individuals was found closer to the nest and with higher ant traffic. We recorded pregnant females and juveniles in the nest suggesting that the life cycle can be completed inside the nests. Lab experiments showed that females died sooner and invested less in reproduction in presence of red wood ants. Porcellio scaber rarely provoked an aggression response, but large numbers were carried as prey to the nest. These preyed isopods were mainly dried out corpses. Our results showed that the ant association incurred several costs for a facultative associate. Consequently, red wood ant nests and their surrounding territory act as an alternative habitat where demographic costs are offset by a stable resource provisioning and protection.

Characterization of Queen Supergene Pheromone in the Red Imported Fire Ant Using Worker Discrimination Assays.

Ants use chemical signals to communicate for various purposes related to colony function. Social organization in the red imported fire ant, Solenopsis invicta, is determined by the Sb supergene, with colonies of the monogyne (single-queen) form lacking the element and colonies of the polygyne (multiple-queen) form possessing it. Polygyne workers accept new reproductive queens in their nest, but only those carrying Sb; young winged queens lacking this genetic element are executed as they mature sexually in their natal nest or as they attempt to enter a foreign nest to initiate reproduction after mating and shedding their wings. It has been suggested that queen supergene genotype status is signaled to workers by unsaturated cuticular hydrocarbons, while queen reproductive status is signaled by piperidines (venom alkaloids). We used high-throughput behavioral assays to study worker acceptance of paper dummies dosed with fractions of extracts of polygyne queens, or blends of synthetic counterparts of queen cuticular compounds. We show that the queen supergene pheromone comprises a blend of monoene and diene unsaturated hydrocarbons. Our assays also reveal that unsaturated hydrocarbons elicit discrimination by polygyne workers only when associated with additional compounds that signal queen fertility. This synergistic effect was obtained with a polar fraction of queen extracts, but not by the piperidine alkaloids, suggesting that the chemical(s) indicating queen reproductive status are compounds more polar than cuticular hydrocarbons but are not the piperidine alkaloids. Our results advance understanding of the role of chemical signaling that is central to the regulation of social organization in an important invasive pest and model ant species.

Linked supergenes underlie split sex ratio and social organization in an ant.

Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent-offspring conflict, genomic conflict, and cooperative breeding. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work predicted that worker control of sex ratio and variation in relatedness asymmetry among colonies would cause each colony to specialize in the production of one sex. While some empirical tests supported theoretical predictions, others deviated from them, leaving many questions about how split sex ratio emerges. One factor yet to be investigated is whether colony sex ratio may be influenced by the genotypes of queens or workers. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens future research on the evolutionary drivers of split sex ratio.

The Complexity of Social Complexity: A Quantitative Multidimensional Approach for Studies of Social Organization.

AbstractThe rapid increase in "big data" during the postgenomic era makes it crucial to appropriately measure the level of social complexity in comparative studies. We argue that commonly used qualitative classifications lump together species showing a broad range of social complexity and falsely imply that social evolution always progresses along a single linear stepwise trajectory that can be deduced from comparing extant species. To illustrate this point, we compared widely used social complexity measures in "primitively eusocial" bumble bees with "advanced eusocial" stingless bees, honey bees, and attine ants. We find that a single species can have both higher and lower levels of complexity compared with other taxa, depending on the social trait measured. We propose that measuring the complexity of individual social traits switches focus from semantic discussions and offers several directions for progress. First, quantitative social traits can be correlated with molecular, developmental, and physiological processes within and across lineages of social animals. This approach is particularly promising for identifying processes that influence or have been affected by social evolution. Second, key social complexity traits can be combined into multidimensional lineage-specific quantitative indices, enabling fine-scale comparison across species that are currently bundled within the same level of social complexity.

Interaction of red crabs with yellow crazy ants during migration on Christmas Island.

Invasive species have had a profound impact on ecosystems all over the world. Their presence can lead to fundamental changes in the biodiversity of a given ecosystem as well as the extinction of native species. In particular, this work looks at the effect on the Gecarcoidea natalis (Red Crab) population on Christmas Island due to the presence of vast arrays of supercolonies containing Anoplolepis gracilipes (Yellow Crazy Ant). We primarily study the inter-species interaction occurring during the crab migration to the island coast. We propose a microscopic model for the dynamics of the crabs and ants with the goal of increasing crab survival. Through analysis of the model, we investigate a range of potential preventative measures that could be taken to preserve the native crab population dependent on their locations. The main result of this work is that by considering the locations of ant supercolonies incorporated into Monte Carlo simulations of the model, we can identify the order that the supercolonies need to be removed to provide the greatest chance at survival for the crabs per migration cycle.

The social supergene dates back to the speciation time of two Solenopsis fire ant species.

Colony social organization of multiple Solenopsis fire ant species is determined by a supergene with two haplotypes SB and Sb, which are similar to X/Y sex chromosomes. The ancestral monogyne (single-queen) social form has been associated with homozygous SB/SB queens, while queens in colonies with the derived polygyne (multi-queen) social structure are heterozygous SB/Sb. By comparing 14 Solenopsis invicta genomes and the outgroup S. fugax, we dated the formation of the supergene to 1.1 (0.7-1.6) million years ago, much older than previous estimates, and close to the estimated time of speciation of the two socially polymorphic species S. invicta and S. richteri. We also used 12 S. invicta and S. richteri genomes to compare the evolutionary distances between these species and the distances between the social haplotypes, and found them to be similar. A phylogenetic analysis suggested that the monophyletic Sb clade is more closely related to S. richteri SB haplotypes than to S. invicta SB haplotypes. We conclude that the formation of the supergene occurred concomitantly with the process of speciation of the Solenopsis socially-polymorphic clade, and hypothesize that the Sb variant first arouse in one incipiently-speciating population and then introgressed into the other populations or species.

Maternal effect killing by a supergene controlling ant social organization.

Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.

Optimal foraging and the information theory of gambling.

At a macroscopic level, part of the ant colony life cycle is simple: a colony collects resources; these resources are converted into more ants, and these ants in turn collect more resources. Because more ants collect more resources, this is a multiplicative process, and the expected logarithm of the amount of resources determines how successful the colony will be in the long run. Over 60 years ago, Kelly showed, using information theoretic techniques, that the rate of growth of resources for such a situation is optimized by a strategy of betting in proportion to the probability of pay-off. Thus, in the case of ants, the fraction of the colony foraging at a given location should be proportional to the probability that resources will be found there, a result widely applied in the mathematics of gambling. This theoretical optimum leads to predictions as to which collective ant movement strategies might have evolved. Here, we show how colony-level optimal foraging behaviour can be achieved by mapping movement to Markov chain Monte Carlo (MCMC) methods, specifically Hamiltonian Monte Carlo (HMC). This can be done by the ants following a (noisy) local measurement of the (logarithm of) resource probability gradient (possibly supplemented with momentum, i.e. a propensity to move in the same direction). This maps the problem of foraging (via the information theory of gambling, stochastic dynamics and techniques employed within Bayesian statistics to efficiently sample from probability distributions) to simple models of ant foraging behaviour. This identification has broad applicability, facilitates the application of information theory approaches to understand movement ecology and unifies insights from existing biomechanical, cognitive, random and optimality movement paradigms. At the cost of requiring ants to obtain (noisy) resource gradient information, we show that this model is both efficient and matches a number of characteristics of real ant exploration.

Colony entropy-Allocation of goods in ant colonies.

Allocation of goods is a key feature in defining the connection between the individual and the collective scale in any society. Both the process by which goods are to be distributed, and the resulting allocation to the members of the society may affect the success of the population as a whole. One of the most striking natural examples of a highly successful cooperative society is the ant colony which often acts as a single superorganism. In particular, each individual within the ant colony has a "communal stomach" which is used to store and share food with the other colony members by mouth to mouth feeding. Sharing food between communal stomachs allows the colony as a whole to get its food requirements and, more so, allows each individual within the colony to reach its nutritional intake target. The vast majority of colony members do not forage independently but obtain their food through secondary interactions in which food is exchanged between individuals. The global effect of this exchange is not well understood. To gain better understanding into this process we used fluorescence imaging to measure how food from a single external source is distributed and mixed within a Camponotus sanctus ant colony. Using entropic measures to quantify food-blending, we show that while collected food flows into all parts of the colony it mixes only partly. We show that mixing is controlled by the ants' interaction rule which implies that only a fraction of the maximal potential is actually transferred. This rule leads to a robust blending process: i.e., neither the exact food volume that is transferred, nor the interaction schedule are essential to generate the global outcome. Finally, we show how the ants' interaction rules may optimize a trade-off between fast dissemination and efficient mixing. Our results regarding the distribution of a single food source provide a baseline for future studies on distributed regulation of multiple food sources in social insect colonies.

Ant colonies maintain social homeostasis in the face of decreased density.

Interactions lie at the heart of social organization, particularly in ant societies. Interaction rates are presumed to increase with density, but there is little empirical evidence for this. We manipulated density within carpenter ant colonies of the species Camponotus pennsylvanicus by quadrupling nest space and by manually tracking 6.9 million ant locations and over 3200 interactions to study the relationship between density, spatial organization and interaction rates. Colonies divided into distinct spatial regions on the basis of their underlying spatial organization and changed their movement patterns accordingly. Despite a reduction in both overall and local density, we did not find the expected concomitant reduction in interaction rates across all colonies. Instead, we found divergent effects across colonies. Our results highlight the remarkable organizational resilience of ant colonies to changes in density, which allows them to sustain two key basic colony life functions, that is food and information exchange, during environmental change.

Social Complexity and Brain Evolution: Comparative Analysis of Modularity and Integration in Ant Brain Organization.

The behavioral demands of living in social groups have been linked to the evolution of brain size and structure, but how social organization shapes investment and connectivity within and among functionally specialized brain regions remains unclear. To understand the influence of sociality on brain evolution in ants, a premier clade of eusocial insects, we statistically analyzed patterns of brain region size covariation as a proxy for brain region connectivity. We investigated brain structure covariance in young and old workers of two formicine ants, the Australasian weaver ant Oecophylla smaragdina, a pinnacle of social complexity in insects, and its socially basic sister clade Formica subsericea. As previously identified in other ant species, we predicted that our analysis would recognize in both species an olfaction-related brain module underpinning social information processing in the brain, and a second neuroanatomical cluster involved in nonolfactory sensorimotor processes, thus reflecting conservation of compartmental connectivity. Furthermore, we hypothesized that covariance patterns would reflect divergence in social organization and life histories either within this species pair or compared to other ant species. Contrary to our predictions, our covariance analyses revealed a weakly defined visual, rather than olfactory, sensory processing cluster in both species. This pattern may be linked to the reliance on vision for worker behavioral performance outside of the nest and the correlated expansion of the optic lobes to meet navigational demands in both species. Additionally, we found that colony size and social organization, key measures of social complexity, were only weakly correlated with brain modularity in these formicine ants. Worker age also contributed to variance in brain organization, though in different ways in each species. These findings suggest that brain organization may be shaped by the divergent life histories of the two study species. We compare our findings with patterns of brain organization of other eusocial insects.

No mate preference associated with the supergene controlling social organization in Alpine silver ants.

Disassortative mating is a powerful mechanism stabilizing polymorphisms at sex chromosomes and other supergenes. The Alpine silver ant, Formica selysi, has two forms of social organization-single-queen and multiple-queen colonies-determined by alternate haplotypes at a large supergene. Here, we explore whether mate preference contributes to the maintenance of the genetic polymorphism at the social supergene. With mate choice experiments, we found that females and males mated randomly with respect to social form. Moreover, queens were able to produce offspring irrespective of whether they had mated with a male from the same or the alternative social form. Yet, females originating from single-queen colonies were more fertile, suggesting that they may be more successful at independent colony founding. We conclude that the pattern of asymmetric assortative mating documented from mature F. selysi colonies in the field is not caused by mate preferences or major genetic incompatibilities between social forms. More generally, we found no evidence that disassortative mate preference contributes to the maintenance of polymorphism at this supergene controlling ant social organization.

Optimal construction of army ant living bridges.

Integrating the costs and benefits of collective behaviors is a fundamental challenge to understanding the evolution of group living. These costs and benefits can rarely be quantified simultaneously due to the complexity of the interactions within the group, or even compared to each other because of the absence of common metrics between them. The construction of 'living bridges' by New World army ants - which they use to shorten their foraging trails - is a unique example of a collective behavior where costs and benefits have been experimentally measured and related to each other. As a result, it is possible to make quantitative predictions about when and how the behavior will be observed. In this paper, we extend a previous mathematical model of these costs and benefits to much broader domain of applicability. Specifically, we exhibit a procedure for analyzing the optimal formation, and final configuration, of army ant living bridges given a means to express the geometrical configuration of foraging path obstructions. Using this procedure, we provide experimentally testable predictions of the final bridge position, as well as the optimal formation process for certain cases, for a wide range of scenarios, which more closely resemble common terrain obstacles that ants encounter in nature. As such, our framework offers a rare benchmark for determining the evolutionary pressures governing the evolution of a naturally occurring collective animal behavior.

orco Mutagenesis Causes Loss of Antennal Lobe Glomeruli and Impaired Social Behavior in Ants.

Life inside ant colonies is orchestrated with diverse pheromones, but it is not clear how ants perceive these social signals. It has been proposed that pheromone perception in ants evolved via expansions in the numbers of odorant receptors (ORs) and antennal lobe glomeruli. Here, we generate the first mutant lines in the clonal raider ant, Ooceraea biroi, by disrupting orco, a gene required for the function of all ORs. We find that orco mutants exhibit severe deficiencies in social behavior and fitness, suggesting they are unable to perceive pheromones. Surprisingly, unlike in Drosophila melanogaster, orco mutant ants also lack most of the ∼500 antennal lobe glomeruli found in wild-type ants. These results illustrate that ORs are essential for ant social organization and raise the possibility that, similar to mammals, receptor function is required for the development and/or maintenance of the highly complex olfactory processing areas in the ant brain. VIDEO ABSTRACT.

Worker brain development and colony organization in ants: Does division of labor influence neuroplasticity?

Brain compartment size allometries may adaptively reflect cognitive needs associated with behavioral development and ecology. Ants provide an informative system to study the relationship of neural architecture and development because worker tasks and sensory inputs may change with age. Additionally, tasks may be divided among morphologically and behaviorally differentiated worker groups (subcastes), reducing repertoire size through specialization and aligning brain structure with task-specific cognitive requirements. We hypothesized that division of labor may decrease developmental neuroplasticity in workers due to the apparently limited behavioral flexibility associated with task specialization. To test this hypothesis, we compared macroscopic and cellular neuroanatomy in two ant sister clades with striking contrasts in worker morphological differentiation and colony-level social organization: Oecophylla smaragdina, a socially complex species with large colonies and behaviorally distinct dimorphic workers, and Formica subsericea, a socially basic species with small colonies containing monomorphic workers. We quantified volumes of functionally distinct brain compartments in newly eclosed and mature workers and measured the effects of visual experience on synaptic complex (microglomeruli) organization in the mushroom bodies-regions of higher-order sensory integration-to determine the extent of experience-dependent neuroplasticity. We demonstrate that, contrary to our hypothesis, O. smaragdina workers have significant age-related volume increases and synaptic reorganization in the mushroom bodies, whereas F. subsericea workers have reduced age-related neuroplasticity. We also found no visual experience-dependent synaptic reorganization in either species. Our findings thus suggest that changes in the mushroom body with age are associated with division of labor, and therefore social complexity, in ants. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 77: 1072-1085, 2017.

Inter-group cooperation in humans and other animals.

Social interactions are often characterized by cooperation within groups and conflict or competition between groups. In certain circumstances, however, cooperation can arise between social groups. Here, we examine the circumstances under which inter-group cooperation is expected to emerge and present examples with particular focus on groups in two well-studied but dissimilar taxa: humans and ants. Drivers for the evolution of inter-group cooperation include overarching threats from predators, competitors or adverse conditions, and group-level resource asymmetries. Resources can differ between groups in both quantity and type. Where the difference is in type, inequalities can lead to specialization and division of labour between groups, a phenomenon characteristic of human societies, but rarely seen in other animals. The ability to identify members of one's own group is essential for social coherence; we consider the proximate roles of identity effects in shaping inter-group cooperation and allowing membership of multiple groups. Finally, we identify numerous valuable avenues for future research that will improve our understanding of the processes shaping inter-group cooperation.

Onset of fights and mutual assessment in ant founding queens.

In animals, the progress and outcome of contests can be influenced by an individual's own condition, their opponent's condition or a combination of the two. The use of chemical information to assess the quality of rivals has been underestimated despite its central role in the regulation of social interactions in many taxa. Here, we studied pairwise contests between founding queens of the ant Lasius niger to investigate whether the decision to engage in agonistic interactions relies on self-assessment or mutual assessment. Queens modulated their aggressive behaviours depending on both their own status and their opponent's status. We found no influence of lipid stores or size on the onset of fights. However, differences in cuticular chemical signatures linked to fertility status accurately predicted the probability of behaving aggressively in pairs. Our study thus suggests that ant queens could rely on mutual assessment via chemical cues to make informed decisions about fight initiation.