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Evolution of neuronal anatomy and circuitry in two highly divergent nematode species

The nematodes C. elegans and P. pacificus populate diverse habitats and display distinct patterns of behavior. To understand how their nervous systems have diverged, we undertook a detailed examination of the neuroanatomy of the chemosensory system of P. pacificus. Using independent features such as...

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Autores principales: Hong, Ray L, Riebesell, Metta, Bumbarger, Daniel J, Cook, Steven J, Carstensen, Heather R, Sarpolaki, Tahmineh, Cochella, Luisa, Castrejon, Jessica, Moreno, Eduardo, Sieriebriennikov, Bogdan, Hobert, Oliver, Sommer, Ralf J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6748829/
https://www.ncbi.nlm.nih.gov/pubmed/31526477
http://dx.doi.org/10.7554/eLife.47155
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author Hong, Ray L
Riebesell, Metta
Bumbarger, Daniel J
Cook, Steven J
Carstensen, Heather R
Sarpolaki, Tahmineh
Cochella, Luisa
Castrejon, Jessica
Moreno, Eduardo
Sieriebriennikov, Bogdan
Hobert, Oliver
Sommer, Ralf J
author_facet Hong, Ray L
Riebesell, Metta
Bumbarger, Daniel J
Cook, Steven J
Carstensen, Heather R
Sarpolaki, Tahmineh
Cochella, Luisa
Castrejon, Jessica
Moreno, Eduardo
Sieriebriennikov, Bogdan
Hobert, Oliver
Sommer, Ralf J
author_sort Hong, Ray L
collection PubMed
description The nematodes C. elegans and P. pacificus populate diverse habitats and display distinct patterns of behavior. To understand how their nervous systems have diverged, we undertook a detailed examination of the neuroanatomy of the chemosensory system of P. pacificus. Using independent features such as cell body position, axon projections and lipophilic dye uptake, we have assigned homologies between the amphid neurons, their first-layer interneurons, and several internal receptor neurons of P. pacificus and C. elegans. We found that neuronal number and soma position are highly conserved. However, the morphological elaborations of several amphid cilia are different between them, most notably in the absence of ‘winged’ cilia morphology in P. pacificus. We established a synaptic wiring diagram of amphid sensory neurons and amphid interneurons in P. pacificus and found striking patterns of conservation and divergence in connectivity relative to C. elegans, but very little changes in relative neighborhood of neuronal processes. These findings demonstrate the existence of several constraints in patterning the nervous system and suggest that major substrates for evolutionary novelty lie in the alterations of dendritic structures and synaptic connectivity.
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spelling pubmed-67488292019-09-20 Evolution of neuronal anatomy and circuitry in two highly divergent nematode species Hong, Ray L Riebesell, Metta Bumbarger, Daniel J Cook, Steven J Carstensen, Heather R Sarpolaki, Tahmineh Cochella, Luisa Castrejon, Jessica Moreno, Eduardo Sieriebriennikov, Bogdan Hobert, Oliver Sommer, Ralf J eLife Neuroscience The nematodes C. elegans and P. pacificus populate diverse habitats and display distinct patterns of behavior. To understand how their nervous systems have diverged, we undertook a detailed examination of the neuroanatomy of the chemosensory system of P. pacificus. Using independent features such as cell body position, axon projections and lipophilic dye uptake, we have assigned homologies between the amphid neurons, their first-layer interneurons, and several internal receptor neurons of P. pacificus and C. elegans. We found that neuronal number and soma position are highly conserved. However, the morphological elaborations of several amphid cilia are different between them, most notably in the absence of ‘winged’ cilia morphology in P. pacificus. We established a synaptic wiring diagram of amphid sensory neurons and amphid interneurons in P. pacificus and found striking patterns of conservation and divergence in connectivity relative to C. elegans, but very little changes in relative neighborhood of neuronal processes. These findings demonstrate the existence of several constraints in patterning the nervous system and suggest that major substrates for evolutionary novelty lie in the alterations of dendritic structures and synaptic connectivity. eLife Sciences Publications, Ltd 2019-09-17 /pmc/articles/PMC6748829/ /pubmed/31526477 http://dx.doi.org/10.7554/eLife.47155 Text en © 2019, Hong et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Hong, Ray L
Riebesell, Metta
Bumbarger, Daniel J
Cook, Steven J
Carstensen, Heather R
Sarpolaki, Tahmineh
Cochella, Luisa
Castrejon, Jessica
Moreno, Eduardo
Sieriebriennikov, Bogdan
Hobert, Oliver
Sommer, Ralf J
Evolution of neuronal anatomy and circuitry in two highly divergent nematode species
title Evolution of neuronal anatomy and circuitry in two highly divergent nematode species
title_full Evolution of neuronal anatomy and circuitry in two highly divergent nematode species
title_fullStr Evolution of neuronal anatomy and circuitry in two highly divergent nematode species
title_full_unstemmed Evolution of neuronal anatomy and circuitry in two highly divergent nematode species
title_short Evolution of neuronal anatomy and circuitry in two highly divergent nematode species
title_sort evolution of neuronal anatomy and circuitry in two highly divergent nematode species
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6748829/
https://www.ncbi.nlm.nih.gov/pubmed/31526477
http://dx.doi.org/10.7554/eLife.47155
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