Nascent life cycles and the emergence of higher-level individuality

Abstract

Evolutionary transitions in individuality (ETIs) occur when formerly autonomous organisms evolve to become parts of a new, 'higher-level' organism. One of the first major hurdles that must be overcome during an ETI is the emergence of Darwinian evolvability in the higher-level entity (e.g. a multicellular group), and the loss of Darwinian autonomy in the lower-level units (e.g. individual cells). Here, we examine how simple higher-level life cycles are a key innovation during an ETI, allowing this transfer of fitness to occur 'for free'. Specifically, we show how novel life cycles can arise and lead to the origin of higher-level individuals by (i) mitigating conflicts between levels of selection, (ii) engendering the expression of heritable higher-level traits and (iii) allowing selection to efficiently act on these emergent higher-level traits. Further, we compute how canonical early life cycles vary in their ability to fix beneficial mutations via mathematical modelling. Life cycles that lack a persistent lower-level stage and develop clonally are far more likely to fix 'ratcheting' mutations that limit evolutionary reversion to the pre-ETI state. By stabilizing the fragile first steps of an evolutionary transition in individuality, nascent higher-level life cycles may play a crucial role in the origin of complex life.This article is part of the themed issue 'Process and pattern in innovations from cells to societies'.

Keywords: complexity; cooperation; division of labour; innovation; major transitions.

Figure 1.

Nascent microbial multicellular life cycles in extant microorganisms.

Figure 2.

Schematics of canonical early microbial multicellular life cycles. We depict three multicellular life cycles in which groups of cells replicate. The top two life cycles alternate between unicellular and multicellular stages. The primary difference between them is how they form groups. In the aggregative group life cycle, cells form groups through random binding similar to flocculating yeast. The groups eventually dissociate, releasing cells so as to return to the unicellular phase. In the clonal development alternating life cycle, groups are formed from single cells, similar to the formation of wrinkly mats by smooth cells in the Pseudomonas fluorescens experimental system [29]. Groups release single cells, usually through a phenotypic switch, indicated by the box- and circle-shaped cells. Finally, there is the strictly multicellular life cycle in which there is no unicellular phase. Cells reproduce within groups and groups eventually split into smaller groups, similar to snowflake yeast [36]. (Online version in colour.)

Figure 3.

Filament reproduction. Filaments reproduce through binary fission. The mutant (shaded red) increases in relative frequency within the filament when s_c > 0 and decreases when s_c < 0. In either case, because the mutant increases in absolute numbers, this can lead to offspring filaments with high proportions of mutants. (Online version in colour.)

Figure 4.

Spreading dynamics of mutations beneficial to both cells and groups in different life cycles. The plots show the proportion of the mutation in a population as a function of the number of rounds through different life cycles for different values of s_c > 0 and s_g > 0. The aggregative life cycles are shown in the red area (spanning N = 5 to N = 100), the alternating clonal life cycle is in black and the strictly multicellular life cycles are in the blue area (spanning k = 2 to k = 50). In all cases, the mutation spreads fastest in the alternating clonal life cycle. When s_g ≤ s_c, the mutation spreads faster in the aggregative life cycle than the strictly multicellular life cycle.

Figure 5.

Spreading dynamics of mutations beneficial for groups but deleterious for cells in different life cycles. The plots show the proportion of the mutation in a population as a function of the number of rounds through different life cycles for different values of s_c < 0 and s_g > 0. The colouring is the same as in figure 4. In all cases, the mutation spreads fastest in the strictly multicellular life cycle. It does not spread in the aggregative life cycle and only spreads in the alternating clonal life cycle when s_g > −s_c. (Online version in colour.)