The Genetic Architecture of Reproductive Caste Determination in Ants

The evolution of sociality is one of lifes major transitions. In the highly social insect societies some individuals, the queens, specialize at reproduction while others, the workers, carry out all of the other tasks necessary for colony survival. This division of labor system is the very foundation of social insect societies, which are among the most evolutionarily and ecologically successful animals on Earth. The primary objective of this project is to find and validate the genes primarily responsible for generating reproductive division of labor (castes) in an ant society. In Pogonomyrmex barbatus seed harvester ants the queens are over 3 times the size of workers (by mass), and primarily differ from workers in having well developed ovaries and wings. These dramatic differences in morphology and physiology arise as a result of differences in larval development. While in most social insects the developmental pathways leading to queens and workers result from differences in environmental factors, in some Pogonomyrmex populations they result from genetic differences (genetic caste determination, GCD). This unique mode of caste determination allows for the differentiation of queen- and worker-destined larvae prior to any observable differences in morphology (using genetic markers). Furthermore, the evolution of this system has necessitated the linkage of genes involved in the development of caste differences. This proposal outlines two complementary approaches to find candidate genes involved in caste determination 1) genetic mapping to find genes in genomic regions associated with GCD, and 2) comparisons of gene expression between queen- and worker-destined larvae during development. Candidate genes generated from both approaches will then be validated by qRT-PCR and ultimately dsRNAi. To achieve these objectives it will be essential to develop genomic infrastructure in order to map, locate and amplify the candidate genes. This will involve the de novo sequencing of the first ant genome. In addition to providing the resources to unmask the quintessential genes for complex sociality (caste genes), a sequenced ant genome will lead to a better understanding of how social living impacts life processes such as aging, immunity, and communication, as well as how genes and genomes interact to produce emergent properties (i.e., the superorganism). In terms of broader impacts, this proposal includes activities involving K-12, undergraduate, graduate, and post-doctoral education. Through collaborations with local high schools (the Great Hearts Academies) this project will help develop the next generation of scientists and teach tools necessary for an integrative modern biological approach. This research will impact undergraduate and graduate training in science through partnerships with several local programs designed to increase minority student involvement in the sciences and a graduate study collaboration with the Universidad de Quertaro in Mexico. Furthermore, both the PIs of this proposal have organized a workshop on ant genomics to bring together the ant research community in a collaborative effort to solve major evolutionary questions using ant genomics; this workshop hosts representatives from 18 universities across 6 countries. With the sequenced ant genome from this proposal, along with resources generated throughout the ant research community, the infrastructure will be available to ask questions related to phenotypic plasticity, evolutionary novelty, the interaction of environment and genotype in the production of adaptive phenotypes, kinship and the evolution of sociality, reproductive conflict and other fundamental questions in development, behavior, ecology, and evolutionary biology.