Neural Mechanisms for Evaluating Environmental Variability in Caenorhabditis elegans

Calhoun, Adam J.; Tong, Ada; Pokala, Navin; Fitzpatrick, James A.J.; Sharpee, Tatyana O.; Chalasani, Sreekanth H.

doi:10.1016/j.neuron.2015.03.026

Cited by 86 publications

(104 citation statements)

References 60 publications

(88 reference statements)

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“…This form of public goods production, which may be incidental to the foraging behavior of the worms, is qualitatively different from situations in which the good production is associated only with the explicit metabolic cost of chemical synthesis of the good, a mechanism often at play in microbial systems (6,(8)(9)(10), which lack complex behaviors. In contrast, the mechanism of public goods production that we describe here could be associated with neurobehavioral traits, such as exploration-exploitation strategies (18,19,29,(40)(41)(42) or the use of spatial memory (42,43), in addition to potential metabolic costs associated with carrying the bacteria (37,38). Moreover, C. elegans also appear to be capable of dispersing Dictyostelium discoideum spores (44), another food source; given that D. discoideum themselves farm bacteria (7), we anticipate a rich set of multitrophic level dynamics and niche partitioning to emerge in multispecies interactions involving the kind of effects that we have uncovered here.…”

Section: Resultsmentioning

confidence: 89%

Farming and public goods production in Caenorhabditis elegans populations

Thutupalli

Uppaluri

Constable

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The ecological and evolutionary dynamics of populations are shaped by the strategies they use to produce and use resources. However, our understanding of the interplay between the genetic, behavioral, and environmental factors driving these strategies is limited. Here, we report on a Caenorhabditis elegansEscherichia coli (worm-bacteria) experimental system in which the worm-foraging behavior leads to a redistribution of the bacterial food source, resulting in a growth advantage for both organisms, similar to that achieved via farming. We show experimentally and theoretically that the increased resource growth represents a public good that can benefit all other consumers, regardless of whether or not they are producers. Mutant worms that cannot farm bacteria benefit from farming by other worms in direct proportion to the fraction of farmers in the worm population. The farming behavior can therefore be exploited if it is associated with either energetic or survival costs. However, when the individuals compete for resources with their own type, these costs can result in an increased population density. Altogether, our findings reveal a previously unrecognized mechanism of public good production resulting from the foraging behavior of C. elegans, which has important population-level consequences. This powerful system may provide broad insight into explorationexploitation tradeoffs, the resultant ecoevolutionary dynamics, and the underlying genetic and neurobehavioral driving forces of multispecies interactions.foraging behavior | public goods | predator-prey | population dynamics | farming T he fitness of an organism is affected by its strategies to produce, explore, and exploit resources (1, 2). These strategies are influenced, in large part, by interdependencies among organisms, such as competition, predation (3, 4), mutualism (5-7), or the production of public good resources (8-10). Despite the wide prevalence of such interactions in nature as well as numerous theoretical and empirical studies, we are still limited in our mechanistic understanding of the interplay between different survival strategies, the resultant evolutionary dynamics and the underlying genetic, neurobehavioral, and ecological driving forces. In this pursuit, model systems in the laboratory have served as a useful bridge between the complexity of nature and the simplifications inherent in theoretical investigations. Such model systems have predominantly been either microbial (11, 12) or higher organisms, such as primates and humans (13-16). Microbial systems are very convenient due to their genetic tractability and short generation times but are limited in the space of behavioral traits they exhibit. At the other extreme, higher organisms exhibit rich neurobehavioral and genetic traits, but they are difficult to experimentally manipulate and generation times are very long.Recently, organisms such as the nematode worm Caenorhabditis elegans and the fruit fly Drosophila melanogaster have been increasingly used in evolutionary and behavioral stu...

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Section: Resultsmentioning

confidence: 89%

Farming and public goods production in Caenorhabditis elegans populations

Thutupalli

Uppaluri

Constable

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Velocity/frequency, amplitude, direction, and persistence are changed in a manner characteristic of coordinated forward movement after specific sensory stimulation (Gaglia and Kenyon 2009;Lüersen et al 2016) or during global food search behavior (Calhoun et al 2014(Calhoun et al , 2015Wakabayashi et al 2004). KIN-1/PKA is an established sensor of internal and external cues (Centonze et al 2001;Valjent et al 2005;Yang et al 2014;Goto et al 2015).…”

Section: Discussionmentioning

confidence: 99%

Locomotion Behavior Is Affected by the GαS Pathway and the Two-Pore-Domain K+ Channel TWK-7 Interacting in GABAergic Motor Neurons in Caenorhabditis elegans

Gottschling¹,

Döring²,

Lüersen

2017

Genetics

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Adjusting the efficiency of movement in response to environmental cues is an essential integrative characteristic of adaptive locomotion behavior across species. However, the modulatory molecules and the pathways involved are largely unknown. Recently, we demonstrated that in Caenorhabditis elegans, a loss-of-function of the two-pore-domain potassium (K 2 P) channel TWK-7 causes a fast, coordinated, and persistent forward crawling behavior in which five central aspects of stimulated locomotion-velocity, direction, wave parameters, duration, and straightness-are affected. Here, we isolated the reduction-of-function allele cau1 of the C. elegans gene kin-2 in a forward genetic screen and showed that it phenocopies the locomotor activity and locomotion behavior of twk-7(null) animals. Kin-2 encodes the negative regulatory subunit of protein kinase A (KIN-1/PKA). Consistently, we found that other gain-of-function mutants of the Ga S -KIN-1/PKA pathway resemble kin-2(cau1) and twk-7(null) in locomotion phenotype. Using the powerful genetics of the C. elegans system in combination with cell type-specific approaches and detailed locomotion analyses, we identified TWK-7 as a putative downstream target of the Ga S -KIN-1/PKA pathway at the level of the g-aminobutyric acid (GABA)ergic D-type motor neurons. Due to this epistatic interaction, we suggest that KIN-1/PKA and TWK-7 may share a common pathway that is probably involved in the modulation of both locomotor activity and locomotion behavior during forward crawling.

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“…The dopaminergic mechanism of energy allocation appears to be evolutionarily preserved and found even in model organisms like Caenorhabditis elegans (Calhoun et al, 2015). Recent studies implicate dopamine in a final common pathway that couples energy sensing with regulated voluntary energy expenditure (Beeler et al, , 2010.…”

Section: Dopamine Modulates Energy Homeostasis and Thriftinessmentioning

confidence: 99%

Altered reward anticipation: Potential explanation for weight gain in schizophrenia?

Grimm

Kaiser

Plichta

et al. 2017

Neuroscience & Biobehavioral Reviews

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a b s t r a c tObesity and weight gain are severe complications of mental illness, especially schizophrenia. They result from changes in lifestyle and nutrition, side effects of medication and other, less well-understood factors. Recent studies suggest that obesity and weight gain are linked to psychopathology. Specifically, severe psychopathology is associated with greater weight dysregulation, typically weight gain. However, our knowledge about the neuroscientific basis of weight gain in schizophrenia is currently limited. We propose that altered reward anticipation, which in turn is related to striatal dopaminergic dysregulation, may explain why obesity is more prevalent in individuals with mental illness. We review evidence that reward anticipation and weight change are linked by a core deficit in dopaminergic striatal circuits. Several lines of evidence, running from animal studies to preclinical and clinical studies, suggest that striatal dopaminergic neurotransmission is a major hub for the regulation of eating behavior and that dopamine links eating behavior to other motivated behavior. From this perspective, the present review outlines a unifying perspective on dopaminergic reward anticipation as a theoretical frame to link weight gain, medication effects and psychopathology. We derive important but open empirical questions and present perspectives for new therapeutic concepts.

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Neural Mechanisms for Evaluating Environmental Variability in Caenorhabditis elegans

Cited by 86 publications

References 60 publications

Farming and public goods production in Caenorhabditis elegans populations

Farming and public goods production in Caenorhabditis elegans populations

Locomotion Behavior Is Affected by the GαS Pathway and the Two-Pore-Domain K+ Channel TWK-7 Interacting in GABAergic Motor Neurons in Caenorhabditis elegans

Altered reward anticipation: Potential explanation for weight gain in schizophrenia?

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