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

Ray L Hong,Eduardo Moreno,Bogdan Sieriebriennikov,Ralf J Sommer,Heather R Carstensen,Daniel J Bumbarger,Steven J Cook,Jessica Castrejon,Luisa Cochella,Metta Riebesell,Oliver Hobert,Tahmineh Sarpolaki

doi:10.7554/elife.47155

Abstract

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.

Highlights

Comparative studies on nervous system anatomy have a long tradition of offering fundamental insights into the evolution of nervous systems and, the evolution of behavior (Schmidt-Rhaesa, 2007)
Using a combination of 3D reconstructions from transmission electron microscopy (TEM) sections of two young adult hermaphrodites, as well as live dye uptake and transgene reporter analysis, we set out to characterize the amphid sensory circuitry of P. pacificus in order to undertake a comparative analysis with the amphid sensory circuitry of C. elegans
Despite being approximately 40 years old, the EMs used by John White and colleagues to create The Mind of a Worm remain the most complete publicly available data of the adult hermaphrodite C. elegans nervous system

Summary

Introduction

Comparative studies on nervous system anatomy have a long tradition of offering fundamental insights into the evolution of nervous systems and, the evolution of behavior (Schmidt-Rhaesa, 2007) Such comparative studies have relied on relatively coarse anatomical and morphometric comparisons. We examine here specific neuroanatomical features, from subcellular specializations to synaptic connectivity, of the nematode Pristionchus pacificus and compare these features with those of the nematode Caenorhabditis elegans The species shared their last common ancestor around 100 million years ago, which is longer than the human-mouse separation (Nei et al, 2001; Prabh et al, 2018; Rota-Stabelli et al, 2013; Werner et al, 2018), and have since diverged to populate very discrete habitats and engage in distinct sets of behaviors.

Methods

Results

Conclusion