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Which Comes First in Major Transitions: The Behavioral Chicken, or the Evolutionary Egg?

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Abstract

This paper takes a close look at the role of behavior in the “major transitions” in evolution—events during which inheritance and development, and therefore the process of adaptation by natural selection, are reorganized at a new level of compositional hierarchy—and at the requirements for sufficiently explaining these important events in the history of life. I argue that behavior played a crucial role in driving at least some of the major transitions. Because behavioral interactions can become stably organized in novel ways on timescales faster than the lifetime of an organism, behavior can lead the way into a transition—becoming organized at the new level prior to inheritance and development. It is widely acknowledged that behavioral plasticity can play an important role in evolution; environmental novelty can elicit novel behavior that may feed back on the evolutionary process through niche selection or cultural inheritance, for example (Jablonka and Lamb 2005). I argue here that not just novel behaviors but novel forms of behavioral organization (distributed or hierarchical control that produces functional coherence) can emerge, binding the evolutionary fates of a group of organisms which were previously independent in terms of behavior as well as reproduction, and leading the way into a transition to an aggregative or “higher-level” mode of reproduction.

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Notes

  1. Behavior is not unique in this regard. Newman and Müller (2010) discuss the importance of the action of physical forces, such as adhesion and diffusion, for the creation of pattern and form early in metazoan history. These epigenetic mechanisms played a role in the transition to multicellularity, by generating novel structure at the multicellular level that had not been subject to natural selection, similar to the role of behavior that I describe here.

  2. See Dawkins (1989, Chap. 14) for a discussion of the importance of behavioral unity in defining individual animals; see Trestman (2012a, b) for discussion of these notions of behavior and behavioral organization.

  3. Metazoa are thought to be monophyletic (reviewed in King 2004), so this was a singular transition to multicellularity, although other multicellular organisms such as “true” plants, algaes, kelps, and fungi have made this transition independently.

  4. The basic difference is that in group selection (multilevel selection 1), fitness benefits are conferred on level n individuals in virtue of their membership in a group. The level n individuals are still autonomous reproducers. In aggregate-level individual selection (multilevel selection 2), the level n individuals are no longer reproductively autonomous; their lineage is only propagated into the future on evolutionary timescales by reproduction of aggregates, i.e., level n + 1 individuals. Level n “fitness” has been replaced by the fitness of level n + 1 individuals, i.e., aggregates of level n individuals.

  5. Contrast the scenario described here with the experimental setup of Ratcliff et al. (2012), who induced multicellular aggregation in yeast by selecting for cells that sank to the bottom of the medium rapidly. Aggregated cells sank more quickly, and so were selected preferentially; simple among-cell division of labor evolved quickly in the presence of selection for mere aggregation. However, in this case no emergent behavioral organization was needed—only the passive property of sinking through the medium.

  6. Even if this hypothesis is incorrect, my point—that the possibility of this kind of explanation depends on conceiving of units of behavior in a way that does depend logically on their having been subject to natural selection—stands.

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Acknowledgments

Many thanks to Jim Griesemer, Bert Baumgaertner, Jared Poon, and two anonymous referees for their help in refining this paper.

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Correspondence to Michael Trestman.

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Trestman, M. Which Comes First in Major Transitions: The Behavioral Chicken, or the Evolutionary Egg?. Biol Theory 7, 48–55 (2013). https://doi.org/10.1007/s13752-012-0072-0

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