The role of biotic forces in driving macroevolution: beyond the Red Queen

A multitude of hypotheses claim that abiotic factors are the main drivers of macroevolutionary change. By contrast, Van Valen's Red Queen hypothesis is often put forward as the sole representative of the view that biotic forcing is the main evolutionary driver. This imbalance of hypotheses does not reflect our current knowledge: theoretical work demonstrates the plausibility of biotically driven long-term evolution, whereas empirical work suggests a central role for biotic forcing in macroevolution. We call for a more pluralistic view of how biotic forces may drive long-term evolution that is compatible with both phenotypic stasis in the fossil record and with non-constant extinction rates. Promising avenues of research include contrasting predictions from relevant theories within ecology and macroevolution, as well as embracing both abiotic and biotic proxies while modelling long-term evolutionary data. By fitting models describing hypotheses of biotically driven macroevolution to data, we could dissect their predictions and transcend beyond pattern description, possibly narrowing the divide between our current understanding of micro- and macroevolution.

[1]  L. V. Valen,et al.  A new evolutionary law , 1973 .

[2]  D. Rankin The social side of Homo economicus. , 2011, Trends in ecology & evolution.

[3]  E. Vrba Paleoclimate and evolution, with emphasis on human origins , 1995 .

[4]  G. Simpson Tempo and mode in evolution. , 1946, Transactions of the New York Academy of Sciences.

[5]  Yasuhiro Takeuchi,et al.  On evolution under symmetric and asymmetric competitions. , 2008, Journal of theoretical biology.

[6]  S. Pimm The complexity and stability of ecosystems , 1984, Nature.

[7]  G. Hunt Measuring rates of phenotypic evolution and the inseparability of tempo and mode , 2012, Paleobiology.

[8]  P. Gingerich Rates of evolution on the time scale of the evolutionary process , 2004, Genetica.

[9]  Geerat J. Vermeij,et al.  Reining in the Red Queen: the dynamics of adaptation and extinction reexamined , 2013, Paleobiology.

[10]  Éva Kisdi,et al.  Red Queen Evolution by Cycles of Evolutionary Branching and Extinction , 2000 .

[11]  Richard Speare,et al.  Spread of Chytridiomycosis Has Caused the Rapid Global Decline and Extinction of Frogs , 2007, EcoHealth.

[12]  Thomas Lenormand,et al.  Gene flow and the limits to natural selection , 2002 .

[13]  Charles C. Elton The Ecology of Invasions by Animals and Plants , 1959, Biodiversity & Conservation.

[14]  D. Rabosky,et al.  Phenotypic Evolution in Fossil Species: Pattern and Process , 2014 .

[15]  J. Bascompte,et al.  Compartmentalization increases food-web persistence , 2011, Proceedings of the National Academy of Sciences.

[16]  Robert M May,et al.  Food-web assembly and collapse: mathematical models and implications for conservation , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[17]  J. Alroy Cenozoic bolide impacts and biotic change in North American mammals. , 2003, Astrobiology.

[18]  B. Drossel,et al.  Evolutionary food web model based on body masses gives realistic networks with permanent species turnover , 2014, Scientific Reports.

[19]  John Alroy,et al.  Geographical, environmental and intrinsic biotic controls on Phanerozoic marine diversification , 2010 .

[20]  J. Sepkoski,et al.  Stratigraphic biases in the analysis of taxonomic survivorship , 1975, Paleobiology.

[21]  John Maynard Smith,et al.  The causes of extinction. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[22]  Genetics, Paleontology, and Macroevolution: Frontmatter , 2001 .

[23]  W. Kiessling,et al.  Testing the role of biological interactions in the evolution of mid-Mesozoic marine benthic ecosystems , 2006, Paleobiology.

[24]  T. Ikegami,et al.  Coevolutionary dynamics of adaptive radiation for food-web development , 2008, Population Ecology.

[25]  E. Mayr Animal Species and Evolution , 1964 .

[26]  M. Hori,et al.  Frequency-Dependent Natural Selection in the Handedness of Scale-Eating Cichlid Fish , 1993, Science.

[27]  E. Nevo,et al.  Is Evolution of Blind Mole Rats Determined by Climate Oscillations? , 2012, PloS one.

[28]  M. Fortescue Pattern and Process: A Whiteheadian perspective on linguistics , 2001 .

[29]  R. Ricklefs,et al.  Darwin's bridge between microevolution and macroevolution , 2009, Nature.

[30]  D. Rabosky Diversity-Dependence, Ecological Speciation, and the Role of Competition in Macroevolution , 2013 .

[31]  Stephen Jay Gould,et al.  The paradox of the first tier: an agenda for paleobiology , 1985, Paleobiology.

[32]  J. Merilä Evolution in response to climate change: In pursuit of the missing evidence , 2012, BioEssays : news and reviews in molecular, cellular and developmental biology.

[33]  U. Dieckmann,et al.  Abrupt community transitions and cyclic evolutionary dynamics in complex food webs☆ , 2013, Journal of theoretical biology.

[34]  A. Zhuravlev,et al.  Escalation and ecological selectively of mineralogy in the Cambrian Radiation of skeletons , 2012 .

[35]  Si Tang,et al.  Stability criteria for complex ecosystems , 2011, Nature.

[36]  A. Behrensmeyer,et al.  Climate change and faunal turnover: testing the mechanics of the turnover-pulse hypothesis with South African fossil data , 2013, Paleobiology.

[37]  Abrams Modelling the adaptive dynamics of traits involved in inter‐ and intraspecific interactions: An assessment of three methods , 2001 .

[38]  N. Stenseth,et al.  COEVOLUTION IN ECOSYSTEMS: RED QUEEN EVOLUTION OR STASIS? , 1984, Evolution; international journal of organic evolution.

[39]  Ulf Dieckmann,et al.  The adaptive dynamics of community structure , 2007 .

[40]  Why the null matters: Statistical tests, random walks and evolution , 2001 .

[41]  W. Kiessling Long-term relationships between ecological stability and biodiversity in Phanerozoic reefs , 2005, Nature.

[42]  Jülich Evolutionary Cycling in Predator – Prey Interactions : Population Dynamics and the Red Queen , 1994 .

[43]  Andreas Wagner,et al.  The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems , 2011 .

[44]  E. Vrba Turnover-pulses, the Red Queen, and related topics , 1993 .

[45]  R. Bambach,et al.  Paleoecologic Megatrends in Marine Metazoa , 2011 .

[46]  S. J. Arnold,et al.  Resolving the Paradox of Stasis: Models with Stabilizing Selection Explain Evolutionary Divergence on All Timescales , 2007, The American Naturalist.

[47]  P. Roopnarine Red queen for a day: models of symmetry and selection in paleoecology , 2011, Evolutionary Ecology.

[48]  B. Rensch,et al.  Evolution above the species level , 1959 .

[49]  Paul Marrow,et al.  The coevolution of predator—prey interactions : ESSS and Red Queen dynamics , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[50]  J. Biesmeijer,et al.  Global pollinator declines: trends, impacts and drivers. , 2010, Trends in ecology & evolution.

[51]  S. Gould The Structure of Evolutionary Theory , 2002 .

[52]  G. Hunt Fitting and comparing models of phyletic evolution: random walks and beyond , 2006, Paleobiology.

[53]  Michael J Benton,et al.  The Red Queen and the Court Jester: Species Diversity and the Role of Biotic and Abiotic Factors Through Time , 2009, Science.

[54]  Robert M. May,et al.  Stability and Complexity in Model Ecosystems , 2019, IEEE Transactions on Systems, Man, and Cybernetics.

[55]  L. H. Liow,et al.  Red Queen: from populations to taxa and communities. , 2011, Trends in ecology & evolution.

[56]  J. Sepkoski,et al.  Competitive displacement among post-Paleozoic cyclostome and cheilostome bryozoans , 2000, Paleobiology.

[57]  G. Vermeij Evolution and Escalation: An Ecological History of Life , 1987 .

[58]  S. Chenoweth,et al.  Intralocus sexual conflict. , 2009, Trends in ecology & evolution.

[59]  H. Wernli,et al.  Global Genetic Change Tracks Global Climate Warming in Drosophila subobscura , 2006 .

[60]  M R Kearney,et al.  A Rapid Shift in a Classic Clinal Pattern in Drosophila Reflecting Climate Change , 2005, Science.

[61]  S. Lidgard,et al.  Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation , 1999, Paleobiology.

[62]  A. Barnosky,et al.  DISTINGUISHING THE EFFECTS OF THE RED QUEEN AND COURT JESTER ON MIOCENE MAMMAL EVOLUTION IN THE NORTHERN ROCKY MOUNTAINS , 2001 .

[63]  U Dieckmann,et al.  Evolutionary Cycling of Predator-Prey Interactions : Population Dynamics and the Red Queen , 1999 .

[64]  Charles C. Elton,et al.  The Ecology of Invasions by Animals and Plants. , 1959 .

[65]  D. Schluter,et al.  The Ecology of Adaptive Radiation , 2000 .

[66]  B. Lieberman Adaptive Radiations in the Context of Macroevolutionary Theory: A Paleontological Perspective , 2012, Evolutionary Biology.

[67]  A. Hoffman Testing the Red Queen Hypothesis , 1991 .

[68]  D. Houle Comparing evolvability and variability of quantitative traits. , 1992, Genetics.

[69]  J. Bengtsson Interspecific competition increases local extinction rate in a metapopulation system , 1989, Nature.

[70]  S. J. Arnold Phenotypic Evolution: The Ongoing Synthesis , 2014, The American Naturalist.

[71]  Thomas L. Vincent,et al.  Red Queens and ESS: the coevolution of evolutionary rates , 2005, Evolutionary Ecology.

[72]  Barbara Drossel,et al.  When do evolutionary food web models generate complex networks? , 2013, Journal of theoretical biology.

[73]  David M. Raup,et al.  Taxonomic survivorship curves and Van Valen's Law , 1975, Paleobiology.

[74]  R. Macarthur Fluctuations of Animal Populations and a Measure of Community Stability , 1955 .

[75]  Tracy Aze,et al.  Interplay Between Changing Climate and Species’ Ecology Drives Macroevolutionary Dynamics , 2011, Science.

[76]  J. Samuels,et al.  Evolution in coyotes (Canis latrans) in response to the megafaunal extinctions , 2012, Proceedings of the National Academy of Sciences.

[77]  T. Benton,et al.  Biodiversity tracks temperature over time , 2012, Proceedings of the National Academy of Sciences.

[78]  T. F. Hansen,et al.  Heritability is not Evolvability , 2011, Evolutionary Biology.

[79]  M. Friberg,et al.  Selective Predation on Wing Morphology in Sympatric Damselflies , 2007, The American Naturalist.

[80]  P. Mein,et al.  Long-period astronomical forcing of mammal turnover , 2006, Nature.

[81]  David Jablonski,et al.  Biotic Interactions and Macroevolution: Extensions and Mismatches Across Scales and Levels , 2008, Evolution; international journal of organic evolution.

[82]  Arnold I. Miller,et al.  Biotic transitions in global marine diversity. , 1998, Science.

[83]  R. A. Fisher,et al.  The Genetical Theory of Natural Selection , 1931 .

[84]  G. Vermeij THE EVOLUTIONARY INTERACTION AMONG SPECIES: Selection, Escalation, and Coevolution , 1994 .

[85]  E. Saupe,et al.  A macroevolutionary expansion of the modern synthesis and the importance of extrinsic abiotic factors , 2013 .

[86]  Takashi Ikegami,et al.  Food-web formation with recursive evolutionary branching. , 2006, Journal of theoretical biology.

[87]  Jeffrey S. Levinton,et al.  Genetics, Paleontology, and Macroevolution: References , 2001 .

[88]  W. Bradshaw,et al.  Genetic shift in photoperiodic response correlated with global warming , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[89]  L. W. Alvarez,et al.  Extraterrestrial Cause for the Cretaceous-Tertiary Extinction , 1980, Science.

[90]  R. Ferrière,et al.  Unifying evolutionary dynamics: from individual stochastic processes to macroscopic models. , 2006, Theoretical population biology.

[91]  J. Maynard Smith,et al.  A Comment on the Red Queen , 1976, The American Naturalist.

[92]  J. Downing,et al.  Biodiversity and stability in grasslands , 1996, Nature.

[93]  Josef C. Uyeda,et al.  The million-year wait for macroevolutionary bursts , 2011, Proceedings of the National Academy of Sciences.

[94]  A. Hoffman,et al.  Evolution in a pelagic planktic system: A paleobiologic test of models of multispecies evolution , 1984, Paleobiology.

[95]  D. Wake,et al.  On the problem of stasis in organismal evolution , 1983 .