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Ding, S. S.

Publications and source records attributed to Ding, S. S..

8 recordsLinked to original sources

From Networks to Traveling Waves and Back: Persistent Pattern Generation Across Collective Phases in C. elegans

Thousands of C. elegans placed adjacent to a food patch self-organize sequentially into a visible branching network off-food and then a coherent traveling consumption wave -- a multi-phase collective phenomenon we term wurmuration. Dynamical networks and traveling waves have previously only been described separately in this organism. Using a minimal agent-based model, we show that a single generative program produces both collective phases and their topological continuity. Four components (elongated body geometry, roaming-dwelling switching, preferred local worm density navigation, and food chemotaxis) are necessary and sufficient; what changes between phases is only the food environment they act on. We show that network-like organization persists cryptically (visible only through temporal integration) across the qualitatively distinct wave phase, indicating that the two phases differ in environmental context rather than in underlying behavioral rules. Finally, tuning the preferred density component alone recapitulates N2 vs. DA609 differences in wave dynamics; N2 additionally shows greater per-trial variability in cryptic network topology than DA609, in line with less consistent collective engagement in this lower-sociality strain. Our findings suggest that complex multi-phase collective phenomena can be unified by a shared generative program, shifting the description of spatial organization from the emergent patterns to their underlying components.

biophysics↗

Differential phoretic host use among sympatric Caenorhabditis nematodes and an association with invasive nitidulid beetles in southwestern Germany

Little is known about the natural history of many Caenorhabditis nematodes, despite their relationship to the model species C. elegans. While these nematodes rely on invertebrate vectors to disperse to new habitats (phoresy), vector use for most species has not been characterized. We surveyed the invertebrate community of a habitat containing three sympatric Caenorhabditis in southwestern Germany, determining differential and specific vector use for each of these co-occurring species. We documented a specific association between C. apta n. sp. and two species of invasive nitidulid beetles, and a particularly strong association of the nematode with the beetle Stelidota geminata, where we recovered more nematodes per individual beetle and a higher proportion of beetles carrying nematodes compared to the co-occurring Epuraea ocularis. Our results provide evidence for group dispersal using beetles in C. apta, supporting previous observations of collective dispersal behavior in this species, and establish a starting point for further dissecting the evolutionary and mechanistic causes and consequences of interactions between Caenorhabditis nematodes and their vector species in ecologically relevant conditions.

ecology↗

Intrinsic strain-specific behaviour predicts emergent collective aggregation in heterogeneous C. elegans groups

Collective animal behaviour research to date typically specifies members of the group as identical individuals, even though within group heterogeneity is commonplace. We exploit the tractable C. elegans study system to explicitly define and manipulate heterogeneity to investigate how individuals with different behavioural phenotypes interact and aggregate in heterogeneous group settings. Using controlled mixing experiments between pairs of strains that have defined aggregation tendencies, we apply a quantitative behavioural analysis framework and show that individuals maintain their intrinsic movement patterns and interaction rules regardless of group composition. Notably, neither behavioural differences nor distant genetic relatedness between strains lead to a modulation of individual behaviour; instead, distinct strains behave and coexist without influencing each others intrinsic behavioural tendencies. Using a simulation model, we further show that aggregation in mixed C. elegans groups can be accurately predicted from strain-specific individual-level parameters measured in homogeneous settings. Our integrated approach provides a generalised framework for understanding collective behaviour in diverse heterogeneous systems, which may offer insights into population-level consequences of phenotypic variation and broader ecological processes.

animal behavior and cognition↗

Natural variation in Caenorhabditis elegans collective behavior reveals potential adaptation to novel environments

Animal behavior can diverge in natural populations in response to different environmental conditions, but if and how natural selection also shapes the evolution of collective behavior in groups of animals remains underexplored. With their cosmopolitan distribution and known collective behaviours, wild populations of Caenorhabditis elegans provide a powerful system to address how collective behavior could evolve across natural habitats on a global scale. We screened a panel of 196 genetically diverse C. elegans strains sampled from around the world, conducting aggregation behavior experiments and analysis to quantify natural variation among these populations. We found substantial variation in the spatial magnitude and the temporal dynamics of aggregation across strains, which were significantly explained by the elevation of the source habitats. Accounting for neutral evolutionary processes, our maximum likelihood population effects (MLPE) models further support a role of selection on aggregation. Furthermore, the two behavioral traits are highly heritable, and genome-wide association studies (GWAS) revealed a quantitative trait locus (QTL) containing several candidate genes associated with oxygen response and foraging behaviors. Our results showcase C. elegans aggregation as a collective behavior that has diverged globally across elevational gradients, and support that natural selection has shaped the evolution of this collective behavior.

evolutionary biology↗

Megapixel camera arrays for high-resolution animal tracking in multiwell plates

Tracking small laboratory animals such as flies, fish, and worms is used for phenotyping in neuroscience, genetics, disease modelling, and drug discovery. Current imaging systems are limited either in spatial resolution or throughput. A system capable of imaging a large number of animals with sufficient resolution to estimate their pose would enable a new class of experiments where detailed behavioural differences are quantified but at a scale where hundreds of treatments can be tested simultaneously. Here we report a new imaging system consisting of an array of six 12-megapixel cameras that can simultaneously record from all the wells of a 96-well plate with a resolution of 80 pixels/mm at 25 frames per second. We show that this resolution is sufficient to estimate the pose of nematode worms including head identification and to extract high-dimensional phenotypic fingerprints. We use the system to study behavioural variability across wild isolates, the sensitisation of worms to repeated blue light stimulation, the phenotypes of worm disease models, and worms behavioural responses to drug treatment. Because the system is compatible with standard multiwell plates, it makes computational ethological approaches accessible in existing high-throughput pipelines and greatly increases the scale of possible phenotypic screening experiments in C. elegans.

animal behavior and cognition↗

Measuring C. elegans spatial foraging and food intake using bioluminescent bacteria

For most animals, feeding includes two behaviours: foraging to find a food patch and food intake once a patch is found. The nematode Caenorhabditis elegans is a useful model for studying the genetics of both behaviours. However, most methods of measuring feeding in worms quantify either foraging behaviour or food intake but not both. Imaging the depletion of fluorescently labelled bacteria provides information on both the distribution and amount of consumption, but even after patch exhaustion a prominent background signal remains, which complicates quantification. Here, we used a bioluminescent Escherichia coli strain to quantify C. elegans feeding. With light emission tightly coupled to active metabolism, only living bacteria are capable of bioluminescence so the signal is lost upon ingestion. We quantified the loss of bioluminescence using N2 reference worms and eat-2 mutants, and found a nearly 100-fold increase in signal-to-background ratio and lower background compared to loss of fluorescence. We also quantified feeding using aggregating npr-1 mutant worms. We found that groups of npr-1 mutants first clear bacteria from each other before foraging collectively for more food; similarly, during high density swarming, only worms at the migrating front are in contact with bacteria. These results demonstrate the usefulness of bioluminescent bacteria for quantifying feeding and suggest a hygiene hypothesis for the function of C. elegans aggregation and swarming.

animal behavior and cognition↗

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 strain-specific behavioural parameters of npr-1 and N2 worms into our model and computationally identified N2s 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.

animal behavior and cognition↗

Common behavioral mechanisms underlie C. elegans aggregation and swarming

In complex biological systems, simple individual-level behavioral rules can give rise to emergent group-level behavior. While such 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 fluorescent multi-worm tracking, we quantify aggregation behavior in terms of individual dynamics and population-level statistics. Based on our quantification, we use agent-based simulations and approximate Bayesian inference to identify three key behavioral rules that give rise to 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. Hence, mesoscopic C. elegans uses mechanisms familiar from microscopic systems for aggregation, but implemented via more complex behaviors characteristic of macroscopic organisms.

biophysics↗