Collective behavior of C. elegans and C. briggsae starved L1 larvae

Working with starved L1 larvae of C. elegans and C. briggsae we noticed that these two species behave quite differently in starvation. First, C. elegans adults stop laying eggs after exhausting bacterial food, which eventually leads to internal hatching and bagging. C. briggsae do not show this behavior. This difference has been observed before (McCulloch and Gems, 2003). Second, at high enough density of worms, arrested C. elegans L1s aggregate on agar plates after several days of starvation (Fig. 1a). C. briggsae L1s do not form aggregates (Fig. 1b). Aggregation may serve several purposes ranging from decrease of surface to volume ratio and use of diffusible “public goods” to sharing information about quality of the environment. Third, survival of starved C. elegans L1s strongly depends on their density – the higher the worm density, the longer they survive (Fig. 1c) (Artyukhin et al., 2013). This holds true for starvation on plates as well as in suspension. Survival of C. briggsae L1s is independent of worm density (Fig. 1d). We believe that the aggregation and the density dependence are naturally connected as they seem to be correlated across Caenorhabditis species. Forth, starved C. elegans L1s release plenty of ascarosides (Fig. 1e,f). C. briggsae L1s release far less, both in variety (Fig. 1e) and in amounts (Fig. 1f). More than 100 ascarosides have been found in C. elegans (von Reuss et al., 2012), and although we do not know physiological functions for many of them, functions of the ones that we do know and the high degree of structural conservation in other nematodes suggest that ascarosides constitute a vital part of nematode chemical language. Hence, we interpret the data in Fig. 1e,f as suggesting that C. elegans L1s “talk” more with each other in starvation than C. briggsae. Finally, C. elegans is one of a couple Caenorhabditis species susceptible to environmental RNAi (Winston et al., 2007), which has been speculated to play a role in communication between organisms (perhaps, conspecifics) (Whangbo and Hunter, 2008).  Based on everything above, we speculate that in unfavorable conditions (starvation) C. elegans tend to become more social than C. briggsae. In variable and unpredictable environments genotypic fitness can be maximized either by reducing individual-level variance in fitness or by reducing between-individual correlations in fitness (or some combination of the two) (Starrfelt and Kokko, 2012). Aggregating or social species may choose to minimize individual-level variance by having a mechanism that helps them to adjust to unfavorable conditions, in part through collective behavior. Non-aggregating species may use dispersal as a strategy to minimize between-individual correlations. Based on this hypothesis we would predict that lack of aggregation and density dependence in C. briggsae implies that their starved L1s hardly ever find themselves at high density in nature and the optimal strategy for them is to disperse and actively look for food.

Figures

Fig1
Figure 1: C. elegans L1 worms show more signs of collective behavior than C. briggsae. (a) Starved C. elegans L1s aggregate at high worm density. One million N2 L1s prestarved for 3.5 days were pipetted on an unseeded NGM plate and the image was taken 15 h later. (b) Under identical conditions C. briggsae (AF16) L1s disperse and do not aggregate. (c) N2 L1s survive starvation longer at higher worm density. (d) Survival of C. briggsae (JU757) L1s does not depend on worm density during starvation. For (c) and (d) the numbers in legends correspond to worm density during starvation, worm/µl. Starvation experiments were performed at 25oC. (e) C. elegans L1s release more ascarosides than C. briggsae. LC-MS/MS chromatograms (parents of m/z 73) of methanol extracts from C. elegans and C. briggsae L1 conditioned media collected after 24h of starvation. For ascaroside names see http://www.smid-db.org (f) Quantification of ascaroside levels in C. elegans and C. briggsae L1 conditioned media based on LC-MS peak areas.

References

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Winston WM, Sutherlin M, Wright AJ, Feinberg EH, and Hunter CP. (2007). Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc. Natl. Acad. Sci. U. S. A. 104, 10565-10570. PubMed

von Reuss SH, Bose N, Srinivasan J, Yim JJ, Judkins JC, Sternberg PW, and Schroeder FC. (2012). Comparative metabolomics reveals biogenesis of ascarosides, a modular library of small-molecule signals in C. elegans. J. Am. Chem. Soc. 134, 1817-1824. PubMed

Published: March 23, 2014 in