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ScienceWeek
BEHAVIORAL GENETICS: ON FORAGING BEHAVIOR IN NEMATODES
The following points are made by C.A. Riedl and M.B. Sokolowski (Current Biology 2004 14:R657):
1) Understanding the intricacies of the relationships between genes, the environment, and behavior is a major challenge for modern biology. The complex interplay between molecular and neuronal networks and the varying effects of environmental contexts complicate our investigations. Work towards this understanding is often impractical in extremely complex and incompletely characterized systems, such as mammals, and so we turn to model organisms, such as the nematode worm Caenorhabditis elegans. C. elegans has a small, well-defined nervous system which it uses to perform complex behaviors. One such behavior that has attracted much interest recently involves a natural foraging behavior dimorphism: upon exposure to a nutritive bacterial lawn, some worms will quickly aggregate and form tight foraging groups, while others continue to feed individually [1].
2) Since the discovery of this natural dimorphism in foraging behavior, researchers have located the gene responsible, npr-1[1], and, remarkably, the single amino acid difference that underlies the dimorphism. They have shown that the npr-1 gene encodes a neuropeptide receptor and is expressed in a small number of cells [1], and identified the receptor's ligands [2]. Furthermore, using mutant and transgenic analyses, together with cellular ablation techniques, they have described several interacting neural circuits and signal transduction cascades that affect the group foraging phenotype [3,4]. New work [5] has extended our understanding of the signaling systems in which the naturally variable NPR-1 protein acts, revealing a novel role for soluble guanylyl cyclase in group foraging behaviors.
3) De Bono et al (3) described how their search for modifiers of group foraging behavior led to the identification of two genes for soluble guanylyl cyclases. The authors demonstrated that these genes are expressed in very few cells, and more specifically, in three critical neurons that express the naturally variable npr-1 gene and a heterodimeric cGMP-gated ion channel, TAX-2-TAX-4, also known to affect group foraging behavior [4]. Signaling by these three neurons influences group foraging, and Cheung et al.[5] discovered that guanylyl cyclase function is essential for their effect.
4) The anatomy of these neurons is of interest, as not only are they directly exposed to the body fluid [4] but at least one of them, URX, also has dendritic extensions to the tip of the worm's nose. The functional implications of this neural anatomy are not yet clear, but it does fit well into a theory that this behavior involves the collection and integration of information from several sources in both the external and internal environments. It will be interesting to learn what internal cues in the body fluid, if any, are being monitored, and how the state of the animal -- its nutrition, for example -- affects group foraging behavior. It has also recently been shown that these neurons may use guanylyl cyclase to monitor external O2 concentrations.
References (abridged):
1 de Bono, M. and Bargmann, C.I. (1998). Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Cell 94, 679-689
2 Rogers, C.X Reale, V.X Kim, K.X Chatwin, H.X Li, C.X Evans, P. and de Bono, M. (2003). Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat. Neurosci. 6, 1178-1185
3 de Bono, M.X Tobin, D.M.X Davis, M.W.X Avery, L. and Bargmann, C.I. (2002). Social feeding in Ceanorhabditi elegans is induced by neurons that detect aversive stimuli. Nature 419, 899-903
4 Coates, J.C. and de Bono, M. (2002). Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Ceanorhabditi elegans. Nature 419, 925-929
5 Cheung, B.H.X Arellano-Carbajal, F.X Rybicki, I. and De Bono, M. (2004). Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior. Curr. Biol. 14, 1105-1111
Current Biology http://www.current-biology.com
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Related Material:
ON HONEYBEE SOCIAL BEHAVIOR, GENES, AND THE ENVIRONMENT
Notes by ScienceWeek:
The so-called social insects live in societies that rival human societies in complexity and internal cohesion. Honey bees, for example, apparently always follow 3 rules: a) they live in colonies with overlapping generations; b) they care cooperatively for offspring other than their own; and, c) they maintain a reproductive division of labor.
The following points are made by Gene E. Robinson (American Scientist 1998 86:456):
1) Genes do not play an exclusive role in regulating behavior: biologists have long realized that behavior is influenced by genes, the environment, and interactions between the two.
2) Genes never act alone. They must operate in an environment where they code for proteins that participate in many systems in an organism, with these systems in turn influencing the expression of genes. Consequently, biologists must take a broad approach in assessing the impact of any gene.
3) The research group of the author uses the Western honey bee, Apis mellifera. Honey bees pass through different life stages as they age, and their behavioral responses to environmental and social stimuli change in predictable ways. Although worker bees go through a consistent path of behavioral development, this path is not rigidly determined. Bees can accelerate, retard, or even reverse their behavioral development in response to changing environmental and colony conditions.
4) Experimental evidence indicates that juvenile hormone, one of the most important hormones influencing insect development, helps time the pace of behavioral maturation in honey bees. The rate of endocrine-mediated behavioral development is influenced by inhibitory social interactions. Older bees inhibit the behavioral development of younger bees: the rate of behavioral development is negatively correlated with the proportion of older bees in a colony. Inhibitory social interactions that influence the rate of behavioral development involve chemical communication between colony members.
5) Evidence from the laboratory of the author in 1993 indicated the so-called mushroom bodies in the bee brain are involved in the behavioral changes occurring during maturation, the volume of the bodies increasing, and the volume increase associated with an increase in synapses with neurons from brain regions devoted to sensory input. The author suggests this was the first report of brain plasticity in an invertebrate.
6) The author suggests that, in general, two-way interactions between the nervous system and the genome contribute fundamentally to the control of social behavior. Information about social conditions that is acquired by the nervous system is likely to induce changes in genomic function that in turn produce adaptive modifications of the structure and function of the nervous system.
7) The author proposes a new research initiative called "sociogenomics", defined as a "wide-ranging approach to identify genes that influence social behavior, determining the influence of these genes on underlying neural and endocrine mechanisms, and exploring the effects of the environment -- particularly the social environment -- on gene action."
American Scientist http://www.americanscientist.org
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Related Material:
ON GENES AND COMPLEX SOCIAL BEHAVIOR
M.J. Krieger and K.G. Ross (University of Georgia, US) discuss genes and social behavior, the authors making the following points:
1) The evolution of complex social behavior is among the most important events in the history of life. Interest in the genes underlying the expression of key social traits is strong because knowledge of the genetic architecture will lead to increasingly realistic models of social evolution, while identification of the products of major genes can elucidate the molecular bases of social behavior. Few studies have succeeded in showing that complex social behaviors have a heritable basis, and fewer still have suggested that variation in these behaviors is attributable to the action of one or few genes of major effect. No candidate genes with major effects on key social polymorphisms have been identified previously.
2) The fire ant Solenopsis invicta displays a fundamental social polymorphism that appears to be under simple genetic control. A basic feature of fire ant colony social organization, the number of egg-laying queens, is associated with variation at the gene Gp-9. In the US, where this species has been introduced, colonies composed of workers bearing only the (B) allele at Gp-9 invariably have a single queen (monogyne social form), whereas colonies with workers bearing the alternate (b) allele have multiple queens (polygyne social form). The two social forms differ in many key reproductive and life history characteristics.
3) The authors report they sequenced the gene Gp-9 and found that it encodes a pheromone-binding protein, a crucial molecular component in same-species (conspecific) chemical recognition. The authors suggest this indicates that differences in worker Gp-9 genotypes between social forms may cause differences in the abilities of workers to recognize queens and regulate their numbers. The authors conclude: "This study demonstrates that single genes of major effect can underlie the expression of complex behaviors important in social evolution."
Science 2002 295:328
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