New Research In
Physical Sciences
Social Sciences
Featured Portals
Articles by Topic
Biological Sciences
Featured Portals
Articles by Topic
- Agricultural Sciences
- Anthropology
- Applied Biological Sciences
- Biochemistry
- Biophysics and Computational Biology
- Cell Biology
- Developmental Biology
- Ecology
- Environmental Sciences
- Evolution
- Genetics
- Immunology and Inflammation
- Medical Sciences
- Microbiology
- Neuroscience
- Pharmacology
- Physiology
- Plant Biology
- Population Biology
- Psychological and Cognitive Sciences
- Sustainability Science
- Systems Biology
Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity
-
Edited by James W. Valentine, University of California, Berkeley, CA, and approved November 14, 2008 (received for review July 1, 2008)

Online Impact
Article Information
- Published in issue January 6, 2009.
- Published first December 23, 2008.
Article Versions
- Previous version (December 23, 2008 - 11:08).
- You are viewing the most recent version of this article.
Author Information
- Jonathan L. Paynea,1,
- Alison G. Boyerb,
- James H. Brownb,
- Seth Finnegana,
- Michał Kowalewskic,
- Richard A. Krause, Jr.d,
- S. Kathleen Lyonse,
- Craig R. McClainf,
- Daniel W. McSheag,
- Philip M. Novack-Gottshallh,
- Felisa A. Smithb,
- Jennifer A. Stempieni, and
- Steve C. Wangj
- aDepartment of Geological and Environmental Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, CA 94305;
- bDepartment of Biology, University of New Mexico, Albuquerque, NM 87131;
- cDepartment of Geosciences, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061;
- dMuseum für Naturkunde der Humboldt–Universität zu Berlin, D-10115, Berlin, Germany;
- eDepartment of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560;
- fMonterey Bay Aquarium Research Institute, Moss Landing, CA 95039;
- gDepartment of Biology, Box 90338, Duke University, Durham, NC 27708;
- hDepartment of Geosciences, University of West Georgia, Carrollton, GA 30118;
- iDepartment of Geological Sciences, University of Colorado, Boulder, CO 80309; and
- jDepartment of Mathematics and Statistics, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081
-
Edited by James W. Valentine, University of California, Berkeley, CA, and approved November 14, 2008 (received for review July 1, 2008)
Footnotes
- 1To whom correspondence should be addressed. E-mail: jlpayne{at}stanford.edu
-
Author contributions: J.L.P., A.G.B., J.H.B., S.F., M.K., R.A.K., S.K.L., C.R.M., D.W.M., P.M.N.-G., F.A.S., J.A.S., and S.C.W. designed research, performed research, analyzed data, and wrote the paper.
-
The authors declare no conflict of interest.
-
This article is a PNAS Direct Submission.
-
This article contains supporting information online at www.pnas.org/cgi/content/full/0806314106/DCSupplemental.
-
Freely available online through the PNAS open access option.
- © 2008 by The National Academy of Sciences of the USA
Cited By...
This article has been cited by the following articles in journals that are participating in Crossref Cited-by Linking.
- C. T. Reinhard, N. J. Planavsky, L. J. Robbins, C. A. Partin, B. C. Gill, S. V. Lalonde, A. Bekker, K. O. Konhauser, T. W. LyonsProceedings of the National Academy of Sciences 2013 110 14
- Lawrence M. Och, Graham A. Shields-ZhouEarth-Science Reviews 2012 110 1-4
- T. W. Dahl, E. U. Hammarlund, A. D. Anbar, D. P. G. Bond, B. C. Gill, G. W. Gordon, A. H. Knoll, A. T. Nielsen, N. H. Schovsbo, D. E. CanfieldProceedings of the National Academy of Sciences 2010 107 42
- J. P. DeLong, J. G. Okie, M. E. Moses, R. M. Sibly, J. H. BrownProceedings of the National Academy of Sciences 2010 107 29
- F. A. Smith, A. G. Boyer, J. H. Brown, D. P. Costa, T. Dayan, S. K. M. Ernest, A. R. Evans, M. Fortelius, J. L. Gittleman, M. J. Hamilton, L. E. Harding, K. Lintulaakso, S. K. Lyons, C. McCain, J. G. Okie, J. J. Saarinen, R. M. Sibly, P. R. Stephens, J. Theodor, M. D. UhenScience 2010 330 6008
- Xi Chen, Hong-Fei Ling, Derek Vance, Graham A. Shields-Zhou, Maoyan Zhu, Simon W. Poulton, Lawrence M. Och, Shao-Yong Jiang, Da Li, Lorenzo Cremonese, Corey ArcherNature Communications 2015 6 1
- Michael J. Benton, Andrew J. NewellGondwana Research 2014 25 4
- Alex L. Sessions, David M. Doughty, Paula V. Welander, Roger E. Summons, Dianne K. NewmanCurrent Biology 2009 19 14
- Nicholas J. ButterfieldTrends in Ecology & Evolution 2011 26 2
- Jianguo Wang, Daizhao Chen, Detian Yan, Hengye Wei, Lei XiangChemical Geology 2012 306-307
- S. Maruyama, M. Ikoma, H. Genda, K. Hirose, T. Yokoyama, M. SantoshGeoscience Frontiers 2013 4 2
- Minglei Wang, Ying-Ying Jiang, Kyung Mo Kim, Ge Qu, Hong-Fang Ji, Jay E. Mittenthal, Hong-Yu Zhang, Gustavo Caetano-AnollésMolecular Biology and Evolution 2011 28 1
- Will Steffen, Reinhold Leinfelder, Jan Zalasiewicz, Colin N. Waters, Mark Williams, Colin Summerhayes, Anthony D. Barnosky, Alejandro Cearreta, Paul Crutzen, Matt Edgeworth, Erle C. Ellis, Ian J. Fairchild, Agnieszka Galuszka, Jacques Grinevald, Alan Haywood, Juliana Ivar do Sul, Catherine Jeandel, J.R. McNeill, Eric Odada, Naomi Oreskes, Andrew Revkin, Daniel deB. Richter, James Syvitski, Davor Vidas, Michael Wagreich, Scott L. Wing, Alexander P. Wolfe, H.J. SchellnhuberEarth's Future 2016 4 8
- Yaacov Davidov, Edouard JurkevitchBioEssays 2009 31 7
- Erik A. Sperling, Andrew H. Knoll, Peter R. GirguisAnnual Review of Ecology, Evolution, and Systematics 2015 46 1
- Felisa A. Smith, S. Kathleen LyonsPhilosophical Transactions of the Royal Society B: Biological Sciences 2011 366 1576
- Lorenzo Cremonese, Graham Shields-Zhou, Ulrich Struck, Hong-Fei Ling, Lawrence Och, Xi Chen, Da LiPrecambrian Research 2013 225
- Simon Brewer, Stephen T. Jackson, John W. WilliamsTrends in Ecology & Evolution 2012 27 2
- Jonathan L. Payne, Craig R. McClain, Alison G. Boyer, James H. Brown, Seth Finnegan, Michał Kowalewski, Richard A. Krause, S. Kathleen Lyons, Daniel W. McShea, Philip M. Novack-Gottshall, Felisa A. Smith, Paula Spaeth, Jennifer A. Stempien, Steve C. WangPhotosynthesis Research 2011 107 1
- Adele Williamson, Brendon Conlan, Warwick Hillier, Tom WydrzynskiPhotosynthesis Research 2011 107 1
- M. Santosh, S. Maruyama, Yusuke Sawaki, Joseph G. MeertGondwana Research 2014 25 3
- Shanan E. Peters, Ce Zhang, Miron Livny, Christopher Ré, Christos A. OuzounisPLoS ONE 2014 9 12
- Geerat J. Vermeij, Pasquale RaiaPLOS ONE 2016 11 1
- Aviv Bachan, Lee R. KumpProceedings of the National Academy of Sciences 2015 112 21
- W.-H. HE, R. J. TWITCHETT, Y. ZHANG, G. R. SHI, Q.-L. FENG, J.-X. YU, S.-B. WU, X.-F. PENGGeobiology 2010 8 5
- David K. Moss, Linda C. Ivany, Emily J. Judd, Patrick W. Cummings, Claire E. Bearden, Woo-Jun Kim, Emily G. Artruc, Jeremy R. DriscollProceedings of the Royal Society B: Biological Sciences 2016 283 1836
- Jordan G. OkieThe American Naturalist 2013 181 3
- Kyung Mo Kim, Tao Qin, Ying-Ying Jiang, Ling-Ling Chen, Min Xiong, Derek Caetano-Anollés, Hong-Yu Zhang, Gustavo Caetano-AnollésStructure 2012 20 1
- David George, Alain Blieck, Brock FentonPLoS ONE 2011 6 7
- Mark Williams, Jan Zalasiewicz, Colin N. Waters, Matt Edgeworth, Carys Bennett, Anthony D. Barnosky, Erle C. Ellis, Michael A. Ellis, Alejandro Cearreta, Peter K. Haff, Juliana A. Ivar do Sul, Reinhold Leinfelder, John R. McNeill, Eric Odada, Naomi Oreskes, Andrew Revkin, Daniel deB Richter, Will Steffen, Colin Summerhayes, James P. Syvitski, Davor Vidas, Michael Wagreich, Scott L. Wing, Alexander P. Wolfe, An ZhishengEarth's Future 2016 4 3
- Yin-Long QIU, Alexander B. TAYLOR, Hilary A. McMANUSJournal of Systematics and Evolution 2012 50 3
- S. Maruyama, Y. Sawaki, T. Ebisuzaki, M. Ikoma, S. Omori, T. KomabayashiGondwana Research 2014 25 3
- Masaki Yoshida, Yuuhiko Tanabe, Natsuki Yonezawa, Makoto M WatanabeBiofuels 2012 3 6
- Warren D. Allmon, Ronald E. MartinPaleobiology 2014 40 2
- Supriyo Ray, Adam Kassan, Anna R. Busija, Padmini Rangamani, Hemal H. PatelAmerican Journal of Physiology-Cell Physiology 2016 310 3
- Marina MacLean, Jeffrey Nadeau, Taylor Gurnea, Claus Tittiger, Gary J. BlomquistInsect Biochemistry and Molecular Biology 2018 102
- Bradley Deline, Jennifer M. Greenwood, James W. Clark, Mark N. Puttick, Kevin J. Peterson, Philip C. J. DonoghueProceedings of the National Academy of Sciences 2018 115 38
- Jeong-Hyun Lee, Robert RidingEarth-Science Reviews 2018 181
- Craig R. McClain, Alison G. BoyerProceedings of the Royal Society B: Biological Sciences 2009 276 1665
- James H. Brown, Charles A. S. Hall, Richard M. SiblyNature Ecology & Evolution 2018 2 2
- Jonathan L. Payne, John R. Groves, Adam B. Jost, Thienan Nguyen, Sarah E. Moffitt, Tessa M. Hill, Jan M. SkotheimEvolution 2012 66 9
- Gianniantonio Domina, Gianpietro Giusso del Galdo, Domenico Gargano, Massimo Labra, Simonetta Peccenini, Lorenzo Peruzzi, Francesco M. RaimondoTAXON 2012 61 6
- Felisa A. Smith, Jonathan L. Payne, Noel A. Heim, Meghan A. Balk, Seth Finnegan, Michał Kowalewski, S. Kathleen Lyons, Craig R. McClain, Daniel W. McShea, Philip M. Novack-Gottshall, Paula Spaeth Anich, Steve C. WangAnnual Review of Earth and Planetary Sciences 2016 44 1
- Konstantin V Gunbin, Valentin V Suslov, Igor I Turnaev, Dmitry A Afonnikov, Nikolay A KolchanovBMC Evolutionary Biology 2011 11 1
- Phylogenetic origins of biological cognition: convergent patterns in the early evolution of learningMarc van DuijnInterface Focus 2017 7 3
- Weihong He, G.R. Shi, Yifan Xiao, Kexin Zhang, Tinglu Yang, Huiting Wu, Yang Zhang, Bing Chen, Mingliang Yue, Jun Shen, Yongbiao Wang, Hao Yang, Shunbao WuPalaeogeography, Palaeoclimatology, Palaeoecology 2017 486
- Erin L. Seifert, Mark Bastianelli, Céline Aguer, Cynthia Moffat, Carmen Estey, Lauren G. Koch, Steven L. Britton, Mary-Ellen HarperJournal of Applied Physiology 2012 113 10
- Adiël A. Klompmaker, Patricia H. Kelley, Devapriya Chattopadhyay, Jeff C. Clements, John Warren Huntley, Michal KowalewskiEarth-Science Reviews 2019 194
- Yang Zhang, G.R. Shi, Wei-hong He, Hui-ting Wu, Yong Lei, Ke-xin Zhang, Cheng-chen Du, Ting-lu Yang, Ming-liang Yue, Yi-fan XiaoPalaeogeography, Palaeoclimatology, Palaeoecology 2016 448
- Christian Klug, Kenneth De Baets, Björn Kröger, Mark A. Bell, Dieter Korn, Jonathan L. PayneLethaia 2015 48 2
- Marek Mentel, Mayo Röttger, Sally Leys, Aloysius G. M. Tielens, William F. MartinBioEssays 2014 36 10
- Connie C. W. Hsia, Anke Schmitz, Markus Lambertz, Steven F. Perry, John N. Maina2013
- Noel A. Heim, Jonathan L. Payne, Seth Finnegan, Matthew L. Knope, Michał Kowalewski, S. Kathleen Lyons, Daniel W. McShea, Philip M. Novack-Gottshall, Felisa A. Smith, Steve C. WangProceedings of the Royal Society B: Biological Sciences 2017 284 1857
- Ying-Ying Jiang, De-Xin Kong, Tao Qin, Hong-Yu ZhangBiochemical and Biophysical Research Communications 2010 391 2
- Adiël A. Klompmaker, Carrie E. Schweitzer, Rodney M. Feldmann, Michał KowalewskiProceedings of the Royal Society B: Biological Sciences 2015 282 1811
- Junpeng Zhang, Tailiang Fan, Yuandong Zhang, Gary G. Lash, Yifan Li, Yue WuScientific Reports 2017 7 1
- Zixiang Zhang, Michael Augustin, Jonathan L. PaynePaleobiology 2015 41 3
- Andrew M. Bush, Philip M. Novack-GottshallBiology Letters 2012 8 1
- A. V. Markov, V. A. Anisimov, A. V. KorotayevPaleontological Journal 2010 44 4
- Weihong He, G. R. Shi, Yang Zhang, Tinglu Yang, Fei Teng, Shunbao WuAlcheringa: An Australasian Journal of Palaeontology 2012 36 4
- Tais W. Dahl, Emma U. HammarlundCommunicative & Integrative Biology 2011 4 1
- Shan Chang, Qinglai Feng, Lei ZhangJournal of Earth Science 2018 29 4
- Jennifer F. Hoyal Cuthill, Simon Conway MorrisNature Ecology & Evolution 2017 1 8
- Carlo Doglioni, Johannes Pignatti, Max ColemanGeoscience Frontiers 2016 7 6
- Yoko Kunimitsu, Yusuke Setsuda, Seishiro Furuyama, Wei Wang, Akihiro KanoPrecambrian Research 2011 191 3-4
- Shan Huang, Jussi T. Eronen, Christine M. Janis, Juha J. Saarinen, Daniele Silvestro, Susanne A. FritzProceedings of the Royal Society B: Biological Sciences 2017 284 1849
- John T. BonnerJournal of Experimental Zoology Part B: Molecular and Developmental Evolution 2019 332 8
- Mariko Harada, Eiichi Tajika, Yasuhito SekineEarth and Planetary Science Letters 2015 419
- Bruno Labate Vale da Costa, Thiago Olitta Basso, Vijayendran Raghavendran, Andreas Karoly GombertApplied Microbiology and Biotechnology 2018 102 5
- Anais Pagès, Susanne SchmidPalaeogeography, Palaeoclimatology, Palaeoecology 2016 461
- Rémy Burcelin, Chantal Chabo, Vincent Blasco-Baque, Matteo Sérino, Jacques Amarmédecine/sciences 2013 29 8-9
- Yusuke Sawaki, Miyuki Tahata, Tsuyoshi Komiya, Takafumi Hirata, Jian Han, Degan ShuGeoscience Frontiers 2018 9 1
- Javier Robalino, Blake Wilkins, Heather D. Bracken-Grissom, Tin-Yam Chan, Maureen A. O’Leary, William Oki WongPLOS ONE 2016 11 7
- Z. T. Zhang, Y. D. Sun, P. B. Wignall, J. L. Fu, H. X. Li, M. Y. Wang, X. L. LaiJournal of the Geological Society 2018 175 6
- Alexander Pohle, Christian KlugLethaia 2018 51 1
- Rogier BraakmanFree Radical Biology and Medicine 2019 140
- Manasvi Lingam, Abraham LoebInternational Journal of Astrobiology 2019 18 6
- Ulrich Zeller, Thomas GöttertGlobal Ecology and Conservation 2019 20
- N. J. ButterfieldProceedings of the National Academy of Sciences 2011 108 9
- Jonathan L. Payne, Felisa A. Smith, Michal Kowalewski, Richard A. Krause Jr., Alison G. Boyer, Craig R. McClain, Seth Finnegan, Philip M. Novack-Gottshall, Laura ShebleTAXON 2012 61 6
- Weihong He, Kexin Zhang, Zhong-Qiang Chen, Jiaxin Yan, Tinglu Yang, Yang Zhang, Songzhu Gu, Shunbao WuJournal of Paleontology 2015 89 6
- Miyuki Tahata, Yusuke Sawaki, Yuichiro Ueno, Manabu Nishizawa, Naohiro Yoshida, Toshikazu Ebisuzaki, Tsuyoshi Komiya, Shigenori MaruyamaGeoscience Frontiers 2015 6 1
- Mao Luo, G.R. Shi, Luis A. Buatois, Zhong-Qiang ChenEarth-Science Reviews 2020 203
- Lee Hsiang Liow, Paul D. TaylorEvolution 2019 73 9
- María Rebolleda-Gómez, Michael TravisanoThe American Naturalist 2018 192 6
- Michał Kowalewski, Seth FinneganPaleobiology 2010 36 1
- Jimin Pei, Wenlin Li, Lisa N. Kinch, Nick V. GrishinProtein Science 2014 23 9
- John N. MainaCell and Tissue Research 2017 367 3
- Caitlin R. Keating-Bitonti, Jonathan L. PayneMarine Ecology 2017 38 3
- Martin Schobben, Bas van de SchootbruggeFrontiers in Earth Science 2019 7
- A. V. Maslov, V. N. PodkovyrovLithology and Mineral Resources 2018 53 3
- Seth FinneganThe Paleontological Society Papers 2013 19
- Corentin Bochaton, Melissa E. KempJournal of Vertebrate Paleontology 2017 37 1
- Martin KennedyThe American Naturalist 2013 181 S1
- Fergus SimpsonInternational Journal of Astrobiology 2017 16 3
- S. Kathleen Lyons, Felisa A. SmithThe Paleontological Society Papers 2010 16
- Daniel W. McSheaBiology & Philosophy 2015 30 3
- Brendan M. Anderson, Warren D. AllmonPalaeogeography, Palaeoclimatology, Palaeoecology 2020 544
- Gary J. Blomquist, Claus Tittiger, Russell Jurenka2018
- Andrew M. Bush, Sara B. PrussThe Paleontological Society Papers 2013 19
- Iaroslav Ispolatov, Evgeniia Alekseeva, Michael Doebeli, James O’DwyerPLOS Computational Biology 2019 15 10
- Mark A. Bell, Simon J. BraddyHistorical Biology 2012
- Andrey Yu. Zhuravlev, Rachel WoodScientific Reports 2020 10 1
- Alain BlieckPalaeobiodiversity and Palaeoenvironments 2017 97 3
- Wei Wei, Thomas J. AlgeoGeochimica et Cosmochimica Acta 2020 287
- Michael P. D'Antonio, C. Kevin BoyceNew Phytologist 2020 228 2
- Are Sigurdsen, Øyvind HammerPalaeogeography, Palaeoclimatology, Palaeoecology 2016 443
- Josef Buttigieg, Colin A. NurseRespiratory Physiology & Neurobiology 2012 181 2
- Guo-Xin Sun, Song-Can Chen, Gang Li, Xiao-Ming Li, Long-Jun Ding, Brian J. Reid, Philippe Ciais, Yong-Guan ZhuCritical Reviews in Environmental Science and Technology 2020
- Alla Sidorova, Vsevolod Tverdislov, Natalia Levashova, Anastasia GaraevaBiosystems 2020 198
- Crystal LaFlamme, Guillaume Barré, Marco L. Fiorentini, Georges Beaudoin, Sandra Occhipinti, Joshua BellGeochimica et Cosmochimica Acta 2021 295
- 2014
- K.J. Pienta, E.U. Hammarlund, R.H. Austin, R. Axelrod, J.S. Brown, S.R. AmendSeminars in Cancer Biology 2020
- K. J. Pienta, E. U. Hammarlund, J. S. Brown, S. R. Amend, R. M. AxelrodProceedings of the National Academy of Sciences 2021 118 7
- Gary J. Blomquist, Matthew D. GinzelAnnual Review of Entomology 2021 66 1
- Matthew D. Ginzel, Claus Tittiger, Marina MacLean, Gary J. Blomquist2021
- Charles W. Diamond, Richard E. Ernst, Shuan‐Hong Zhang, Timothy W. Lyons2020
- 2012
- Hugh DesmondStudies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences 2018 68-69
- Qiangfen Ma, Qinglai Feng, Yan Ye, Jun ShenPalaeogeography, Palaeoclimatology, Palaeoecology 2021 566
- 2016
- Yan Feng, Haijun Song, David P. G. BondPaleobiology 2020 46 4
- Lars WittingEvolutionary Biology 2020 47 1
- Jennifer E James, Sara M Willis, Paul G Nelson, Catherine Weibel, Luke J Kosinski, Joanna MaseleLife 2021 10