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Evolution of fungal phenotypic disparity

Nature Ecology & Evolution volume 6, pages 1489–1500 (2022)Cite this article

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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.

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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.

References

  1. Niklas, K. J. & Newman, S. A. The many roads to and from multicellularity. J. Exp. Bot. 71, 3247–3253 (2020).

    Article  CAS  PubMed  Google Scholar 

  2. Maynard Smith, J. & Szathmary, E. The Major Transitions in Evolution (W. H. Freeman Spektrum, 1995).

  3. Grosberg, R. K. & Strathmann, R. R. The evolution of multicellularity: a minor major transition?. Annu. Rev. Ecol. Evol. Syst. 38, 621–654 (2007).

    Article  Google Scholar 

  4. Erwin, D. H. Disparity: morphological pattern and developmental context. Palaeontology 50, 57–73 (2007).

    Article  Google Scholar 

  5. Foote, M. The evolution of morphological diversity. Annu. Rev. Ecol. Syst. 28, 129–152 (1997).

    Article  Google Scholar 

  6. Deline, B. et al. Evolution of metazoan morphological disparity. Proc. Natl Acad. Sci. USA 115, E8909–E8918 (2018).

  7. Hughes, M., Gerber, S. & Wills, M. A. Clades reach highest morphological disparity early in their evolution. Proc. Natl Acad. Sci. USA 110, 13875–13879 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kües, U., Khonsuntia, W. & Subba, S. Complex fungi. Fungal Biol. Rev. 32, 205–218 (2018).

    Article  Google Scholar 

  9. Blackwell, M. The fungi: 1, 2, 3 … 5.1 million species? Am. J. Bot. 98, 426–438 (2011).

    Article  PubMed  Google Scholar 

  10. Li, Y. et al. A genome-scale phylogeny of the kingdom Fungi. Curr. Biol. 31, 1653–1665.e5 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Chang, Y. et al. Genome-scale phylogenetic analyses confirm Olpidium as the closest living zoosporic fungus to the non-flagellated, terrestrial fungi. Sci. Rep. 11, 3217 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. James, T. Y., Stajich, J. E., Hittinger, C. T. & Rokas, A. Toward a fully resolved fungal tree of life. Annu. Rev. Microbiol. 74, 291–313 (2020).

    Article  CAS  PubMed  Google Scholar 

  13. Naranjo-Ortiz, M. A. & Gabaldón, T. Fungal evolution: diversity, taxonomy and phylogeny of the Fungi. Biol. Rev. Camb. Philos. Soc. 94, 2101–2137 (2019).

    Article  PubMed  Google Scholar 

  14. Celio, G. J., Padamsee, M., Dentinger, B. T. M., Bauer, R. & McLaughlin, D. J. Assembling the Fungal Tree of Life: constructing the structural and biochemical database. Mycologia 98, 850–859 (2006).

    Article  CAS  PubMed  Google Scholar 

  15. Gerber, S. Use and misuse of discrete character data for morphospace and disparity analyses. Palaeontology 62, 305–319 (2019).

    Article  Google Scholar 

  16. Smith, T. J., Puttick, M. N., O’Reilly, J. E., Pisani, D. & Donoghue, P. C. J. Phylogenetic sampling affects evolutionary patterns of morphological disparity. Palaeontology 64, 765–787 (2021).

    Article  Google Scholar 

  17. Adl, S. M. et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 66, 4–119 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Berbee, M. L. et al. Genomic and fossil windows into the secret lives of the most ancient fungi. Nat. Rev. Microbiol. 18, 717–730 (2020).

    Article  CAS  PubMed  Google Scholar 

  19. Taylor, T. N., Krings, M. & Taylor, E. Fossil Fungi (Elsevier, 2015).

  20. McShea, D. W. & Brandon, R. N. Biology’s First Law: the Tendency for Diversity and Complexity to Increase in Evolutionary Systems (Univ. of Chicago Press, 2010).

  21. McShea, D. W. Metazoan complexity and evolution: is there a trend? Evolution 50, 477–492 (1996).

    PubMed  Google Scholar 

  22. Ispolatov, I., Alekseeva, E. & Doebeli, M. Competition-driven evolution of organismal complexity. PLoS Comput. Biol. 15, e1007388 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hobern, D. et al. Towards a global list of accepted species VI: The Catalogue of Life checklist. Org. Divers. Evol. 21, 677–690 (2021).

    Article  Google Scholar 

  24. Bauer, R. et al. Entorrhizomycota: a new fungal phylum reveals new perspectives on the evolution of Fungi. PLoS ONE 10, e0128183 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Jones, M. D. M. et al. Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474, 200–203 (2011).

    Article  CAS  PubMed  Google Scholar 

  26. Yoshida, M., Nakayama, T. & Inouye, I. Nuclearia thermophila sp. nov. (Nucleariidae), a new nucleariid species isolated from Yunoko Lake in Nikko (Japan). Eur. J. Protistol. 45, 147–155 (2009).

    Article  PubMed  Google Scholar 

  27. Hibbett, D. S. et al. A higher-level phylogenetic classification of the Fungi. Mycol. Res. 111, 509–547 (2007).

    Article  PubMed  Google Scholar 

  28. Grigoriev, I. V. et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 42, D699–D704 (2014).

    Article  CAS  PubMed  Google Scholar 

  29. Guillerme, T. & Cooper, N. Time for a rethink: time sub-sampling methods in disparity-through-time analyses. Palaeontology 61, 481–493 (2018).

    Article  Google Scholar 

  30. Nagy, L. G., Kovács, G. M. & Krizsán, K. Complex multicellularity in fungi: evolutionary convergence, single origin, or both? Biol. Rev. Camb. Philos. Soc. 93, 1778–1794 (2018).

    Article  PubMed  Google Scholar 

  31. Whittaker, R. H. New concepts of kingdoms of organisms: evolutionary relations are better represented by new classifications than by the traditional two kingdoms. Science 163, 150–160 (1969).

    Article  CAS  PubMed  Google Scholar 

  32. Naranjo-Ortiz, M. A. & Gabaldón, T. Fungal evolution: cellular, genomic and metabolic complexity. Biol. Rev. Camb. Philos. Soc. 95, 1198–1232 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Nguyen, T. A. et al. Innovation and constraint leading to complex multicellularity in the Ascomycota. Nat. Commun. 8, 14444 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Briggs, D. E., Fortey, R. A. & Wills, M. A. Morphological disparity in the Cambrian. Science 256, 1670–1673 (1992).

    Article  CAS  PubMed  Google Scholar 

  35. Gould, S. J. Wonderful Life: the Burgess Shale and the Nature of History (Hutchinson Radius, 1990).

  36. Wan, J. et al. Decoupling of morphological disparity and taxonomic diversity during the end-Permian mass extinction. Paleobiology 47, 402–417 (2021).

    Article  Google Scholar 

  37. Grossnickle, D. M. & Newham, E. Therian mammals experience an ecomorphological radiation during the Late Cretaceous and selective extinction at the K-Pg boundary. Proc. Biol. Sci. 283, 20160256 (2016).

    PubMed Central  Google Scholar 

  38. Ruta, M., Angielczyk, K. D., Fröbisch, J. & Benton, M. J. Decoupling of morphological disparity and taxic diversity during the adaptive radiation of anomodont therapsids. Proc. Biol. Sci. 280, 20131071 (2013).

    PubMed  PubMed Central  Google Scholar 

  39. Bapst, D. W., Bullock, P. C., Melchin, M. J., Sheets, H. D. & Mitchell, C. E. Graptoloid diversity and disparity became decoupled during the Ordovician mass extinction. Proc. Natl Acad. Sci. USA 109, 3428–3433 (2012).

  40. Guillerme, T. et al. Disparities in the analysis of morphological disparity. Biol. Lett. 16, 20200199 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Guillerme, T., Puttick, M. N., Marcy, A. E. & Weisbacker, V. Shifting spaces: which disparity or dissimilarity measurement best summarize occupancy in multidimensional spaces? Ecol. Evol. 10, 7261–7275 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  42. Svardal, H., Rueffler, C. & Doebeli, M. Organismal complexity and the potential for evolutionary diversification. Evolution 68, 3248–3259 (2014).

    Article  PubMed  Google Scholar 

  43. Tenaillon, O., Silander, O. K., Uzan, J.-P. & Chao, L. Quantifying organismal complexity using a population genetic approach. PLoS ONE 2, e217 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Valentine, J. W., Collins, A. G. & Meyer, C. P. Morphological complexity increase in metazoans. Paleobiology 20, 131–142 (1994).

    Article  Google Scholar 

  45. Yang, J., Lusk, R. & Li, W.-H. Organismal complexity, protein complexity, and gene duplicability. Proc. Natl Acad. Sci. USA 100, 15661–15665 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Prochnik, S. E. et al. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science 329, 223–226 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hobern, D. et al. Towards a global list of accepted species VI: the Catalogue of Life checklist. Org. Divers. Evol. 21, 677–690 (2021).

    Article  Google Scholar 

  48. Guillerme, T. dispRity: a modular R package for measuring disparity. Methods Ecol. Evol. 9, 1755–1763 (2018).

    Article  Google Scholar 

  49. Tedersoo, L. et al. High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers. 90, 135–159 (2018).

    Article  Google Scholar 

  50. He, M.-Q. et al. Notes, outline and divergence times of Basidiomycota. Fungal Divers. 99, 105–367 (2019).

    Article  Google Scholar 

  51. Beimforde, C. et al. Estimating the Phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol. Phylogenet. Evol. 78, 386–398 (2014).

    Article  PubMed  Google Scholar 

  52. Bollback, J. P. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 7, 88 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  54. O’Reilly, J. E. et al. Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data. Biol. Lett. 12, 20160081 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Sanderson, M. J. & Donoghue, M. J. Patterns of variation in levels of homoplasy. Evolution 43, 1781–1795 (1989).

    Article  PubMed  Google Scholar 

  56. Lloyd, G. T. Estimating morphological diversity and tempo with discrete character-taxon matrices: implementation, challenges, progress, and future directions. Biol. J. Linn. Soc. Lond. 118, 131–151 (2016).

    Article  Google Scholar 

  57. Gower, J. C. General coefficient of similarity and some of its properties. Biometrics 27, 857–871 (1971).

    Article  Google Scholar 

  58. Anderson, P. S. L. & Friedman, M. Using cladistic characters to predict functional variety: experiments using early gnathostomes. J. Vertebr. Paleontol. 32, 1254–1270 (2012).

    Article  Google Scholar 

  59. Wills, M. A. in Fossils, Phylogeny, and Form: an Analytical Approach (eds Adrain, J. M. et al.) 55–144 (Springer, 2001).

  60. Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2019).

    Article  CAS  PubMed  Google Scholar 

  61. Clarke, K. R. & Warwick, R. M. Change in Marine Communities: an Approach to Statistical Analysis and Interpretation (PRIMER-E Ltd, 2001).

  62. Cailliez, F. The analytical solution of the additive constant problem. Psychometrika 48, 305–308 (1983).

    Article  Google Scholar 

  63. Smith, T. J. & Donoghue, P. C. J. Data from: Evolution of fungal phenotypic disparity, Dryad, Dataset (2022). https://doi.org/10.5061/dryad.wwpzgmsm9

  64. Letcher, P. M. & Powell, M. J. A taxonomic summary and revision of Rozella (Cryptomycota). IMA Fungus 9, 383–399 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  65. James, T., Porter, T. M. & Martin, W. W. in Systematics and Evolution. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research) Vol. 7A (eds McLaughlin, D. J. & Spatafora, J. W.), 177–207 (Springer, 2014).

  66. Seto, K., Van den Wyngaert, S., Degawa, Y. & Kagami, M. Taxonomic revision of the genus Zygorhizidium: Zygorhizidiales and Zygophlyctidales ord. nov. (Chytridiomycetes, Chytridiomycota). Fungal Syst. Evol. 5, 17–38 (2020).

    Article  CAS  PubMed  Google Scholar 

  67. Joshi, A. et al. Liebetanzomyces polymorphus gen. et sp. nov., a new anaerobic fungus (Neocallimastigomycota) isolated from the rumen of a goat. MycoKeys 89–110 (2018).

  68. Błaszkowski, J. et al. Dominikia bonfanteae and Glomus atlanticum, two new species in the Glomeraceae (phylum Glomeromycota) with molecular phylogenies reconstructed from two unlinked loci. Mycol. Prog. 20, 131–148 (2021).

    Article  Google Scholar 

  69. Walther, G., Wagner, L. & Kurzai, O. Outbreaks of Mucorales and the species involved. Mycopathologia 185, 765–781 (2020).

    PubMed  Google Scholar 

  70. Reynolds, N. K. et al. Phylogenetic and morphological analyses of the mycoparasitic genus Piptocephalis. Mycologia 111, 54–68 (2019).

    Article  CAS  PubMed  Google Scholar 

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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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Authors and Affiliations

  1. Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK

    Thomas J. Smith & Philip C. J. Donoghue

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Contributions

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.

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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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