Dataset Information

Robustness and plasticity in Drosophila heat avoidance.

ABSTRACT: Simple innate behavior is often described as hard-wired and largely inflexible. Here, we show that the avoidance of hot temperature, a simple innate behavior, contains unexpected plasticity in Drosophila. First, we demonstrate that hot receptor neurons of the antenna and their molecular heat sensor, Gr28B.d, are essential for flies to produce escape turns away from heat. High-resolution fly tracking combined with a 3D simulation of the thermal environment shows that, in steep thermal gradients, the direction of escape turns is determined by minute temperature differences between the antennae (0.1°-1 °C). In parallel, live calcium imaging confirms that such small stimuli reliably activate both peripheral thermosensory neurons and central circuits. Next, based on our measurements, we evolve a fly/vehicle model with two symmetrical sensors and motors (a "Braitenberg vehicle") which closely approximates basic fly thermotaxis. Critical differences between real flies and the hard-wired vehicle reveal that fly heat avoidance involves decision-making, relies on rapid learning, and is robust to new conditions, features generally associated with more complex behavior.

SUBMITTER: Simoes JM

PROVIDER: S-EPMC8024383 | biostudies-literature | 2021 Apr

REPOSITORIES: biostudies-literature

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Robustness and plasticity in Drosophila heat avoidance.

Simões José Miguel JM Levy Joshua I JI Zaharieva Emanuela E EE Vinson Leah T LT Zhao Peixiong P Alpert Michael H MH Kath William L WL Para Alessia A Gallio Marco M

Nature communications 20210406 1

Simple innate behavior is often described as hard-wired and largely inflexible. Here, we show that the avoidance of hot temperature, a simple innate behavior, contains unexpected plasticity in Drosophila. First, we demonstrate that hot receptor neurons of the antenna and their molecular heat sensor, Gr28B.d, are essential for flies to produce escape turns away from heat. High-resolution fly tracking combined with a 3D simulation of the thermal environment shows that, in steep thermal gradients, ...[more]

PMID: 33824330

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Project description:There is a growing interest in the physiology underpinning heat tolerance of ectotherms and their responses to the ongoing rise in temperature. However, there is no consensus about the underlying physiological mechanisms. According to "the maintain aerobic scope and regulate oxygen supply" hypothesis, responses to warming at different organizational levels contribute to the ability to safeguard energy metabolism via aerobic pathways. At the cellular level, a decrease in cell size increases the capacity for the uptake of resources (e.g., food and oxygen), but the maintenance of electrochemical gradients across cellular membranes implies greater energetic costs in small cells. In this study, we investigated how different rearing temperatures affected cell size and heat tolerance in the fruit fly Drosophila melanogaster. We tested the hypothesis that smaller-celled flies are more tolerant to acute, intense heat stress whereas larger-celled flies are more tolerant to chronic, mild heat stress. We used the thermal tolerance landscape framework, which incorporates the intensity and duration of thermal challenge. Rearing temperatures strongly affected both cell size and survival times. We found different effects of developmental plasticity on tolerance to either chronic or acute heat stress. Warm-reared flies had both smaller cells and exhibited higher survival times under acute, intense heat stress when compared to cold-reared flies. However, under chronic, mild heat stress, the situation was reversed and cold-reared flies, consisting of larger cells, showed better survival. These differences in heat tolerance could have resulted from direct effects of rearing temperature or they may be mediated by the correlated changes in cell size. Notably, our results are consistent with the idea that a smaller cell size may confer tolerance to acute temperatures via enhanced oxygen supply, while a larger cell may confer greater tolerance to chronic and less intense heat stress via more efficient use of resources.

Project description:In the last decade, case studies in plants and animals provided increasing insight into the molecular mechanisms of developmental plasticity. When complemented with evolutionary and ecological analyses, these studies suggest that plasticity represents a mechanism facilitating adaptive change, increasing diversity and fostering the evolution of novelty. Here, we summarize genetic, molecular and evolutionary studies on developmental plasticity of feeding structures in nematodes, focusing on the model organism Pristionchus pacificus and its relatives. Like its famous cousin Caenorhabditis elegans, P. pacificus reproduces as a self-fertilizing hermaphrodite and can be cultured in the laboratory on E. coli indefinitely with a four-day generation time. However, in contrast to C. elegans, Pristionchus worms show more complex feeding structures in adaptation to their life history. Pristionchus nematodes live in the soil and are reliably found in association with scarab beetles, but only reproduce after the insects' death. Insect carcasses usually exist only for a short time period and their turnover is partially unpredictable. Strikingly, Pristionchus worms can have two alternative mouth-forms; animals are either stenostomatous (St) with a single tooth resulting in strict bacterial feeding, or alternatively, they are eurystomatous (Eu) with two teeth allowing facultative predation. Laboratory-based studies revealed a regulatory network that controls the irreversible decision of individual worms to adopt the St or Eu form. These studies revealed that a developmental switch controls the mouth-form decision, confirming long-standing theory about the role of switch genes in developmental plasticity. Here, we describe the current understanding of P. pacificus mouth-form regulation. In contrast to plasticity, robustness describes the property of organisms to produce unchanged phenotypes despite environmental perturbations. While largely opposite in principle, the relationship between developmental plasticity and robustness has only rarely been tested in particular study systems. Based on a study of the Hsp90 chaperones in nematodes, we suggest that robustness and plasticity are indeed complementary concepts. Genetic switch networks regulating plasticity require robustness to produce reproducible responses to the multitude of environmental inputs and the phenotypic output requires robustness because the range of possible phenotypic outcomes is constrained. Thus, plasticity and robustness are actually not mutually exclusive, but rather complementary concepts.

Dataset Information

Robustness and plasticity in Drosophila heat avoidance.

Publications

Robustness and plasticity in Drosophila heat avoidance.

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