Abstract

BackgroundAvoidance of noxious stimuli is essential for the survival of an animal in its natural habitat. Some avoidance responses require polymodal sensory neurons, which sense a range of diverse stimuli, whereas other stimuli require a unimodal sensory neuron, which senses a single stimulus. Polymodality might have evolved to help animals quickly detect and respond to diverse noxious stimuli. Nematodes inhabit diverse habitats and most nematode nervous systems are composed of a small number of neurons, despite a wide assortment in nematode sizes. Given this observation, we speculated that cellular contribution to stereotyped avoidance behaviors would also be conserved between nematode species. The ASH neuron mediates avoidance of three classes of noxious stimuli in Caenorhabditis elegans. Two species of parasitic nematodes also utilize the ASH neuron to avoid certain stimuli. We wanted to extend our knowledge of avoidance behaviors by comparing multiple stimuli in a set of free-living nematode species.ResultsWe used comparative behavioral analysis and laser microsurgery to examine three avoidance behaviors in six diverse species of free-living nematodes. We found that all species tested exhibit avoidance of chemo-, mechano- and osmosensory stimuli. In C. elegans, the bilaterally symmetric polymodal ASH neurons detect all three classes of repellant. We identified the putative ASH neurons in different nematode species by their anatomical positions and showed that in all six species ablation of the ASH neurons resulted in an inability to avoid noxious stimuli. However, in the nematode Pristionchus pacificus, the ADL neuron in addition to the ASH neuron contributed to osmosensation. In the species Caenorhabditis sp. 3, only the ASH neuron was required to mediate nose touch avoidance instead of three neurons in C. elegans. These data suggest that different species can increase or decrease the contribution of additional, non-ASH sensory neurons mediating osmosensation and mechanosensation.ConclusionThe overall conservation of ASH mediated polymodal nociception suggests that it is an ancestral evolutionarily stable feature of sensation. However, the finding that contribution from non-ASH sensory neurons mediates polymodal nociception in some nematode species suggests that even in conserved sensory behaviors, the cellular response network is dynamic over evolutionary time, perhaps shaped by adaptation of each species to its environment.

Highlights

  • Avoidance of noxious stimuli is essential for the survival of an animal in its natural habitat

  • Comparative neuroanatomy and identification of amphid neurons in different nematode species Cellular anatomy is essentially invariant between individuals of the same nematode species and the number of neurons is highly conserved between nematode species, allowing the identification of neurons across different species of nematodes [6,10,17,34,35]

  • By comparing multiple aversive behaviors in many nematode species at a cellular level, we demonstrate the relative flexibility of the sensory system of nematodes

Read more

Summary

Introduction

Avoidance of noxious stimuli is essential for the survival of an animal in its natural habitat. Nematodes inhabit diverse habitats and most nematode nervous systems are composed of a small number of neurons, despite a wide assortment in nematode sizes Given this observation, we speculated that cellular contribution to stereotyped avoidance behaviors would be conserved between nematode species. Despite a more than 1000-fold range in the sizes of different nematode species, nematode nervous systems are composed of a small number of neurons: Caenorhabditis elegans, which is 1 mm long, has 302 neurons [1], whereas the parasite Ascaris lumbricoides, which grows to be 20 cm long, has 298 neurons [2]. It is surprising that even in the distantly related nematode parasite S. stercoralis, there is remarkable similarity of the amphid structure with C. elegans [6,7,10] Given this similarity, it is highly likely that similar cells would mediate the same behaviors across these diverse nematode species

Methods
Results
Conclusion
Full Text
Published version (Free)

Talk to us

Join us for a 30 min session where you can share your feedback and ask us any queries you have

Schedule a call