Hierarchy and Flexibility in Caenorhabditis elegans foraging

Abstract

Foraging is an ecologically relevant and evolutionary ancient behavior underlying some of the most important decisions made by all animals. Foraging in the nematode worm C. elegans is thought to be organized into two distinct states - the exploratory phase of roaming and the exploitative phase of dwelling. During roaming, the worm moves quickly across the bacterial lawn of food with low frequency of turns, whereas during dwelling, it moves rather slowly with frequent turns, thus confining itself to a very small region. This thesis was aimed at understanding the organizational principles underlying foraging behavior in the nematode worm C. elegans. It is currently unknown whether hierarchical organization can explain C. elegans foraging behavior. Given also that flexibility is an integral part of animal behavior, this thesis also aimed towards understanding how the principle of hierarchy can be tied to the flexible generation of behavior by the worm. • We first observed that the principle of substitution can relate hierarchical organization with flexible behavior generation using C. elegans foraging behavior as a use case. Substitution in a behaving system that leads to flexible behavior could be realized via: - Degeneracy : Different motor signals can generate the same behavior - Re-usability : Similar motor signals can generate completely different behaviors based on the context in which they occur. • Treating worm behavior as a sequence of changes in its body posture and refraining from using any human defined labels for such postures, we show that worm foraging behavior (not just the stereotypical portions) is hierarchically organized. We use mutual replaceability to obtain chunks containing mutually substitutable worm postures, just like the chunk named adjective contains mutually substitutable words like "black" and "white". • Furthermore, we elucidate a grammar of worm roaming and dwelling states, outlining rules of interaction between such chunks containing substitutable postures. We find that the stereotypical worm roaming behavior is captured by a specific grammatical rule involving specific chunks in a particular order and that even such stereotypical behavior is characterized by variability at the lowest level of postures. Variability in worm roaming behavior comes about through substitution where postures in a chunk can be substituted with each other without changing the nature of the higher order behavior - roaming (degeneracy). • We also delineate grammatical rules that specify how the same chunks are used in multiple combinations to produce relatively less-stereotypical dwelling like behavior patterns. Thus substitution, in terms of re-use of the same chunks in different ways can generate two different worm behaviors - roaming and dwelling (re-usability). • Body morphology cannot account for the dynamics underlying worm roaming behavior. • Such a generative grammar for worm foraging demonstrates how flexible behavior emerges from a hierarchically organized behavioral scaffolding. • We then tied the grammar of worm foraging with ideas that are commonplace in computer science and linguistics. Specifically, we proposed that the worm foraging grammar could conform to a context free grammar (CFG in computer science and linguistics parlance) that has hierarchical structure built into it. And indeed, we defined a CFG that can capture the worm foraging behavior. It was also shown that a less expressive grammar - a regular grammar, cannot capture worm foraging behavior. • The organization principles captured by the proposed grammar can elucidate novel molecular mechanisms important for regulating worm foraging behavior. After validating the robustness of the proposed grammar by replicating previous findings that npr-1 and npr-9 mutants show increased and impaired roaming behavior respectively. We then showed that the proposed worm foraging grammar reveals hitherto uncharacterized role of npr-3 and npr-10 genes in affecting foraging behavior. • The proposed grammatical rules correctly predict worm behavior patterns in off food environment as well. We found that the proposed grammatical rules can recapitulate variations in worm behavior that are caused by changes in its environment. Specifically, the amount of time spent by N2 worms in roaming type grammatical rules is considerably higher than the time spent in dwelling type rules, in off food conditions, as reported in prior literature.