An atlas of the developing Tribolium castaneum brain reveals conservation in anatomy and divergence in timing to Drosophila melanogaster.

Drosophila melanogaster Tribolium castaneum brain atlas brain evolution development macroconnectivity tracts

Journal

The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041

Informations de publication

Date de publication:
10 May 2022
Historique:
revised: 12 04 2022
received: 29 11 2021
accepted: 13 04 2022
entrez: 10 5 2022
pubmed: 11 5 2022
medline: 11 5 2022
Statut: aheadofprint

Résumé

Insect brains are formed by conserved sets of neural lineages whose fibers form cohesive bundles with characteristic projection patterns. Within the brain neuropil, these bundles establish a system of fascicles constituting the macrocircuitry of the brain. The overall architecture of the neuropils and the macrocircuitry appear to be conserved. However, variation is observed, for example, in size, shape, and timing of development. Unfortunately, the developmental and genetic basis of this variation is poorly understood, although the rise of new genetically tractable model organisms such as the red flour beetle Tribolium castaneum allows the possibility to gain mechanistic insights. To facilitate such work, we present an atlas of the developing brain of T. castaneum, covering the first larval instar, the prepupal stage, and the adult, by combining wholemount immunohistochemical labeling of fiber bundles (acetylated tubulin) and neuropils (synapsin) with digital 3D reconstruction using the TrakEM2 software package. Upon comparing this anatomical dataset with the published work in Drosophila melanogaster, we confirm an overall high degree of conservation. Fiber tracts and neuropil fascicles, which can be visualized by global neuronal antibodies like antiacetylated tubulin in all invertebrate brains, create a rich anatomical framework to which individual neurons or other regions of interest can be referred to. The framework of a largely conserved pattern allowed us to describe differences between the two species with respect to parameters such as timing of neuron proliferation and maturation. These features likely reflect adaptive changes in developmental timing that govern the change from larval to adult brain.

Identifiants

pubmed: 35535818
doi: 10.1002/cne.25335
pmc: PMC9646932
mid: NIHMS1799007
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NINDS NIH HHS
ID : R56 NS054814
Pays : United States

Informations de copyright

© 2022 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.

Références

Development. 2003 Aug;130(16):3621-37
pubmed: 12835380
Elife. 2020 Sep 07;9:
pubmed: 32894223
BMC Dev Biol. 2010 May 19;10:53
pubmed: 20482875
J Comp Neurol. 2004 Jun 28;474(3):325-39
pubmed: 15174077
BMC Evol Biol. 2014 Mar 20;14(1):52
pubmed: 24646345
Dev Biol. 2015 Apr 1;400(1):159-67
pubmed: 25657058
Cell Signal. 2011 May;23(5):763-71
pubmed: 20940043
PLoS One. 2016 Dec 14;11(12):e0166253
pubmed: 27973569
Nature. 1999 Nov 25;402(6760):370-1
pubmed: 10586872
J Neurosci. 2006 May 17;26(20):5534-53
pubmed: 16707805
Dev Biol. 2014 Apr 1;388(1):103-16
pubmed: 24525296
Development. 2010 Jan;137(1):53-61
pubmed: 20023160
Neuron. 2006 Mar 16;49(6):833-44
pubmed: 16543132
Dev Genes Evol. 2017 Jul;227(4):253-269
pubmed: 28752327
Dev Biol. 2013 Dec 15;384(2):258-89
pubmed: 23872236
J Neurosci Methods. 2008 Jul 30;172(2):220-30
pubmed: 18585788
Eur J Neurosci. 2004 Aug;20(3):611-22
pubmed: 15255973
Sci Adv. 2020 Mar 11;6(11):eaaz7238
pubmed: 32195354
J Exp Biol. 2019 Feb 6;222(Pt Suppl 1):
pubmed: 30728235
Curr Biol. 2019 Feb 4;29(3):412-425.e3
pubmed: 30661802
Dev Genes Evol. 2016 Jun;226(3):209-19
pubmed: 27056385
Neuron. 2014 Feb 19;81(4):755-65
pubmed: 24559671
J Neurogenet. 2009;23(1-2):78-91
pubmed: 19132598
Dev Biol. 2021 Jul;475:165-180
pubmed: 32017903
Development. 2003 Aug;130(16):3589-606
pubmed: 12835378
Curr Biol. 2013 Apr 22;23(8):633-43
pubmed: 23541733
PLoS One. 2012;7(6):e38011
pubmed: 22723842
Dev Genes Evol. 1998 Sep;208(7):357-68
pubmed: 9732550
Cold Spring Harb Protoc. 2009 Aug;2009(8):pdb.prot5258
pubmed: 20147234
Development. 2016 Apr 15;143(8):1290-301
pubmed: 27095493
Science. 2014 Nov 7;346(6210):763-7
pubmed: 25378627
J Comp Neurol. 2010 Aug 1;518(15):2996-3023
pubmed: 20533357
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Development. 1988 May;103(1):145-56
pubmed: 3143540
Development. 2015 Aug 15;142(16):2832-9
pubmed: 26160901
J Exp Biol. 2018 Jun 8;221(Pt 11):
pubmed: 29884732
J Comp Neurol. 2018 Jan 1;526(1):33-58
pubmed: 28875566
Nature. 1984 Jul 19-25;310(5974):203-7
pubmed: 6462206
Elife. 2021 Mar 23;10:
pubmed: 33755020
J Comp Neurol. 2006 Nov 20;499(3):317-56
pubmed: 16998934
Development. 1990 Dec;110(4):1327-40
pubmed: 2100266
J Comp Neurol. 1994 Nov 22;349(4):633-45
pubmed: 7860793
Trends Neurosci. 2011 May;34(5):247-57
pubmed: 21397959
Cold Spring Harb Protoc. 2009 Aug;2009(8):pdb.emo126
pubmed: 20147228
J Neurosci. 1996 May 15;16(10):3154-65
pubmed: 8627354
J Comp Neurol. 2017 Nov 1;525(16):3458-3475
pubmed: 28675433
Dev Neurobiol. 2008 Nov;68(13):1487-502
pubmed: 18792069
J Comp Neurol. 2018 Jan 1;526(1):6-32
pubmed: 28730682
Proc Biol Sci. 2020 Jul 8;287(1930):20200807
pubmed: 32635870
Front Syst Neurosci. 2010 Mar 03;4:3
pubmed: 20339482
Curr Biol. 2002 Feb 5;12(3):R85-6
pubmed: 11839285
Dev Biol. 2013 Dec 15;384(2):228-57
pubmed: 23880429
Cell. 1989 Nov 3;59(3):447-60
pubmed: 2805067
Am Nat. 2021 May;197(5):576-591
pubmed: 33908824
J Comp Neurol. 2017 Feb 1;525(2):363-379
pubmed: 27350102
J Comp Neurol. 1996 Jul 01;370(3):313-29
pubmed: 8799858
Dev Biol. 2009 Nov 15;335(2):289-304
pubmed: 19538956
Dev Cell. 2008 Apr;14(4):535-46
pubmed: 18342578
PLoS Biol. 2020 Oct 26;18(10):e3000881
pubmed: 33104689
Curr Top Dev Biol. 2020;137:333-361
pubmed: 32143748
Front Neural Circuits. 2018 Nov 27;12:103
pubmed: 30546298
Neuron. 1997 Jul;19(1):77-89
pubmed: 9247265
Elife. 2019 Oct 18;8:
pubmed: 31625505
PLoS Biol. 2010 Oct 05;8(10):
pubmed: 20957184
Nature. 1999 Sep 30;401(6752):447-52
pubmed: 10519548
Elife. 2021 Aug 24;10:
pubmed: 34427185
Elife. 2020 Apr 07;9:
pubmed: 32255422
Cell Motil Cytoskeleton. 1989;12(4):273-82
pubmed: 2655938
Science. 2020 Dec 18;370(6523):
pubmed: 33335034
Sci Rep. 2016 May 17;6:26041
pubmed: 27185464
Neuroscience. 2013 Dec 19;254:26-44
pubmed: 24042037
Methods Mol Biol. 2020;2047:233-251
pubmed: 31552658
Curr Biol. 2013 Apr 22;23(8):644-55
pubmed: 23541729
Dev Genes Evol. 2010 Jun;220(1-2):1-10
pubmed: 20306203
Dev Neurobiol. 2008 Aug;68(9):1185-95
pubmed: 18548484
J Comp Neurol. 2017 Jun 1;525(8):1879-1908
pubmed: 28074466
Development. 2021 Oct 1;148(19):
pubmed: 34415334
Cell Tissue Res. 1986;244(2):243-52
pubmed: 3521878
Curr Biol. 2017 Jan 23;27(2):R77-R82
pubmed: 28118595
Proc Natl Acad Sci U S A. 2021 Feb 9;118(6):
pubmed: 33547240
J Comp Neurol. 2011 Dec 1;519(17):3367-86
pubmed: 21858820
Brain Behav Evol. 2013;82(1):9-18
pubmed: 23979452
Nat Commun. 2015 Jul 28;6:7822
pubmed: 26215380
Dev Biol. 2015 Oct 1;406(1):14-39
pubmed: 26141956
Development. 1995 Dec;121(12):3989-96
pubmed: 8575299
Nature. 1976 Mar 4;260(5546):54-6
pubmed: 1264194
Neural Dev. 2008 Feb 19;3:5
pubmed: 18284664
J Comp Neurol. 2009 Nov 1;517(1):87-104
pubmed: 19711412
J Comp Neurol. 2018 Oct 1;526(14):2215-2230
pubmed: 29907958
Proc Natl Acad Sci U S A. 2005 Nov 29;102(48):17394-9
pubmed: 16293692
Evol Dev. 2011 Sep-Oct;13(5):436-47
pubmed: 23016905
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2014 Jun;200(6):575-89
pubmed: 24589854
Front Neuroanat. 2015 Feb 04;8:166
pubmed: 25698935
Arthropod Struct Dev. 2003 Aug;32(1):103-23
pubmed: 18088998

Auteurs

Max S Farnworth (MS)

Department of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach Institute, GZMB, University of Göttingen, Göttingen, Germany.
Evolution of Brains and Behaviour lab, School of Biological Sciences, University of Bristol, Bristol, UK.

Gregor Bucher (G)

Department of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach Institute, GZMB, University of Göttingen, Göttingen, Germany.

Volker Hartenstein (V)

Department of Molecular Cell and Developmental Biology, University of California/Los Angeles, Los Angeles, USA.

Classifications MeSH