Evolution of phenotypic disparity in the plant kingdom.


Journal

Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677

Informations de publication

Date de publication:
10 2023
Historique:
received: 15 04 2023
accepted: 07 08 2023
medline: 23 10 2023
pubmed: 5 9 2023
entrez: 4 9 2023
Statut: ppublish

Résumé

The plant kingdom exhibits diverse bodyplans, from single-celled algae to complex multicellular land plants, but it is unclear how this phenotypic disparity was achieved. Here we show that the living divisions comprise discrete clusters within morphospace, separated largely by reproductive innovations, the extinction of evolutionary intermediates and lineage-specific evolution. Phenotypic complexity correlates not with disparity but with ploidy history, reflecting the role of genome duplication in plant macroevolution. Overall, the plant kingdom exhibits a pattern of episodically increasing disparity throughout its evolutionary history that mirrors the evolutionary floras and reflects ecological expansion facilitated by reproductive innovations. This pattern also parallels that seen in the animal and fungal kingdoms, suggesting a general pattern for the evolution of multicellular bodyplans.

Identifiants

pubmed: 37666963
doi: 10.1038/s41477-023-01513-x
pii: 10.1038/s41477-023-01513-x
pmc: PMC10581900
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1618-1626

Subventions

Organisme : RCUK | Natural Environment Research Council (NERC)
ID : NE/N002067/1
Organisme : RCUK | Natural Environment Research Council (NERC)
ID : NE/P013678/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/N000919/1
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : BB/T012773/1
Organisme : Leverhulme Trust
ID : RF-2022-167
Organisme : Leverhulme Trust
ID : RPG-2019-004
Organisme : John Templeton Foundation (JTF)
ID : JTF 62574

Informations de copyright

© 2023. The Author(s).

Références

Foote, M. The evolution of morphological diversity. Annu. Rev. Ecol. Syst. 28, 129–152 (1997).
doi: 10.1146/annurev.ecolsys.28.1.129
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).
pubmed: 23884651 pmcid: 3752257 doi: 10.1073/pnas.1302642110
Niklas, K. J. Morphological evolution through complex domains of fitness. Proc. Natl Acad. Sci. USA 91, 6772–6779 (1994).
pubmed: 8041696 pmcid: 44282 doi: 10.1073/pnas.91.15.6772
Niklas, K. J. Computer models of early land plant evolution. Annu. Rev. Earth Planet. Sci. 32, 47–66 (2004).
doi: 10.1146/annurev.earth.32.092203.122440
Chartier, M. et al. How (much) do flowers vary? Unbalanced disparity among flower functional modules and a mosaic pattern of morphospace occupation in the order Ericales.Proc. R Soc. B 284, 20170066 (2017).
pubmed: 28381623 pmcid: 5394665 doi: 10.1098/rspb.2017.0066
Chartier, M. et al. Global patterns and a latitudinal gradient of flower disparity: perspectives from the angiosperm order Ericales. New Phytol. 230, 821–831 (2021).
pubmed: 33454991 pmcid: 8048689 doi: 10.1111/nph.17195
Jardine, P. E., Palazzesi, L., Telleria, M. C. & Barreda, V. D. Why does pollen morphology vary? Evolutionary dynamics and morphospace occupation in the largest angiosperm order (Asterales).New Phytol. 234, 1075–1087 (2022).
pubmed: 35147224 doi: 10.1111/nph.18024
Leslie, A. B., Simpson, C. & Mander, L. Reproductive innovations and pulsed rise in plant complexity. Science 373, 1368–1372 (2021).
pubmed: 34529461 doi: 10.1126/science.abi6984
Yu, Y., Schneider, H., Li, D. Z. & Wang, H. Evolutionary constraints on disparity of ericaceous pollen grains. Ann. Bot. 123, 805–813 (2019).
pubmed: 30629108 pmcid: 6526368 doi: 10.1093/aob/mcy212
Boyce, C. K. Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31, 117–140 (2005).
doi: 10.1666/0094-8373(2005)031<0117:POSACI>2.0.CO;2
Xue, J. et al. Stepwise evolution of Paleozoic tracheophytes from South China: Contrasting leaf disparity and taxic diversity. Earth Sci. Rev. 148, 77–93 (2015).
doi: 10.1016/j.earscirev.2015.05.013
Wilson, J. P. & Knoll, A. H. A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants. Paleobiology 36, 335–355 (2010).
doi: 10.1666/08071.1
Oyston, J. W., Hughes, M., Gerber, S. & Wills, M. A. Why should we investigate the morphological disparity of plant clades? Ann. Bot. 117, 859–879 (2016).
pubmed: 26658292 doi: 10.1093/aob/mcv135
Clark, J. W. & Donoghue, P. C. J. Whole-genome duplication and plant macroevolution. Trends Plant Sci. 23, 933–945 (2018).
pubmed: 30122372 doi: 10.1016/j.tplants.2018.07.006
Walden, N. et al. Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae. Nat. Commun. 11, 3795 (2020).
pubmed: 32732942 pmcid: 7393125 doi: 10.1038/s41467-020-17605-7
Garbary, D. J., Renzaglia, K. S. & Duckett, J. G. The phylogeny of land plants: a cladistic analysis based on male gametogenesis. Plant Syst. Evol. 188, 237–269 (1993).
doi: 10.1007/BF00937730
Renzaglia, K. S. & Garbary, D. J. Motile gametes of land plants: diversity, development, and evolution. Crit. Rev. Plant Sci. 20, 107–213 (2001).
doi: 10.1080/20013591099209
Schneider, H., Smith, A. R. & Pryer, K. M. Is morphology really at odds with molecules in estimating fern phylogeny? Syst. Bot. 34, 455–475 (2009).
doi: 10.1600/036364409789271209
Doyle, J. A. & Endress, P. K. Integrating Early Cretaceous fossils into the phylogeny of living angiosperms: Magnoliidae and eudicots. J. Syst. Evol. 48, 1–35 (2010).
doi: 10.1111/j.1759-6831.2009.00058.x
Mishler, B. D. & Churchill, S. P. Transition to a land flora: phylogenetic relationships of the green algae and bryophytes. Cladistics 1, 305–328 (1985).
pubmed: 34965680 doi: 10.1111/j.1096-0031.1985.tb00431.x
Kenrick, P. & Crane, P. R. The Origin and Early Diversification of Land Plants: A Cladistic Study (Smithsonian Institution Press, 1997).
Hilton, J. & Bateman, R. M. Pteridosperms are the backbone of seed-plant phylogeny. J. Torrey Bot. Soc. 133, 119–168 (2006).
doi: 10.3159/1095-5674(2006)133[119:PATBOS]2.0.CO;2
Puttick, M. N. et al. The interrelationships of land plants and the nature of the ancestral embryophyte. Curr. Biol. 28, R210–R213 (2018).
doi: 10.1016/j.cub.2018.01.063
Floyd, S. K. & Bowman, J. L. The ancestral developmental tool kit of land plants. Int. J. Plant Sci. 168, 1–35 (2007).
doi: 10.1086/509079
Villarreal, J. C., Cargill, D. C., Hagborg, A., Soderstrom, L. & Renzaglia, K. S. A synthesis of hornwort diversity: patterns, causes and future work. Phytotaxa 9, 150–166 (2010).
doi: 10.11646/phytotaxa.9.1.8
Doyle, J. A. in Annual Plant Reviews Vol. 45 (eds B. A. Ambrose & M. D. Purugganan) Ch. 1, 1–50 (Blackwell, 2013).
Brandon, R. & McShea, D. W. The Missing Two-thirds of Evolutionary Theory (Cambridge Univ. Press, 2020).
McShea, D. W. Metazoan complexity and evolution: is there a trend? Evolution 50, 477–492 (1996).
pubmed: 28568940
McShea, D. W. & Brandon, R. N. Biology’s First Law. The Tendency for Diversity and Complexity to Increase in Evolutionary Systems (Univ. Chicago Press, 2010).
Bowman, J. L. et al. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171, 287–304.e215 (2017).
pubmed: 28985561 doi: 10.1016/j.cell.2017.09.030
Harris, B. J. et al. Divergent evolutionary trajectories of bryophytes and tracheophytes from a complex common ancestor of land plants. Nat. Ecol. Evol. 6, 1634–1643 (2022).
pubmed: 36175544 pmcid: 9630106 doi: 10.1038/s41559-022-01885-x
Rensing, S. A. Gene duplication as a driver of plant morphogenetic evolution. Curr. Opin. Plant Biol. 17, 43–48 (2014).
pubmed: 24507493 doi: 10.1016/j.pbi.2013.11.002
Donoghue, M. J., Doyle, J., Gauthier, J., Kluge, A. & Rowe, T. The importance of fossils in phylogeny reconstruction. Annu. Rev. Ecol. Syst. 20, 431–460 (1989).
doi: 10.1146/annurev.es.20.110189.002243
Edwards, D., Morris, J. L., Axe, L. & Duckett, J. G. Picking up the pieces: new charcoalified plant mesofossils (eophytes) from a Lower Devonian Lagerstӓtte in the Welsh Borderland, UK.Rev. Palaeobot. Palynol. 297, 104567 (2022).
doi: 10.1016/j.revpalbo.2021.104567
Deline, B. The effects of rarity and abundance distributions on measurements of local morphological disparity. Paleobiology 35, 175–189 (2009).
doi: 10.1666/08028.1
Deline, B. et al. Evolution of metazoan morphological disparity. Proc. Natl Acad. Sci. USA 115, E8909–E8918 (2018).
pubmed: 30181261 pmcid: 6156614 doi: 10.1073/pnas.1810575115
Nordén, K. K., Stubbs, T. L., Prieto-Márquez, A. & Benton, M. J. Multifaceted disparity approach reveals dinosaur herbivory flourished before the end-Cretaceous mass extinction. Paleobiology 44, 620–637 (2018).
doi: 10.1017/pab.2018.26
Cleal, C. J. & Cascales-Miñana, B. Composition and dynamics of the great Phanerozoic Evolutionary Floras. Lethaia 47, 469–484 (2014).
doi: 10.1111/let.12070
Bowles, A. M. C., Bechtold, U. & Paps, J. The origin of land plants is rooted in two bursts of genomic novelty. Curr. Biol. 30, 530–536 (2020).
pubmed: 31956023 doi: 10.1016/j.cub.2019.11.090
Valentine, J. W., Tiffney, B. H. & Sepkoski, J. J. Jr. Evolutionary dynamics of plants and animals: a comparative approach. Palaios 6, 81–88 (1991).
pubmed: 11538488 doi: 10.2307/3514955
Donoghue, P. C. J., Harrison, C. J., Paps, J. & Schneider, H. The evolutionary emergence of land plants. Curr. Biol. 31, R1281–R1298 (2021).
pubmed: 34637740 doi: 10.1016/j.cub.2021.07.038
Smith, T. J. & Donoghue, P. C. J. Evolution of fungal phenotypic disparity. Nat. Ecol. Evol. 6, 1489–1500 (2022).
pubmed: 35970862 doi: 10.1038/s41559-022-01844-6
Erwin, D. H. Evolutionary uniformitarianism. Dev. Biol. 357, 27–34 (2011).
pubmed: 21276788 doi: 10.1016/j.ydbio.2011.01.020
Davidson, E. H. & Erwin, D. H. Gene regulatory networks and the evolution of animal body plans. Science 311, 796–800 (2006).
pubmed: 16469913 doi: 10.1126/science.1113832
Hanschen, E. R. et al. The Gonium pectorale genome demonstrates co-option of cell cycle regulation during the evolution of multicellularity. Nat. Commun. 7, 11370 (2016).
pubmed: 27102219 pmcid: 4844696 doi: 10.1038/ncomms11370
Vivancos, J. et al. The function of the RNA-binding protein TEL1 in moss reveals ancient regulatory mechanisms of shoot development. Plant Mol. Biol. 78, 323–336 (2012).
pubmed: 22170036 doi: 10.1007/s11103-011-9867-9
Erwin, D. H. A conceptual framework of evolutionary novelty and innovation. Biol. Rev. Camb. Philos. Soc. 96, 1–15 (2021).
pubmed: 32869437 doi: 10.1111/brv.12643
Mishler, B. D. et al. Phylogenetic relationships of the ‘green algae’ and ‘bryophytes’. Ann. Mo. Bot. Gard. 81, 451–483 (1994).
doi: 10.2307/2399900
Huelsenbeck, J. P., Nielsen, R., Bollback, J. P. & Schultz, T. Stochastic mapping of morphological characters. Syst. Biol. 52, 131–158 (2003).
pubmed: 12746144 doi: 10.1080/10635150390192780
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
doi: 10.1111/j.2041-210X.2011.00169.x
Gower, J. C. A general coefficient of similarity and some of its properties. Biometrics 27, 857–874 (1971).
doi: 10.2307/2528823
Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.0-7 http://CRAN.R-project.org/package=vegan (2013).
Foote, M. Contributions of individual taxa to overall morphological disparity. Paleobiology 19, 403–419 (1993).
doi: 10.1017/S0094837300014056
Guillerme, T. & Poisot, T. dispRity: a modular R package for measuring disparity. Methods Ecol. Evol. 9, 1755–1763 (2018).
doi: 10.1111/2041-210X.13022
Guillerme, T. & Cooper, N. Time for a rethink: time sub-sampling methods in disparity-through-time analyses.Palaeontology 61, 481–493 (2018).
doi: 10.1111/pala.12364
Morris, J. L. et al. The timescale of early land plant evolution. Proc. Natl Acad. Sci. USA 115, E2274–E2283 (2018).
pubmed: 29463716 pmcid: 5877938 doi: 10.1073/pnas.1719588115

Auteurs

James W Clark (JW)

Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK. james.clark@bristol.ac.uk.
School of Biological Sciences, University of Bristol, Bristol, UK. james.clark@bristol.ac.uk.
Milner Centre for Evolution, Department of Life Sciences, University of Bath, Bath, UK. james.clark@bristol.ac.uk.

Alexander J Hetherington (AJ)

Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK. sandy.hetherington@ed.ac.uk.
Institute of Molecular Plant Sciences, School of Biological Sciences, University of Edinburgh, Edinburgh, UK. sandy.hetherington@ed.ac.uk.

Jennifer L Morris (JL)

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

Silvia Pressel (S)

The Natural History Museum, London, UK.

Jeffrey G Duckett (JG)

The Natural History Museum, London, UK.

Mark N Puttick (MN)

Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK.
Milner Centre for Evolution, Department of Life Sciences, University of Bath, Bath, UK.

Harald Schneider (H)

Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK.
The Natural History Museum, London, UK.
Center of Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, China.

Paul Kenrick (P)

The Natural History Museum, London, UK.

Charles H Wellman (CH)

School of Biosciences, University of Sheffield, Sheffield, UK.

Philip C J Donoghue (PCJ)

Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK. phil.donoghue@bristol.ac.uk.

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