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.
Similar content being viewed by others
Notes
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.
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.
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.
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.
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.
References
Bateson P (2004) The active role of behavior in evolution. Biol Philos 19:283–298
Buss L (1987) The evolution of individuality. Princeton University Press, Princeton
Clarke E (2010) The problem of biological individuality. Biol Theory 5:312–325
Dawkins R (1989) The extended phenotype. Oxford University Press, Oxford
Godfrey-Smith P (2009) Darwinian populations and natural selection. Oxford University Press, New York
Griesemer JR (2000a) Development, culture and the units of inheritance. Philos Sci 67:S348–S368
Griesemer JR (2000b) The units of evolutionary transition. Selection 1:67–80
Hamilton WD (1964) The genetical evolution of social behaviour, I, II. J Theor Biol 7:1–52
Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioral, and symbolic variation in the history of life. MIT Press, Cambridge
Jeanson R, Kukuk PF, Fewell JH (2005) Emergence of division of labour in halictine bees: contributions of social interactions and behavioural variance. Anim Behav 70:1183–1193
King N (2004) The unicellular ancestry of animal development. Dev Cell 7:313–325
Kirk D (1998) Volvox: molecular-genetic origins of multicellularity and cellular differentiation. Cambridge University Press, Cambridge
Lewontin RC (1970) The units of selection. Annu Rev Ecol Syst 1:1–17
Maynard Smith J, Szathmáry E (1995) The major transitions in evolution. Oxford University Press, Oxford
Michod R (1999) Darwinian dynamics: evolutionary transitions in fitness and individuality. Princeton University Press, Princeton
Nadarajah B, Brunstrom J, Grutzendler J, Wong R, Pearlman A (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143–150
Newman SA, Müller GB (2010) Morphological evolution: epigenetic mechanisms. In: Encyclopedia of life sciences. Wiley, Chichester. http://www.els.net/. Accessed 10 April 2012
Okasha S (2005) Multilevel selection and the major transitions in evolution. Philos Sci 72:1013–1025
Okasha S (2006) Evolution and the levels of selection. Oxford University Press, Oxford
Parker A (2003) In the blink of an eye. Perseus, Cambridge
Ratcliff WC, Denison RF, Borrello M, Travisano M (2012) Experimental evolution of multicellularity. Proc Natl Acad Sci USA 109:1595–1600
Ricci N (1990) The behaviour of ciliated Protozoa. Anim Behav 40:1048–1069
Sakagami SF, Maeta Y (1987) Sociality, induced and/or natural, in the basically solitary small carpenter bees (Ceratina). In: Itô Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Scientific Societies Press, Tokyo, pp 1–16
Schwab I (2012) Evolution’s witness. Oxford University Press, New York
Trestman M (2012a) The environment, from a behavioral perspective. Topics in contemporary philosophy: the environment. MIT Press, Cambridge, pp 57–73
Trestman M (2012b) Implicit and explicit goal-directedness. Erkenntnis 77:207–236
Wcislo WT (1997) Social interactions and behavioral context in a largely solitary bee, Lasioglossum (Dialictus) figueresi (Hymenoptera, Halictidae). Insectes Soc 44:199–208
Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. Bioscience 58:17–25
Acknowledgments
Many thanks to Jim Griesemer, Bert Baumgaertner, Jared Poon, and two anonymous referees for their help in refining this paper.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13752-012-0072-0