Skip to main content Accessibility help

The Red Queen revisited: reevaluating the age selectivity of Phanerozoic marine genus extinctions

  • Seth Finnegan (a1), Jonathan L. Payne (a1) and Steve C. Wang (a2)


Extinction risk is inversely related to genus age (time since first appearance) in most intervals of the Phanerozoic marine fossil record, in apparent contradiction to the macroevolutionary Red Queen's Hypothesis, which posits that extinction risk is independent of taxon age. Age-dependent increases in the mean species richness and geographic range of genera have been invoked to reconcile this genus-level observation with the presumed prevalence of Red Queen dynamics at the species level. Here we test these explanations with data from the Paleobiology Database. Multiple logistic regression demonstrates that the association of extinction risk with genus age is not adequately explained by species richness or geographic range: there is a residual association between age and extinction risk even when range and richness effects are accounted for. Throughout most of the Phanerozoic the age selectivity gradient is highest among the youngest age cohorts, whereas there is no association between age and extinction risk among older age cohorts. Some of the apparent age selectivity of extinction in the global fauna is attributable to differences in extinction rate among taxonomic groups, but extinction risk declines with genus age even within most taxonomic orders. Notable exceptions to this pattern include the Cambrian-Ordovician, latest Permian, Triassic, and Paleocene intervals. The association of age with extinction risk could reflect sampling heterogeneity or taxonomic practice more than biological reality, but at present it is difficult to evaluate or correct for such biases. Alternatively, the pattern may reflect consistent extinction selectivity on some as-yet unidentified covariate of genus age. Although this latter explanation is not compatible with a Red Queen model if most genus extinctions have resulted from biological interactions, it may be applicable if most genus extinctions have instead been caused by recurrent physical disturbances that repeatedly impose similar selective pressures.



Hide All
Albert, A., and Anderson, J. A. 1984. On the existence of maximum likelihood estimates in logistic regression models. Biometrika 71:110.
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich, F. T., Hansen, T. A., Holland, S. M., Ivany, L. C., Jablonski, D., Jacobs, D. K., Jones, D. C., Kosnik, M. A., Lidgard, S., Low, S., Miller, A. I., Novack-Gottshall, P. M., Olszewski, T. D., Patzkowsky, M. E., Raup, D. M., Roy, K., Sepkoski, J. J. Jr., Sommers, M. G., Wagner, P. J., and Webber, A. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences USA 98:62616266.
Anstey, R. L. 1978. Taxonomic survivorship and morphologic complexity in Paleozoic bryozoan genera. Paleobiology 4:407418.
Arnold, A. J., Kelly, D. C., and Parker, W. C. 1995. Causality and Cope's rule: evidence from the planktonic foraminifera. Journal of Paleontology 69:203210.
Bambach, R. K. 2002. Supporting predators: changes in the global ecosystem inferred from changes in predator diversity. Pp. 319352 in Kowalewski, M. and Kelley, P. H., eds. The fossil record of predation. The Paleontological Society, New Haven.
Bambach, R. K., Knoll, A. H., and Sepkoski, J. J. Jr. 2002. Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm. Proceedings of the National Academy of Sciences USA 99:68546859.
Baumiller, T. K. 1993. Survivorship analysis of Paleozoic Crinoidea: effect of filter morphology on evolutionary rates. Paleobiology 19:304321.
Berg, H. C. 1983. Random walks in biology. Princeton University Press, Princeton, N.J.
Boucot, A. J. 1978. Community evolution and rates of cladogenesis. Evolutionary Biology 11:545655.
Boyajian, G. E. 1986. Phanerozoic trends in background extinction; consequences of an aging fauna. Geology 14:955958.
Boyajian, G. E. 1991. Taxon age and selectivity of extinction. Paleobiology 17:4957.
Boyajian, G. E., and Lutz, T. 1992. Evolution of biological complexity and its relation to taxonomic longevity in the Ammonoidea. Geology 20:983986.
Burnham, K. P., and Anderson, D. R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.
Bush, A. M., and Bambach, R. K. 2004a. Are secular changes in tiering, motility, and predation real? Quantifying and testing changes in ecospace use between the Paleozoic and Cenozoic. Geological Society of America Annual Meeting Abstracts with Program 36:457.
Bush, A. M. 2004b. Phanerozoic increases in alpha diversity and evenness: linked consequences of increased ecospace use. Geological Society of America Meeting Abstracts with Programs 36:457.
Clay, K. K., and Kover, P. P. X. 1996. The Red Queen hypothesis and plant/pathogen interactions. Annual Review of Phytopathology 34:2950.
Dawkins, R., and Krebs, J. R. 1979. Arms races between and within species. Proceedings of the Royal Society of London B 205:489511.
Dieckmann, U., Marrow, P., and Law, R. 1995. Evolutionary cycling in predator-prey interactions: population dynamics and the Red Queen Journal of Theoretical Biology 176:91102.
Doran, N. A., Arnold, A. J., Parker, W. C., and Huffer, F. W. 2004. Deviation from Red Queen behaviour at stratigraphic boundaries: evidence for directional recovery. Geological Society special publication 230:3546.
Doran, N. A. 2006. Is extinction age-dependent? Palaios 21:571579.
Flessa, K. W., and Jablonski, D. 1983. Extinction is here to stay. Paleobiology 9:315.
Flessa, K. W. 1985. Declining Phanerozoic background extinction rates: effect of taxonomic structure. Nature 313:216218.
Foin, T. C., Valentine, J. W., and Ayala, F. J. 1975. Extinction of taxa and Van Valen's law. Nature 257:514515.
Foote, M. 1988. Survivorship analysis of Cambrian and Ordovician trilobites. Paleobiology 14:258271.
Foote, M. 1997. Estimating taxonomic durations and preservation probability. Paleobiology 23:278300.
Foote, M. 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74102.
Foote, M. 2001a. Evolutionary rates and the age distributions of living and extinct taxa. Pp. 245294 in Jackson, J. B. C., Lidgard, S., and McKinney, F. K., eds. Evolutionary patterns: growth form and tempo in the fossil record. University of Chicago Press, Chicago.
Foote, M. 2001b. Inferring temporal patterns of preservation, origination, and extinction from taxonomic survivorship analysis. Paleobiology 27:602630.
Foote, M. 2005. Pulsed origination and extinction in the marine realm. Paleobiology 31:620.
Foote, M. 2007. Extinction and quiescence in marine animal genera. Paleobiology 33:261272.
Foote, M., and Miller, A. I. 2007. Principles of paleontology, 3d ed. W. H. Freeman, New York.
Foote, M., and Raup, D. M. 1996. Fossil preservation and the stratigraphic ranges of taxa. Paleobiology 22:121140.
Forey, P. L. 2004. Taxonomy and fossils: a critical appraisal. Philosophical transactions of the Royal Society of London B 359:639653.
Gilinsky, N. L. 1988. Survivorship in the Bivalvia: comparing living and extinct genera and families. Paleobiology 14:370386.
Gretener, P. E. 1967. Significance of the rare event in geology. AAPG Bulletin 51:21972206.
Hallam, A. 1976. Red Queen dethroned. Nature 259:1213.
Hallam, A., and Wignall, P. B. 1997. Mass extinctions and their aftermaths. Oxford University Press, New York.
Hoffman, A., and Kitchell, J. A. 1984. Evolution in a pelagic planktic system: a paleobiologic test of models of multispecies evolution. Paleobiology 10:933.
Holman, E. W. 1983. Time scales and taxonomic survivorship. Paleobiology 9:2025.
Hosmer, D. W., and Lemeshow, S. 2000. Applied logistic regression. Wiley, New York.
Jablonski, D. 1986. Background and mass extinctions: the alternation of macroevolutionary regimes. Science 231:129133.
Jablonski, D. Heritability at the species level: analysis of geographic ranges of cretaceous mollusks. Science 238:360363.
Jones, D. S., and Nicol, D. 1986. Origination, survivorship, and extinction of rudist taxa. Journal of Paleontology 60:107115.
Lively, C. M. 1990. Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864.
Lively, C. M. 1996. Host-Parasite Coevolution and Sex. Bio-Science 46:107.
MacArthur, R. H., and Levins, R. 1964. Competition, habitat selection, and character displacement in a patchy environment. Proceedings of the National Academy of Sciences USA 51:12071210.
MacArthur, R. H., and Wilson, E. O. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, N.J.
Marrow, P., Dieckmann, U., and Law, R. 1996. Evolutionary dynamics of predator-prey systems: an ecological perspective. Journal of Mathematical Biology 34:556578.
Mayr, E. 1942. Systematics and the Origin of Species From the Viewpoint of a Zoologist. Columbia University Press, New York.
McGhee, G. R., Sheehan, P. M., Bottjer, D. J., and Droser, M. L. 2004. Ecological ranking of Phanerozoic biodiversity crises: ecological and taxonomic severities are decoupled. Palaeogeography, Palaeoclimatology, Palaeoecology 211:289297.
McKinney, M. L. 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28:495516.
Miller, A. I. 1997. A new look at age and area: the geographic and environmental expansion of genera during the Ordovician Radiation. Paleobiology 23:410419.
Morris, P. J., Ivany, L. C., Schopf, K. M., and Brett, C. E. 1995. The challenge of paleoecological stasis: reassessing sources of evolutionary stability. Proceedings of the National Academy of Sciences USA 92:1126911273.
Payne, J. L., and Finnegan, S. 2007. The effect of geographic range on extinction risk during background and mass extinction. Proceedings of the National Academy of Sciences USA 104:1050610511.
Pearson, P. N. 1992. Survivorship analysis of fossil taxa when real-time extinction rates vary: the Paleogene planktonic foraminifera. Paleobiology 18:115131.
Pearson, P. N. 1995. Investigating age-dependency of species extinction rates using dynamic survivorship analysis. Historical Biology 10:119136.
Peduzzi, P., Concato, J., Kemper, E., Holford, T. R., and Feinstein, A. R. 1996. A simulation study of the number of events per variable in logistic regression analysis. Journal of Clinical Epidemiology 49:13731379.
Peters, S. E. 2005. Geologic constraints on the macroevolutionary history of marine animals. Proceedings of the National Academy of Sciences USA 102:1232612331.
Peters, S. E. 2006. Genus richness in Cambrian-Ordovician benthic marine communities in North America. Palaios 21:580587.
Peters, S. E., and Foote, M. 2002. Determinants of extinction in the fossil record. Nature 416:420424.
Plotnick, R. E., and Wagner, P. J. 2006. Round up the usual suspects: common genera in the fossil record and the nature of wastebasket taxa. Paleobiology 32:126146.
Raup, D. M. 1972. Taxonomic diversity during the Phanerozoic. Science 177:10651071.
Raup, D. M. 1975. Taxonomic survivorship curves and Van Valen's Law. Paleobiology 1:8296.
Raup, D. M. 1978a. Approaches to the extinction problem. Journal of Paleontology 52:517523.
Raup, D. M. 1978b. Cohort analysis of generic survivorship. Paleobiology 4:115.
Raup, D. M. 1991. A kill curve for Phanerozoic marine species. Paleobiology 17:3748.
Raup, D. M. 1992. Extinction: bad genes or bad luck? Norton, New York.
Raup, D. M., Gould, S. J., Schopf, T. J. M., and Simberloff, D. S. 1973. Stochastic-models of phylogeny and evolution of diversity. Journal of Geology 81:525542.
Raup, D. M., and Sepkoski, J. J. Jr. 1982. Mass extinctions in the marine fossil record. Science 215:15011503.
Robeck, H. E., Maley, C. C., and Donoghue, M. J. 2000. Taxonomy and temporal diversity patterns. Paleobiology 26:171187.
Sadler, P. M. 2004. Quantitative biostratigraphy—achieving finer resolution in global correlation. Annual Review of Earth and Planetary Sciences 32:187213.
Salthe, S. N. 1975. Some comments on Van Valen's law of extinction. Paleobiology 1:356358.
Sepkoski, J. J. Jr. 1975. Stratigraphic biases in the analysis of taxonomic survivorship. Paleobiology 1:343355.
Sepkoski, J. J. Jr. 1993. Ten years in the library; new data confirm paleontological patterns. Paleobiology 19:4351.
Sepkoski, J. J. Jr. 2002. A compendium of fossil marine animal genera. Bulletins of American Paleontology 363:560.
Sepkoski, J. J. Jr., and Kendrick, D. C. 1993. Numerical experiments with model monophyletic and paraphyletic taxa. Paleobiology 19:168184.
Simpson, G. G. 1944. Tempo and mode in evolution. Columbia University Press, New York.
Smith, A. B., and Jeffery, C. H. 1998. Selectivity of extinction among sea urchins at the end of the Cretaceous period. Nature 392:6971.
Smith, A. B., and Patterson, C. 1988. The influence of taxonomic method on the perception of patterns of evolution. Evolutionary Biology 23:127216.
Stanley, S. M. 1979. Macroevolution: pattern and process. W. H. Freeman, San Francisco.
Stanley, S. M. 1990. Delayed recovery and the spacing of major extinctions. Paleobiology 16:401414.
Stenseth, N. C., and Maynard-Smith, J. 1984. Coevolution in ecosystems: Red Queen evolution or stasis? Evolution 38:870880.
Uhen, M. D. 1996. An evaluation of clade-shape statistics using simulations and extinct families of mammals. Paleobiology 22:822.
Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1:130.
Van Valen, L. 1976a. Energy and evolution. Evolutionary Theory 1:179229.
Van Valen, L. 1976b. The red queen lives. Nature 260:575.
Van Valen, L. 1979. Taxonomic survivorship curves. Evolutionary Theory 4:129142.
Van Valen, L. M., and Boyajian, G. E. 1987. Phanerozoic trends in background extinction: consequence of an aging fauna—Comment and reply. Geology 15:875876.
Vermeij, G. J. 2004. Nature: an economic history. Princeton University Press, Princeton, N.J.
Wagner, P. J. 1995. Diversification among early Paleozoic gastropods: contrasting taxonomic and phylogenetic descriptions. Paleobiology 21:410439.
Wagner, P. J., and Erwin, D. H. 2006. Patterns of convergence in general shell form among Paleozoic gastropods. Paleobiology 32:316337.
Wagner, P. J., Kosnik, M. A., and Lidgard, S. 2006. Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science 314:12891292.
Wagner, P. J., Aberhan, M., Hendy, A., and Kiessling, W. 2007. The effects of taxonomic standardization on sampling-standardized estimates of historical diversity. Proceedings of the Royal Society B 274:439444.
Warwick, R. M., and Clarke, K. R. 1996. Relationships between body-size, species abundance and diversity in marine benthic assemblages: facts or artefacts? Journal of Experimental Marine Biology and Ecology 202:6371.
Willis, J. C. 1922. Age and area. Cambridge University Press, Cambridge.

Related content

Powered by UNSILO
Type Description Title
Supplementary materials

Finnegan et al. supplementary material
Supplementary Table S1

 Excel (94 KB)
94 KB
Supplementary materials

Finnegan et al. supplementary material
Supplementary Figure 1

 Unknown (692 KB)
692 KB
Supplementary materials

Finnegan et al. supplementary material
Supplementary Figure 2

 Unknown (695 KB)
695 KB
Supplementary materials

Finnegan et al. supplementary material
Supplementary Figure 3

 Unknown (322 KB)
322 KB
Supplementary materials

Finnegan et al. supplementary material
Supplementary Figure 4

 Unknown (341 KB)
341 KB

The Red Queen revisited: reevaluating the age selectivity of Phanerozoic marine genus extinctions

  • Seth Finnegan (a1), Jonathan L. Payne (a1) and Steve C. Wang (a2)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.