CAREER: Genomic and Phenotypic Evolution of a Social Symbiosis

The biosphere is a network of ecological relationships connecting organisms across all grades of complexity. Whether between microbes or mammals, ecological relationships depend on features that enable organisms to interact across species boundaries. A major goal of modern biology is to identify these traits, understand how they function, and infer how they evolved at the genetic level.

An outstanding challenge in the study of biological interactions is explaining how animals evolve relationships with other species via changes in the brain, behavior and communication. This proposal addresses this challenge by examining a symbiosis between two animals—an ant species, and a rove beetle that lives as a social impostor inside the ant’s colony.

By studying the beetle’s nervous system and chemical glands, mechanisms will be uncovered that enable the beetle to accurately detect and chemically manipulate its ant partner, consequently integrating into colony life. Comparisons with related beetle species that live independently of ants will reveal how the symbiotic beetle’s behavior and chemical communication systems evolved.

This work will illuminate how different animal species recognize and interact with each other, informing our understanding of how brains process sensory information about other organisms and generate social behavior. This research could advance agricultural control strategies by discovering novel compounds that disrupt pest species biology. It may also aid in countering invasive species.

This program also provides undergraduate research experience that is trans-disciplinary, preparing the next generation of scientists to participate in the bioeconomy.

Complex interspecies relationships pervade the Metazoa, but knowledge of the molecular and neurobiological mechanisms underlying these lifestyles is scarce. Animal symbioses are often hard to reconstitute in the laboratory, whereas classical models such as Drosophila and mice exhibit negligible interactions with other species. Rove beetles (Staphylinidae) comprise a remarkable clade in which numerous lineages have convergently evolved into 'myrmecophiles': behavioral symbionts of ant colonies.

Evolution of this way of life involves radical changes in behavior and chemical communication, allowing rove beetles to hijack ant chemical cues and assimilate into the social fabric of the nest. This proposal will break open the molecular architecture of animal symbiosis by pioneering the myrmecophile rove beetle Sceptobius as a model. This goal will be achieved by: 1) Uncovering adaptive chemosensory and neuroanatomical changes enabling Sceptobius to recognize and socially interact with its host ant; 2) Revealing cellular and molecular mechanisms permitting Sceptobius to chemically mimic and behaviorally manipulate ants; and 3) Leveraging population genomic variation in this ant-myrmecophile system to illuminate coevolutionary dynamics of symbiotic animals and their hosts.

Development of a behaviorally symbiotic model insect will impact understanding of species interactions across the spectrum of biological complexity. This proposal has ramifications for the fields of neuroscience, behavior and chemical ecology, and will enhance our knowledge of genomic, cellular and developmental evolutionary processes.

This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.