Clade Age and Not Diversification Rate Explains Species Richness among Animal Taxa

Animal taxa show remarkable variability in species richness across phylogenetic groups. Most explanations for this disparity postulate that taxa with more species have phenotypes or ecologies that cause higher diversification rates (i.e., higher speciation rates or lower extinction rates). Here we show that clade longevity, and not diversification rate, has primarily shaped patterns of species richness across major animal clades: more diverse taxa are older and thus have had more time to accumulate species. Diversification rates calculated from 163 species‐level molecular phylogenies were highly consistent within and among three major animal phyla (Arthropoda, Chordata, Mollusca) and did not correlate with species richness. Clades with higher estimated diversification rates were younger, but species numbers increased with increasing clade age. A fossil‐based data set also revealed a strong, positive relationship between total extant species richness and crown group age across the orders of insects and vertebrates. These findings do not negate the importance of ecology or phenotype in influencing diversification rates, but they do show that clade longevity is the dominant signal in major animal biodiversity patterns. Thus, some key innovations may have acted through fostering clade longevity and not by heightening diversification rate.

[1]  A. Møller,et al.  SPECIATION AND FEATHER ORNAMENTATION IN BIRDS , 1998, Evolution; international journal of organic evolution.

[2]  J. Dransfield,et al.  The Tropical Flora Remains Undercollected , 2000 .

[3]  Harry F. Recher,et al.  On the Relation between Habitat Selection and Species Diversity , 1966, The American Naturalist.

[4]  D. Jablonski,et al.  Larval Ecology, Geographic Range, and Species Survivorship in Cretaceous Mollusks: Organismic versus Species‐Level Explanations , 2006, The American Naturalist.

[5]  W. B. Harland,et al.  A Geologic time scale , 1982 .

[6]  P. Harvey,et al.  Sexual selection and taxonomic diversity in passerine birds , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  G. E. Hutchinson,et al.  A Theoretical Ecological Model of Size Distributions Among Species of Animals , 1959, The American Naturalist.

[8]  J. da Silva,et al.  Diversity in Relation to Body Size in Mammals: A Comparative Study , 1999, The American Naturalist.

[9]  S. Stanley,et al.  AN EXPLANATION FOR COPE'S RULE , 1973, Evolution; international journal of organic evolution.

[10]  E. Wilson The Diversity of Life , 1992 .

[11]  S. Pruett-Jones,et al.  Species Richness Covaries with Mating System in Birds , 1996 .

[12]  Michael J. Benton,et al.  The fossil record 2 , 1993 .

[13]  C. Orme,et al.  Body size does not predict species richness among the metazoan phyla , 2002 .

[14]  K. Dial,et al.  Are the Smallest Organisms the Most Diverse , 1988 .

[15]  J. S. Nelson,et al.  Fishes of the world. , 1978 .

[16]  Kate E. Jones,et al.  Multiple Causes of High Extinction Risk in Large Mammal Species , 2005, Science.

[17]  T. Britton,et al.  Phylogenetic dating with confidence intervals using mean path lengths. , 2002, Molecular phylogenetics and evolution.

[18]  C. Pond,et al.  Walker's Mammals of the World, 4th Edition, Ronald M. Nowak, John L. Paradiso. The Johns Hopkins University Press, Baltimore, Maryland (1983), 1xi, +1-568 (Vol. I), xxv+569-1362 (Vol. II). Price $65.00 , 1984 .

[19]  A. Brower Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[20]  J. Sepkoski,et al.  Rates of speciation in the fossil record. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[21]  P. Wagner Diversity patterns among early gastropods: contrasting taxonomic and phylogenetic descriptions , 1995, Paleobiology.

[22]  J. L. Gittleman,et al.  Body size and species–richness in carnivores and primates , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[23]  R. Ricklefs Global variation in the diversification rate of passerine birds. , 2006, Ecology.

[24]  L. V. Van BODY SIZE AND NUMBERS OF PLANTS AND ANIMALS. , 1973 .

[25]  G. Bechly Morphologische Untersuchungen am Flugelgeader der rezenten Libellen und deren Stammgruppenvertreter (Insecta ; Pterygota ; Odonata) unter besonderer Berucksichtigung der phylogenetischen Systematik und des Grundplanes der Odonata , 1996 .

[26]  J. Sepkoski,et al.  Insect diversity in the fossil record. , 1993, Science.

[27]  W. Norton,et al.  Extinction: bad genes or bad luck? , 1991, New scientist.

[28]  S. P. Parker Synopsis and classification of living organisms , 1982 .

[29]  P. Herendeen,et al.  Phylogenetic pattern, diversity, and diversification of Eudicots , 1999 .

[30]  P. Coley,et al.  Insect herbivory, plant defense, and early Cenozoic climate change , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Sepkoski,et al.  A kinetic model of Phanerozoic taxonomic diversity II. Early Phanerozoic families and multiple equilibria , 1979, Paleobiology.

[32]  C. Mitter,et al.  Diversification of Carnivorous Parasitic Insects: Extraordinary Radiation or Specialized Dead End? , 1993, The American Naturalist.

[33]  C. Wiklund,et al.  Sexual selection and speciation in mammals, butterflies and spiders , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  M. Sanderson,et al.  ABSOLUTE DIVERSIFICATION RATES IN ANGIOSPERM CLADES , 2001, Evolution; international journal of organic evolution.

[35]  L. V. Valen BODY SIZE AND NUMBERS OF PLANTS AND ANIMALS. , 1973 .

[36]  Arnold I. Miller,et al.  Modeling bivalve diversification: the effect of interaction on a macroevolutionary system , 1988, Paleobiology.

[37]  Robert M. May,et al.  How Many Species Are There on Earth? , 1988, Science.

[38]  D. Jablonski The biology of mass extinction: a palaeontological view. , 1989, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[39]  S. Nee,et al.  INFERRING SPECIATION RATES FROM PHYLOGENIES , 2001, Evolution; international journal of organic evolution.

[40]  I. Owens,et al.  Species richness among birds: body size, life history, sexual selection or ecology? , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[41]  M. Arnold,et al.  Spurring plant diversification: are floral nectar spurs a key innovation? , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  L. Trueb,et al.  Biology of Amphibians , 1986 .

[43]  M. Sanderson,et al.  Age and rate of diversification of the Hawaiian silversword alliance (Compositae). , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  I. Owens,et al.  Species richness in agamid lizards: chance, body size, sexual selection or ecology? , 2003, Journal of evolutionary biology.

[45]  G. Arnqvist,et al.  Sexual conflict promotes speciation in insects. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Brian D. Farrell,et al.  The Phylogenetic Study of Adaptive Zones: Has Phytophagy Promoted Insect Diversification? , 1988, The American Naturalist.

[47]  T. Hansen,et al.  Larval Dispersal and Species Longevity in Lower Tertiary Gastropods , 1978, Science.

[48]  E. H. Morrow,et al.  No evidence that sexual selection is an ‘engine of speciation’ in birds , 2003 .

[49]  Robert M. May,et al.  The Search for Patterns in the Balance of Nature: Advances and Retreats , 1986 .

[50]  D. Grimaldi,et al.  Evolution of the insects , 2005 .

[51]  R M May,et al.  The reconstructed evolutionary process. , 1994, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  E C Dickinson,et al.  THE HOWARD AND MOORE COMPLETE CHECKLIST OF THE BIRDS OF THE WORLD. 4 th EDITION VOLUME 2 (2014) , 2003 .

[53]  J. Alroy Constant extinction, constrained diversification, and uncoordinated stasis in North American mammals , 1996 .

[54]  P H Harvey,et al.  Tempo and mode of evolution revealed from molecular phylogenies. , 1992, Proceedings of the National Academy of Sciences of the United States of America.