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

Published online by Cambridge University Press:  08 April 2016

Seth Finnegan
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, California 94305. E-mail: sethf@stanford.edu
Jonathan L. Payne
Affiliation:
Department of Geological and Environmental Sciences, Stanford University, 450 Serra Mall, Building 320, Stanford, California 94305. E-mail: sethf@stanford.edu
Steve C. Wang
Affiliation:
Department of Mathematics and Statistics, Swarthmore College, 500 College Ave, Swarthmore, Pennsylvania 19081

Abstract

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.

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Copyright © The Paleontological Society 

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References

Literature Cited

Albert, A., and Anderson, J. A. 1984. On the existence of maximum likelihood estimates in logistic regression models. Biometrika 71:110.Google Scholar
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.Google Scholar
Anstey, R. L. 1978. Taxonomic survivorship and morphologic complexity in Paleozoic bryozoan genera. Paleobiology 4:407418.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Baumiller, T. K. 1993. Survivorship analysis of Paleozoic Crinoidea: effect of filter morphology on evolutionary rates. Paleobiology 19:304321.CrossRefGoogle Scholar
Berg, H. C. 1983. Random walks in biology. Princeton University Press, Princeton, N.J. Google Scholar
Boucot, A. J. 1978. Community evolution and rates of cladogenesis. Evolutionary Biology 11:545655.Google Scholar
Boyajian, G. E. 1986. Phanerozoic trends in background extinction; consequences of an aging fauna. Geology 14:955958.Google Scholar
Boyajian, G. E. 1991. Taxon age and selectivity of extinction. Paleobiology 17:4957.Google Scholar
Boyajian, G. E., and Lutz, T. 1992. Evolution of biological complexity and its relation to taxonomic longevity in the Ammonoidea. Geology 20:983986.2.3.CO;2>CrossRefGoogle Scholar
Burnham, K. P., and Anderson, D. R. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York.Google Scholar
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.Google Scholar
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.Google Scholar
Clay, K. K., and Kover, P. P. X. 1996. The Red Queen hypothesis and plant/pathogen interactions. Annual Review of Phytopathology 34:2950.CrossRefGoogle ScholarPubMed
Dawkins, R., and Krebs, J. R. 1979. Arms races between and within species. Proceedings of the Royal Society of London B 205:489511.Google ScholarPubMed
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.Google Scholar
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.Google Scholar
Doran, N. A. 2006. Is extinction age-dependent? Palaios 21:571579.Google Scholar
Flessa, K. W., and Jablonski, D. 1983. Extinction is here to stay. Paleobiology 9:315.Google Scholar
Flessa, K. W. 1985. Declining Phanerozoic background extinction rates: effect of taxonomic structure. Nature 313:216218.CrossRefGoogle Scholar
Foin, T. C., Valentine, J. W., and Ayala, F. J. 1975. Extinction of taxa and Van Valen's law. Nature 257:514515.Google Scholar
Foote, M. 1988. Survivorship analysis of Cambrian and Ordovician trilobites. Paleobiology 14:258271.Google Scholar
Foote, M. 1997. Estimating taxonomic durations and preservation probability. Paleobiology 23:278300.Google Scholar
Foote, M. 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74102.Google Scholar
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.Google Scholar
Foote, M. 2001b. Inferring temporal patterns of preservation, origination, and extinction from taxonomic survivorship analysis. Paleobiology 27:602630.Google Scholar
Foote, M. 2005. Pulsed origination and extinction in the marine realm. Paleobiology 31:620.Google Scholar
Foote, M. 2007. Extinction and quiescence in marine animal genera. Paleobiology 33:261272.CrossRefGoogle Scholar
Foote, M., and Miller, A. I. 2007. Principles of paleontology, 3d ed. W. H. Freeman, New York.Google Scholar
Foote, M., and Raup, D. M. 1996. Fossil preservation and the stratigraphic ranges of taxa. Paleobiology 22:121140.CrossRefGoogle ScholarPubMed
Forey, P. L. 2004. Taxonomy and fossils: a critical appraisal. Philosophical transactions of the Royal Society of London B 359:639653.Google Scholar
Gilinsky, N. L. 1988. Survivorship in the Bivalvia: comparing living and extinct genera and families. Paleobiology 14:370386.CrossRefGoogle Scholar
Gretener, P. E. 1967. Significance of the rare event in geology. AAPG Bulletin 51:21972206.Google Scholar
Hallam, A. 1976. Red Queen dethroned. Nature 259:1213.Google Scholar
Hallam, A., and Wignall, P. B. 1997. Mass extinctions and their aftermaths. Oxford University Press, New York.Google Scholar
Hoffman, A., and Kitchell, J. A. 1984. Evolution in a pelagic planktic system: a paleobiologic test of models of multispecies evolution. Paleobiology 10:933.Google Scholar
Holman, E. W. 1983. Time scales and taxonomic survivorship. Paleobiology 9:2025.Google Scholar
Hosmer, D. W., and Lemeshow, S. 2000. Applied logistic regression. Wiley, New York.CrossRefGoogle Scholar
Jablonski, D. 1986. Background and mass extinctions: the alternation of macroevolutionary regimes. Science 231:129133.Google Scholar
Jablonski, D. Heritability at the species level: analysis of geographic ranges of cretaceous mollusks. Science 238:360363.Google Scholar
Jones, D. S., and Nicol, D. 1986. Origination, survivorship, and extinction of rudist taxa. Journal of Paleontology 60:107115.Google Scholar
Lively, C. M. 1990. Red Queen hypothesis supported by parasitism in sexual and clonal fish. Nature 344:864.Google Scholar
Lively, C. M. 1996. Host-Parasite Coevolution and Sex. Bio-Science 46:107.Google Scholar
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.Google Scholar
MacArthur, R. H., and Wilson, E. O. 1967. The Theory of Island Biogeography. Princeton University Press, Princeton, N.J. Google Scholar
Marrow, P., Dieckmann, U., and Law, R. 1996. Evolutionary dynamics of predator-prey systems: an ecological perspective. Journal of Mathematical Biology 34:556578.Google Scholar
Mayr, E. 1942. Systematics and the Origin of Species From the Viewpoint of a Zoologist. Columbia University Press, New York.Google Scholar
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.Google Scholar
McKinney, M. L. 1997. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28:495516.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Pearson, P. N. 1992. Survivorship analysis of fossil taxa when real-time extinction rates vary: the Paleogene planktonic foraminifera. Paleobiology 18:115131.CrossRefGoogle Scholar
Pearson, P. N. 1995. Investigating age-dependency of species extinction rates using dynamic survivorship analysis. Historical Biology 10:119136.Google Scholar
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.Google Scholar
Peters, S. E. 2005. Geologic constraints on the macroevolutionary history of marine animals. Proceedings of the National Academy of Sciences USA 102:1232612331.Google Scholar
Peters, S. E. 2006. Genus richness in Cambrian-Ordovician benthic marine communities in North America. Palaios 21:580587.Google Scholar
Peters, S. E., and Foote, M. 2002. Determinants of extinction in the fossil record. Nature 416:420424.Google Scholar
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.Google Scholar
Raup, D. M. 1972. Taxonomic diversity during the Phanerozoic. Science 177:10651071.CrossRefGoogle ScholarPubMed
Raup, D. M. 1975. Taxonomic survivorship curves and Van Valen's Law. Paleobiology 1:8296.CrossRefGoogle Scholar
Raup, D. M. 1978a. Approaches to the extinction problem. Journal of Paleontology 52:517523.Google Scholar
Raup, D. M. 1978b. Cohort analysis of generic survivorship. Paleobiology 4:115.Google Scholar
Raup, D. M. 1991. A kill curve for Phanerozoic marine species. Paleobiology 17:3748.Google Scholar
Raup, D. M. 1992. Extinction: bad genes or bad luck? Norton, New York.Google Scholar
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.CrossRefGoogle Scholar
Raup, D. M., and Sepkoski, J. J. Jr. 1982. Mass extinctions in the marine fossil record. Science 215:15011503.Google Scholar
Robeck, H. E., Maley, C. C., and Donoghue, M. J. 2000. Taxonomy and temporal diversity patterns. Paleobiology 26:171187.Google Scholar
Sadler, P. M. 2004. Quantitative biostratigraphy—achieving finer resolution in global correlation. Annual Review of Earth and Planetary Sciences 32:187213.Google Scholar
Salthe, S. N. 1975. Some comments on Van Valen's law of extinction. Paleobiology 1:356358.Google Scholar
Sepkoski, J. J. Jr. 1975. Stratigraphic biases in the analysis of taxonomic survivorship. Paleobiology 1:343355.Google Scholar
Sepkoski, J. J. Jr. 1993. Ten years in the library; new data confirm paleontological patterns. Paleobiology 19:4351.CrossRefGoogle ScholarPubMed
Sepkoski, J. J. Jr. 2002. A compendium of fossil marine animal genera. Bulletins of American Paleontology 363:560.Google Scholar
Sepkoski, J. J. Jr., and Kendrick, D. C. 1993. Numerical experiments with model monophyletic and paraphyletic taxa. Paleobiology 19:168184.Google Scholar
Simpson, G. G. 1944. Tempo and mode in evolution. Columbia University Press, New York.Google Scholar
Smith, A. B., and Jeffery, C. H. 1998. Selectivity of extinction among sea urchins at the end of the Cretaceous period. Nature 392:6971.Google Scholar
Smith, A. B., and Patterson, C. 1988. The influence of taxonomic method on the perception of patterns of evolution. Evolutionary Biology 23:127216.Google Scholar
Stanley, S. M. 1979. Macroevolution: pattern and process. W. H. Freeman, San Francisco.Google Scholar
Stanley, S. M. 1990. Delayed recovery and the spacing of major extinctions. Paleobiology 16:401414.Google Scholar
Stenseth, N. C., and Maynard-Smith, J. 1984. Coevolution in ecosystems: Red Queen evolution or stasis? Evolution 38:870880.Google Scholar
Uhen, M. D. 1996. An evaluation of clade-shape statistics using simulations and extinct families of mammals. Paleobiology 22:822.CrossRefGoogle Scholar
Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1:130.Google Scholar
Van Valen, L. 1976a. Energy and evolution. Evolutionary Theory 1:179229.Google Scholar
Van Valen, L. 1976b. The red queen lives. Nature 260:575.Google Scholar
Van Valen, L. 1979. Taxonomic survivorship curves. Evolutionary Theory 4:129142.Google Scholar
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.Google Scholar
Vermeij, G. J. 2004. Nature: an economic history. Princeton University Press, Princeton, N.J. Google Scholar
Wagner, P. J. 1995. Diversification among early Paleozoic gastropods: contrasting taxonomic and phylogenetic descriptions. Paleobiology 21:410439.CrossRefGoogle Scholar
Wagner, P. J., and Erwin, D. H. 2006. Patterns of convergence in general shell form among Paleozoic gastropods. Paleobiology 32:316337.Google Scholar
Wagner, P. J., Kosnik, M. A., and Lidgard, S. 2006. Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science 314:12891292.Google Scholar
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.Google Scholar
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.Google Scholar
Willis, J. C. 1922. Age and area. Cambridge University Press, Cambridge.Google Scholar
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