Behavioral diversity in microbes and low-dimensional phenotypic spaces

David Jordan, Seppe Kuehn, Eleni Katifori, and Stanislas Leibler
PNAS August 20, 2013 110 (34) 14018-14023; https://doi.org/10.1073/pnas.1308282110

  1. Edited* by Michael E. Fisher, University of Maryland, College Park, MD, and approved July 1, 2013 (received for review May 2, 2013)

Abstract

Systematic studies of phenotypic diversity—required for understanding evolution—lag behind investigations of genetic diversity. Here we develop a quantitative approach to studying behavioral diversity, which we apply to swimming of the ciliate Tetrahymena. We measure the full-lifetime behavior of hundreds of individual organisms at high temporal resolution, over several generations and in diverse nutrient conditions. To characterize population diversity and temporal variability we introduce a unique statistical framework grounded in the notion of a phenotypic space of behaviors. We show that this space is effectively low dimensional with dimensions that correlate with a two-state “roaming and dwelling” model of swimming behavior. Temporal variability over the lifetime of an individual is correlated with the fraction of time spent roaming whereas diversity between individuals is correlated with the speed of roaming. Quantifying the dynamics of behavioral variation shows that behavior over the lifetime of an individual is strongly nonstationary. Analysis of behavioral dynamics between generations reveals complex patterns of behavioral heritability that point to the importance of considering correlations beyond mothers and daughters. Our description of a low-dimensional behavioral space should enable the systematic study of the evolutionary and ecological bases of phenotypic constraints. Future experimental and theoretical studies of behavioral diversity will have to account for the possibility of nonstationary and environmentally dependent behavioral dynamics that we observe.

Footnotes

  • ↵1D.J. and S.K. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. E-mail: skuehn{at}rockefeller.edu.

  • Author contributions: D.J., S.K., and S.L. designed research; D.J. performed research; D.J., S.K., and E.K. analyzed data; and D.J., S.K., and S.L. wrote the paper.

  • The authors declare no conflict of interest.

  • ↵*This Direct Submission article had a prearranged editor.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1308282110/-/DCSupplemental.

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Behavioral diversity and phenotypic spaces
David Jordan, Seppe Kuehn, Eleni Katifori, Stanislas Leibler
Proceedings of the National Academy of Sciences Aug 2013, 110 (34) 14018-14023; DOI: 10.1073/pnas.1308282110
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