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Published February 19, 2010 | Published
Journal Article Open

A comparison of experience-dependent locomotory behaviors and biogenic amine neurons in nematode relatives of Caenorhabditis elegans

Abstract

Background: Survival of an animal depends on its ability to match its responses to environmental conditions. To generate an optimal behavioral output, the nervous system must process sensory information and generate a directed motor output in response to stimuli. The nervous system should also store information about experiences to use in the future. The diverse group of free-living nematodes provides an excellent system to study macro- and microevolution of molecular, morphological and behavioral character states associated with such nervous system function. We asked whether an adaptive behavior would vary among bacterivorous nematodes and whether differences in the neurotransmitter systems known to regulate the behavior in one species would reflect differences seen in the adaptive behavior among those species. Caenorhabditis elegans worms slow in the presence of food; this 'basal' slowing is triggered by dopaminergic mechanosensory neurons that detect bacteria. Starved worms slow more dramatically; this 'enhanced' slowing is regulated by serotonin. Results: We examined seven nematode species with known phylogenetic relationship to C. elegans for locomotory behaviors modulated by food (E. coli), and by the worm's recent history of feeding (being well-fed or starved). We found that locomotory behavior in some species was modulated by food and recent feeding experience in a manner similar to C. elegans, but not all the species tested exhibited these food-modulated behaviors. We also found that some worms had different responses to bacteria other than E. coli. Using histochemical and immunological staining, we found that dopaminergic neurons were very similar among all species. For instance, we saw likely homologs of four bilateral pairs of dopaminergic cephalic and deirid neurons known from C. elegans in all seven species examined. In contrast, there was greater variation in the patterns of serotonergic neurons. The presence of presumptive homologs of dopaminergic and serotonergic neurons in a given species did not correlate with the observed differences in locomotory behaviors. Conclusions: This study demonstrates that behaviors can differ significantly between species that appear morphologically very similar, and therefore it is important to consider factors, such as ecology of a species in the wild, when formulating hypotheses about the adaptive significance of a behavior. Our results suggest that evolutionary changes in locomotory behaviors are less likely to be caused by changes in neurotransmitter expression of neurons. Such changes could be caused either by subtle changes in neural circuitry or in the function of the signal transduction pathways mediating these behaviors.

Additional Information

© 2010 Rivard et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Received: 19 August 2009. Accepted: 19 February 2010 Published: 19 February 2010. We thank David Fitch for strains and advice, and Karin Kiontke for discussions about nematode sensilla evolution. Some strains were obtained from the Caenorhabditis Genetics Center, an NIH Research Resource. We thank Kris Carter and Jason Kehrer (USD) who also contributed to the project. CL is supported by an endowment from the Fletcher Jones Foundation; some of this work was also supported by NIGMS Grant R15GM60203 (to CL). We also thank Christopher Cronin for assistance in worm locomotion scripts and members of the Sternberg lab for comments and discussions on the manuscript. JS is an Associate and PWS is an Investigator of the Howard Hughes Medical Institute, which supported this research. Authors' contributions: LR, AS, and SO performed manual locomotion studies, LR, AS and CL performed anti-serotonin staining studies, CL performed FIF and 5HTP/antiserotonin studies, JS and PWS designed tracker experiments and JS performed automated tracker locomotion experiments, and LR, JS, CL and PWS wrote the paper. All the authors have read and approved the final manuscript.

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