title: The evolutionary consequences of oxygenic photosynthesis: a body size perspective.
abstract: The high concentration of molecular oxygen in Earth's atmosphere is arguably the most conspicuous and geologically important signature of life. Earth's early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0-2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O(2):CO(2). Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio-rather than mass or volume-predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.
authors.affiliation: Department of Geological and Environmental Sciences, Stanford University, 450 Serra Mall, Bldg. 320, Stanford, CA 94305, USA. jlpayne@stanford.edu
authors.forename: Jonathan L
authors.initials: JL
authors.lastname: Payne
authors.forename: Craig R
authors.initials: CR
authors.lastname: McClain
authors.forename: Alison G
authors.initials: AG
authors.lastname: Boyer
authors.forename: James H
authors.initials: JH
authors.lastname: Brown
authors.forename: Seth
authors.initials: S
authors.lastname: Finnegan
authors.forename: Michał
authors.initials: M
authors.lastname: Kowalewski
authors.forename: Richard A
authors.initials: RA
authors.lastname: Krause
authors.forename: S Kathleen
authors.initials: SK
authors.lastname: Lyons
authors.forename: Daniel W
authors.initials: DW
authors.lastname: McShea
authors.forename: Philip M
authors.initials: PM
authors.lastname: Novack-Gottshall
authors.forename: Felisa A
authors.initials: FA
authors.lastname: Smith
authors.forename: Paula
authors.initials: P
authors.lastname: Spaeth
authors.forename: Jennifer A
authors.initials: JA
authors.lastname: Stempien
authors.forename: Steve C
authors.initials: SC
authors.lastname: Wang
mesh_terms: D000332:Aerobiosis; D000693:Anaerobiosis; D000818:Animals; D001272:Atmosphere / Q000737:chemistry; D005075:Biological Evolution; D049628:Body Size / Q000235:genetics / Q000502:physiology*; D000458:Cyanobacteria / Q000254:growth & development; D055593:Geological Phenomena; D006801:Humans; D010100:Oxygen / Q000378:metabolism*; D010788:Photosynthesis / Q000235:genetics; D063245:Plant Development; D013997:Time Factors
chemical_list: D010100:Oxygen
references.citation: Nature. 2010 Jul 1;466(7302):100-4
references.pmid: 20596019
references.citation: J Exp Biol. 1996;199(Pt 9):2061-70
references.pmid: 9319971
references.citation: Science. 2004 Jan 9;303(5655):207-10
references.pmid: 14716007
references.citation: PLoS One. 2009;4(1):e3876
references.pmid: 19127286
references.citation: Am J Sci. 1989 Apr;289(4):333-61
references.pmid: 11539776
references.citation: J Exp Biol. 2005 Apr;208(Pt 7):1385-92
references.pmid: 15781898
references.citation: J Pediatr. 2000 Mar;136(3):324-9
references.pmid: 10700688
references.citation: Nature. 2007 Jan 4;445(7123):47-52
references.pmid: 17183269
references.citation: Science. 1997 Apr 4;276(5309):122-6
references.pmid: 9082983
references.citation: J Theor Biol. 2003 Mar 21;221(2):301-7
references.pmid: 12628236
references.citation: Curr Biol. 2009 Jul 28;19(14):R567-74
references.pmid: 19640495
references.citation: J Exp Biol. 2008 Nov;211(Pt 21):3409-20
references.pmid: 18931314
references.citation: Nature. 2009 Sep 10;461(7261):179-81
references.pmid: 19741692
references.citation: Biol Lett. 2008 Feb 23;4(1):106-9
references.pmid: 18029297
references.citation: Science. 1965 Feb 5;147(3658):563-75
references.pmid: 17783259
references.citation: Nature. 2004 Sep 30;431(7008):549-52
references.pmid: 15457255
references.citation: Respir Physiol Neurobiol. 2005 Feb 15;145(2-3):251-63
references.pmid: 15705540
references.citation: Tree Physiol. 2007 Mar;27(3):433-40
references.pmid: 17241985
references.citation: Respir Physiol. 1974 Jul;21(1):61-70
references.pmid: 4846939
references.citation: J Physiol. 2008 Jan 1;586(1):83-95
references.pmid: 17947307
references.citation: Science. 1993 Apr 30;260:640-6
references.pmid: 11539831
references.citation: Science. 1982 Mar 19;215(4539):1501-3
references.pmid: 17788674
references.citation: Comp Biochem Physiol A Mol Integr Physiol. 2002 Apr;131(4):713-24
references.pmid: 11897182
references.citation: Am Nat. 1993 Oct;142(4):573-84
references.pmid: 19425961
references.citation: Science. 2003 Jan 24;299(5606):558-60
references.pmid: 12543973
references.citation: Science. 1999 Jun 25;284(5423):2129-37
references.pmid: 10381872
references.citation: Science. 2001 Sep 21;293(5538):2248-51
references.pmid: 11567137
references.citation: Nature. 2009 Sep 10;461(7261):250-3
references.pmid: 19741707
references.citation: Proc Natl Acad Sci U S A. 2007 Oct 16;104(42):16576-80
references.pmid: 17913882
references.citation: Proc Natl Acad Sci U S A. 2010 Jul 20;107(29):12941-5
references.pmid: 20616006
references.citation: Integr Comp Biol. 2002 Aug;42(4):853-61
references.pmid: 21708784
references.citation: Physiol Biochem Zool. 2001 Sep-Oct;74(5):641-50
references.pmid: 11517449
references.citation: J Theor Biol. 1995 Oct 21;176(4):433-45
references.pmid: 8551742
references.citation: Plant Physiol. 1975 Jan;55(1):102-7
references.pmid: 16659010
references.citation: Nature. 2005 Dec 1;438(7068):576
references.pmid: 16319874
references.citation: Science. 1965 Apr 2;148(3666):27-35
references.pmid: 17773767
references.citation: Science. 1954 Apr 30;119(3096):606-8
references.pmid: 17777442
references.citation: Nature. 1996 Nov 7;384(6604):55-9
references.pmid: 8900275
references.citation: J Insect Physiol. 2010 May;56(5):461-9
references.pmid: 19682996
references.citation: J Appl Physiol. 1967 Mar;22(3):453-60
references.pmid: 6020227
references.citation: Nature. 2008 Oct 23;455(7216):1101-4
references.pmid: 18948954
references.citation: J Exp Zool A Comp Exp Biol. 2005 Nov 1;303(11):968-75
references.pmid: 16217805
references.citation: Science. 1999 Jan 29;283(5402):674-6
references.pmid: 9924024
references.citation: Am J Phys Anthropol. 1970 Mar;32(2):279-92
references.pmid: 5437839
references.citation: Science. 2005 Sep 30;309(5744):2202-4
references.pmid: 16195457
references.citation: Astrobiology. 2005 Jun;5(3):415-38
references.pmid: 15941384
references.citation: Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20416-20
references.pmid: 18077334
references.citation: Proc Biol Sci. 2003 Nov 7;270 Suppl 2:S166-7
references.pmid: 14667371
references.citation: Ecology. 2010 Apr;91(4):964-76
references.pmid: 20462112
references.citation: Science. 1992 May 1;256(5057):622-7
references.pmid: 1585174
references.citation: J Appl Physiol (1985). 1994 Dec;77(6):2748-52
references.pmid: 7896616
references.citation: Philos Trans R Soc Lond B Biol Sci. 2006 Jun 29;361(1470):903-15
references.pmid: 16754606
references.citation: Respir Physiol. 1981 Nov;46(2):81-8
references.pmid: 7335987
references.citation: Nature. 2006 Dec 7;444(7120):744-7
references.pmid: 17151665
references.citation: J Evol Biol. 2009 Dec;22(12):2496-504
references.pmid: 19878502
references.citation: Can J Physiol Pharmacol. 1990 Dec;68(12):1590-4
references.pmid: 2085803
references.citation: J Theor Biol. 2001 Mar 7;209(1):9-27
references.pmid: 11237567
references.citation: Nature. 2002 May 2;417(6884):70-3
references.pmid: 11986667
references.citation: Nature. 1970 Dec 5;228(5275):1003-5
references.pmid: 5482098
references.citation: Proc Biol Sci. 2010 Jul 7;277(1690):1937-46
references.pmid: 20219733
references.citation: Nature. 2010 Feb 18;463(7283):934-8
references.pmid: 20139963
references.citation: J Exp Biol. 2005 Jan;208(Pt 1):31-9
references.pmid: 15601875
references.citation: J Exp Biol. 2009 May;212(Pt 9):1237-47
references.pmid: 19376944
references.citation: Nature. 2007 Aug 30;448(7157):1033-6
references.pmid: 17728754
references.citation: Proc Natl Acad Sci U S A. 2007 Aug 7;104(32):13198-203
references.pmid: 17666530
references.citation: Endothelium. 2007 Nov-Dec;14(6):353-60
references.pmid: 18080872
references.citation: Proc Biol Sci. 2009 Mar 22;276(1659):1069-75
references.pmid: 19129117
references.citation: Curr Biol. 2007 Nov 20;17(22):R969-71
references.pmid: 18029253
references.citation: J Exp Biol. 2007 Apr;210(Pt 7):1288-96
references.pmid: 17371927
references.citation: Science. 2007 Jan 5;315(5808):92-5
references.pmid: 17158290
references.citation: Am J Respir Cell Mol Biol. 2009 May;40(5):507-10
references.pmid: 18978299
references.citation: J Exp Biol. 2004 Sep;207(Pt 20):3559-67
references.pmid: 15339952
references.citation: Respir Physiol Neurobiol. 2006 Nov;154(1-2):4-17
references.pmid: 16595193
references.citation: Proc Natl Acad Sci U S A. 2010 Jan 26;107(4):1447-51
references.pmid: 20080600
references.citation: Nature. 2006 Jun 8;441(7094):714-8
references.pmid: 16760969
references.citation: Nature. 2002 May 9;417(6885):166-70
references.pmid: 12000958
references.citation: Respir Physiol Neurobiol. 2005 May 12;147(1):105-15
references.pmid: 15848128
references.citation: Evolution. 1949 Jun;3(2):103-24
references.pmid: 18129723
references.citation: Physiol Biochem Zool. 2002 Mar-Apr;75(2):145-54
references.pmid: 12024290
references.citation: J Exp Biol. 1998 Apr;201(Pt 8):1043-50
references.pmid: 9510518
references.citation: J Exp Biol. 2000 Oct;203(Pt 20):3117-24
references.pmid: 11003822
references.citation: Biol Lett. 2007 Apr 22;3(2):165-8
references.pmid: 17272234
references.citation: Physiol Genomics. 2005 Aug 11;22(3):292-307
references.pmid: 15928208
references.citation: Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16994-9
references.pmid: 18952839
references.citation: Perspect Biol Med. 1960;4:58-71
references.pmid: 13705237
references.citation: Arch Dis Child Fetal Neonatal Ed. 2007 Sep;92(5):F372-7
references.pmid: 17329275
references.citation: Respir Physiol. 1993 May;92(2):127-38
references.pmid: 8327786
references.citation: Nature. 2008 Mar 27;452(7186):456-9
references.pmid: 18368114
references.citation: J Physiol. 2007 Dec 15;585(Pt 3):911-7
references.pmid: 17962335
references.citation: Nature. 2008 Jan 17;451(7176):277-8
references.pmid: 18202642
references.citation: Geobiology. 2010 Dec;8(5):391-402
references.pmid: 20550584
references.citation: Science. 1999 Aug 13;285(5430):1033-6
references.pmid: 10446042
references.citation: Physiol Biochem Zool. 1999 Mar-Apr;72(2):179-88
references.pmid: 10068621
references.citation: Science. 2007 Apr 27;316(5824):557-8
references.pmid: 17463279
references.citation: Ann N Y Acad Sci. 1963 Jun 29;108:451-2
references.pmid: 13966660
references.citation: Proc Natl Acad Sci U S A. 2009 Apr 21;106(16):6696-9
references.pmid: 19346469
references.citation: Respir Physiol. 1983 Apr;52(1):1-11
references.pmid: 6867500
references.citation: J Exp Zool. 1995 Sep 1;273(1):44-50
references.pmid: 7561723
references.citation: Evolution. 1973 Mar;27(1):1-26
references.pmid: 28563664
references.citation: J Exp Biol. 2005 Aug;208(Pt 15):3003-12
references.pmid: 16043604
references.citation: Physiol Plant. 2007 Oct;131(2):226-40
references.pmid: 18251894
references.citation: Science. 2005 Apr 15;308(5720):398-401
references.pmid: 15831755
references.citation: J Physiol. 2007 Jul 15;582(Pt 2):883-95
references.pmid: 17510190
references.citation: Science. 1987 Jul 3;237:70-3
references.pmid: 11539686
references.citation: Evolution. 1994 Dec;48(6):1747-1763
references.pmid: 28565153
references.citation: Proc Natl Acad Sci U S A. 2005 Jun 21;102(25):8927-32
references.pmid: 15956194
references.citation: Am J Physiol. 1981 Jan;240(1):R3-9
references.pmid: 6257122
references.citation: Science. 1996 May 24;272(5265):1155-8
references.pmid: 8662450
references.citation: Science. 2008 Aug 29;321(5893):1197-200
references.pmid: 18755974
references.citation: Plant Physiol. 1988 Jun;87(2):346-50
references.pmid: 16666145
references.citation: J Appl Physiol. 1974 Sep;37(3):362-6
references.pmid: 4414528
references.citation: Proc Natl Acad Sci U S A. 2009 Jan 6;106(1):24-7
references.pmid: 19106296
references.citation: J Exp Biol. 2004 Jan;207(Pt 3):497-508
references.pmid: 14691097