Shared behavioral mechanisms underlie <i>C. elegans</i> aggregation and swarming

In complex biological systems, simple individual-level behavioral rules can give rise to emergent group-level behavior. While collective behavior has been well studied in cells and larger organisms, the mesoscopic scale is less understood, as it is unclear which sensory inputs and physical processes matter a priori. Here, we investigate collective feeding in the roundworm C. elegans at this intermediate scale, using quantitative phenotyping and agent-based modeling to identify behavioral rules underlying both aggregation and swarming—a dynamic phenotype only observed at longer timescales. Using fluorescence multi-worm tracking, we quantify aggregation in terms of individual dynamics and population-level statistics. Then we use agent-based simulations and approximate Bayesian inference to identify three key behavioral rules for aggregation: cluster-edge reversals, a density-dependent switch between crawling speeds, and taxis towards neighboring worms. Our simulations suggest that swarming is simply driven by local food depletion but otherwise employs the same behavioral mechanisms as the initial aggregation

Comparison of solitary and collective foraging strategies of Caenorhabditis elegans in patchy food distributions

Collective foraging has been shown to benefit organisms in environments where food is patchily distributed, but whether this is true in the case where organisms do not rely on long range communications to coordinate their collective behaviour has been understudied. To address this question, we use the tractable laboratory model organism Caenorhabditis elegans, where a social strain (npr-1 mutant) and a solitary strain (N2) are available for direct comparison of foraging strategies. We first developed an on-lattice minimal model for comparing collective and solitary foraging strategies, finding that social agents benefit from feeding faster and more efficiently simply due to group formation. Our laboratory foraging experiments with npr-1 and N2 worm populations, however, show an advantage for solitary N2 in all food distribution environments that we tested. We incorporated additional strain43 specific behavioural parameters of npr-1 and N2 worms into our model and computationally identified N2’s higher feeding rate to be the key factor underlying its advantage, without which it is possible to recapitulate the advantage of collective foraging in patchy environments. Our work highlights the theoretical advantage of collective foraging due to group formation alone without long-range interactions, and the valuable role of modelling to guide experiments

brightfieldPheromoneImaging_N2_rep12

This experiment is part of the Bright field pheromone imaging dataset for the following publication: https://www.biorxiv.org/content/early/2018/11/01/398370 strain : N2 timestamp : 20170703 strain_description : N2: lab reference strain. sex : hermaphrodite stage : adult media : NGM agar low peptone arena : style : petri size : 35 food : OP50, diluted OD = 0.75, freshly seeded who : S. Serena Ding protocol : Method in Ding, Schumacher et al. doi.org/10.1101/398370. Alternatively, visit dx.doi.org/10.17504/protocols.io.vyie7ue. lab : name : Behavioural Genomics location : London, United Kingdom software : name : tierpsy (https://github.com/ver228/tierpsy-tracker) days_of_adulthood : 1 total time (s) : 3600 frames per second : 25 video micrometers per pixel : 1

Elucidating the role of non-muscle myosin II in Caenorhabditis elegans stem-like seam cell divisions

Caenorhabiditis elegans seam cells (SC) are multipotent neuroectodermal cells that undergo both symmetrical and asymmetrical divisions throughout larval development, thus providing a valuable model system to gain mechanistic insights into the regulation of asymmetric divisions and the switch between the symmetric and asymmetric modes of division. Reiterative SC asymmetric division typically produces a differentiative anterior daughter that moves out of the seam line and joins the hyp7 syncytium and a proliferative posterior daughter that retains seam fate and carries on dividing. Non-muscle myosin II (NMY II) has emerged as a key regulator in the asymmetric divisions of the C. elegans zygote, the C. elegans Q neuroblast, and the Drosophila neuroblast systems. In addition to being an essential player in cytokinesis, nmy-2's roles in cell adhesion and migration processes further underline its potential as a regulator of seam cell asymmetric divisions. In this thesis work, I investigated the role of NMY-2 in C. elegans seam cell divisions. I found that nmy-2 is expressed in the seam and its protein localization is dynamic during SC divisions. Post-embryonic nmy-2 knockdown using a combination of temperature sensitive mutants and RNA interference robustly reduces terminal SC number. This reduction is due to progressive SC loss after each asymmetric division as a consequence of aberrant cell fate determination. I identified three classes of cell fate transformation phenotypes following nmy-2 knockdown, and sought to dissect the cell molecular basis of these phenotypes using a dual-color fate reporter strain. Although prevalent in nmy-2 knockdown, cytokinesis defects are not the only cause of SC losses. nmy-2 also does not appear to regulate SC divisions by affecting spindle positioning. In summary, nmy-2 function is crucial to ensure the proper division and fate specification in post-embryonic SC development.</p

Elucidating the role of non-muscle myosin II in Caenorhabditis elegans stem-like seam cell divisions

Caenorhabiditis elegans seam cells (SC) are multipotent neuroectodermal cells that undergo both symmetrical and asymmetrical divisions throughout larval development, thus providing a valuable model system to gain mechanistic insights into the regulation of asymmetric divisions and the switch between the symmetric and asymmetric modes of division. Reiterative SC asymmetric division typically produces a differentiative anterior daughter that moves out of the seam line and joins the hyp7 syncytium and a proliferative posterior daughter that retains seam fate and carries on dividing. Non-muscle myosin II (NMY II) has emerged as a key regulator in the asymmetric divisions of the C. elegans zygote, the C. elegans Q neuroblast, and the Drosophila neuroblast systems. In addition to being an essential player in cytokinesis, nmy-2's roles in cell adhesion and migration processes further underline its potential as a regulator of seam cell asymmetric divisions. In this thesis work, I investigated the role of NMY-2 in C. elegans seam cell divisions. I found that nmy-2 is expressed in the seam and its protein localization is dynamic during SC divisions. Post-embryonic nmy-2 knockdown using a combination of temperature sensitive mutants and RNA interference robustly reduces terminal SC number. This reduction is due to progressive SC loss after each asymmetric division as a consequence of aberrant cell fate determination. I identified three classes of cell fate transformation phenotypes following nmy-2 knockdown, and sought to dissect the cell molecular basis of these phenotypes using a dual-color fate reporter strain. Although prevalent in nmy-2 knockdown, cytokinesis defects are not the only cause of SC losses. nmy-2 also does not appear to regulate SC divisions by affecting spindle positioning. In summary, nmy-2 function is crucial to ensure the proper division and fate specification in post-embryonic SC development.</p

fluorescenceAggregationImaging_twoColour_npr-1_rep3

This experiment is part of Fluorescence Aggregation Imaging dataset for the following publication: https://www.biorxiv.org/content/early/2018/11/01/398370 strain : OMG2 (green), OMG19 (red) timestamp : 20170208 strain_description : OMG2: mIs12[myo-2p::GFP]II; npr-1(ad609)X. OMG19: rmIs349[myo3p::RFP]; npr-1(ad609)X. sex : hermaphrodite stage : adult media : NGM agar low peptone arena : style : petri size : 35 food : OP50, diluted OD = 0.75, freshly seeded who : S. Serena Ding protocol : Method in Ding, Schumacher et al. doi.org/10.1101/398370. Alternatively, visit dx.doi.org/10.17504/protocols.io.vzje74n. lab : name : Behavioural Genomics location : London, United Kingdom software : name : tierpsy (https://github.com/ver228/tierpsy-tracker) days_of_adulthood : 1 total time (s) : 3600 frames per second : 9 video micrometers per pixel : 5.12

brightfieldBigPatchSwarmingImaging_npr-1_rep8_part1

This experiment is part of the Bright field big patch swarming imaging dataset for the following publication: https://www.biorxiv.org/content/early/2018/11/01/398370 strain : DA609 timestamp : 20180611 strain_description : DA609: npr-1(ad609)X. sex : hermaphrodite stage : adult media : NGM agar low peptone arena : style : petri size : 35 food : OP50, diluted OD = 0.38, inoculated overnight at room temperature who : S. Serena Ding protocol : Method in Ding, Schumacher et al. doi.org/10.1101/398370. Alternatively, visit dx.doi.org/10.17504/protocols.io.vyhe7t6. lab : name : Behavioural Genomics location : London, United Kingdom software : name : tierpsy (https://github.com/ver228/tierpsy-tracker) days_of_adulthood : 1 total time (s) : 3600 per file frames per second : 25 video micrometers per pixel : 1

brightfieldPheromoneImaging_npr-1_rep11

This experiment is part of the Bright field pheromone imaging dataset for the following publication: https://www.biorxiv.org/content/early/2018/11/01/398370 strain : DA609 timestamp : 20170703 strain_description : DA609: npr-1(ad609)X. sex : hermaphrodite stage : adult media : NGM agar low peptone arena : style : petri size : 35 food : OP50, diluted OD = 0.75, freshly seeded who : S. Serena Ding protocol : Method in Ding, Schumacher et al. doi.org/10.1101/398370. Alternatively, visit dx.doi.org/10.17504/protocols.io.vyie7ue. lab : name : Behavioural Genomics location : London, United Kingdom software : name : tierpsy (https://github.com/ver228/tierpsy-tracker) days_of_adulthood : 1 total time (s) : 3600 frames per second : 25 video micrometers per pixel : 1

brightfieldPheromoneImaging_daf-22_rep2

This experiment is part of the Bright field pheromone imaging dataset for the following publication: https://www.biorxiv.org/content/early/2018/11/01/398370 strain : DR476 timestamp : 20170630 strain_description : AX994: daf-22(m130)II. sex : hermaphrodite stage : adult media : NGM agar low peptone arena : style : petri size : 35 food : OP50, diluted OD = 0.75, freshly seeded who : S. Serena Ding protocol : Method in Ding, Schumacher et al. doi.org/10.1101/398370. Alternatively, visit dx.doi.org/10.17504/protocols.io.vyie7ue. lab : name : Behavioural Genomics location : London, United Kingdom software : name : tierpsy (https://github.com/ver228/tierpsy-tracker) days_of_adulthood : 1 total time (s) : 3600 frames per second : 25 video micrometers per pixel : 1