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The Early Evolution of the Tetrapod Humerus

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The Early Evolution of the Tetrapod Humerus R EPORTS seafloor anoxia during the mid-Proterozoic oxides on the seafloor. Hence, ␦97/95Mo in crusts and portionality constants that parameterize the par- was expanded compared to today during at nodules is probably representative of ␦97/95Mo in Mn titioning of Mo between water and sediment (i.e., ϳ oxide–associated Mo. these constants parameterize diffusion coeffi- least two intervals separated by 300 million 29. J. Barling, A. D. Anbar, Earth Planet. Sci. Lett. 217, 315 cients, sedimentation rates, chemical partition ␦97/95 ϭ years. The Mo data are consistent with (2004). functions, etc.). Hence, fox/feux kox/keux • Aox/ globally extensive seafloor anoxia persisting 30. G. R. Helz et al., Geochim. Cosmochim. Acta 60, 3631 Aeux.Ifkox and keux are constant, then variations in f /f can be directly related to variations in after oxygenation of the atmosphere ϳ2.3 (1996). ox eux 31. J. W. Murray, Z. Top, E. Ozsoy, Deep-Sea Res. 38, Aox/Aeux. The assumption of constant kox and keux Ga. The identification of mid-Proterozoic Mn S663 (1991). is simplistic, but useful for schematic purposes. 97/95 ϩ ϭ oxides with a ␦ Mo value ϳ2‰ lighter 32. I. H. Crick, C. J. Boreham, A. C. Cook, T. G Powell, Am. 40. Although fox feux 1, it is not necessarily the case that A ϩ A ϭ constant. Hence a change than in coeval euxinic sediments would Assoc. Petrol. Geol. Bull. 72, 1495 (1988). ox eux 33. T. H. Donnelly, M. J. Jackson, Sediment. Geol. 58, 145 in Aox need not be complemented by a change in strengthen these arguments. Nevertheless, the (1988). Aeux (and vice versa). This difference arises because full impact of nearly a billion years of ocean 34. D. E. Canfield, T. W. Lyons, R. Raiswell, Am. J. Sci. 296, a change in Aox or Aeux can be compensated by a anoxia on Proterozoic ecosystems and biogeo- 818 (1996). change in the areal extent of suboxic seafloor, 35. The use of basinal Mo concentrations to infer global whereas the Mo mass balance model assumes that chemical cycles must be seriously considered. ocean Mo concentrations is not straightforward, as suboxic sediments are a negligible sink for Mo. evidenced by the nearly 10-fold difference in Mo 41. H. D. Klemme, G. F. Ulmishek, Am. Assoc. Petrol. concentrations between euxinic sediments in the Geol. Bull. 75, 1809 (1991). References and Notes Cariaco Basin and Black Sea. Local effects specific to 42. We thank Y. Shen, J. Brocks, A. H. Knoll, and H. D. 1. A. H. Knoll, in Origin and Early Evolution of the the depositional setting presumably dominate. Holland for providing samples of Proterozoic black Metazoa, J. H. Lipps, P. W. Signor, Eds. (Plenum, New Hence, Mo concentrations in sediments cannot easily shales, and G. Ravizza for Black Sea samples. F. York, 1992), p. 53. be used alone to draw inferences about global ocean Ramos, G. Williams, and S. Weyer assisted with sam- 2. A. D. Anbar, A. H. Knoll, Science 297, 1137 (2002). redox conditions. ple analysis. Supported by NSF (EAR 0106712 and 3. D. J. Des Marais et al., Astrobiology 2, 153 (2002). 36. These figures are obtained using the following values: 0230183)and NASA (Exobiology program and the 4. H. D. Holland, The Chemical Evolution of the Atmo- ␦97/95 ϭϪ ⌬ ϭ ␦97/95 ϭ Moin 0.01; sw-ox 1.8; Moeux Astrobiology Institute). sphere and Oceans (Princeton Univ. Press, Princeton, 0.54. NJ, 1984). ␦97/95 37. Moeux of the mid-Proterozoic samples ranges Supporting Online Material 5. H. D. Holland, Geochem. News 100, 20 (1999). from 0.31 to 0.67‰; correspondingly, the euxinic www.sciencemag.org/cgi/content/full/1091785/DC1 6. J. Farquhar, H. Bao, M. H. Thiemens, Science 289, 756 sink could range from 82 to 62%. Materials and Methods (2000). 38. A. D. Anbar, in Geochemistry of Non-Traditional Iso- SOM Text 7. D. E. Canfield, A. Teske, Nature 382, 127 (1996). topes, C. Johnson, B. Beard, F. Albarede, Eds. (Miner- Fig. S1 8. D. E. Canfield, Nature 396, 450 (1998). alogical Society of America, Washington, DC, 2004), Tables S1 and S2 9. D. E. Canfield, R. Raiswell, Am. J. Sci. 299, 697 (1999). pp. 429–454. References and Notes 10. A. A. Pavlov, M. T. Hurtgen, J. F. Kasting, M. A. Arthur, 39. As an illustrative model, assume that f ϭ Geology 31, 87 (2003). ϭ ox kox • Aox • [Mo]sw and feux keux • Aeux • [Mo]sw, 23 September 2003; accepted 24 February 2004 11. A. J. Kaufman, S. Xiao, Nature 425, 279 (2003). where [Mo] is the concentration of Mo in the Published online 4 March 2004; 12. Y. Shen, D. E. Canfield, A. H. Knoll, Am. J. Sci. 302,81 sw oceans, Aox and Aeux are the areas of oxic and 10.1126/science.1091785 (2002). euxinic sedimentation, and k and k are pro- Include this information when citing this paper. 13. Y. Shen, A. H. Knoll, M. R. Walter, Nature 423, 632 ox eux (2003). 14. L. C. Kah, T. W. Lyons, J. T. Chesley, Precambrian Res. 111, 203 (2001). 15. S. R. Emerson, S. S. Huested, Mar. Chem. 34, 177 The Early Evolution of the (1991). 16. B. E. Erickson, G. R. Helz, Geochim. Cosmochim. Acta 64, 1149 (2000). Tetrapod Humerus 17. Y. Zheng, R. F. Anderson, A. van Geen, J. Kuwabara, Geochim. Cosmochim. Acta 64, 4165 (2000). 1 2 1 18. J. L. Morford, S. Emerson, Geochim. Cosmochim. Acta Neil H. Shubin, * Edward B. Daeschler, Michael I. Coates 63, 1735 (1999). 19. K. K. Bertine, K. K Turekian, Geochim. Cosmochim. A tetrapod humerus from the Late Devonian of Pennsylvania has a novel mix Acta 37, 1415 (1973). 20. J. McManus, T. F. Nagler, C. Siebert, C. G. Wheat, D. E. of primitive and derived characters. A comparative analysis of this fossil and Hammond, Geochem. Geophys. Geosyst. 3, 10.1029/ other relevant humeri from the Devonian shows that the role of the limb in 2002GC000356 (2002). propping the body arose first in fish fins, not tetrapod limbs. The functional 21. Data are reported using the ␦ notation, relative to a Mo standard (Johnson Matthey Chemical, Specpure diversity of the earliest known limbs includes several different kinds of ap- lot #702499I)where pendage design. This functional diversity was achieved with a humeral archi- 97Mo/95Mo tecture that was remarkably conserved during the Devonian. ␦97/95 ϭ ͩ sample ͪ ϫ Mo 97 95 –1 1000 Mo/ Mostandard 22. J. Barling, G. L. Arnold, A. D. Anbar, Earth Planet. Sci. The evolution of limbed vertebrates from adaptations, including flipper-like append- Lett. 193, 447 (2001). lobe-finned fish is one of the key transitions ages, internal gills, and a broad finned tail. 23. C. Siebert, T. F. Nagler, F. von Blanckenburg, J. D. in the history of life. The origin of the tetra- Unfortunately, our limited ability to make Kramers, Earth Planet. Sci. Lett. 211, 159 (2003). 24. Values reported in text are the mean Ϯ 2 SD for all pod body plan has classically been associated comparisons between homologous features in analyses of each sample grouping, unless otherwise with the invasion of land; accordingly, limbs the humeri of basal tetrapods and their closest noted. were seen to have arisen to support and move fish relatives has hampered our understand- 25. Details of materials, methods, sample descriptions, and alternative hypotheses are available as support- the body in a terrestrial habitat (1, 2). In ing of the fin-limb transition. Theories about ing material on Science Online. recent years this view has changed with new the origin of tetrapod limbs have relied main- 26. Molybdenite ores are assumed to consist of Mo ex- descriptions of Devonian forms, such as Ac- ly on comparisons of humeri of Carbonifer- tracted by hydrothermal processes from surrounding anthostega (3, 4). Although clearly a tetrap- ous and Permian tetrapods with that of Eus- crustal rocks, and hence are a rough proxy for crustal Mo. od, Acanthostega retains a variety of aquatic thenopteron (5), a well-known Devonian 27. Siebert et al.(23)found no Mo isotope fractionation lobe-finned fish. In recent years, these tem- during mild acid leaching of Mo from granite and poral and anatomical gaps have narrowed, basalt. Therefore, it is reasonable to hypothesize that 1 Department of Organismal Biology and Anatomy, with new descriptions of limbs of the basal Mo released during crustal weathering is isotopically University of Chicago, Chicago, IL 60637, USA. 2Acad- similar to Mo in granite, basalt, and molybdenite. emy of Natural Sciences, 1900 Benjamin Franklin tetrapods Acanthostega (3, 6), Ichthyostega 28. Although ferromanganese crusts and nodules them- Parkway, Philadelphia, PA 19103, USA. (7), and Tulerpeton (8) and emerging details selves are not major sinks for Mo, a correlation of Mo and Mn is observed in pelagic sediments (19). This *To whom correspondence should be addressed. E- of the pectoral fin in Panderichthys (9, 10), presumably reflects coprecipitation of Mo with Mn mail: [email protected] the most crownward fish on the tetrapod stem 90 2 APRIL 2004 VOL 304 SCIENCE www.sciencemag.org R EPORTS lineage. Here we describe a tetrapod humerus Panderichthyids and the most basal tetra- osteolepid, and rhizodontid fish (4, 5), be- that provides the basis for new interpretations pods underwent a reorganization of the upper comes anteroposteriorly elongate and dorso- of structural and functional stages in the ori- limb in the Late Devonian. Compared to out- ventrally flattened in Panderichthys, Acan- gin of the tetrapod limb. groups, Panderichthys, ANSP 21350, and thostega, and ANSP 21350. In the shoulder, The new humerus, ANSP 21350, (Fig.
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