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Evolution of fungal phenotypic disparity

Abstract

Organismal-grade multicellularity has been achieved only in animals, plants and fungi. All three kingdoms manifest phenotypically disparate body plans but their evolution has only been considered in detail for animals. Here we tested the general relevance of hypotheses on the evolutionary assembly of animal body plans by characterizing the evolution of fungal phenotypic variety (disparity). The distribution of living fungal form is defined by four distinct morphotypes: flagellated; zygomycetous; sac-bearing; and club-bearing. The discontinuity between morphotypes is a consequence of extinction, indicating that a complete record of fungal disparity would present a more homogeneous distribution of form. Fungal disparity expands episodically through time, punctuated by a sharp increase associated with the emergence of multicellular body plans. Simulations show these temporal trends to be non-random and at least partially shaped by hierarchical contingency. These trends are decoupled from changes in gene number, genome size and taxonomic diversity. Only differences in organismal complexity, characterized as the number of traits that constitute an organism, exhibit a meaningful relationship with fungal disparity. Both animals and fungi exhibit episodic increases in disparity through time, resulting in distributions of form made discontinuous by extinction. These congruences suggest a common mode of multicellular body plan evolution.

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Fig. 1: The evolutionary interrelationships of the nine major fungal lineages.
Fig. 2: The distribution of fungi in morphospace.
Fig. 3: The relationship between phenotypic disparity and organismal complexity in fungi.
Fig. 4: How phenotypic disparity relates to taxonomic diversity, genome size and gene number in fungi.
Fig. 5: Changes in the size of the area of morphospace occupied by fungi through time.
Fig. 6: Changes in the density with which fungi occupy morphospace through time.

Data availability

All original data (empirical and simulated) used in this study have been deposited at Dryad63 and are publicly available at https://doi.org/10.5061/dryad.wwpzgmsm9.

Code availability

All code used in this study has been deposited at Dryad63 and is publicly available at https://doi.org/10.5061/dryad.wwpzgmsm9.

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Acknowledgements

We thank G. Storey, A. Larkin, D. Rainey, R. Wheeler and all the other Twitter users who kindly provided photographs of fungi for consideration for inclusion in this paper. We also thank P. Godoy for his thoughtful comments during the review process; the manuscript was much improved for his input. T.J.S. was funded by a Natural Environment Research Council (NERC) PhD Studentship within the GW4+ Doctoral Training Programme. P.C.J.D. was funded by the NERC (no. NE/P013678/1; part of the Biosphere Evolution, Transitions and Resilience programme, cofunded by the Natural Science Foundation of China), the Biotechnology and Biological Sciences Research Council (nos. BB/T012773/1 and BB/N000919/1), the Gordon and Betty Moore Foundation (no. GBMF9741), the John Templeton Foundation (grant no. 62220; the opinions expressed in this publication are those of the authors and do not necessarily reflect the views of the John Templeton Foundation) and the Leverhulme Trust (no. RF-2022–167).

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Both authors contributed to the conceptualization and design of the study, its component experiments and the interpretation of the results. T.J.S. collected the data, conducted the analyses and drafted the manuscript, to which P.C.J.D. contributed.

Corresponding authors

Correspondence to Thomas J. Smith or Philip C. J. Donoghue.

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Nature Ecology & Evolution thanks P. Godoy 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 Mean distance from centroid of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 2 Sum of variances of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 3 Average nearest neighbour Euclidean distance of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 4 Subcellular mean distance from centroid of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 5 Subcellular sum of variances of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 6 Supracellular mean distance from centroid of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 7 Supracellular sum of variances of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Extended Data Fig. 8 Supracellular average nearest neighbour Euclidean distance of 1000 bootstraps of the four morphotypes, Dikarya, and non-dikaryotic fungi.

Box plot whiskers extend to minima and maxima of data; boxes capture interquartile range and median.

Supplementary information

Supplementary Information

Supplementary Figs. 1–6 and references.

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Peer Review File

Supplementary Data 1

Discrete character dataset characterizing fungal phenotypic variety.

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Smith, T.J., Donoghue, P.C.J. Evolution of fungal phenotypic disparity. Nat Ecol Evol 6, 1489–1500 (2022). https://doi.org/10.1038/s41559-022-01844-6

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