TY - JOUR
T1 - An Engineered orco Mutation Produces Aberrant Social Behavior and Defective Neural Development in Ants
AU - Yan, Hua
AU - Opachaloemphan, Comzit
AU - Mancini, Giacomo
AU - Yang, Huan
AU - Gallitto, Matthew
AU - Mlejnek, Jakub
AU - Leibholz, Alexandra
AU - Haight, Kevin
AU - Ghaninia Tabarestani, Majid
AU - Huo, Lucy
AU - Perry, Michael
AU - Slone, Jesse
AU - Zhou, Xiaofan
AU - Traficante, Maria
AU - Penick, Clint
AU - Dolezal, Kelly
AU - Gokhale, Kaustubh
AU - Stevens, Kelsey
AU - Fetter-Pruneda, Ingrid
AU - Bonasio, Roberto
AU - Zwiebel, Laurence J.
AU - Berger, Shelley L.
AU - Liebig, Juergen
AU - Reinberg, Danny
AU - Desplan, Claude
N1 - Funding Information:
We appreciate the advice and assistance from Gregory Pask, Daniel Simola, and Takahiro Ohde in designing orco sgRNAs and improving reproduction of individually isolated ants; from Brittany Enzmann for embryo injections; from Christopher Albin-Brooks for behavioral responses to odorants; from Waring (Buck) Trible (Daniel Kronauer's lab) for deep sequencing to test somatic mutation efficiency; from Haiyan Zheng and Shengjiang Tu for mass spectrometry; and from Lynne Vales for helping in manuscript preparation. We also appreciate the assistance from Heike Pelka, Anika Paradkar, Nicholas Rogers, and Chen Dong in managing the ant room, maintaining ant colonies, or analyzing behavioral videos. This work was supported by a Howard Hughes Medical Institute Collaborative Innovation Award (CIA; #2009005) (to D.R., S.L.B., and J.L.), HCIA #2009005 (to D.R., S.L.B., J.L., C.D., and L.J.Z.), NIH grants (R21GM114457 to D.R.; EY13010 to C.D.). H. Yan was an NIH Ruth L. Kirschstein NRSA Postdoctoral Fellow (F32AG044971). M.P. was supported by NIH grant K99 EY027016. R.B. was supported by the Helen Hay Whitney Foundation and by an NIH New Innovator Award (DP2MH107055).
Publisher Copyright:
© 2017 Elsevier Inc.
PY - 2017/8/10
Y1 - 2017/8/10
N2 - 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 to which ORNs project. Therefore, the development of genetics in Harpegnathos establishes this ant species as a model organism to study the complexity of eusociality.
AB - 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 to which ORNs project. Therefore, the development of genetics in Harpegnathos establishes this ant species as a model organism to study the complexity of eusociality.
KW - CRISPR
KW - Harpegnathos saltator
KW - Orco
KW - ant
KW - eusocial insect
KW - glomerulus
KW - neural development
KW - odorant receptor
KW - odorant receptor neurons
KW - pheromone
KW - reproduction
KW - social behavior
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U2 - 10.1016/j.cell.2017.06.051
DO - 10.1016/j.cell.2017.06.051
M3 - Article
C2 - 28802043
AN - SCOPUS:85027531470
SN - 0092-8674
VL - 170
SP - 736-747.e9
JO - Cell
JF - Cell
IS - 4
ER -