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.

Keywords: animal sociality; bottom-up approach; hierarchical evolutionary transitions; life cycle; major evolutionary transitions.

Fig. 1.

Potential multicellular life cycles that could emerge upon the formation of the first multicellular groups. Categorization based on (i) existence of single cell (S), (ii) mechanism of group formation (CT/ST), and (iii) life stage where cell division occurs. Two life cycles have a group life stage formed by both CT and ST; here, aggregated cells divide inside the group. Arrows indicate cell division in solitary life stage, transition between solitary and group life stages, and potential fragmentation of the group (dotted line). Images show examples of species with a life cycle comparable to each life cycle motif. (Top to Bottom) D. discoideum, image courtesy of MJ Grimson and RL Blanton (17, 90), C. owczarzaki, image adapted from ref. , B. subtilis (107, 108), Botryllus schlosseri, reprinted from ref. with permission from Elsevier, Streptomyces coelicolor, image courtesy of VM Zacharia and MF Traxler (52, 107), Schmidtea mediterranea asexual biotype CIW4, image adapted from ref. .

Fig. 2.

Relationship between life stages in hypothesized life cycles of solitary ancestors and group formation in derived group life cycles. (Upper) Simplified depiction of hypothesized ancestral solitary life cycles of V. carteri (33, 88, 89), D. discoideum (90), and Polistes metricus (–105). Life cycles here consist of a life stage expressed under good conditions (black) and a life stage expressed under adverse conditions (green). For the latter life stage, we show an environmental signal that might trigger it and some phenotypic consequences. For P. metricus, high food provisioning at the end of the breeding season is hypothesized to be a cue for the upcoming winter season. (Lower) Simplified depiction of group life cycles of: V. carteri, corresponding to fifth life cycle in Fig. 1 (ST group and nondividing unicellular life stage; zygote, not shown); D. discoideum, corresponding to first life cycle in Fig. 1 (CT group and dividing unicellular life stage); and P. metricus, corresponding to seventh life cycle in SI Appendix, Fig. S3 (ST group and nonreproducing solitary life stage). Developmental program underlying life stages in solitary ancestor is co-opted for group formation (shown in green): differentiation of somatic cells (V. carteri), fruiting body formation (D. discoideum), and appearance of foundress phenotype (P. metricus).