[
International Worm Meeting,
2007]
We are trying to understand how neural circuits evolve to mediate ethologically relevant behaviors. While model systems help elucidate how sensory information from diverse environmental conditions is represented and processed in the neural, remarkably little is known about the evolution of neural circuits, and how selective forces shape the final architecture of neural circuits and processing circuits (Dumont & Richardson, 1986, Science). Nematodes are an ancient phylum comprising millions of species from diverse habitats. They have molecularly diverse nervous systems which in principle can help them sense several types of environmental stimuli. To trace the evolutionary history of such a sensory repertoire, we tested three different avoidance behaviors; osmotic avoidance, response to nose touch, and volatile chemical repellence in six diverse species of free-living nematodes, a) Caenorhabditis elegans (N2), b) Caenorhabditis briggsae (AF16), c) Caenorhabditis sp. 3 (PS1010), d) Pristionchus pacificus (PS312) e) Cruznema tripartitum (PS1351) and f) Panagrellus redivivus (PS2298). We found that all species tested exhibit the three avoidance behaviors. However, we also find that sensory sensitivity to the different stimuli differs among the tested nematode species. In C. elegans , response to these stimuli are mediated by the ‘polymodal ASH neurons (Kaplan and Horvitz PNAS, 1993, Hart et al. Nature, 1995, Hilliard et al Curr Biol. 2002). We identified the pairs of putative ASH neurons in different nematode species by their anatomical positions and ablated them. Ablation of the ASH neurons in these species resulted in an inability to avoid these stimuli. By further ablation experiments, we find that there is increase or decrease in the set of sensory neurons mediating osmosensation and mechanosensation. In P. pacificus , osmosensation involves the ADL neuron. In Caenorhabditis sp. 3 , mechanosensation is solely mediated by the ASH neuron as compared to 3 neurons in C. elegans . The overall conservation of ASH mediated behaviors suggests that polymodality is an ancestral feature and is evolutionarily stable, but can evolve by alterations in the level of sensitivity and the relative contributions of sensory neurons.
[
Neuronal Development, Synaptic Function, and Behavior Meeting,
2006]
Despite the diversity of the nematode phylum, most nematode nervous systems have around 300 neurons. Some neurons (polymodal) respond to multiple stimuli. C. elegans possesses classical "polymodal" neurons that respond to multiple types of stimuli, including chemo - and mechanosensory (1-3). To trace the evolutionary history of polymodality, we tested in six diverse species of free-living nematodes, three different avoidance behaviors; osmotic avoidance, response to nose touch, and volatile chemical repellence in C. elegans (N2), C. briggsae (AF16), Caenorhabditis sp. 3 (PS1010), P. pacificus (PS312) C. tripartitum (PS1351) and P. redivivus (PS2298). Nearly all species tested show conserved avoidance behaviors.
In C. elegans, response to these stimuli are mediated by the ASH neurons. Ablation of the ASH neuron almost completely abolishes osmotic avoidance response in C. elegans (4). However, ASH ablation does not completely abolish osmotic avoidance in other species, suggesting the existence of ASH-independent mechanisms regulating osmotic avoidance in these species. Ablation of additional nociceptive neurons (4) along with ASH resulted in complete abolishment of osmotic avoidance in these species suggesting that additional neurons regulate osmotic avoidance in these other species. In C. elegans, nose touch is mediated by ASH, OLQ and FLP (1). Ablation of the ASH neurons resulted in loss of nose touch avoidance in most species. However in Caenorhabditis sp. 3, ASH-ablated animals completely lack the ability to respond to nose touch. In Caenorhabditis sp. 3, ablation of the FLP and OLQ cells did not result in any significant differences to nose touch than ASH ablated animals, suggesting that the circuitry mediating nose touch might have converged from three sensory neurons (ASH, FLP, OLQ) onto a single sensory neuron (ASH). Repellence to the volatile odorant 1-octanol was mediated by the ASH neuron in all the species.
Hence, our findings suggest that polymodality evolved early during diversification of the rhabditids. However, changes in behavior seen at the cellular level might result from loss or gain of certain components of the sensory signaling or changes in the downstream signaling of the sensory stimulus at both the cellular and synaptic level during evolution. This suggests that polymodality as a trait in nematodes is under negative selection but the underlying cellular network evolves to help survive their respective environments.