Ants, as eusocial insects, exhibit some of the most fascinating and complex programs of social behavior in animals, wherein physiologically-distinct individuals use cooperative behaviors such as nursing, foraging, nest maintenance, defense and policing to sustain colony homeostasis. This division of labor is a central feature of advanced forms of sociality and often involves the allocation of behaviors among phenotypically distinct groups of individuals (termed castes) that vary by morphology, age and social context. Our lab is interested in epigenetic mechanisms that establish, sustain, and modulate caste-based division of behavior, using the evolutionarily divergent ants Camponotus floridanus, Atta cephalotes, and Harpegnathos saltator as model systems.
Camponotus floridanus Research
Our early work in this field produced the first genome-wide map of histone modifications in two distinct worker castes of the ant Camponotus floridanus, and identified the histone acetyl transferase (HAT) and transcriptional co-activator CREB Binding Protein (CBP) as an important regulator of caste specific differences in histone modification patterning and downstream gene expression in the brain. More recently, we have shown that experimental manipulation of HATs and histone deacetylases (HDACs) can reprogram the behavior of ant castes and sustain atypical behavioral programs in a stable manner for more than a month after treatment. This indicates that HATs and HDACs are important enzymatic partners in the dynamic regulation of behavioral programming achieved through the gene expression programs that alter the structure and function of nervous systems.
Our current projects focus on understanding how chromatin factors contribute to critical periods of behavioral plasticity during early adult life, as well as the closing of such critical periods later in life. We are also working on the epigenetic regulation of lifespan as a function of social environment and social enrichment. This work utilizes the effect of isolation on physiology, genetics, and epigenetics. We are also using 3D models within this study in collaboration with the Biomedical Library’s 3D printing lab.
The brain is the most complex tissue with huge diversity of cell types, gene regulation and cellular organization contributing to division of castes and differential social behavioral patterns. We are using single-cell transcriptome and epigenome sequencing techniques to dissect the ant brain heterogenety and identify caste and cell-type features regulating caste specification. Furthermore, we are also interested in studying how caste determination triggered and settled in larval and pupal developmental stages, using multi-omic and single-cell profiling approaches.
Atta cephalotes Research
We are utilizing the unique caste based social structure of Atta cephalotes ants in an effort to study the molecular regulation of behavioral and reproductive plasticity. Among fungus growing ants, only two species of the leaf cutting genera have highly polymorphic workers, with strong differences in size, morphology, and tasks—A. cephalotes one of these species. This makes it a unique model system because they display an extreme degree of castes and tasks performed: The Atta workers organize the gardening operation in the form of an assembly line. The most frequent size group among foragers, at the start of the line, consists of workers with a head width of 2.0 to 2.2 millimeters. At the end of the line, the care of the delicate fungal hyphae requires very small workers, a task filled within the nest by workers with a head width of predominantly 0.8 millimeter. The intervening steps in gardening are conducted by workers of graded intermediate size. After the returning foragers drop the pieces of vegetation onto the floor of a nest chamber, the pieces are picked up by workers of slightly smaller size, who clip them into fragments about 1 to 2 millimeters across. Within minutes, still smaller ants take over, crush and mold the fragments into moist pellets, add fecal droplets, and carefully insert them into a mass of similar material. Next, workers even smaller than those just described pluck loose strands of fungus from places of dense growth and plant them on the newly constructed surfaces. Finally, the very smallest and most abundant workers patrol the beds of fungal strands, delicately probing them with their antennae, licking their surfaces, and plucking out spores and hyphae of alien species of mold. Superimposed on this division of labor, which is based on anatomical worker subcastes, is age polyethism: young workers of most subcastes perform tasks inside the nest, and older workers tend to be involved in tasks outside the nest. This distinction is strikingly illustrated by the smallest worker subcastes (the so-called minim workers), which inside the nest tend the fungus and small brood, but which can also be seen at the harvesting site, even though they are unable to cut and carry leaf fragments. Many of them do not walk back to the nest on their own, but ride (“hitchhike”) on the leaf fragments being carried to the nest.
Using this extremely complex social system, we are trying to identify epigenetic regulators of this advanced caste-based system.
Harpegnathos saltator Research
Yan H, Opachaloemphan C, Mancini G, Yang H, Gallitto M, Mlejnek J, Leibholz A, Haight K, Ghaninia M, Huo L, Perry M, Slone J, Zhou X, Traficante M, Penick CA, Dolezal K, Gokhale K, Stevens K, Fetter-Pruneda I, Bonasio R, Zwiebel LJ, Berger SL, Liebig J, Reinberg D, Desplan C. Cell. 2017 Aug 10;170(4):736-747.
Simola, D. F., L. Wissler, et al. (2013). “Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality.” Genome Research.