An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants

Abstract

Summary Ants exhibit cooperative behaviors and advanced forms of sociality that depend on pheromone-mediated communication. Odorant receptor neurons (ORNs) express specific odorant receptors (ORs) encoded by a dramatically expanded gene family in ants. In most eusocial insects, only the queen can transmit genetic information, restricting genetic studies. In contrast, workers in Harpegnathos saltator ants can be converted into gamergates (pseudoqueens) that can found entire colonies. This feature facilitated CRISPR-Cas9 generation of germline mutations in orco, the gene that encodes the obligate co-receptor of all ORs. orco mutations should significantly impact olfaction. We demonstrate striking functions of Orco in odorant perception, reproductive physiology and social behavior plasticity. Surprisingly, unlike in other insects, loss of OR functionality also dramatically impairs development of the antennal lobe where ORNs project. Therefore, the development of genetics in Harpegnathos establishes this ant species as a model organism to study the complexity of eusociality.

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

“…If this model is correct, then this orco dependent stage of glomerulus expansion could represent an evolutionary change in the development of ants relative to flies that is related to the evolution of expanded OR repertoires. Inspired by our initial findings, colleagues decided to also examine brains of a second ant species in which they had generated an orco mutant, and they found an antennal lobe phenotype similar to what we had observed in O. biroi (reported in this issue of Cell, Yan et al, 2017). These results further indicate that the role of orco in neuro-anatomy is likely conserved throughout the ants.…”

Molecular characterization and evolution of a chemosensory receptor gene family in three notorious rice planthoppers, Nilaparvata lugens, Sogatella furcifera and Laodelphax striatellus, based on genome and transcriptome analyses

“…In addition, these ants were largely missing their antennal lobe glomeruli. 101,102 This study is an addition to the knowledge of the olfactory mechanism in rice planthoppers. Odorant binding proteins are important for binding odorants and in rice-plant seeking behavior.…”

“…The results are similar to recent studies in which Orco knockout ants Harpegnathos saltatory were completely unaware of chemical cues, becoming asocial, leaving their nests, and not foraging for food. In addition, these ants were largely missing their antennal lobe glomeruli …”

Olfactory co‐receptor Orco stimulated by Rice stripe virus is essential for host seeking behavior in small brown planthopper

“…It is now appreciated the striking functions of insect Orco in odorant perception, reproductive physiology, and social behavior plasticity. 24 In this study, we identified the gene encoding Orco protein of SBPH L. striatellus. The sequence alignment and homology analysis demonstrated significant conservation of Orco among different order insects, which were separated by millions of years on the evolutionary scale.…”

“…Orco is also required for OR trafficking past the ciliary constriction into the outer dendrites . In addition, knockout or mutation of Orco gene has also revealed that Orco is required for insect olfaction . In ants, Orco mutagenesis also impaired neural development .…”