Distinct neural circuits establish the same chemosensory behavior in C. elegans

Animals frequently exhibit the same behavior under different environmental or physiological conditions. To what extent these behaviors are generated by similar vs. distinct mechanisms is unclear. Moreover, the circumstances under which divergent neural mechanisms establish the same behavior, and the molecular signals that regulate the same behavior across conditions, are poorly understood. We show that in C. elegans, distinct neural mechanisms mediate the same chemosensory behavior at two different life stages. Both dauer larvae and starved adults are attracted to carbon dioxide (CO2), but CO2 attraction is mediated by distinct sets of interneurons at the two life stages. Some interneurons mediate CO2 response only in dauers, some show CO2-evoked activity in adults and dauers but contribute to CO2 response only in adults, and some show CO2-evoked activity that opposes CO2 attraction in adults but promotes CO2 attraction in dauers. We also identify a novel role for insulin signaling in establishing life-stage-specific CO2 responses by modulating interneuron activity. Further, we show that a combinatorial code of both shared and life-stage-specific molecular signals regulate CO2 attraction. Our results identify a mechanism by which the same chemosensory behavior can be generated by distinct neural circuits, revealing an unexpected complexity to chemosensory processing.

Chemical communication in lizards and a potential role for vasotocin in modulating social interactions

Lizards use chemical communication to mediate many reproductive, competitive, and social behaviors, but the neuroendocrine mechanisms underlying chemical communication in lizards are not well understood and understudied. By implementing a neuroendocrine approach to the study of chemical communication in reptiles, we can address a major gap in our knowledge of the evolutionary mechanisms shaping chemical communication in vertebrates. The neuropeptide arginine vasotocin (AVT) and its mammalian homologue vasopressin are responsible for a broad spectrum of diversity in competitive and reproductive strategies in many vertebrates, mediating social behavior through the chemosensory modality. In this review, we posit that, though limited, the available data on AVT-mediated chemical communication in lizards reveals intriguing patterns that suggest AVT plays a more prominent role in lizard chemosensory behavior than previously appreciated. We argue that these results warrant more research into the mechanisms used by AVT to modify the performance of chemosensory behavior and responses to conspecific chemical signals. We first provide a broad overview of the known social functions of chemical signals in lizards, the glandular sources of chemical signal production in lizards (e.g., epidermal secretory glands), and the chemosensory detection methods and mechanisms used by lizards. Then, we review the locations of vasotocinergic populations and neuronal projections in lizard brains, as well as sites of peripheral receptors for AVT in lizards. Finally, we end with a case study in green anoles (Anolis carolinensis), discussing findings from recently published work on the impact of AVT in adult males on chemosensory communication during social interactions, adding new data from a similar study in which we tested the impact of AVT on chemosensory behavior of adult females. We offer concluding remarks on addressing several fundamental questions regarding the role of AVT in chemosensory communication and social behavior in lizards.

Assessing the impact of static and fluctuating ocean acidification on the behavior of Amphiprion percula

Coral reef organisms are exposed to both an increasing magnitude of pCO2, and natural fluctuations on a diel scale. For coral reef fishes, one of the most profound effects of ocean acidification is the impact on ecologically important behaviors. Previous behavioral research has primarily been conducted under static pCO2 conditions and have recently come under criticism. Recent studies have provided evidence that the negative impacts on behavior may be reduced under more environmentally realistic, fluctuating conditions. We investigated the impact of both present and future day, static (500 and 1000 μatm) and diel fluctuating (500 ± 200 and 1000 ± 200 μatm) pCO2 on the lateralization and chemosensory behavior of juvenile anemonefish, Amphiprion percula. Our static experimental comparisons support previous findings that under elevated pCO2, fish become un-lateralized and lose the ability to discriminate olfactory cues. Diel-fluctuating pCO2 may aid in mitigating the severity of some behavioral abnormalities such as the chemosensory response, where a preference for predator cues was significantly reduced under a future diel-fluctuating pCO2 regime. This research aids in ground truthing earlier findings and contributes to our growing knowledge of the role of fluctuating conditions.

Computational and experimental insights into the chemosensory navigation ofAedes aegyptimosquito larvae

Mosquitoes are prolific disease vectors that affect public health around the world. Although many studies have investigated search strategies used by host-seeking adult mosquitoes, little is known about larval search behavior. Larval behavior affects adult body size and fecundity, and thus the capacity of individual mosquitoes to find hosts and transmit disease. Understanding vector survival at all life stages is crucial for improving disease control. In this study we use experimental and computational methods to investigate the chemical ecology and search behavior ofAedes aegyptimosquito larvae. We show that larvae do not respond to several olfactory cues used by adultAe. aegyptito assess larval habitat quality, but perceive microbial RNA as a potent foraging attractant. Second, we demonstrate thatAe. aegyptilarvae use a strategy consistent with chemokinesis, rather than chemotaxis, to navigate chemical gradients. Using computational modeling, we further show that chemokinesis is more efficient than chemotaxis for avoiding repellents in ecologically relevant larval habitat sizes. Finally, we use experimental observations and computational analyses to demonstrate that larvae respond to starvation pressure by optimizing exploration behavior. Our results identify key characteristics of foraging behavior in a disease vector mosquito, including the identification of a surprising foraging attractant and an unusual behavioral mechanism for chemosensory preference. In addition to implications for better understanding and control of disease vectors, this work establishes mosquito larvae as a tractable model for chemosensory behavior and navigation.

Escherichia coliRemodels the Chemotaxis Pathway for Swarming

ABSTRACTMany flagellated bacteria “swarm” over a solid surface as a dense consortium. In different bacteria, swarming is facilitated by several alterations such as those corresponding to increased flagellum numbers, special stator proteins, or secreted surfactants. We report here a change in the chemosensory physiology of swarmingEscherichia coliwhich alters its normal “run tumble” bias.E. colibacteria taken from a swarm exhibit more highly extended runs (low tumble bias) and higher speeds thanE. colibacteria swimming individually in a liquid medium. The stability of the signaling protein CheZ is higher in swarmers, consistent with the observed elevation of CheZ levels and with the low tumble bias. We show that the tumble bias displayed by wild-type swarmers is the optimal bias for maximizing swarm expansion. In assays performed in liquid, swarm cells have reduced chemotactic performance. This behavior is specific to swarming, is not specific to growth on surfaces, and persists for a generation. Therefore, the chemotaxis signaling pathway is reprogrammed for swarming.IMPORTANCEThe fundamental motile behavior ofE. coliis a random walk, where straight “runs” are punctuated by “tumbles.” This behavior, conferred by the chemotaxis signaling system, is used to track chemical gradients in liquid. Our study results show that when migrating collectively on surfaces,E. colimodifies its chemosensory physiology to decrease its tumble bias (and hence to increase run durations) by post-transcriptional changes that alter the levels of a key signaling protein. We speculate that the low tumble bias may contribute to the observed Lévy walk (LW) trajectories within the swarm, where run durations have a power law distribution. In animals, LW patterns are hypothesized to maximize searches in unpredictable environments. Swarming bacteria face several challenges while moving collectively over a surface—maintaining cohesion, overcoming constraints imposed by a physical substrate, searching for nutrients as a group, and surviving lethal levels of antimicrobials. The altered chemosensory behavior that we describe in this report may help with these challenges.

A functional genomics screen in planarians reveals regulators of whole-brain regeneration

Planarians regenerate all body parts after injury, including the central nervous system (CNS). We capitalized on this distinctive trait and completed a gene expression-guided functional screen to identify factors that regulate diverse aspects of neural regeneration in Schmidtea mediterranea. Our screen revealed molecules that influence neural cell fates, support the formation of a major connective hub, and promote reestablishment of chemosensory behavior. We also identified genes that encode signaling molecules with roles in head regeneration, including some that are produced in a previously uncharacterized parenchymal population of cells. Finally, we explored genes downregulated during planarian regeneration and characterized, for the first time, glial cells in the planarian CNS that respond to injury by repressing several transcripts. Collectively, our studies revealed diverse molecules and cell types that underlie an animal’s ability to regenerate its brain.