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Olfactory receptors are required for social behavior and neural plasticity in ants, as evidenced by CRISPR-mediated gene knockout

Hua Yan, Comzit Opachaloemphan, Giacomo Mancini, Huan Yang, Matthew Gallitto, Jakub Mlejnek, Kevin Haight, Majid Ghaninia, Lucy Huo, Alexandra Leibholz, Jesse Slone, Xiaofan Zhou, Maria Traficante, Clint A. Penick, Kelly Dolezal, Kaustubh Gokhale, Kelsey Stevens, Ingrid Fetter-Pruneda, Roberto Bonasio, Laurence J. Zwiebel, Shelley Berger, Jüergen Liebig, Danny Reinberg, Claude Desplan
doi: https://doi.org/10.1101/142232
Hua Yan
1Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016
7Howard Hughes Medical Institute, New York University School of Medicine, New York, NY 10016
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Comzit Opachaloemphan
1Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016
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Giacomo Mancini
2Department of Biology, New York University, New York, NY 10003
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Huan Yang
1Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016
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Matthew Gallitto
1Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016
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Jakub Mlejnek
2Department of Biology, New York University, New York, NY 10003
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Kevin Haight
3School of Life Sciences, Arizona State University, Tempe, Arizona 85283
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Majid Ghaninia
3School of Life Sciences, Arizona State University, Tempe, Arizona 85283
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Lucy Huo
2Department of Biology, New York University, New York, NY 10003
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Alexandra Leibholz
2Department of Biology, New York University, New York, NY 10003
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Jesse Slone
4Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235
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Xiaofan Zhou
4Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235
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Maria Traficante
2Department of Biology, New York University, New York, NY 10003
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Clint A. Penick
3School of Life Sciences, Arizona State University, Tempe, Arizona 85283
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Kelly Dolezal
3School of Life Sciences, Arizona State University, Tempe, Arizona 85283
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Kaustubh Gokhale
3School of Life Sciences, Arizona State University, Tempe, Arizona 85283
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Kelsey Stevens
2Department of Biology, New York University, New York, NY 10003
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Ingrid Fetter-Pruneda
5Laboratory of Social Evolution and Behavior, The Rockefeller University, New York, NY 10065
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Roberto Bonasio
6Penn Epigenetics Institute, Departments of Cell and Developmental Biology, Genetics, Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania 19104
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Laurence J. Zwiebel
4Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235
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Shelley Berger
6Penn Epigenetics Institute, Departments of Cell and Developmental Biology, Genetics, Biology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania 19104
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Jüergen Liebig
3School of Life Sciences, Arizona State University, Tempe, Arizona 85283
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Danny Reinberg
1Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016
7Howard Hughes Medical Institute, New York University School of Medicine, New York, NY 10016
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Claude Desplan
2Department of Biology, New York University, New York, NY 10003
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Abstract

The chemosensory system is key to establishing and maintaining social structure in eusocial insects. Ants exhibit cooperative colonial behaviors reflective of an advanced form of sociality with an extensive dependency on communication. Cuticular hydrocarbons (CHCs) serve as pheromones and cues that regulate multiple aspects of social interactions and behaviors in ants. The perception of CHCs entails odorant receptor neurons (ORNs) that express specific odorant receptors (ORs) encoded by a dramatically expanded Or gene family in ants. Until recently, studies of the biological functions of ORs in eusocial insects were stymied by the lack of genetic tools. In most eusocial insect species, only one or a few queens in a colony can transmit the genetic information to their progeny. In contrast, any worker in the ant Harpegnathos saltator can be converted into a gamergate (pseudo-queen), and used as a foundress to engender an entire new colony and be crossed for genetic experiments. This feature facilitated CRISPR-Cas9 gene targeting to generate a germline mutation in the orco gene that encodes the obligate co-receptor whose mutation should significantly impact ant olfaction. Our results show that Orco exhibits a conserved role in the perception of general odorants but also a role in reproductive physiology and social behavior plasticity in ants. Surprisingly, and in contrast to other insect systems, the loss of OR functionality also dramatically reduces the development of the ant antennal lobe where ORNs project. Taken together, these findings open the possibility of studying the genetics of eusociality and provide inroads towards understanding the function of the expanded ORs family in eusocial insects in regulating caste determination, social communication and neuronal plasticity.

Footnotes

  • Lead contact: Claude Desplan (cd38{at}nyu.edu)

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 25, 2017.
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Olfactory receptors are required for social behavior and neural plasticity in ants, as evidenced by CRISPR-mediated gene knockout
Hua Yan, Comzit Opachaloemphan, Giacomo Mancini, Huan Yang, Matthew Gallitto, Jakub Mlejnek, Kevin Haight, Majid Ghaninia, Lucy Huo, Alexandra Leibholz, Jesse Slone, Xiaofan Zhou, Maria Traficante, Clint A. Penick, Kelly Dolezal, Kaustubh Gokhale, Kelsey Stevens, Ingrid Fetter-Pruneda, Roberto Bonasio, Laurence J. Zwiebel, Shelley Berger, Jüergen Liebig, Danny Reinberg, Claude Desplan
bioRxiv 142232; doi: https://doi.org/10.1101/142232
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Olfactory receptors are required for social behavior and neural plasticity in ants, as evidenced by CRISPR-mediated gene knockout
Hua Yan, Comzit Opachaloemphan, Giacomo Mancini, Huan Yang, Matthew Gallitto, Jakub Mlejnek, Kevin Haight, Majid Ghaninia, Lucy Huo, Alexandra Leibholz, Jesse Slone, Xiaofan Zhou, Maria Traficante, Clint A. Penick, Kelly Dolezal, Kaustubh Gokhale, Kelsey Stevens, Ingrid Fetter-Pruneda, Roberto Bonasio, Laurence J. Zwiebel, Shelley Berger, Jüergen Liebig, Danny Reinberg, Claude Desplan
bioRxiv 142232; doi: https://doi.org/10.1101/142232

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