Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-05T08:06:44.220Z Has data issue: false hasContentIssue false

Reining in the Red Queen: the dynamics of adaptation and extinction reexamined

Published online by Cambridge University Press:  09 July 2013

Geerat J. Vermeij
Affiliation:
Department of Geology, One Shields Avenue, University of California Davis, Davis, California 95616, U.S.A. E-mail: [email protected]
Peter D. Roopnarine
Affiliation:
Department of Invertebrate Zoology and Geology, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, California 94118, U.S.A. E-mail: [email protected]. Corresponding author

Abstract

One of the most enduring evolutionary metaphors is Van Valen's (1973) Red Queen. According to this metaphor, as one species in a community adapts by becoming better able to acquire and defend resources, species with which it interacts are adversely affected. If those other species do not continuously adapt to compensate for this biotically caused deterioration, they will be driven to extinction. Continuous adaptation of all species in a community prevents any single species from gaining a long-term advantage; this amounts to the Red Queen running in place. We have critically examined the assumptions on which the Red Queen metaphor was founded. We argue that the Red Queen embodies three demonstrably false assumptions: (1) evolutionary adaptation is continuous; (2) organisms are important agents of extinction; and (3) evolution is a zero-sum process in which living things divide up an unchanging quantity of resources. Changes in the selective regime need not always elicit adaptation, because most organisms function adequately under many “suboptimal” conditions and often compensate by demonstrating adaptive flexibility. Likewise, ecosystems are organized in such a way that they tend to be robust and capable of absorbing invasions and extinctions, at least up to a point. With a simple evolutionary game involving three species, we show that Red Queen dynamics (continuous adaptation by all interacting species) apply in only a very small minority of possible outcomes. Importantly, cooperation and facilitation among species enable competitors to increase ecosystem productivity and therefore to enlarge the pool and turnover of resources. The Red Queen reigns only under a few unusual circumstances.

Type
Articles
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Agrawal, A. A. 2001. Phenotypic plasticity in the interaction and evolution of species. Science 294:321326.CrossRefGoogle ScholarPubMed
Allmon, W. D. 1992. A causal analysis of stages in allopatric speciation. Oxford Survey of Evolutionary Biology 8:219257.Google Scholar
Allmon, W. D. 2001. Nutrients, temperature, disturbance, and evolution: a model for the Late Cenozoic marine record of the western Atlantic. Palaeogeography, Palaeoclimatology, Palaeoecology 166:926.CrossRefGoogle Scholar
Arditi, R., and Ginzburg, L. 2012. How species interact: altering the standard view of trophic ecology. Oxford University Press, New York.CrossRefGoogle Scholar
Bambach, R. K. 1999. Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios 32:131144.CrossRefGoogle Scholar
Barash, D. P. 2003. The survival game. Times Books, New York.Google Scholar
Beerling, D. J., and Berner, R. A. 2005. Feedbacks and the coevolution of plants and atmospheric CO2. Proceedings of the National Academy of Sciences USA 102:13021305.CrossRefGoogle ScholarPubMed
Benton, M. J. 1979. Increase in total global biomass over time. Evolutionary Theory 4:123128.Google Scholar
Bertness, M. D. 1981. Conflicting advantages in resource utilization: the hermit crab housing dilemma. American Naturalist 118:432437.CrossRefGoogle Scholar
Boyce, C. K., and Lee, J. E. 2010. An exceptional role for flowering plant physiology in the expansion of tropical rain forests and biodiversity. Proceedings of the Royal Society of London B 277:34373443.Google ScholarPubMed
Boyce, C. K., Brodribb, T. J., Feild, T. S., and Zwieniecki, M. A. 2009. Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society of London B 276:17711776.Google ScholarPubMed
Brockhurst, M. A. 2011. Sex, death and the Red Queen. Science 333:166167.CrossRefGoogle ScholarPubMed
Brodribb, T. J., and Feild, T. S. 2010. Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13:175183.CrossRefGoogle Scholar
Brodribb, T. J., and McAdam, S. A. M. 2011. Passive origins of stomatal control in vascular plants. Science 331:582585.CrossRefGoogle ScholarPubMed
Cornell, H. V., and Hawkins, B. A. 1993. Accumulation of native parasitoid species on introduced herbivores: a comparison of hosts as natives and hosts as invaders. American Naturalist 141:847865.CrossRefGoogle ScholarPubMed
Davis, M. A. 2003. Biotic globalization: does competition from introduced species threaten biodiversity? Bioscience 53:481489.CrossRefGoogle Scholar
Davis, M. A., Chew, M. K., Hobbs, R. J., Lugo, A. E., Ewel, J. J., Vermeij, G. J., Brown, J. H., Rosenzweig, M. L., Gardener, M. R., Carroll, S. P., Thompson, K., Pickett, S. T. A., Strombert, J. C., Tredici, P. D., Suding, K. N., Ehrenfeld, J. G., Grime, J. P., Mascaro, J., and Briggs, J. C. 2011. Don't judge species on their origins. Nature 474:153154.CrossRefGoogle ScholarPubMed
Dayton, P. K. 1973. Two cases of resource partitioning in an intertidal community: making the right prediction for the wrong reasons. American Naturalist 107:662670.CrossRefGoogle Scholar
Dockery, D. T. 1986. Punctuated succession of Paleogene mollusks in the northern Gulf Coastal Plain. Palaios 1:582589.Google Scholar
Doran, N. A., Arnold, A. J., Parker, W. C., and Huffer, F. W. 2006. Is extinction age dependent? Palaios 21:571579.CrossRefGoogle Scholar
Eldredge, N., and Gould, S. J. 1972. Punctuated equilibria: an alternative to phyletic gradualism. Pp. 82115inSchopf, T. J. M., ed. Models in paleobiology. Freeman, Cooper, San Francisco.Google Scholar
Ezard, T. H. G., Aze, T., Pearson, P. N., and Purvis, A. 2011. Interplay between changing climate and species' ecology drives macroevolutionary dynamics. Science 332:349351.CrossRefGoogle ScholarPubMed
Fine, P. V., Mesones, I., and Coley, P. D. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305:663665.CrossRefGoogle ScholarPubMed
Finnegan, S., Payne, J. B., and Wang, S. C. 2008. The Red Queen revisited: reevaluating the age selectivity of Phanerozoic marine genus extinctions. Paleobiology 34:318341.CrossRefGoogle Scholar
Fischer, J. M., Frost, T. M., and Ives, A. R. 2001. Compensatory dynamics in zooplankton community responses to acidification: measurement and mechanisms. Ecological Applications 11:10601072.CrossRefGoogle Scholar
Frank, S. A. 1996. The design of natural and artificial adaptive systems. Pp. 451505inRose, M. R. and Lauder, G. V., eds. Adaptation. Academic Press, San Diego.Google Scholar
Geist, V. 1978. Life strategies, human evolution, developmental design; toward a biological theory of health. Springer, New York.Google Scholar
Geist, V. 1983. On the evolution of ice age mammals and its significance to an understanding of speciations. Association of Southeastern Biologists Bulletin 30:109133.Google Scholar
Gingerich, P. W. 1983. Rates of evolution: effects of time and temporal scaling. Science 222:149161.CrossRefGoogle ScholarPubMed
Glibert, M. 1973. Révision des Gastropoda du Danien et du Montien de la Belgique. I. Les Gastropoda du Calcaire de Mons. Institut Royal des Sciences Naturelles de Belgique Mémoire 173:1116.Google Scholar
Gonzalez, A., and Loreau, M. 2009. The causes and consequences of compensatory dynamics in ecological communities. Annual Review of Ecology, Evolution, and Systematics 40:393414.CrossRefGoogle Scholar
Hansen, T. A. 1988. Early Tertiary radiation of marine molluscs and the long-term effects of the Cretaceous-Tertiary extinction. Paleobiology 14:3751.CrossRefGoogle Scholar
Hautmann, M., Bucher, H., Brühweiler, T., Goudemand, N., Kaim, A., and Nützel, A. 2011. An unusually diverse mollusc fauna from the earliest Triassic of South China and its implications for recovery after the end-Permian biotic crisis. Geobios 44:7185.CrossRefGoogle Scholar
Hautmann, M., Smith, A. B., McGowan, A. J., and Bucher, H. 2013. Bivalves from the Olenekian (Early Triassic) of southwestern Utah: systematics and evolutionary significance. Journal of Systematic Palaeontology 11:263293.CrossRefGoogle Scholar
Houlahan, J. E., Currie, D. J., Cottenie, K., Cumming, G. S., Ernest, S. K. M., Findlay, C. S., Fuhlendorf, S. D., Gaedke, U., Legendre, P., Magnuson, J. J., McArdle, B. H., Muldavin, E. H., Noble, D., Russell, R., Stevens, R. D., Willis, T. J., Woiwod, I. P., and Wondzell, S. M. 2007. Compensatory dynamics are rare in natural ecological communities. Proceedings of the National Academy of Sciences USA104:32733277.CrossRefGoogle Scholar
Huey, R. B., Pianka, E. R., and Vitt, L. J. 2001. How often do lizards “run on empty”? Ecology 82:17.Google Scholar
Hull, P. M., and Norris, R. D. 2009. Evidence for abrupt speciation in a classic case of gradual evolution. Proceedings of the National Academy of Sciences USA106:2122421229.CrossRefGoogle Scholar
Hunt, G. 2007. The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages. Proceedings of the National Academy of Sciences USA 104:1840418408.CrossRefGoogle ScholarPubMed
Irmis, R. B., and Whiteside, J. H. 2012. Delayed recovery of non-marine tetrapods after the end-Permian mass extinction tracks global carbon cycle. Proceedings of the Royal Society of London B 279:13101318.Google ScholarPubMed
Jablonski, D., and Bottjer, D. J. 1990. Onshore-offshore trends in marine invertebrate evolution. Pp. 2175inRoss, R. M. and Allmon, W. D., eds. Causes of evolution: a paleontological perspective. University of Chicago Press, Chicago.Google Scholar
Jablonski, D., Sepkoski, J. J. Jr., Bottjer, D. J., and Sheehan, P. M. 1983. Onshore-offshore patterns in the evolution of Phanerozoic shelf communities. Science 222:11231125.CrossRefGoogle ScholarPubMed
Kirchner, J. W. 2002. Evolutionary speed limits inferred from the fossil record. Nature 415:6568.CrossRefGoogle ScholarPubMed
Kirchner, J. W., and Weil, A. 2000. Delayed biological recovery from extinctions throughout the fossil record. Nature 404:177180.CrossRefGoogle ScholarPubMed
Knauth, L. P., and Kennedy, M. J. 2009. The Late Precambrian greening of the world. Nature 460:728732.CrossRefGoogle Scholar
Krug, A. Z., Jablonski, D., and Valentine, J. W. 2009. Signature of the end-Cretaceous mass extinction in the modern biota. Science 323:767771.CrossRefGoogle ScholarPubMed
Leigh, E. G. 2010. The evolution of mutualisms. Journal of Evolutionary Biology 23:25072528.CrossRefGoogle Scholar
Liow, L. H., Van Valen, L., and Stenseth, N. C. 2011. Red Queen: from populations to taxa and communities. Trends in Ecology and Evolution 26:349358.CrossRefGoogle ScholarPubMed
Lively, C. M. 2010. A review of Red Queen models for the persistence of obligate sexual reproduction. Journal of Heredity 101:S13S20.CrossRefGoogle ScholarPubMed
Lohrer, A. M., Thrush, S. F., and Gibbs, M. M. 2004. Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:10921095.CrossRefGoogle ScholarPubMed
MacGillavry, H. J. 1968. Modes of evolution mainly among marine invertebrates: an observational approach. Bijdragen tot de Dierkunde 38:6974.CrossRefGoogle Scholar
Martin, C. H., and Wainwright, P. C. 2013. Multiple fitness peaks on the adaptive landscape drive adaptive radiation in the wild. Science 339:208211.CrossRefGoogle ScholarPubMed
Maynard Smith, J. 1976. What determines the rate of evolution? American Naturalist 110:331338.CrossRefGoogle Scholar
Maynard Smith, J. 1989. The causes of extinction. Philosophical Transactions of the Royal Society of London B 325:241252.Google Scholar
McCune, A. R. 1982. On the fallacy of constant extinction rates. Evolution 36:610614.CrossRefGoogle ScholarPubMed
Miller, A. I., and Foote, M. 2003. Increased longevities of post-Paleozoic marine genera after mass extinctions. Science 302:10301032.CrossRefGoogle ScholarPubMed
Mitchell, C. E., and Power, A. G. 2003. Release of invasive plants from fungal and viral pathogens. Nature 421:625627.CrossRefGoogle ScholarPubMed
Mitchell, J. S., Roopnarine, P. D., and Angielczyk, K. D. 2012. Late Cretaceous restructuring of terrestrial communities facilitated the End-Cretaceous mass extinction in North America. Proceedings of the National Academy of Sciences USA 109:1885718861.CrossRefGoogle ScholarPubMed
Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish, R. C., and Lively, C. M. 2011. Running with the Red Queen: host-parasite coevolution selects for biparental sex. Science 333:216218.CrossRefGoogle ScholarPubMed
Mougi, A., Kishida, O., and Iwasa, Y. 2011. Coevolution of phenotypic plasticity in predator and prey: why are inducible offenses rarer than inducible defenses? Evolution 65:10791087.CrossRefGoogle ScholarPubMed
Moulton, K. L., and Berner, R. A. 1998. Quantification of the effect of plants on weathering: studies in Iceland. Geology 26:895898.2.3.CO;2>CrossRefGoogle Scholar
Nützel, A., and Schulbert, C. 2005. Facies of two important Early Triassic gastropod Lagerstätten: implications for diversity patterns in the aftermath of the end-Permian mass extinction. Facies 51:480500.CrossRefGoogle Scholar
Pacaud, J.-M., Merle, D., and Meyer, J.-C. 2000. La fauna Danienne de Vigny (Val d'Oise, France): importance pour l'étude de la diversification des mollusques au debut du Tertiaire. Comptes Rendus de l'Académie des Sciences de Paris, Sciences de la Terre et des Planètes 330:867873.Google Scholar
Payne, J. L., Lehrmann, D. J., Wei, J., Orchard, M. J., Schrag, D. P., and Knoll, A. H. 2004. Large perturbations of the carbon cycle during recovery from the end-Permian extinction. Science 305:506509.CrossRefGoogle ScholarPubMed
Pearson, P. N. 1992. Survivorship analysis of fossil taxa when real-time extinction rates vary: the Paleogene planktonic Foraminifera. Paleobiology 18:115131.CrossRefGoogle Scholar
Peters, S. E., Kelly, D. C., and Fraass, A. J. 2013. Oceanographic controls on the diversity and extinction of planktonic foraminifera. Nature 493:398404.CrossRefGoogle ScholarPubMed
Planavsky, N. J., Rouxel, O. J., Bekker, A., Lalonde, S. V., Konhauser, K. O., Reinhard, C. T., and Lyons, T. W. 2010. The evolution of the marine phosphate reservoir. Nature 467:10881090.CrossRefGoogle ScholarPubMed
Poitrineau, K., Brown, S. P., and Hochberg, M. P. 2004. The joint evolution of defense and inducibility against natural enemies. Journal of Theoretical Biology 231:389396.CrossRefGoogle ScholarPubMed
Polis, G. A., Anderson, W. B., and Holt, R. D. 1997. Toward an integration of landscape and food web ecologies: the dynamics of spatially subsidized food webs. Annual Review of Ecology, Evolution, and Systematics 28:289316.CrossRefGoogle Scholar
Pyenson, N. D., and Lindberg, D. R. 2011. What happened to gray whales during the Pleistocene? The ecological impact of sea-level change on benthic feeding areas in the North Pacific Ocean. PLoS ONE 6:e21295. doi: 10.1371/journal.pone.0021295.CrossRefGoogle ScholarPubMed
Rabosky, D. L. 2009. Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. Ecology Letters 12:735743.CrossRefGoogle ScholarPubMed
Ricklefs, R. E. 2006. Global variation in the diversification rate of passerine birds. Ecology 87:24682478.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., and Cox, G. W. 1972. Taxon cycles in the West Indian avifauna. American Naturalist 106:195219.CrossRefGoogle Scholar
Risch, T. S., Dobson, F. S., and Murie, J. O. 1995. Is mean litter size the most productive? A test in Columbian ground squirrels. Ecology 76:16431654.CrossRefGoogle Scholar
Roopnarine, P. D. 2001. The description and classification of evolutionary mode: a computational approach. Paleobiology 27:446465.2.0.CO;2>CrossRefGoogle Scholar
Roopnarine, P. D. 2003. Analysis of rates of morphologic evolution. Annual Review of Ecology, Evolution, and Systematics 34:605632.CrossRefGoogle Scholar
Roopnarine, P. D. 2006. Extinction cascades and catastrophe in ancient food webs. Paleobiology 32:119.CrossRefGoogle Scholar
Roopnarine, P. D. 2012. Red queen for a day: models of symmetry and selection in paleoecology. Evolutionary Ecology 26:110.CrossRefGoogle Scholar
Roopnarine, P. D. 2013. Ecology and the tragedy of the commons. Sustainability 5:749773.CrossRefGoogle Scholar
Roopnarine, P. D., and Angielczyk, K. D. 2012. The evolutionary palaeoecology of species and the tragedy of the commons. Biology Letters 8:147150.CrossRefGoogle ScholarPubMed
Roopnarine, P. D., Angielczyk, K. D., Wang, S. C., and Hertog, R. 2007. Trophic network models explain instability of Early Triassic terrestrial communities. Proceedings of the Royal Society of London B 274:20772086.Google ScholarPubMed
Rosenzweig, M. L., Brown, J. S., and Vincent, T. L. 1987. Red Queens and ESS: the coevolution of evolutionary rates. Evolutionary Ecology 1:5994.CrossRefGoogle Scholar
Seger, J., and Stubblefield, J. W. 1996. Optimization and adaptation. Pp. 93123inRose, M. R. and Lauder, G. V., eds. Adaptation. Academic Press, San Diego.Google Scholar
Sepkoski, J. J. Jr. 1996. Competition in macroevolution: the double wedge revisited. Pp. 211255inErwin, D. H. and Lipps, J. H., eds. Evolutionary paleobiology: in honor of James W. Valentine. University of Chicago Press, Chicago.Google Scholar
Stanley, S. M. 1979. Macroevolution: pattern and process. W. H. Freeman, San Francisco.Google Scholar
Stanley, S. M. 1986. Population size, extinction, and speciation: the fission effect in Neogene Bivalvia. Paleobiology 12:89110.CrossRefGoogle Scholar
Stanley, S. M. 1990. Delayed recovery and the spacing of mass extinctions. Paleobiology 16:401414.CrossRefGoogle Scholar
Stenseth, N. C., and Maynard Smith, J. 1984. Coevolution in ecosystems: Red Queen evolution or stasis? Evolution 38:870880.CrossRefGoogle ScholarPubMed
Thayer, C. W. 1983. Sediment-mediated biological disturbance and the evolution of marine benthos. Pp. 479625inTevesz, M. J. S. and McCall, P. L., eds. Biotic interactions in Recent and fossil benthic communities. Plenum, New York.CrossRefGoogle Scholar
Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J., and Kuris, A. M. 2003. Introduced species and their missing parasites. Nature 421:628630.CrossRefGoogle ScholarPubMed
Turner, J. S. 2007. The Tinkerer's accomplice: how design emerges from life itself. Harvard University Press, Cambridge.CrossRefGoogle Scholar
Van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1:118.Google Scholar
Van Valen, L. 1975. Group selection, sex, and fossils. Evolution 29:8793.CrossRefGoogle ScholarPubMed
Van Valen, L. 1976. Energy and evolution. Evolutionary Theory 1:179229.Google Scholar
Van Valen, L. 1983. How pervasive is coevolution? Pp. 119inNitecki, M. H., ed. Coevolution. University of Chicago Press, Chicago.Google Scholar
Van Valkenburgh, B., Wang, X., and Damuth, J. 2004. Cope's Rule, hypercarnivory, and extinction in North American canids. Science 306:101104.CrossRefGoogle ScholarPubMed
Venditti, C., Meade, A., and Pagel, M. 2010. Phylogenies reveal new interpretation of speciation and the Red Queen. Nature 463:349352.CrossRefGoogle ScholarPubMed
Vercken, E., Wellenreuther, M., Svensson, E. I., and Mauroy, B. 2012. Don't fall off the adaptation cliff: when asymmetrical fitness selects for suboptimal traits. PLoS ONE 7. doi: 10.1371/journal.pone.0034889.CrossRefGoogle ScholarPubMed
Vermeij, G. J. 1982. Unsuccessful predation and evolution. American Naturalist 120:701720.CrossRefGoogle Scholar
Vermeij, G. J. 1987. Evolution and escalation: an ecological history of life. Princeton University Press, Princeton, N.J.CrossRefGoogle Scholar
Vermeij, G. J. 1991. When biotas meet: understanding biotic interchange. Science 253:10991104.CrossRefGoogle ScholarPubMed
Vermeij, G. J. 1994. The evolutionary interaction among species: selection, escalation, and coevolution. Annual Review of Ecology and Systematics 25:219236.CrossRefGoogle Scholar
Vermeij, G. J. 2001. Innovation and evolution at the edge: origins and fates of gastropods with a labral tooth. Biological Journal of the Linnean Society 72:461508.CrossRefGoogle Scholar
Vermeij, G. J. 2004a. Nature: an economic history. Princeton University Press, Princeton, N.J.CrossRefGoogle Scholar
Vermeij, G. J. 2004b. Ecological avalanches and the two kinds of extinction. Evolutionary Ecology Research 6:315337.Google Scholar
Vermeij, G. J. 2005. Invasion as expectation: a historical fact of life. Pp. 315339inSax, D. F., Stachowicz, J. J., and Gaines, S. D., eds. Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, Mass.Google Scholar
Vermeij, G. J. 2008. Escalation and its role in Jurassic biotic history. Palaeogeography, Palaeoclimatology, Palaeoecology 263:38.CrossRefGoogle Scholar
Vermeij, G. J. 2011. The energetics of modernization: the last one hundred million years of biotic history. Paleontological Research 15:5461.CrossRefGoogle Scholar
Vermeij, G. J. 2012. The evolution of gigantism on temperate seashores. Biological Journal of the Linnean Society 106:776793.CrossRefGoogle Scholar
Vermeij, G. J., and Leigh, E. G. 2011. Natural and human economies compared. Ecosphere 2:116.CrossRefGoogle Scholar
Webb, C. 2003. A complete classification of Darwinian extinction in ecological interactions. American Naturalist 161:183205.CrossRefGoogle ScholarPubMed
Wiens, J. J. 2011. The causes of species richness patterns across space, time, and clades and the role of “ecological limits.” Quarterly Review of Biology 86:7596.CrossRefGoogle ScholarPubMed
Wilson, E. O. 1961. The nature of the taxon cycle in the Melanesian ant fauna. American Naturalist 95:179193.CrossRefGoogle Scholar
Wolfe, L. M. 2002. Why alien invaders succeed: support for the escape-from-enemy hypothesis. American Naturalist 160:705711.CrossRefGoogle ScholarPubMed
Zangerl, A. R., and Rutledge, C. E. 1996. The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. American Naturalist 147:599608.CrossRefGoogle Scholar