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On the origin of biological construction, with a focus on multicellularity

  1. Corina E. Tarnitae,1
  1. aDepartment of Evolutionary Biology and Environmental Studies, University of Zürich, 8057 Zürich, Switzerland;
  2. bSwiss Institute of Bioinformatics, 1015 Lausanne, Switzerland;
  3. cDepartment of Environmental Systems Science, ETH Zürich, 8092 Zürich, Switzerland;
  4. dDepartment of Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (EAWAG), 8600 Dübendorf, Switzerland;
  5. eDepartment of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544
  1. Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved September 1, 2017 (received for review April 9, 2017)

Abstract

Biology is marked by a hierarchical organization: all life consists of cells; in some cases, these cells assemble into groups, such as endosymbionts or multicellular organisms; in turn, multicellular organisms sometimes assemble into yet other groups, such as primate societies or ant colonies. The construction of new organizational layers results from hierarchical evolutionary transitions, in which biological units (e.g., cells) form groups that evolve into new units of biological organization (e.g., multicellular organisms). Despite considerable advances, there is no bottom-up, dynamical account of how, starting from the solitary ancestor, the first groups originate and subsequently evolve the organizing principles that qualify them as new units. Guided by six central questions, we propose an integrative bottom-up approach for studying the dynamics underlying hierarchical evolutionary transitions, which builds on and synthesizes existing knowledge. This approach highlights the crucial role of the ecology and development of the solitary ancestor in the emergence and subsequent evolution of groups, and it stresses the paramount importance of the life cycle: only by evaluating groups in the context of their life cycle can we unravel the evolutionary trajectory of hierarchical transitions. These insights also provide a starting point for understanding the types of subsequent organizational complexity. The central research questions outlined here naturally link existing research programs on biological construction (e.g., on cooperation, multilevel selection, self-organization, and development) and thereby help integrate knowledge stemming from diverse fields of biology.

Footnotes

  • ?1To whom correspondence should be addressed. Email: ctarnita{at}princeton.edu.

Online Impact

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