Two-Phase Increase in the Maximum Size of Life Over 3.5 Billion Years Reflects Biological Innovation and Environmental Opportunity
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Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity 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 fu¨r Naturkunde der Humboldt–Universita¨t 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) The maximum size of organisms has increased enormously since and avoids the more substantial empirical difficulties in deter- the initial appearance of life >3.5 billion years ago (Gya), but the mining mean, median, or minimum size for all life or even for pattern and timing of this size increase is poorly known. Conse- many individual taxa. For each era within the Archean Eon quently, controls underlying the size spectrum of the global biota (4,000–2,500 Mya) and for each period within the Proterozoic have been difficult to evaluate. Our period-level compilation of the (2,500–542 Mya) and Phanerozoic (542–0 Mya) eons, we ob- largest known fossil organisms demonstrates that maximum size tained the sizes of the largest known fossil prokaryotes, single- increased by 16 orders of magnitude since life first appeared in the celled eukaryotes, metazoans, and vascular plants by reviewing fossil record. The great majority of the increase is accounted for by the published literature and contacting taxonomic experts. Sizes 2 discrete steps of approximately equal magnitude: the first in the were converted to volume to facilitate comparisons across middle of the Paleoproterozoic Era (Ϸ1.9 Gya) and the second disparate taxonomic groups (see Data and Methods). The data- during the late Neoproterozoic and early Paleozoic eras (0.6–0.45 base is deposited in Data Dryad (www.datadryad.org) and can Gya). Each size step required a major innovation in organismal be accessed at http://hdl.handle.net/10255/dryad.222. complexity—first the eukaryotic cell and later eukaryotic multicel- lularity. These size steps coincide with, or slightly postdate, in- Results creases in the concentration of atmospheric oxygen, suggesting The maximum body volume of organisms preserved in the fossil latent evolutionary potential was realized soon after environmen- record has increased by Ϸ16 orders of magnitude over the last tal limitations were removed. 3.5 billion years (Fig. 1). Increase in maximum size occurred episodically, with pronounced jumps of approximately 6 orders body size ͉ Cambrian ͉ oxygen ͉ Precambrian ͉ trend of magnitude in the mid-Paleoproterozoic (Ϸ1.9 Gya) and during the Ediacaran through Ordovician (600–450 Mya). Thus, espite widespread scientific and popular fascination with Ϸ75% of the overall increase in maximum body size over Dthe largest and smallest organisms and numerous studies of geological time took place during 2 geologically brief intervals body size evolution within individual taxonomic groups (1–9), that together comprise Ͻ20% of the total duration of life on the first-order pattern of body size evolution through the history Earth. of life has not been quantified rigorously. Because size influences Paleoproterozoic size increase occurs as a single step in Fig. (and may be limited by) a broad spectrum of physiological, 1, reflecting the presence of Grypania spiralis in the Paleopro- ecological, and evolutionary processes (10–16), detailed docu- terozoic (Orosirian) Negaunee Iron Formation of Canada (19). mentation of size trends may shed light on the constraints and The taxonomic affinities of these fossils are controversial: Their innovations that have shaped life’s size spectrum over evolu- morphological regularity and size suggest they are the remains of tionary time as well as the role of the body size spectrum in eukaryotic organisms (19, 20), but they have also been inter- structuring global ecosystems. Bonner (17) presented a figure preted as composite microbial filaments (21). Possible trace portraying a gradual, monotonic increase in the overall maxi- fossils of similar age and comparable size occur in the Stirling mum size of living organisms over the past 3.5 billion years. The Quartzite of Australia and the Chorhat Sandstone of India, pattern appears consistent with a simple, continuous underlying suggesting Orosirian size increase may not have been confined process such as diffusion (18), but could also reflect a more to Grypania (22, 23). Slightly younger specimens of similar sizes complex process. Bonner, for example, proposed that lineages from the Changzhougou and Changlinggou formations of China evolve toward larger sizes to exploit unoccupied ecological niches. For decades, Bonner’s has been the only attempt to quantify body size evolution over the entire history of life on 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., Earth, but the data he presented were not tied to particular fossil P.M.N.-G., F.A.S., J.A.S., and S.C.W. designed research, performed research, analyzed data, specimens and were plotted without consistent controls on and wrote the paper. taxonomic scale against a nonlinear timescale. Hence, we have The authors declare no conflict of interest. lacked sufficient data on the tempo and mode of maximum size This article is a PNAS Direct Submission. change to evaluate potential first-order biotic and abiotic con- Freely available online through the PNAS open access option. trols on organism size through the history of life. 1To whom correspondence should be addressed. E-mail: [email protected]. Here, we document the evolutionary history of body size on This article contains supporting information online at www.pnas.org/cgi/content/full/ Earth, focusing on the upper limit to size. Use of maximum size 0806314106/DCSupplemental. allows us to assess constraints on the evolution of large body size © 2008 by The National Academy of Sciences of the USA 24–27 ͉ PNAS ͉ January 6, 2009 ͉ vol. 106 ͉ no. 1 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0806314106 Downloaded by guest on October 2, 2021 history of maximum size at the taxonomic and temporal scales giant 14 14 addressed. Larger fossils and larger fossil species tend to be pO2 < 0.1% PAL pO2 1%-10% PAL pO2 ~ 100% PAL sequioa 12 remarked upon in the paleontological literature; genus and blue species names with roots meaning ‘‘large’’ or ‘‘giant’’ are com- cephalopod 10 10 whale monly applied to particularly sizeable taxa, making them easy to 8 arthropod ) identify in the literature. Because we treat size data on a 3 Dickinsonia 6 largest 6 single-celled logarithmic scale, even moderate sampling biases are unlikely to eukaryote 4 cause observed maxima to vary by Ͼ1 or 2 orders of magnitude. Grypania Ͼ 2 2 In contrast, species in the maximum size dataset span 16 orders of magnitude, and the sizes of all living organisms span Ͼ22 0 largest prokaryote orders of magnitude (27). Although the upper bound error bars -2 -2 for the individual data points cannot be readily estimated, these Biovolume (log mm Biovolume -4 errors are likely to be negligible given the size range addressed Primaevifilum -6 -6 in our study. For example, it is unlikely that dinosaurs, whales, Ͼ -8 or cephalopods 10 times the size of the largest known speci- EoarchaeanPaleoar. Mesoar. Neoar. Paleoproterozoic Mesoprot. Neoprot. Pz. Mz. C Archaean Proterozoic Phan. mens have ever existed. That the largest living plant and animal 4000 3000 2000 1000 species are not much bigger than the largest known fossils (Fig. Age (Ma) 1) suggests fossils reliably sample not only trends but also absolute values of maximum size at the temporal and taxonomic Fig. 1. Sizes of the largest fossils through Earth history. Size maxima are scales considered in this study. Trends in trace fossil sizes are illustrated separately for single-celled eukaryotes, animals, and vascular plants for the Ediacaran and Phanerozoic. The solid line denotes the trend in generally concordant with the body fossil record (28), indicating the overall maximum for all of life. Increases in the overall maximum occurred that the apparent size increase from the Ediacaran through in discrete steps approximately corresponding to increases in atmospheric Ordovician does not merely reflect an increase in preservation oxygen levels in the mid-Paleoproterozoic and Ediacaran–Cambrian–early potential of large animals. Moreover, large-bodied fossils occur Ordovician. Sizes of the largest fossil prokaryotes were not compiled past 1.9 in both well-fossilized clades (e.g., cephalopods) and taxa that Gya. Estimates