1932

Abstract

During the past 541 million years, marine animals underwent three intervals of diversification (early Cambrian, Ordovician, Cretaceous–Cenozoic) separated by nondirectional fluctuation, suggesting diversity-dependent dynamics with the equilibrium diversity shifting through time. Changes in factors such as shallow-marine habitat area and climate appear to have modulated the nondirectional fluctuations. Directional increases in diversity are best explained by evolutionary innovations in marine animals and primary producers coupled with stepwise increases in the availability of food and oxygen. Increasing intensity of biotic interactions such as predation and disturbance may have led to positive feedbacks on diversification as ecosystems became more complex. Important areas for further research include improving the geographic coverage and temporal resolution of paleontological data sets, as well as deepening our understanding of Earth system evolution and the physiological and ecological traits that modulated organismal responses to environmental change.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-012021-035131
2021-11-03
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/52/1/annurev-ecolsys-012021-035131.html?itemId=/content/journals/10.1146/annurev-ecolsys-012021-035131&mimeType=html&fmt=ahah

Literature Cited

  1. Alroy J. 2004. Are Sepkoski's evolutionary faunas dynamically coherent?. Evol. Ecol. Res. 6:1–32
    [Google Scholar]
  2. Alroy J. 2008. Dynamics of origination and extinction in the fossil record. PNAS 105:11536–42
    [Google Scholar]
  3. Alroy J. 2010. The shifting balance of diversity among major marine animal groups. Science 329:1191–94
    [Google Scholar]
  4. Alroy J. 2020. On four measures of taxonomic richness. Paleobiology 46:158–75
    [Google Scholar]
  5. Alroy J, Marshall CR, Bambach RK, Bezusko K, Foote M et al. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversification. PNAS 98:6261–66
    [Google Scholar]
  6. Bachan A, Lau KV, Saltzman MR, Thomas E, Kump LR, Payne JL 2017. A model for the decrease in amplitude of carbon isotope excursions across the Phanerozoic. Am. J. Sci. 317:641–76
    [Google Scholar]
  7. Bambach RK. 1993. Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology 19:372–97
    [Google Scholar]
  8. Bambach RK. 1999. Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131–44
    [Google Scholar]
  9. Bambach RK. 2006. Phanerozoic biodiversity mass extinctions. Annu. Rev. Earth Planet. Sci. 34:127–55
    [Google Scholar]
  10. Benton MJ. 1995. Diversification and extinction in the history of life. Science 268:52–58
    [Google Scholar]
  11. Boyce CK, Lee J-E. 2011. Could land plant evolution have fed the marine revolution?. Paleontol. Res. 15:100–5
    [Google Scholar]
  12. Buatois LA, Mángano MG. 2018. The other biodiversity record: innovations in animal-substrate interactions through geologic time. GSA Today 28:4–10
    [Google Scholar]
  13. Bush AM, Bambach RK. 2004. Did alpha diversity increase through the Phanerozoic? Lifting the veils of taphonomic, latitudinal, and environmental biases. J. Geol. 112:625–42
    [Google Scholar]
  14. Bush AM, Bambach RK. 2011. Paleoecologic megatrends in marine Metazoa. Annu. Rev. Earth Planet. Sci. 39:241–69
    [Google Scholar]
  15. Bush AM, Bambach RK. 2015. Sustained Mesozoic–Cenozoic diversification of marine Metazoa: a consistent signal from the fossil record. Geology 43:979–82
    [Google Scholar]
  16. Bush AM, Hunt G, Bambach RK. 2016. Sex and the shifting biodiversity dynamics of marine animals in deep time. PNAS 113:14073–78
    [Google Scholar]
  17. Bush AM, Wang SC, Payne JL, Heim NA. 2020. A framework for the integrated analysis of the magnitude, selectivity, and biotic effects of extinction and origination. Paleobiology 46:1–22
    [Google Scholar]
  18. Calosi P, Putnam HM, Twitchett RJ, Vermandele F. 2019. Marine metazoan modern mass extinction: improving predictions by integrating fossil, modern, and physiological data. Annu. Rev. Mar. Sci. 11:369–90
    [Google Scholar]
  19. Carrillo JD, Faurby S, Silvestro D, Zizka A, Jaramillo C et al. 2020. Disproportionate extinction of South American mammals drove the asymmetry of the Great American Biotic Interchange. PNAS 117:26281–87
    [Google Scholar]
  20. Chamberlin TC. 1909. Diastrophism as the ultimate basis of correlation. J. Geol. 17:685–93
    [Google Scholar]
  21. Cherns L, Wright VP. 2009. Quantifying the impacts of early diagenetic aragonite dissolution on the fossil record. Palaios 24:756–71
    [Google Scholar]
  22. Clapham ME. 2017. Organism activity levels predict marine invertebrate survival during ancient global change extinctions. Glob. Change Biol. 23:1477–85
    [Google Scholar]
  23. Clapham ME, Renne PR. 2019. Flood basalts and mass extinctions. Annu. Rev. Earth Planet. Sci. 47:275–303
    [Google Scholar]
  24. Close RA, Benson RB, Alroy J, Carrano MT, Cleary TJ et al. 2020a. The apparent exponential radiation of Phanerozoic land vertebrates is an artefact of spatial sampling biases. Proc. R. Soc. B 287:20200372
    [Google Scholar]
  25. Close RA, Benson RB, Saupe E, Clapham M, Butler R. 2020b. The spatial structure of Phanerozoic marine animal diversity. Science 368:420–24
    [Google Scholar]
  26. Cole DB, Mills DB, Erwin DH, Sperling EA, Porter SM et al. 2020. On the co-evolution of surface oxygen levels and animals. Geobiology 18:260–81
    [Google Scholar]
  27. Cooper RA, Sadler PM, Munnecke A, Crampton JS 2014. Graptoloid evolutionary rates track Ordovician–Silurian global climate change. Geol. Mag. 151:349–64
    [Google Scholar]
  28. D'Antonio MP, Ibarra DE, Boyce CK 2020. Land plant evolution decreased, rather than increased, weathering rates. Geology 48:29–33
    [Google Scholar]
  29. Doughty CE, Roman J, Faurby S, Wolf A, Haque A et al. 2016. Global nutrient transport in a world of giants. PNAS 113:868–73
    [Google Scholar]
  30. Edwards CT, Saltzman MR, Royer DL, Fike DA. 2017. Oxygenation as a driver of the Great Ordovician Biodiversification Event. Nat. Geosci. 10:925–29
    [Google Scholar]
  31. Eichenseer K, Balthasar U, Smart CW, Stander J, Haaga KA, Kiessling W. 2019. Jurassic shift from abiotic to biotic control on marine ecological success. Nat. Geosci. 12:638–42
    [Google Scholar]
  32. Erwin DH. 2008. Macroevolution of ecosystem engineering, niche construction and diversity. Trends Ecol. Evol. 23:304–10
    [Google Scholar]
  33. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA et al. 2004. The evolution of modern eukaryotic phytoplankton. Science 305:354–60
    [Google Scholar]
  34. Fan J-X, Shen S-Z, Erwin DH, Sadler PM, MacLeod N et al. 2020. A high-resolution summary of Cambrian to Early Triassic marine invertebrate biodiversity. Science 367:272–77
    [Google Scholar]
  35. Finnegan S, Bergmann K, Eiler JM, Jones DS, Fike DA et al. 2011a. The magnitude and duration of Late Ordovician–Early Silurian glaciation. Science 331:903–6
    [Google Scholar]
  36. Finnegan S, McClain CR, Kosnik MA, Payne JL. 2011b. Escargots through time: an energetic comparison of marine gastropod assemblages before and after the Mesozoic Marine Revolution. Paleobiology 37:252–69
    [Google Scholar]
  37. Foote M 2010. The geological history of biodiversity. Evolution Since Darwin: The First 150 Years MA Bell, DJ Futuyma, WF Eanes, JS Levinton 479–510 Sunderland, MA: Sinauer
    [Google Scholar]
  38. Hannisdal B, Peters SE. 2011. Phanerozoic Earth system evolution and marine biodiversity. Science 334:1121–24
    [Google Scholar]
  39. Harmon LJ, Harrison S. 2015. Species diversity is dynamic and unbounded at local and continental scales. Am. Nat. 185:584–93
    [Google Scholar]
  40. Heim NA, Knope ML, Schaal EK, Wang SC, Payne JL 2015. Cope's rule in the evolution of marine animals. Science 347:867–70
    [Google Scholar]
  41. Hillebrand H. 2004. On the generality of the latitudinal diversity gradient. Am. Nat. 163:192–211
    [Google Scholar]
  42. Hofmann R, Tietje M, Aberhan M 2019. Diversity partitioning in Phanerozoic benthic marine communities. PNAS 116:79–83
    [Google Scholar]
  43. Holland SM. 2012. Sea level change and the area of shallow-marine habitat: implications for marine biodiversity. Paleobiology 38:205–17
    [Google Scholar]
  44. Hull PM, Bornemann A, Penman DE, Henehan MJ, Norris RD et al. 2020. On impact and volcanism across the Cretaceous-Paleogene boundary. Science 367:266–72
    [Google Scholar]
  45. Husson JM, Peters SE. 2017. Atmospheric oxygenation driven by unsteady growth of the continental sedimentary reservoir. Earth Planet. Sci. Lett. 460:68–75
    [Google Scholar]
  46. Jablonski D, Huang S, Roy K, Valentine JW 2017. Shaping the latitudinal diversity gradient: new perspectives from a synthesis of paleobiology and biogeography. Am. Nat. 189:1–12
    [Google Scholar]
  47. Jackson JBC, Johnson KG 2001. Measuring past biodiversity. Science 293:2401–4
    [Google Scholar]
  48. Joachimski MM, Lai X, Shen S, Jiang H, Luo G et al. 2012. Climate warming in the latest Permian and the Permian–Triassic mass extinction. Geology 40:195–98
    [Google Scholar]
  49. Johnston DT, Wolfe-Simon F, Pearson A, Knoll AH 2009. Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age. PNAS 106:16925–29
    [Google Scholar]
  50. Jones LA, Dean CD, Mannion PD, Farnsworth A, Allison PA. 2021. Spatial sampling heterogeneity limits the detectability of deep time latitudinal biodiversity gradients. Proc. R. Soc. B 288:20202762
    [Google Scholar]
  51. Kidwell SM. 2005. Shell composition has no net impact on large-scale evolutionary patterns in mollusks. Science 307:914–17
    [Google Scholar]
  52. Kiessling W, Simpson C. 2011. On the potential for ocean acidification to be a general cause of ancient reef crises. Glob. Change Biol. 17:56–67
    [Google Scholar]
  53. Knoll AH, Bambach RK, Payne JL, Pruss S, Fischer WW 2007. Paleophysiology and end-Permian mass extinction. Earth Planet. Sci. Lett. 256:295–313
    [Google Scholar]
  54. Knope ML, Bush AM, Frishkoff LO, Heim NA, Payne JL. 2020. Ecologically diverse clades dominate the oceans via extinction resistance. Science 367:1035–38
    [Google Scholar]
  55. Knope ML, Heim NA, Frishkoff LO, Payne JL. 2015. Limited role of functional differentiation in early diversification of animals. Nat. Commun. 6:6455
    [Google Scholar]
  56. Kocsis AT, Reddin CJ, Alroy J, Kiessling W 2019. The R package divDyn for quantifying diversity dynamics using fossil sampling data. Methods Ecol. Evol. 10:735–43
    [Google Scholar]
  57. Kowalewski M, Finnegan S. 2010. Theoretical diversity of the marine biosphere. Paleobiology 36:1–15
    [Google Scholar]
  58. Kowalewski M, Flessa KW. 1996. Improving with age: the fossil record of lingulide brachiopods and the nature of taphonomic megabiases. Geology 24:977–80
    [Google Scholar]
  59. LaBarbera M. 1981. The ecology of Mesozoic Gryphaea, Exogyra, and Ilymatogyra (Bivalvia: Mollusca) in a modern ocean. Paleobiology 7:510–26
    [Google Scholar]
  60. Lazarus D, Barron J, Renaudie J, Diver P, Türke A. 2014. Cenozoic planktonic marine diatom diversity and correlation to climate change. PLOS ONE 9:e84857
    [Google Scholar]
  61. Leprieur F, Descombes P, Gaboriau T, Cowman PF, Parravicini V et al. 2016. Plate tectonics drive tropical reef biodiversity dynamics. Nat. Commun. 7:11461
    [Google Scholar]
  62. Liow LH, Reitan T, Harnik PG 2015. Ecological interactions on macroevolutionary time scales: Clams and brachiopods are more than ships that pass in the night. Ecol. Lett. 18:1030–39
    [Google Scholar]
  63. Lomolino MV. 2000. Ecology's most general, yet protean pattern: the species-area relationship. J. Biogeogr. 27:17–26
    [Google Scholar]
  64. Louca S, Pennell MW. 2020. Extant timetrees are consistent with a myriad of diversification histories. Nature 580:502–5
    [Google Scholar]
  65. Lowery CM, Bown PR, Fraass AJ, Hull PM. 2020. Ecological response of plankton to environmental change: thresholds for extinction. Annu. Rev. Earth Planet. Sci. 48:403–29
    [Google Scholar]
  66. Lu W, Ridgwell A, Thomas E, Hardisty DS, Luo G et al. 2018. Late inception of a resiliently oxygenated upper ocean. Science 361:174–77
    [Google Scholar]
  67. MacRae RA, Fensome RA, Williams GL. 1996. Fossil dinoflagellate diversity, originations, and extinctions and their significance. Can. J. Bot. 74:1687–94
    [Google Scholar]
  68. Mannion PD, Upchurch P, Benson RB, Goswami A. 2014. The latitudinal biodiversity gradient through deep time. Trends Ecol. Evol. 29:42–50
    [Google Scholar]
  69. Marshall CR. 2006. Explaining the Cambrian “explosion” of animals. Annu. Rev. Earth Planet. Sci. 34:355–84
    [Google Scholar]
  70. Marshall CR, Quental TB. 2016. The uncertain role of diversity dependence in species diversification and the need to incorporate time-varying carrying capacities. Philos. Trans. R. Soc. B 371:20150217
    [Google Scholar]
  71. Martin RE, Servais T. 2020. Did the evolution of the phytoplankton fuel the diversification of the marine biosphere?. Lethaia 53:5–31
    [Google Scholar]
  72. Mayhew PJ, Bell MA, Benton TG, McGowan AJ 2012. Biodiversity tracks temperature over time. PNAS 109:15141–45
    [Google Scholar]
  73. Melott AL, Bambach RK. 2011. A ubiquitous ∼62-Myr periodic fluctuation superimposed on general trends in fossil biodiversity. I. Documentation. Paleobiology 37:92–112
    [Google Scholar]
  74. Melott AL, Bambach RK, Petersen KD, McArthur JM. 2012. An ∼60-million-year periodicity is common to marine 87Sr/86Sr, fossil biodiversity, and large-scale sedimentation: What does the periodicity reflect?. J. Geol. 120:217–26
    [Google Scholar]
  75. Meyer KM, Ridgwell A, Payne JL 2016. The influence of the biological pump on ocean chemistry: implications for long-term trends in marine redox chemistry, the global carbon cycle, and marine animal ecosystems. Geobiology 14:207–19
    [Google Scholar]
  76. Meyers SR, Peters SE. 2011. A 56 million year rhythm in North American sedimentation during the Phanerozoic. Earth Planet. Sci. Lett. 303:174–80
    [Google Scholar]
  77. Novack-Gottshall PM. 2007. Using a theoretical ecospace to quantify the ecological diversity of Paleozoic and modern marine biotas. Paleobiology 33:273–94
    [Google Scholar]
  78. Novack-Gottshall PM. 2008. Ecosystem-wide body-size trends in Cambrian–Devonian marine invertebrate lineages. Paleobiology 34:210–28
    [Google Scholar]
  79. Nursall J. 1959. Oxygen as a prerequisite to the origin of the Metazoa. Nature 183:1170–72
    [Google Scholar]
  80. Ozaki K, Tajima S, Tajika E 2011. Conditions required for oceanic anoxia/euxinia: constraints from a one-dimensional ocean biogeochemical cycle model. Earth Planet. Sci. Lett. 304:270–79
    [Google Scholar]
  81. Pellissier L, Heine C, Rosauer DF, Albouy C. 2018. Are global hotspots of endemic richness shaped by plate tectonics?. Biol. J. Linn. Soc. 123:247–61
    [Google Scholar]
  82. Penn JL, Deutsch C, Payne JL, Sperling EA. 2018. Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction. Science 362:eaat1327
    [Google Scholar]
  83. Pennington JT. 1985. The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol. Bull. 169:417–30
    [Google Scholar]
  84. Peters SE. 2005. Geologic constraints on the macroevolutionary history of marine animals. PNAS 102:12326–31
    [Google Scholar]
  85. Peters SE. 2007. The problem with the Paleozoic. Paleobiology 33:165–81
    [Google Scholar]
  86. Peters SE, Heim NA. 2011. Macrostratigraphy and macroevolution in marine environments: testing the common-cause hypothesis. Geol. Soc. Spec. Publ. 358:95–104
    [Google Scholar]
  87. Peters SE, Husson JM 2017. Sediment cycling on continental and oceanic crust. Geology 45:323–26
    [Google Scholar]
  88. Powell M, Kowalewski M 2002. Increase in evenness and sampled alpha diversity through the Phanerozoic: comparison of Early Paleozoic and Cenozoic marine fossil assemblages. Geology 30:331–34
    [Google Scholar]
  89. Pruss SB, Finnegan S, Fischer WW, Knoll AH. 2010. Carbonates in skeleton-poor seas: new insights from Cambrian and Ordovician strata of Laurentia. Palaios 25:73–84
    [Google Scholar]
  90. Quental TB, Marshall CR. 2010. Diversity dynamics: molecular phylogenies need the fossil record. Trends Ecol. Evol. 25:434–41
    [Google Scholar]
  91. Quigg A, Finkel ZV, Irwin AJ, Rosenthal Y, Ho T-Y et al. 2003. The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425:291–94
    [Google Scholar]
  92. R Core Team 2019. R: A language and environment for statistical computing. The R Foundation for Statistical Computing https://www.R-project.org/
    [Google Scholar]
  93. Rabosky DL, Hurlbert AH. 2015. Species richness at continental scales is dominated by ecological limits. Am. Nat. 185:572–83
    [Google Scholar]
  94. Raup DM. 1972. Taxonomic diversity during the Phanerozoic. Science 177:1065–71
    [Google Scholar]
  95. Raup DM, Sepkoski JJ Jr 1982. Mass extinctions in the marine fossil record. Science 215:1501–3
    [Google Scholar]
  96. Reinhard CT, Planavsky NJ, Olson SL, Lyons TW, Erwin DH. 2016. Earth's oxygen cycle and the evolution of animal life. PNAS 113:8933–38
    [Google Scholar]
  97. Renema W, Bellwood D, Braga J, Bromfield K, Hall R et al. 2008. Hopping hotspots: global shifts in marine biodiversity. Science 321:654–57
    [Google Scholar]
  98. Rohde RA, Muller RA. 2005. Cycles in fossil diversity. Nature 434:208–10
    [Google Scholar]
  99. Roman J, McCarthy JJ 2010. The whale pump: marine mammals enhance primary productivity in a coastal basin. PLOS ONE 5:e13255
    [Google Scholar]
  100. Royer DL, Berner RA, Montañez IP, Tabor NJ, Beerling DJ 2004. CO2 as a primary driver of Phanerozoic climate. GSA Today 14:4–10
    [Google Scholar]
  101. Sadler PM. 2004. Quantitative biostratigraphy—achieving finer resolution in global correlation. Annu. Rev. Earth Planet. Sci. 32:187–213
    [Google Scholar]
  102. Saltzman MR, Thomas E 2012. Carbon isotope stratigraphy. The Geologic Timescale 2012 F Gradstein, J Ogg, G Ogg, M Schmitz 207–33 Amsterdam: Elsevier
    [Google Scholar]
  103. Schachat SR, Labandeira CC, Saltzman MR, Cramer BD, Payne JL, Boyce CK. 2018. Phanerozoic pO2 and the early evolution of terrestrial animals. Proc. R. Soc. B 285:20172631
    [Google Scholar]
  104. Schubert JK, Kidder DL, Erwin DH. 1997. Silica-replaced fossils through the Phanerozoic. Geology 25:1031–34
    [Google Scholar]
  105. Sepkoski JJ Jr. 1979. A kinetic model of Phanerozoic taxonomic diversity. II. Early Phanerozoic families and multiple equilibria. Paleobiology 5:222–51
    [Google Scholar]
  106. Sepkoski JJ Jr. 1981. A factor analytic description of the Phanerozoic marine fossil record. Paleobiology 7:36–53
    [Google Scholar]
  107. Sepkoski JJ Jr. 1984. A kinetic model of Phanerozoic taxonomic diversity. III. Post-Paleozoic families and mass extinctions. Paleobiology 10:246–67
    [Google Scholar]
  108. Sibert EC, Norris RD. 2015. New Age of Fishes initiated by the Cretaceous−Paleogene mass extinction. PNAS 112:8537–42
    [Google Scholar]
  109. Smith AB, McGowan AJ. 2005. Cyclicity in the fossil record mirrors rock outcrop area. Biol. Lett. 1:443–45
    [Google Scholar]
  110. Sperling EA, Frieder CA, Raman AV, Girguis PR, Levin LA, Knoll AH. 2013. Oxygen, ecology, and the Cambrian radiation of animals. PNAS 110:13446–51
    [Google Scholar]
  111. Sperling EA, Stockey RG. 2018. The temporal and environmental context of early animal evolution: Considering all the ingredients of an “explosion. .” Integr. Comp. Biol 58:605–22
    [Google Scholar]
  112. Stanley SM. 2007. Memoir 4: An analysis of the history of marine animal diversity. Paleobiology 33:4 Suppl1–55
    [Google Scholar]
  113. Thayer CW 1983. Sediment-mediated biological disturbance and the evolution of the marine benthos. Biotic Interactions in Recent and Fossil Benthic Communities MJS Tevesz, PL McCall 479–625 New York: Plenum
    [Google Scholar]
  114. Tyrrell T. 1999. The relative influences of nitrogen and phosphorus on oceanic primary production. Nature 400:525–31
    [Google Scholar]
  115. Valentine JW. 1969. Patterns of taxonomic and ecological structure of the shelf benthos during Phanerozoic time. Palaeontology 12:684–709
    [Google Scholar]
  116. Valentine JW, Jablonski D, Krug AZ, Berke SK. 2013. The sampling and estimation of marine paleodiversity patterns: implications of a Pliocene model. Paleobiology 39:1–20
    [Google Scholar]
  117. Valentine JW, Moores EM. 1970. Plate-tectonic regulation of faunal diversity and sea level: a model. Nature 228:657–59
    [Google Scholar]
  118. van der Niet T, Johnson SD. 2012. Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends Ecol. Evol. 27:353–61
    [Google Scholar]
  119. Vermeij GJ. 1987. Evolution and Escalation: An Ecological History of Life Princeton, NJ: Princeton Univ. Press
  120. Vermeij GJ. 1995. Economics, volcanoes, and Phanerozoic revolutions. Paleobiology 21:125–52
    [Google Scholar]
  121. Zaffos A, Finnegan S, Peters SE. 2017. Plate tectonic regulation of global marine animal diversity. PNAS 114:5653–58
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-012021-035131
Loading
/content/journals/10.1146/annurev-ecolsys-012021-035131
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error