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The Tempo and Mode of Body Mass Evolution in Cenozoic Mammals

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The Tempo and Mode of Body Mass Evolution in Cenozoic Mammals The Evolution of Maximum Body Size of Terrestrial Mammals Felisa A. Smith, et al. Science 330, 1216 (2010); DOI: 10.1126/science.1194830 This copy is for your personal, non-commercial use only. If you wish to distribute this article to others, you can order high-quality copies for your colleagues, clients, or customers by clicking here. Permission to republish or repurpose articles or portions of articles can be obtained by following the guidelines here. The following resources related to this article are available online at www.sciencemag.org (this infomation is current as of April 6, 2011 ): Updated information and services, including high-resolution figures, can be found in the online version of this article at: http://www.sciencemag.org/content/330/6008/1216.full.html Supporting Online Material can be found at: http://www.sciencemag.org/content/suppl/2010/11/22/330.6008.1216.DC1.html on April 6, 2011 This article cites 21 articles, 8 of which can be accessed free: http://www.sciencemag.org/content/330/6008/1216.full.html#ref-list-1 This article appears in the following subject collections: Paleontology http://www.sciencemag.org/cgi/collection/paleo www.sciencemag.org Downloaded from Science (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. Copyright 2010 by the American Association for the Advancement of Science; all rights reserved. The title Science is a registered trademark of AAAS. REPORTS Eurasia, with the evolution of Indricotherium transouralicum (Perissodactyla) and again in the The Evolution of Maximum Body Size Miocene by several Deinotherium species (Pro- boscidea) in Eurasia and Africa (Fig. 1B; fig. S2); of Terrestrial Mammals North America never supported a mammal of 1 2 1 3 4 this size. Strikingly, the overall pattern was not Felisa A. Smith, * Alison G. Boyer, James H. Brown, Daniel P. Costa, Tamar Dayan, driven by a single taxon or an individual con- S. K. Morgan Ernest,5 Alistair R. Evans,6 Mikael Fortelius,7 John L. Gittleman,8 1 9 7 10 tinent. At one time or another, six different orders Marcus J. Hamilton, Larisa E. Harding, Kari Lintulaakso, S. Kathleen Lyons, and three of the four continents contained the Christy McCain,11 Jordan G. Okie,1 Juha J. Saarinen,7 Richard M. Sibly,12 Patrick R. Stephens,8 13 14 largest mammal. Because of the current paucity Jessica Theodor, Mark D. Uhen of data for South America, body mass values for this continent should be considered an under- The extinction of dinosaurs at the Cretaceous/Paleogene (K/Pg) boundary was the seminal estimate; nonetheless, results illustrate the same event that opened the door for the subsequent diversification of terrestrial mammals. Our general trends. Contrary to earlier suggestions compilation of maximum body size at the ordinal level by sub-epoch shows a near-exponential (13–15), increases in body mass were not driven increase after the K/Pg. On each continent, the maximum size of mammals leveled off after by increasing generic or ordinal diversity: Mam- 40 million years ago and thereafter remained approximately constant. There was remarkable mals were not consistently larger when they were congruence in the rate, trajectory, and upper limit across continents, orders, and trophic guilds, more diverse (9)(fig.S3). despite differences in geological and climatic history, turnover of lineages, and ecological We tested two hypotheses for the evolution variation. Our analysis suggests that although the primary driver for the evolution of giant of maximum body size. The first is a simple mammals was diversification to fill ecological niches, environmental temperature and land area growth model, in which maximum body size (M) may have ultimately constrained the maximum size achieved. evolves following a geometric Brownian motion, that is, an unconstrained random walk on the or the first 140 million years of their evo- (7). It marked the onset of rapid morphological, logarithmic scale. This model implicitly assumes lutionary history, mammals were small and ecological, and phylogenetic diversification in that niche space is uniformly distributed. Under occupied a fairly narrow range of body terrestrial mammals that led to an expansion in arandomwalk,M is predicted to increase as a on April 6, 2011 F g sizes and niches (1, 2). Although diverse feeding mass by four orders of magnitude and the occu- power law of the form log M = M0t ,whereM0 is adaptations evolved by the middle Mesozoic, and pation of a full range of ecological roles (8). initial maximum body size, t is time, and g =1/2, larger mammals may have preyed on small dino- Here we analyze maximum size of terrestrial so that maximum body size increases as the saurs (3, 4), their body size range extended only mammals across different continents, taxonomic square root of time (15). from ~3 to 5 g to ~10 to 15 kg (4, 5). This re- groups, phylogenetic lineages, and feeding guilds. The second model has growth saturating over stricted range almost certainly constrained the We compiled and analyzed data on the maximum time, reflecting limits of resources or physio- ecological roles of early mammals in paleocom- body size of each taxonomic order in each sub- logical, allometric, biomechanical, or ecological munities. For example, herbivory was probably epoch on each continent over their entire evolu- constraints, such as the slower life histories of limited; allometric, anatomical, and physiological tionary history (9). Information about body mass larger mammals. Thus, the initial change in body www.sciencemag.org constraints set a lower threshold of ~5 kg for ru- was obtained for fossil taxa from primary sources mass M with time is proportional to body mass dM minant herbivores (6). The Cretaceous/Paleogene or estimated directly from taxon-specific allomet- that is, dt ºM and increases at some intrinsic (K/Pg) mass extinction, which eliminated non- ric regressions based on measurements of teeth rateð a.However,asmaximumbodysizeevolves,Þ avian dinosaurs as well as many vertebrate, plant, or limbs (table S1). Because of taphonomic con- the evolutionary possibilities for increasing size and invertebrate taxa, was followed by a whole- siderations, we focused on the maximum size are progressively exhausted. Consequently, the sale reorganization of ecological communities achieved by each order; it tends to be reported in rate of change is also proportional to the avail- the literature and is robustly related to the overall ability of open niche space, which is captured by body size distribution and hence to the mean and the difference between asymptotic (K)andcur- Downloaded from 1Department of Biology, MSC03 2020, University of New 2 median body size (10). Fossil ages were stan- rent log body mass [that is, log(K) – log(M )], or Mexico, Albuquerque, NM 87131, USA. Department of Ecol- K ogy and Evolutionary Biology, Yale University, Box 208106, dardized using the midpoint for each Cenozoic log M .Combiningtheseecologicalandevolution- New Haven, CT 06520, USA. 3Department of Ecology and sub-epoch on the Gradstein geological time scale ary growth dynamics yields the Gompertz equa- Evolutionary Biology, University of California, Santa Cruz, (11). Diversity estimates were extracted from the tionÀÁdM aM log K ,asigmoidalgrowthmodel 4 dt M Santa Cruz, CA 95064, USA. Department of Zoology, Tel-Aviv Paleobiology Database (12), using the range- often used¼ in time series analyses. The integrated University, Tel Aviv 69978, Israel. 5Department of Biology and ÀÁ Ecology Center, Utah State University, Logan, UT 84322, USA. through option for each interval of time. We con- K −at form is log M log K − log e ,whereM0 6School of Biological Sciences, Monash University, VIC 3800, ducted simulations to assess the potential effect ¼ M0 Australia. 7Department of Geosciences and Geography, In- of sampling on the probability of detecting the is initial maximum body size. The Gompertz model stitute of Biotechnology, Post Office Box 64, FIN-00014 Uni- largest mammal; including as few as 10% of fossil is more biologically plausible than the random versity of Helsinki, Finland. 8Odum School of Ecology, 140 East Green Street, University of Georgia, Athens, GA 30602, USA. sites yielded nearly 100% probability of recover- walk model, because it captures both the multipli- 9Landscape Ecology, Tvistevägen 48, Department of Ecology ing the largest mammal onacontinent(fig.S1). cative nature of body size evolution and the sat- and Environmental Science, Umea University, Umea, Sweden The data show that the pattern of body size urating effects of exponentially decreasing niche SE-90187. 10Smithsonian Institution, Post Office Box 37012, 11 evolution was similar across continents, lineages, space availability at larger body sizes. MRC 121, Washington, DC 20013–7012, USA. Department and trophic groups. Globally, and on each con- We compared model fits using corrected Akaike of Ecology and Evolutionary Biology, CU Natural History Museum, Campus Box 265, University of Colorado at Boulder, tinent, maximum body mass increased rapidly information criteria (AICc). The results suggested Boulder, CO 80309–0265, USA. 12School of Biological Sci- during the early Cenozoic (Fig. 1). By the late that the random walk was not an appropriate ences, Harborne Building, University of Reading, Reading, UK. Eocene [42.9 million years ago (Ma)], maximum model (Table 1). Although a power function pro- 13 Department of Biological Sciences, 2500 University Drive body mass was three orders of magnitude larger vided a reasonable fit to the data, the fitted ex- North West, University of Calgary, Calgary, Alberta T2N 1N4, Canada. 14Department of Atmospheric, Oceanic, and Earth than at the beginning of the Cenozoic. Our results ponent g was 0.25, significantly less than the Sciences, George Mason University, Fairfax, VA, USA. are consistent with a previous analysis of North predicted value of 0.50.
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