Sparse and stereotyped encoding implicates a core glomerulus for ant alarm behavior.

Ants communicate via large arrays of pheromones and possess expanded, highly complex olfactory systems, with antennal lobes in the brain comprising up to ∼500 glomeruli. This expansion implies that odors could activate hundreds of glomeruli, which would pose challenges for higher-order processing. To study this problem, we generated transgenic ants expressing the genetically encoded calcium indicator GCaMP in olfactory sensory neurons. Using two-photon imaging, we mapped complete glomerular responses to four ant alarm pheromones. Alarm pheromones robustly activated ≤6 glomeruli, and activity maps for the three pheromones inducing panic alarm in our study species converged on a single glomerulus. These results demonstrate that, rather than using broadly tuned combinatorial encoding, ants employ precise, narrowly tuned, and stereotyped representations of alarm pheromones. The identification of a central sensory hub glomerulus for alarm behavior suggests that a simple neural architecture is sufficient to translate pheromone perception into behavioral outputs.

A caste differentiation mutant elucidates the evolution of socially parasitic ants.

Most ant species have two distinct female castes-queens and workers-yet the developmental and genetic mechanisms that produce these alternative phenotypes remain poorly understood. Working with a clonal ant, we discovered a variant strain that expresses queen-like traits in individuals that would normally become workers. The variants show changes in morphology, behavior, and fitness that cause them to rely on workers in wild-type (WT) colonies for survival. Overall, they resemble the queens of many obligately parasitic ants that have evolutionarily lost the worker caste and live inside colonies of closely related hosts. The prevailing theory for the evolution of these workerless social parasites is that they evolve from reproductively isolated populations of facultative intermediates that acquire parasitic phenotypes in a stepwise fashion. However, empirical evidence for such facultative ancestors remains weak, and it is unclear how reproductive isolation could gradually arise in sympatry. In contrast, we isolated these variants just a few generations after they arose within their WT parent colony, implying that the complex phenotype reported here was induced in a single genetic step. This suggests that a single genetic module can decouple the coordinated mechanisms of caste development, allowing an obligately parasitic variant to arise directly from a free-living ancestor. Consistent with this hypothesis, the variants have lost one of the two alleles of a putative supergene that is heterozygous in WTs. These findings provide a plausible explanation for the evolution of ant social parasites and implicate new candidate molecular mechanisms for ant caste differentiation.

Hourglass Model for Developmental Evolution of Ant Castes.

Classic models for the development and evolution of ant castes struggle to explain recent empirical results. Here, we propose an hourglass model compatible with all existing data, providing a formal, falsifiable framework for future study. This illustrates how phenotypic variation can be used to infer underlying developmental and genetic architecture.

Globally invasive populations of the clonal raider ant are derived from Bangladesh.

Identifying the native range of invasive species is useful to understand their evolution and natural history, as well as to develop new methods to control potentially harmful introduced organisms. The clonal raider ant, Ooceraea biroi, is an introduced species and an increasingly important social insect model organism, but its native range remains unknown. Here, we report a new series of O. biroi collections from Bangladesh, Singapore, Vietnam and China. We use a molecular phylogeny constructed with five gene fragments from 27 samples to determine that invasive lineages of O. biroi originated in Bangladesh. These lineages may have spread from Bangladesh via the historically significant Bay of Bengal shipping ports. Ooceraea biroi shares multiple features of its biology with other introduced ants, including parthenogenesis, retention of heterozygosity and presence of multiple egg-layers in the colony. Using laboratory rearing and microsatellite markers, we show that colonies collected from disturbed habitat in Bangladesh have these traits in common with colonies from the invasive range. Ancestral populations with sexual reproduction in primary habitats either remain to be discovered or have gone extinct. Our findings advance our understanding of the global spread of the clonal raider ant and highlight a suite of general traits that make certain ants prone to becoming invasive.

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.

Caste development and evolution in ants: it's all about size.

Female ants display a wide variety of morphological castes, including workers, soldiers, ergatoid (worker-like) queens and queens. Alternative caste development within a species arises from a variable array of genetic and environmental factors. Castes themselves are also variable across species and have been repeatedly gained and lost throughout the evolutionary history of ants. Here, we propose a simple theory of caste development and evolution. We propose that female morphology varies as a function of size, such that larger individuals possess more queen-like traits. Thus, the diverse mechanisms that influence caste development are simply mechanisms that affect size in ants. Each caste-associated trait has a unique relationship with size, producing a phenotypic space that permits some combinations of worker- and queen-like traits, but not others. We propose that castes are gained and lost by modifying the regions of this phenotypic space that are realized within a species. These modifications can result from changing the size-frequency distribution of individuals within a species, or by changing the association of tissue growth and size. We hope this synthesis will help unify the literature on caste in ants, and facilitate the discovery of molecular mechanisms underlying caste development and evolution.