Near-Stasis in the Long-Term Diversification of Mesozoic Tetrapods

PLoS Biology

Volumn 14, Issue 1, 2016, Pages

  Benson, Roger B J ^a   Butler, Richard J ^b   Alroy, John ^c   Mannion, Philip D ^d   Carrano, Matthew T ^e   Lloyd, Graeme T ^c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c MACQUARIE UNIVERSITY   (Australia)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e SMITHSONIAN INSTITUTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIBIA; CLADISTICS; CRETACEOUS; DINOSAUR; DISEASE MODEL; ECOSYSTEM; FOSSIL; MAMMAL; MASS EXTINCTION; MESOZOIC; MODEL; MOLECULAR PHYLOGENY; PALEOGENE; QUANTITATIVE STUDY; RADIATION; SPECIES DIFFERENTIATION; SPECIES DIVERSITY; SPECIES RICHNESS; SQUAMATE; STANDARDIZATION; ANIMAL; BIODIVERSITY; EVOLUTION; THEORETICAL MODEL; VERTEBRATE;

ANIMALS; BIODIVERSITY; BIOLOGICAL EVOLUTION; FOSSILS; MODELS, THEORETICAL; VERTEBRATES;

EID: 84961290140     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002359     Document Type: Article

References (100)

1. Alfaro ME, Santini ME, Brock C, Alamillo H, Dornburg A, Rabosky DL, et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc Natl Acad Sci USA. 2009;106: 13410–13414. doi: 10.1073/pnas.0811087106 19633192
2. Benton MJ, The origins of modern biodiversity on land. Phil Trans Roy Soc Lond B. 2010;365: 3667–3679.
3. Roelants K, Gower DJ, Wilkinson M, Loader S, Biju SD, Guillaume K, et al. Global patterns of diversification in the history of modern amphibians. Proc Natl Acad Sci USA. 2007;104: 887–892. 17213318
4. Brown JW, Rest JS, García-Moreno J, Sorenson MD, Mindell DP, Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. BMC Biol. 2008;6: e6.
5. Meredith RW, Janečka JE, Gatesy J, Ryder OA, Fisher CA, Teeling EC, et al. Impacts of the Cretaceous Terrestrial Revolution and KPg extinction on mammal diversification. Science. 2011;334: 521–524. doi: 10.1126/science.1211028 21940861
6. Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO, The global diversity of birds in space and time. Nature. 2012;491: 444–448. doi: 10.1038/nature11631 23123857
7. Jones MEH, Anderson CL, Hipsley CA, Müller J, Evans SE, Schoch RR, Intergration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara). BMC Evol Biol. 2013;13: e208.
8. O’Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, et al. The placental mammal ancestor and the post—K-Pg radiation of placentals. Science. 2013;339: 662–667.
9. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science. 2014;346: 1320–1331. doi: 10.1126/science.1253451 25504713
10. Benton MJ, The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science. 2009;323: 728–732. doi: 10.1126/science.1157719 19197051
11. Vermeij GJ, Grosberg RK, The great divergence: when did diversity on land exceed that in the sea? Integr Comp Biol. 2010;50: 675–682. doi: 10.1093/icb/icq078 21558232
12. Benton MJ, Mass extinction among non-marine tetrapods. Nature. 1985;316: 811–814.
13. Benton MJ, Diversification and Extinction in the history of life. Science. 1995;268: 52–58. 7701342
14. Kalmar A, Currie DJ, The completeness of the continental fossil record and its impact on patterns of diversification. Paleobiology. 2010;36: 51–60.
15. Sepkoski JJ, JrA kinetic model of Phanerozoic taxonomic diversity I. Analysis of marine orders. Paleobiology. 1978;4: 223–251.
16. Foote M, Origination and extinction components of taxonomic diversity: Paleozoic and post-Paleozoic dynamics. Paleobiology. 2000;26: 578–605.
17. Alroy J, Dynamics of origination and extinction in the marine fossil record. Proc Natl Acad Sci USA. 2008;105: 11536–11542.
18. Alroy J, The shifting balance of diversity among major marine animal groups. Science. 2010;329: 1191–1194. doi: 10.1126/science.1189910 20813951
19. Raup DM, Taxonomic diversity during the Phanerozoic. Science. 1972;177: 1065–1071. 17840596
20. Ezard THG, Aze T, Pearson PN, Purvis A, Interplay between changing climate and species’ ecology drives macroevolutionary dynamics. Science. 2011;332: 349–351. doi: 10.1126/science.1203060 21493859
21. Etienne RS, Haegeman B, Stadler T, Aze T, Pearson PN, Purvis A, et al. Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record. Proc Roy Soc B. 2012;279: 1300–1309.
22. Alroy J, Butlin RK, Bridle JR, Schluter D, Speciation and extinction in the fossil record of North American mammals. In: Speciation and Patterns of Diversity. Cambridge: Cambridge University Press; 2009. pp. 301–323.
23. Quental TB, Marshall CR, How the Red Queen drives terrestrial mammals to extinction. Science. 2013;341: 290–292. doi: 10.1126/science.1239431 23788731
24. Liow LH, Finarelli JA, A dynamic global equilibrium in carnivoran diversification over 20 million years. Proc Roy Soc B. 2014;281: e20132312.
25. Silvestro D, Antonelli A, Salamin N, Quental TB, The role of clade competition in the diversification of North American canids. Proc Natl Acad Sci USA. 2015;112: 8684–8689. doi: 10.1073/pnas.1502803112 26124128
26. MacArthur RH, Wilson EO, The Theory of Island Biogeography. Princeton: Princeton University Press; 1967.
27. Sepkoski JJ, JrA kinetic model of Phanerozoic taxonomic diversity. III. Post-Paleozoic families and mass extinctions. Paleobiology. 1984;10: 246–267.
28. Rabosky DL, Hurlbert AH, Species richness at continental scales is dominated by ecological limits. Amer Nat. 2015;185: 572–583.
29. Rabosky DL, Diversity-dependence, ecological speciation, and the role of competition in macroevolution. Annu Rev Ecol Syst. 2013;44: 481–502.
30. Valentine JW, Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time. Paleontology. 1969;12: 684–709.
31. Walker TD, Valentine JW, Equilibrium models of evolutionary species diversity and the number of empty niches. Amer Nat. 1984;124: 887–899.
32. Harmon LJ, Harrison S, Species diversity is dynamic and unbounded at local and continental scales. Amer Nat. 2015;185: 584–593.
33. Marshall CR, Marine biodiversity dynamics over deep time. Science. 2010;329: 1156–1157. doi: 10.1126/science.1194924 20813942
34. Costello MJ, May RM, Stork NE, Can we name Earth’s species before they go extinct? Science. 2013;339: 413–416. doi: 10.1126/science.1230318 23349283
35. May RM, Biological diversity: differences between land and sea. Phil Trans Roy Soc Lond B. 1994;343: 105–111.
36. Mora C, Tittensor DP, Adl S, Simpson AGB, Worm B, How many species are there on Earth and in the ocean? PLoS Biol. 2011;9(8): e1001127. doi: 10.1371/journal.pbio.1001127 21886479
37. Benton MJ, Emerson BC, How did life become so diverse? The dynamics of diversification according to the fossil record and molecular phylogenetics. Palaeontology. 2007;50: 23–40.
38. Sahney S, Benton MJ, Ferry PA, Links between global taxonomic diversity, ecological diversity and the expansion of vertebrates on land. Biol Lett. 2010;6: 544–547. doi: 10.1098/rsbl.2009.1024 20106856
39. Smith AB, Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies. Phil Trans Roy Soc Lond B. 2001;356: 351–367.
40. Smith AB, Marine diversity through the Phanerozoic: problems and prospects. J Geol Soc Lond. 2007;164: 731–745.
41. Alroy J, Aberhan M, Bottjer DJ, Foote M, Fürsich FT, Harries PJ, et al. Phanerozoic trends in the global diversity of marine invertebrates. Science. 2008;321: 97–100. doi: 10.1126/science.1156963 18599780
42. Signor PW, IIILipps JH, Sampling bias, gradual extinction patterns and catastrophes in the fossil record. Spec Pap Geol Soc Amer. 1982;190: 291–296.
43. Wagner PJ, The quality of the fossil record and the accuracy of phylogenetic inferences about sampling and diversity. Syst Biol. 2000;49: 65–86. 12116484
44. Smith AB, Systematics and the Fossil Record. Oxford: Wiley-Blackwell; 1994.
45. Stadler T, Rabosky DL, Ricklefs RE, Bokma F, On age and species richness of higher taxa. Amer Nat. 2014;184: 447–455.
46. Alroy J, Geographical, environmental and intrinsic biotic controls on Phanerozoic marine diversification. Palaeontology. 2010;53: 1121–1235.
47. Carrano MT, Alroy J, Butler RJ, Mannion P, Benson RBJ, Rees AM, et al. Taxonomic occurrences of Mesozoic to Ypresian Tetrapoda recorded in Fossilworks, the Evolution of Terrestrial Ecosystems database, the Paleobiology Database, and the Paleogeographic Atlas Project database; 2015. http://fossilworks.org.
48. Benson RBJ, Butler RJ, Alroy J, Mannion PD, Carrano MT, Lloyd GT, Data from: Near-stasis in the long-term diversification of Mesozoic tetrapods; 2016. Dryad Digital Repository. Openly available via http://doi.org/10.5061/dryad.9fr76.
49. Signor PW, Valentine J, Real and apparent trends in species richness through time. In: Phanerozoic Diversity Patterns. Princeton: Princeton University Press; 1985. pp. 129–150.
50. Benton MJ, Models for the diversification of life. Trends Ecol Evol. 1997;12: 490–495. 21238171
51. Nagelkerke MJD, A note on the general definition of the coefficient of determination. Biometrika. 1991;78: 691–692.
52. Bush AM, Markey MJ, Marshall CR, Removing bias from diversity curves: the effects of spatially organized biodiversity on sampling-standardization. Paleobiology. 2004;30: 666–686.
53. Vilhena DA, Smith AB, Spatial bias in the marine fossil record. PLoS ONE. 2013;8(10): e74470. doi: 10.1371/journal.pone.0074470 24204570
54. Barnosky AD, Carrasco MA, Davis EB, The impact of the species-area relationship on estimates of paleodiversity. PLoS Biol. 2005;3(8): e266. 16004509
55. Peters SE, Geologic constraints on the macroevolutionary history of marine animals. Proc Natl Acad Sci USA. 2005;102: 12326–12331. 16105949
56. Burnham KP, Anderson D, Model Selection and Multimodel Inference. 2nd Edition. New York: Springer; 2002.
57. Freckleton RP, Watkinson AR, Green RE, Sutherland WJ, Census error and the detection of diversity dependence. J Animal Ecol. 2006;75: 837–851.
58. Clack JA, Gaining Ground. Bloomington: Indiana University Press; 2012.
59. Benson RBJ, Upchurch P, Diversity trends in the establishment of terrestrial vertebrate ecosystems: interactions between spatial and temporal sampling biases. Geology. 2013;41: 43–46.
60. Irmis RB, Whiteside JH, Delayed recovery of non-marine tetrapods after the end-Permian mass extinction tracks global carbon cycle. Proc Roy Soc B. 2011;279: 1310–1318.
61. Raup DM, Mathematical models of cladogenesis. Paleobiology. 1985;11: 42–52.
62. Alroy J, The fossil record of North American mammals: evidence for a Paleocene evolutionary radiation. Syst Biol. 1999;48: 107–118. 12078635
63. Clemens WA, Evolution of the mammalian fauna across the Cretaceous–Tertiary boundary in northeastern Montana and other areas of the Western Interior. Spec Pap Geol Soc Amer. 2002;361: 217–245.
64. Longrich NR, Bhullar B- A, Gauthier JA, Mass extinction of lizards and snakes at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci USA. 2012;109: 21396–21401. doi: 10.1073/pnas.1211526110 23236177
65. Nicholson DB, Holroyd PA, Benson RBJ, Barrett PM, Climate mediated diversification of turtles in the time of dinosaurs. Nature Commun. 2015;6: e7848.
66. Fiorillo AR, Padian K, Musikasinthorn C, Taphonomy and depositional setting of the Placerias Quarry (Chinle Formation: Late Triassic, Arizona). Palaios. 2000;15: 373–386.
67. Carrano MT, Velez-Juarbe J, Paleoecology of the Quarry 9 vertebrate assemblage from Como Bluff, Wyoming (Morrison Formation, Late Jurassic). Palaeogeogr Palaeoclimatol Palaeoecol; 2006;234: 147–159.
68. Martin T, Krebs B, Guimarota: a Jurassic ecosystem. Munich: Verlag Dr Friedrich Pfeil; 2000.
69. Estes R, Fossil vertebrates from the Late Cretaceous Lance Formation, eastern Wyoming. Univ Calif Publ Geol Sci. 1964;49: 1–180.
70. Cornell HV, Is regional species diversity bounded or unbounded? Biol Rev. 2013;88: 140–165. doi: 10.1111/j.1469-185X.2012.00245.x 22958676
71. Quental TB, Marshall CR, Diversity dynamics: molecular phylogenies need the fossil record. Trends Ecol Evol. 2010;25: 434–441. doi: 10.1016/j.tree.2010.05.002 20646780
72. Fritz SA, Schnitzler J, Eronen JT, Hof C, Böhning-Gaese K, Graham CH, Diversity in time and space: wanted dead and alive. Trends Ecol Evol. 2013;28: 509–516. doi: 10.1016/j.tree.2013.05.004 23726658
73. Foote M, Symmetrical waxing and waning of marine invertebrate genera. Paleobiology. 2007;33: 2745–2752.
74. Liow LH, Stenseth NC, The rise and fall of species: implications for macroevolutionary and macroecological studies. Proc Roy Soc B. 2007; 274: 2745–2752.
75. Miller AI, Sepkoski JJ, JrBivalve diversification: the effect of interaction on a macroevolutionary system. Paleobiology. 1988;14: 364–369. 11542146
76. Sepkoski JJ, JrWalliser OH, Patterns of Phanerozoic extinction: a perspective from global data bases. In: Global Events and Event Stratigraphy. Heidelberg: Springer; 1996. pp. 35–51.
77. Vrba ES, Environment and evolution: alternative causes of the temporal distribution of evolutionary events. S Afr J Sci. 1985;81: 229–236.
78. Moen D, Morlon H, Why does diversification slow down? Trends Ecol Evol. 2014;29: 190–197. doi: 10.1016/j.tree.2014.01.010 24612774
79. Linnert C, Robinson SA, Lees JA, Bown PR, Pérez-Rodríguez I, Petrizzo MR, et al. Evidence for global cooling in the Late Cretaceous. Nature Commun. 2014;5: 4194.
80. Olsen PE, Kent DV, Milankovitch climate forcing in the tropics of Pangaea during the Late Triassic. Palaeogeogr Palaeoclimatol Palaeoecol. 1996;122: 1–26.
81. Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz ME, et al. The Phanerozoic record of sea level change. Science. 2005;310: 1293–1298. 16311326
82. Fielding CR, Frank TD, Birgenheier LP, Rygel MC, Jones AT, Stratigraphic imprint of the Late Paleozoic Ice Age in eastern Australia: a record of alternating glacial and nonglacial climate regimes. J Geol Soc Lond. 2008;165: 129–140.
83. Alvarez LW, Experimental evidence that an asteroid impact led to the extinction of many species 65 million years ago. Proc Natl Acad Sci USA. 1983;80: 627–642. 16593274
84. Knoll AH, Diamond J, Case TJ, Patterns of change in plant communities through geological times. In: Community Ecology. New York: Harper & Row; 1986. pp. 126–143.
85. Lidgard S, Crane PR, Angiosperm diversification and Cretaceous floristic trends: a comparison of palynofloras and leaf macrofloras. Paleobiology. 1990;16: 77–93.
86. Nicholson DB, Ross AJ, Mayhew PJ, Fossil evidence for key innovations in the evolution of insect diversity. Proc Roy Soc B. 2014;281: e20141823.
87. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA, Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proc Roy Soc B. 2009;276: 1771–1776.
88. Brodribb TJ, Feild TS, Leaf hydraulic vein evolution lead to a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett. 2010;13: 175–183. doi: 10.1111/j.1461-0248.2009.01410.x 19968696
89. Erwin DH, Novelties that change carrying capacity. J Exp Zool (Mol Dev Evol). 2011;318: 460–465.
90. O'Connor J, Chiappe LM, Bell A, Dyke G, Kaiser G, Pre-modern birds: avian divergences in the Mesozoic. In: Living Dinosaurs: The Evolutionary History of Modern Birds. Oxford: Wiley; 2011. pp. 39–114.
91. Benson RBJ, Choiniere JN, Rates of dinosaur limb evolution provide evidence for exceptional radiation in Mesozoic birds. Proc Roy Soc B. 2013;280: e20131780.
92. Alroy J, Accurate and precise estimates of origination and extinction rates. Paleobiology. 2014;40: 374–397.
93. Butler RJ, Barrett PM, Nowbath S, Upchurch P, Estimating the effects of sampling biases on pterosaur diversity patterns: implications for hypotheses of bird/pterosaur competitive replacement. Paleobiology. 2009;35: 432–446.
94. Eiting TP, Gunnell GF, Global completeness of the bat fossil record. Journal of Mammalian Evolution. 2009;16: 151–173.
95. Brocklehurst N, Upchurch P, Mannion PD, O’Connor J, The completeness of the fossil record of Mesozoic birds: implications for early avian evolution. PLoS ONE. 2012;7(6): e39056. doi: 10.1371/journal.pone.0039056 22761723
96. Zhou ZH, Wang Y, Vertebrate diversity of the Jehol Biota as compared with other Lagerstätten. Sci China, Earth Sci 2010;53: 1894–1907.
97. R Core TeamR: a language and environment for statistical computing; 2013. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
98. Venables WN, Ripley BD, Modern Applied Statistics with S. 4th Edition. Springer: New York; 2002.
99. Canty A, Ripley B. boot: Bootstrap R (S-Plus) Functions; 2013. R package version 1.3–9.
100. Ives AR, For testing the significance of regression coefficients, go ahead and log-transform count data. Methods Ecol Evol. 2015;6: 828–835.