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Direct benefits are not necessary for the evolution of multicellularity


Abstract

The evolution of multicellularity required nascent multicellular life to persist in a unicellular world. Because grouping usually comes with steep costs, multicellularity had to confer some benefits. While direct benefits—in which cells in groups outperform single cells under the same conditions—can clearly suffice for multicellularity to evolve, whether they were also necessary has not been systematically explored. Here we develop a general model for the evolution of multicellularity in a spatially heterogeneous environment and show that direct benefits are, in fact, not necessary. When nascent multicellular groups differ from their unicellular ancestor in their spatial distribution (for example, because groups sink), two distinct indirect benefits can emerge: escape from competition from the unicellular ancestor and increased exploitation of desirable environments. Either benefit can drive the evolution of multicellularity in the absence of direct benefits. As a case study, we show that in the Proterozoic Ocean, where several multicellular eukaryotic lineages originated, escape from competition could have driven the evolution of multicellularity by offsetting the costs of diffusion limitation and oxygen deprivation. Our work systematically uncovers hitherto underappreciated mechanisms by which multicellularity can evolve, even under seemingly adverse conditions, and highlights the importance of ecology in explaining major evolutionary transitions.

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Fig. 1: Model overview.
The alternative text for this image may have been generated using AI.
Fig. 2: Spatial heterogeneity can drive the evolution of multicellularity through indirect benefits.
The alternative text for this image may have been generated using AI.
Fig. 3: Multicellularity can evolve via escaping competition, environmental exploitation or both.
The alternative text for this image may have been generated using AI.
Fig. 4: Diverse evolutionary outcomes in a model of indirectly beneficial multicellularity in the Proterozoic Ocean.
The alternative text for this image may have been generated using AI.
Fig. 5: Evolutionary outcomes are shaped by oxygen availability.
The alternative text for this image may have been generated using AI.

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Data availability

The study is theoretical; no new empirical data were generated. All simulated data are available via Zenodo at https://doi.org/10.5281/zenodo.18749114 (ref. 98).

Code availability

All scripts needed to replicate the results presented here are available via Zenodo at https://doi.org/10.5281/zenodo.18749114 (ref. 98).

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Acknowledgements

We thank J. Levine, members of the Tarnita lab, and Princeton’s Theory Tea community for helpful feedback. C.E.T. gratefully acknowledges support from a Guggenheim Fellowship.

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Authors and Affiliations

Authors

Contributions

All authors contributed equally to conceptual development, model design and paper writeup. D.J. and M.S. performed the simulations, analysed the results and conducted the mathematical analysis.

Corresponding author

Correspondence to
Corina E. Tarnita.

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The authors declare no competing interests.

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Nature Ecology & Evolution thanks Daniel Mills, Vidyanand Nanjundiah and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Ecological outcomes of 2+1 invasion: coexistence or exclusion.

Possible outcomes of the invasion of 2+1 in the fast migration limit, depending on the spatial distribution of solitary cells (qA = p1,A) and 2-cell groups (p2,A). The space is colored based on the presence of indirect benefits: escaping competition (blue), environmental exploitation (orange), or both (purple). In (a), the white hatched region indicates where indirect benefits are strong enough to facilitate the invasion of multicellularity (R2 > C2). In (b), the white hatched region indicates where the multicellular mutant eventually displaces the unicellular ancestor. In each panel of (a) and (b), a different reduction in growth rates for cells in groups, relative to single cells, is assumed: (i) r2 = 0.8r1, (ii) r2 = 0.94r1, and (iii) r2 = 0.98r1. We set r1,A = 15 and r1,B = 5.

Extended Data Fig. 2 Robustness analysis across life cycles: results for N + 1, N × 1 and N/2 + N/2 life cycles.

Evolutionarily stable communities (ESCs) for the different life cycle types: (a) N + 1, (b) N × 1, (c) N/2 + N/2. Colored regions indicate the different types of ESCs. For each life cycle type, we present: (i) ESC outcomes as a function of NU and NL (as in Fig. 5, when NUNS, the value of NU becomes irrelevant as all cells in the upper layer have access to oxygen); (ii) Maximum attained group sizes as a function of oxygen concentration, under the assumption that NU = 2NL; (iii) The full life cycle community present at each NU = 2NL (each black square indicates the presence of the corresponding life cycle in the ESC). In (ii) and (iii), the colors in the background indicate the ESC reached for the given NL. For the N × 1 and N/2 + N/2 life cycles, the dominance ESC region is characterized by either a single dominant sinking life cycle or two adjacent sinking life cycles (two life cycles whose fragmentation sizes N and M differ by one cell, that is, NM=1). Across different life cycles, the results remain qualitatively consistent. The only exception is a new ESC (purple) that appears for NL = 0 in the N/2 + N/2 life cycle, where all non-sinking life cycles that do not experience oxygen limitation coexist with all life cycles that never inhabit the lower layer (that is, N + N with NNS). Simulations used ro = 6.8, rf = 1, and γ = 1. Life cycles N + 1 and N/2 + N/2 used NS = 20 while N × 1 used NS = 10. See Section S3.6 of the Supplementary Information for a brief discussion of these results.

Extended Data Fig. 3 Robustness analysis across fermentation growth rates: N + 1 results for low rf.

Evolutionarily stable communities (ESCs) for different fermentation growth rates: (a) rf=0.01, (b) rf=2, (c) rf=3. Colored regions indicate the different types of ESCs. For each fermentation rate, we present: (i) ESC outcomes as a function of NU and NL (as in Fig. 5, when NU ≥ NS, the value of NU becomes irrelevant as all cells in the upper layer have access to oxygen); (ii) Maximum attained group sizes as a function of oxygen concentration, under the assumption that NU = 2NL; (iii) The full life cycle community present at each NU = 2NL (each black square indicates the presence of the corresponding life cycle in the ESC). In (ii) and (iii), the colors in the background indicate the ESC reached for the given NL. Simulations used ro=6.8, NS=20, and γ =1. Across low fermentation growth rates (0.01≤ rf≤ 3), the results for N+1 remain qualitatively consistent relative to Fig. 5 (rf=1). See Section S3.6 of the Supplementary Information for a brief discussion of these results.

Extended Data Fig. 4 Robustness analysis across fermentation growth rates: N + 1 results for high rf.

Evolutionarily stable communities (ESCs) for different fermentation growth rates: (a) rf = 4, (b) rf = 5, (c) rf = 6. Colored regions indicate the different types of ESCs. For each fermentation rate, we present: (i) ESC outcomes as a function of NU and NL (as in Fig. 5, when NUNS, the value of NU becomes irrelevant as all cells in the upper layer have access to oxygen); (ii) Maximum attained group sizes as a function of oxygen concentration, under the assumption that NU = 2NL; (iii) The full life cycle community present at each NU = 2NL (each black square indicates the presence of the corresponding life cycle in the ESC). In (ii) and (iii), the colors in the background indicate the ESC reached for the given NL. Simulations used ro = 6.8, NS = 20, and γ =1. Across high fermentation growth rates (4≤rf≤6), the results for N + 1 remain qualitatively consistent, except when rf becomes too high. For rf = 5 (b) and rf = 6 (c), we find a new evolutionary outcome (purple): non-sinking life cycles are displaced, and all sinking life cycles that grow past a threshold coexist neutrally (iii). In Section S4 of the Supplementary Information, we analytically show that the ESC regimes described in the main text, together with the additional regime highlighted above (purple), are the only possible ESCs for the N + 1 life cycle. See Section S3.6 of the Supplementary Information for a brief discussion of these results.

Extended Data Fig. 5 Robustness analysis across different degrees of mixing.

(a) ESC outcomes when there is some mixing and a proportion qL of single cells and groups below size NS inhabit the lower layer (see Section S3.6 of the Supplementary Information for a brief discussion of these results). In part of the gray region, evolving non-trivial multicellularity is impossible altogether; in the other part, it can only evolve for very high fragmentation sizes, not captured in our simulations. Thus, for the N + 1 life cycle, we calculate the smallest fragmentation size able to invade the unicellular ancestor as a function of NU and NL, and across different mixing (qL) values (b). To determine if multicellularity can invade, we first numerically evaluate Result S2.3 (see Section S2 of the Supplementary Information) for all N + 1 life cycles up to fragmentation size 121. If none of these life cycles can invade but ρ(N) is increasing with N for N > NS (and, therefore, ({T}_{B}^{* } > {r}_{f}/gamma)), we know that eventually a very large life cycle (N + 1 with N > 120; darkest orange in the figure) will invade (see Section S4.5 of the Supplementary Information).

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Jorge, D., Staps, M., Pichugin, Y. et al. Direct benefits are not necessary for the evolution of multicellularity.
Nat Ecol Evol (2026). https://doi.org/10.1038/s41559-026-03044-y

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