Interspecies variation of larval locomotion kinematics in the genus Drosophila and its relation to habitat temperature.
Ontology highlight
ABSTRACT: Background
Speed and trajectory of locomotion are the characteristic traits of individual species. Locomotion kinematics may have been shaped during evolution towards increased survival in the habitats of each species. Although kinematics of locomotion is thought to be influenced by habitats, the quantitative relation between the kinematics and environmental factors has not been fully revealed. Here, we performed comparative analyses of larval locomotion in 11 Drosophila species.Results
We found that larval locomotion kinematics are divergent among the species. The diversity is not correlated to the body length but is correlated instead to the habitat temperature of the species. Phylogenetic analyses using Bayesian inference suggest that the evolutionary rate of the kinematics is diverse among phylogenetic tree branches.Conclusions
The results of this study imply that the kinematics of larval locomotion has diverged in the evolutionary history of the genus Drosophila and evolved under the effects of the ambient temperature of habitats.
SUBMITTER: Matsuo Y
PROVIDER: S-EPMC8411537 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Efforts to define the neural circuits generating locomotor behavior have produced an initial understanding of some of the components within the spinal cord, as well as a basic understanding of several invertebrate motor pattern generators. However, how these circuits are assembled during development is poorly understood. We are defining the neural circuit that generates larval locomotion in the genetically tractable fruit fly Drosophila melanogaster to study locomotor circuit development. Forward larval locomotion involves a stereotyped posterior-to-anterior segmental translocation of body wall muscle contraction and is generated by a relatively small number of identified muscles, motor and sensory neurons, plus an unknown number of the ~270 bilaterally-paired interneurons per segment of the 1st instar larva. To begin identifying the relevant interneurons, we have conditionally inactivated synaptic transmission of interneuron subsets and assayed for the effects on locomotion. From this screen we have identified a subset of 25 interneurons per hemisegment, called the lateral locomotor neurons (LLNs), that are required for locomotion. Both inactivation and constitutive activation of the LLNs disrupt locomotion, indicating that patterned output of the LLNs is required. By expressing a calcium indicator in the LLNs, we found that they display a posterior-to-anterior wave of activity within the CNS corresponding to the segmental translocation of the muscle contraction wave. Identification of the LLNs represents the first step toward elucidating the circuit generating larval locomotion.
| S-EPMC4698040 | biostudies-literature
Project description:We report the discovery that the locomotor trajectories of Drosophila larvae follow the power-law relationship between speed and curvature previously found in the movements of human and non-human primates. Using high-resolution behavioural tracking in controlled but naturalistic sensory environments, we tested the law in maggots tracing different trajectory types, from reaching-like movements to scribbles. For most but not all flies, we found that the law holds robustly, with an exponent close to three-quarters rather than to the usual two-thirds found in almost all human situations, suggesting dynamic effects adding on purely kinematic constraints. There are different hypotheses for the origin of the law in primates, one invoking cortical computations, another viscoelastic muscle properties coupled with central pattern generators. Our findings are consistent with the latter view and demonstrate that the law is possible in animals with nervous systems orders of magnitude simpler than in primates. Scaling laws might exist because natural selection favours processes that remain behaviourally efficient across a wide range of neural and body architectures in distantly related species.
| S-EPMC5095195 | biostudies-literature
Project description:Drosophila larval locomotion, which entails rhythmic body contractions, is controlled by sensory feedback from proprioceptors. The molecular mechanisms mediating this feedback are little understood. By using genetic knock-in and immunostaining, we found that the Drosophila melanogaster transmembrane channel-like (tmc) gene is expressed in the larval class I and class II dendritic arborization (da) neurons and bipolar dendrite (bd) neurons, both of which are known to provide sensory feedback for larval locomotion. Larvae with knockdown or loss of tmc function displayed reduced crawling speeds, increased head cast frequencies, and enhanced backward locomotion. Expressing Drosophila TMC or mammalian TMC1 and/or TMC2 in the tmc-positive neurons rescued these mutant phenotypes. Bending of the larval body activated the tmc-positive neurons, and in tmc mutants this bending response was impaired. This implicates TMC's roles in Drosophila proprioception and the sensory control of larval locomotion. It also provides evidence for a functional conservation between Drosophila and mammalian TMCs.
| S-EPMC4932980 | biostudies-literature
Project description:Rhythmic movements, such as peristaltic contraction, are initiated by output from central pattern generator (CPG) networks in the CNS. These oscillatory networks elicit locomotion in the absence of external sensory or descending inputs, but CPG circuits produce more directed and behaviorally relevant movement via peripheral nervous system (PNS) input. Drosophila melanogaster larval locomotion results from patterned muscle contractions moving stereotypically along the body segments, but without PNS feedback, contraction of body segments is uncoordinated. We have dissected the role of a subset of mechanosensory neurons in the larval PNS, the chordotonal organs (chos), in providing sensory feedback to the locomotor CPG circuit with dias (Dynamic Image Analysis System) software. We analyzed mutants carrying cho mutations including atonal, a cho proneural gene, beethoven, a cho cilia class mutant, smetana and touch-insensitive larva B, two axonemal mutants, and 5D10, a weak cho mutant. All cho mutants have defects in gross path morphology compared to controls. These mutants exhibit increased frequency and duration of turning (decision-making) and reduced duration of linear locomotion. Furthermore, cho mutants affect locomotor parameters, including reduced average speed, direction change, and persistence. Dias analysis of peristaltic waves indicates that mutants exhibit reduced average speed, positive flow and negative flow, and increased stride period. Thus, cho sensilla are major proprioceptive components that underlie touch sensitivity, locomotion, and peristaltic contraction by providing sensory feedback to the locomotor CPG circuit in larvae.
| S-EPMC307691 | biostudies-literature
Project description:Drosophila melanogaster has been successfully used as a simple model to study the cellular and molecular mechanisms underlying behaviors, including the generation of motor programs. Thus, it has been shown that, as in vertebrates, CNS biogenic amines (BA) including serotonin (5HT) participate in motor control in Drosophila. Several evidence show that BA systems innervate an important association area in the insect brain previously associated to the planning and/or execution of motor programs, the Mushroom Bodies (MB). The main objective of this work is to evaluate the contribution of 5HT and its receptors expressed in MB to motor behavior in fly larva. Locomotion was evaluated using an automated tracking system, in Drosophila larvae (3(rd)-instar) exposed to drugs that affect the serotonergic neuronal transmission: alpha-methyl-L-dopa, MDMA and fluoxetine. In addition, animals expressing mutations in the 5HT biosynthetic enzymes or in any of the previously identified receptors for this amine (5HT1AR, 5HT1BR, 5HT2R and 5HT7R) were evaluated in their locomotion. Finally, RNAi directed to the Drosophila 5HT receptor transcripts were expressed in MB and the effect of this manipulation on motor behavior was assessed. Data obtained in the mutants and in animals exposed to the serotonergic drugs, suggest that 5HT systems are important regulators of motor programs in fly larvae. Studies carried out in animals pan-neuronally expressing the RNAi for each of the serotonergic receptors, support this idea and further suggest that CNS 5HT pathways play a role in motor control. Moreover, animals expressing an RNAi for 5HT1BR, 5HT2R and 5HT7R in MB show increased motor behavior, while no effect is observed when the RNAi for 5HT1AR is expressed in this region. Thus, our data suggest that CNS 5HT systems are involved in motor control, and that 5HT receptors expressed in MB differentially modulate motor programs in fly larvae.
| S-EPMC3934909 | biostudies-literature
Project description:Halorhodopsin (NpHR), a light-driven microbial chloride pump, enables silencing of neuronal function with superb temporal and spatial resolution. Here, we generated a transgenic line of Drosophila that drives expression of NpHR under control of the Gal4/UAS system. Then, we used it to dissect the functional properties of neural circuits that regulate larval peristalsis, a continuous wave of muscular contraction from posterior to anterior segments. We first demonstrate the effectiveness of NpHR by showing that global and continuous NpHR-mediated optical inhibition of motor neurons or sensory feedback neurons induce the same behavioral responses in crawling larvae to those elicited when the function of these neurons are inhibited by Shibire(ts), namely complete paralyses or slowed locomotion, respectively. We then applied transient and/or focused light stimuli to inhibit the activity of motor neurons in a more temporally and spatially restricted manner and studied the effects of the optical inhibition on peristalsis. When a brief light stimulus (1-10 sec) was applied to a crawling larva, the wave of muscular contraction stopped transiently but resumed from the halted position when the light was turned off. Similarly, when a focused light stimulus was applied to inhibit motor neurons in one or a few segments which were about to be activated in a dissected larva undergoing fictive locomotion, the propagation of muscular constriction paused during the light stimulus but resumed from the halted position when the inhibition (>5 sec) was removed. These results suggest that (1) Firing of motor neurons at the forefront of the wave is required for the wave to proceed to more anterior segments, and (2) The information about the phase of the wave, namely which segment is active at a given time, can be memorized in the neural circuits for several seconds.
| S-EPMC3247229 | biostudies-literature
Project description:The generation of coordinated body movements relies on sensory feedback from mechanosensitive proprioceptors. We have found that the proper function of NompC, a putative mechanosensitive TRP channel, is not only required for fly locomotion, but also crucial for larval crawling. Calcium imaging revealed that NompC is required for the activation of two subtypes of sensory neurons during peristaltic muscle contractions. Having isolated a full-length nompC cDNA with a protein coding sequence larger than previously predicted, we demonstrate its function by rescuing locomotion defects in nompC mutants, and further show that antibodies against the extended C terminus recognize NompC in chordotonal ciliary tips. Moreover, we show that the ankyrin repeats in NompC are required for proper localization and function of NompC in vivo and are required for association of NompC with microtubules. Taken together, our findings suggest that NompC mediates proprioception in locomotion and support its role as a mechanosensitive channel.
| S-EPMC2933178 | biostudies-literature
Project description:As in vertebrates, dopaminergic neural systems are key regulators of motor programs in insects, including the fly Drosophila melanogaster. Dopaminergic systems innervate the Mushroom Bodies (MB), an important association area in the insect brain primarily associated to olfactory learning and memory, but that has been also implicated with the execution of motor programs. The main objectives of this work is to assess the idea that dopaminergic systems contribute to the execution of motor programs in Drosophila larvae, and then, to evaluate the contribution of specific dopaminergic receptors expressed in MB to these programs. Our results show that animals bearing a mutation in the dopamine transporter show reduced locomotion, while mutants for the dopaminergic biosynthetic enzymes or the dopamine receptor Dop1R1 exhibit increased locomotion. Pan-neuronal expression of an RNAi for the Dop1R1 confirmed these results. Further studies show that animals expressing the RNAi for Dop1R1 in the entire MB neuronal population or only in the MB ?-lobe forming neurons, exhibit an increased motor output, as well. Interestingly, our results also suggest that other dopaminergic receptors do not contribute to larval motor behavior. Thus, our data support the proposition that CNS dopamine systems innervating MB neurons modulate larval locomotion and that Dop1R1 mediates this effect.
| S-EPMC7043742 | biostudies-literature
Project description:We use Drosophila larval locomotion as a model to elucidate the working principles of motor circuits. Larval locomotion is generated by rhythmic and sequential contractions of body-wall muscles from the posterior to anterior segments, which in turn are regulated by motor neurons present in the corresponding neuromeres. Motor neurons are known to receive both excitatory and inhibitory inputs, combined action of which likely regulates patterned motor activity during locomotion. Although recent studies identified candidate inhibitory premotor interneurons, the identity of premotor interneurons that provide excitatory drive to motor neurons during locomotion remains unknown. In this study, we searched for and identified two putative excitatory premotor interneurons in this system, termed CLI1 and CLI2 (cholinergic lateral interneuron 1 and 2). These neurons were segmentally arrayed and activated sequentially from the posterior to anterior segments during peristalsis. Consistent with their being excitatory premotor interneurons, the CLIs formed GRASP- and ChAT-positive putative synapses with motoneurons and were active just prior to motoneuronal firing in each segment. Moreover, local activation of CLI1s induced contraction of muscles in the corresponding body segments. Taken together, our results suggest that the CLIs directly activate motoneurons sequentially along the segments during larval locomotion.
| S-EPMC4965782 | biostudies-literature
Project description:The cerebellum is involved in coordinating motor behaviour, but how the cerebellar network regulates locomotion is still not well understood. We characterised the activity of putative cerebellar Purkinje cells, Golgi cells and mossy fibres in awake mice engaged in an active locomotion task, using high-density silicon electrode arrays. Analysis of the activity of over 300 neurons in response to locomotion revealed that the majority of cells (53%) were significantly modulated by phase of the stepping cycle. However, in contrast to studies involving passive locomotion on a treadmill, we found that a high proportion of cells (45%) were tuned to the speed of locomotion, and 19% were tuned to yaw movements. The activity of neurons in the cerebellar vermis provided more information about future speed of locomotion than about past or present speed, suggesting a motor, rather than purely sensory, role. We were able to accurately decode the speed of locomotion with a simple linear algorithm, with only a relatively small number of well-chosen cells needed, irrespective of cell class. Our observations suggest that behavioural state modulates cerebellar sensorimotor integration, and advocate a role for the cerebellar vermis in control of high-level locomotor kinematic parameters such as speed and yaw.
| S-EPMC6136788 | biostudies-other