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Comparative Development of the Ant Chemosensory System

2020; Elsevier BV; Volume: 30; Issue: 16 Linguagem: Inglês

10.1016/j.cub.2020.05.072

1879-0445

Anna R. Ryba, Sean K. McKenzie, Leonora Olivos-Cisneros, E. Josephine Clowney, Peter Mussells Pires, Daniel J. C. Kronauer,

Plant and animal studies

The insect antennal lobe (AL) contains the first synapses of the olfactory system, where olfactory sensory neurons (OSNs) contact second-order projection neurons (PNs). In Drosophila melanogaster, OSNs expressing specific receptor genes send stereotyped projections to one or two of about 50 morphologically defined glomeruli [1Laissue P.P. Reiter C. Hiesinger P.R. Halter S. Fischbach K.F. Stocker R.F. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster.J. Comp. Neurol. 1999; 405: 543-552Crossref PubMed Scopus (331) Google Scholar, 2Couto A. Alenius M. Dickson B.J. Molecular, anatomical, and functional organization of the Drosophila olfactory system.Curr. Biol. 2005; 15: 1535-1547Abstract Full Text Full Text PDF PubMed Scopus (614) Google Scholar, 3Vosshall L.B. Olfaction in Drosophila.Curr. Opin. Neurobiol. 2000; 10: 498-503Crossref PubMed Scopus (102) Google Scholar]. The mechanisms for this precise matching between OSNs and PNs have been studied extensively in D. melanogaster, where development is deterministic and independent of neural activity [4Sardana J. Organisti C. Grunwald Kadow I.C. Eph receptor effector ephexin mediates olfactory dendrite targeting in Drosophila.Dev. Neurobiol. 2018; 78: 873-888Crossref PubMed Scopus (3) Google Scholar, 5Technau G.M. Brain Development in Drosophila melanogaster. Springer Science+Business Media/Landes Bioscience, 2008Crossref Google Scholar, 6Jefferis G.S.X.E. Vyas R.M. Berdnik D. Ramaekers A. Stocker R.F. Tanaka N.K. Ito K. Luo L. Developmental origin of wiring specificity in the olfactory system of Drosophila.Development. 2004; 131: 117-130Crossref PubMed Scopus (165) Google Scholar]. However, a number of insect lineages, most notably the ants, have receptor gene repertoires many times larger than D. melanogaster and exhibit more structurally complex antennal lobes [7Robertson H.M. Wanner K.W. The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family.Genome Res. 2006; 16: 1395-1403Crossref PubMed Scopus (371) Google Scholar, 8Salecker I. Boeckh J. Embryonic development of the antennal lobes of a hemimetabolous insect, the cockroach Periplaneta americana: light and electron microscopic observations.J. Comp. Neurol. 1995; 352: 33-54Crossref PubMed Scopus (32) Google Scholar, 9Gascuel J. Masson C. A quantitative ultrastructural study of the honeybee antennal lobe.Tissue Cell. 1991; 23: 341-355Crossref PubMed Scopus (46) Google Scholar, 10d’Ettorre P. Genomic and brain expansion provide ants with refined sense of smell.Proc. Natl. Acad. Sci. USA. 2016; 113: 13947-13949Crossref PubMed Scopus (3) Google Scholar, 11McKenzie S.K. Fetter-Pruneda I. Ruta V. Kronauer D.J.C. Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication.Proc. Natl. Acad. Sci. USA. 2016; 113: 14091-14096Crossref PubMed Scopus (47) Google Scholar, 12Zube C. Kleineidam C.J. Kirschner S. Neef J. Rössler W. Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus.J. Comp. Neurol. 2008; 506: 425-441Crossref PubMed Scopus (97) Google Scholar]. Moreover, perturbation of OSN function via knockout of the odorant receptor (OR) co-receptor, Orco, results in drastic AL reductions in ants [13Trible W. Olivos-Cisneros L. McKenzie S.K. Saragosti J. Chang N.-C. Matthews B.J. Oxley P.R. Kronauer D.J.C. orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants.Cell. 2017; 170: 727-735.e10Abstract Full Text Full Text PDF PubMed Scopus (106) Google Scholar, 14Yan H. Opachaloemphan C. Mancini G. Yang H. Gallitto M. Mlejnek J. Leibholz A. Haight K. Ghaninia M. Huo L. et al.An engineered orco mutation produces aberrant social behavior and defective neural development in ants.Cell. 2017; 170: 736-747.e9Abstract Full Text Full Text PDF PubMed Scopus (95) Google Scholar], but not in Drosophila [15Larsson M.C. Domingos A.I. Jones W.D. Chiappe M.E. Amrein H. Vosshall L.B. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction.Neuron. 2004; 43: 703-714Abstract Full Text Full Text PDF PubMed Scopus (846) Google Scholar]. Here, we characterize AL development in the clonal raider ant, Ooceraea biroi. We find that, unlike in Drosophila, ORs and Orco are expressed before the onset of glomerulus formation, and Orco protein is trafficked to developing axon terminals, raising the possibility that ORs play a role during ant AL development. Additionally, ablating ant antennae at the onset of pupation results in AL defects that recapitulate the Orco mutant phenotype. Thus, early loss of functional OSN innervation reveals latent structure in the AL that develops independently of peripheral input, suggesting that the AL is initially pre-patterned and later refined in an OSN-dependent manner. This two-step process might increase developmental flexibility and thereby facilitate the rapid evolution and expansion of the ant chemosensory system.