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

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.

Interacting cells driving the evolution of multicellular life cycles

“…The role of these interactions in the emergence (or prevention) of multicellularity is an open question. Recently, there is a rising interest in the evolution of life cycles including multicellular stages from both experimentalists [Rossetti et al, 2011, Ratcliff et al, 2012, 2013b,a, Hammerschmidt et al, 2014] and theoreticians [Rainey and Kerr, 2010, Tarnita et al, 2013, Libby et al, 2014, De Monte and Rainey, 2014, Rashidi et al, 2015, van Gestel and Tarnita, 2017, Pichugin et al, 2017]. In the present study, we focus on competition between various multicellular and unicellular life cycles.…”

Universal scaling across biochemical networks on Earth

“…For example, while individual organismal lineages fluctuate through time and space, the functional and metabolic composition of ecological communities is dynamically stable 23,24 . To understand the general principles governing biology, we must understand how living systems organize across levels, not just within a given level 25,26 .…”

Evolution of multicellularity by collective integration of spatial information

“…The importance of a bottom-up approach to study the evolution of multicellularity has been repeatedly emphasised [48, 49], and a broader understanding of cells self-organisation and evolution may have applications to clinically relevant multiscale evolutionary problems, such as the evolution of collective metastatic migration of cancer cells [50–53]. Our work highlights that the properties of single cells emergently give rise to novel properties of cell clusters.…”