EXTINCTION, ECOLOGICAL OPPORTUNITY, AND THE ORIGINS OF GLOBAL SNAKE DIVERSITY

Snake diversity varies by at least two orders of magnitude among extant lineages, with numerous groups containing only one or two species, and several young clades exhibiting exceptional richness (>700 taxa). With a phylogeny containing all known families and subfamilies, we find that these patterns cannot be explained by background rates of speciation and extinction. The majority of diversity appears to derive from a radiation within the superfamily Colubroidea, potentially stemming from the colonization of new areas and the evolution of advanced venom‐delivery systems. In contrast, negative relationships between clade age, clade size, and diversification rate suggest the potential for possible bias in estimated diversification rates, interpreted by some recent authors as support for ecologically mediated limits on diversity. However, evidence from the fossil record indicates that numerous lineages were far more diverse in the past, and that extinction has had an important impact on extant diversity patterns. Thus, failure to adequately account for extinction appears to prevent both rate‐ and diversity‐limited models from fully characterizing richness dynamics in snakes. We suggest that clade‐level extinction may provide a key mechanism for explaining negative or hump‐shaped relationships between clade age and diversity, and the prevalence of ancient, species‐poor lineages in numerous groups.

[1]  J. Wiens,et al.  The Causes Of Species Richness Patterns Across Space, Time, And Clades And The Role Of “Ecological Limits” , 2011, The Quarterly Review of Biology.

[2]  F. Lapointe,et al.  Retrieving a mitogenomic mammal tree using composite taxa. , 2011, Molecular phylogenetics and evolution.

[3]  L. Vitt,et al.  The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. , 2011, Molecular phylogenetics and evolution.

[4]  L. Vitt,et al.  Coming to America: multiple origins of New World geckos , 2011, Journal of evolutionary biology.

[5]  H. Ota,et al.  Accommodating heterogenous rates of evolution in molecular divergence dating methods: an example using intercontinental dispersal of Plestiodon (Eumeces) lizards. , 2011, Systematic biology.

[6]  Caitlin A. Kuczynski,et al.  Combining phylogenomics and fossils in higher-level squamate reptile phylogeny: molecular data change the placement of fossil taxa. , 2010, Systematic biology.

[7]  D. Rabosky Primary controls on species richness in higher taxa. , 2010, Systematic biology.

[8]  D. Gower,et al.  Phylogeny and divergence times of filesnakes (Acrochordus): inferences from morphology, fossils and three molecular loci. , 2010, Molecular phylogenetics and evolution.

[9]  Ziheng Yang,et al.  The Timetree of Life , 2010 .

[10]  S. Hedges,et al.  Blindsnake evolutionary tree reveals long history on Gondwana , 2010, Biology Letters.

[11]  W. Godsoe,et al.  Ecological opportunity and the origin of adaptive radiations , 2010, Journal of evolutionary biology.

[12]  A. Waldron LINEAGES THAT CHEAT DEATH: SURVIVING THE SQUEEZE ON RANGE SIZE , 2010, Evolution; international journal of organic evolution.

[13]  D. Futuyma EVOLUTIONARY CONSTRAINT AND ECOLOGICAL CONSEQUENCES , 2010, Evolution; international journal of organic evolution.

[14]  Daniel L Rabosky,et al.  EXTINCTION RATES SHOULD NOT BE ESTIMATED FROM MOLECULAR PHYLOGENIES , 2010, Evolution; international journal of organic evolution.

[15]  Jonathan B. Losos,et al.  Adaptive Radiation, Ecological Opportunity, and Evolutionary Determinism , 2010, The American Naturalist.

[16]  M. Massot,et al.  Erosion of Lizard Diversity by Climate Change and Altered Thermal Niches , 2010, Science.

[17]  W. Jetz,et al.  More than “More Individuals”: The Nonequivalence of Area and Energy in the Scaling of Species Richness , 2010, The American Naturalist.

[18]  D. Rabosky,et al.  Reinventing species selection with molecular phylogenies. , 2010, Trends in ecology & evolution.

[19]  R. A. Pyron,et al.  HOW DOES ECOLOGICAL OPPORTUNITY INFLUENCE RATES OF SPECIATION, EXTINCTION, AND MORPHOLOGICAL DIVERSIFICATION IN NEW WORLD RATSNAKES (TRIBE LAMPROPELTINI)? , 2009, Evolution; international journal of organic evolution.

[20]  F. Lapointe,et al.  The use and validity of composite taxa in phylogenetic analysis. , 2009, Systematic biology.

[21]  Chad D. Brock,et al.  Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates , 2009, Proceedings of the National Academy of Sciences.

[22]  D. Rabosky Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions. , 2009, Ecology letters.

[23]  R. A. Pyron,et al.  Can the tropical conservatism hypothesis explain temperate species richness patterns? An inverse latitudinal biodiversity gradient in the New World snake tribe Lampropeltini , 2009 .

[24]  D. Rabosky Ecological Limits on Clade Diversification in Higher Taxa , 2009, The American Naturalist.

[25]  Philip D. Gingerich,et al.  Rates of Evolution , 2009 .

[26]  Christopher M. R. Kelly,et al.  Phylogeny, biogeography and classification of the snake superfamily Elapoidea: a rapid radiation in the late Eocene , 2009, Cladistics : the international journal of the Willi Hennig Society.

[27]  Sudhir Kumar,et al.  The timetree of life , 2009 .

[28]  Dolph Schluter,et al.  Speciation and patterns of diversity , 2009 .

[29]  S. Hedges,et al.  Dissecting the major African snake radiation: a molecular phylogeny of the Lamprophiidae Fitzinger (Serpentes, Caenophidia) , 2008 .

[30]  David Jablonski,et al.  Species Selection: Theory and Data , 2008 .

[31]  D. Posada jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[32]  Caitlin A. Kuczynski,et al.  Branch lengths, support, and congruence: testing the phylogenomic approach with 20 nuclear loci in snakes. , 2008, Systematic biology.

[33]  R. A. Pyron,et al.  The taming of the skew: estimating proper confidence intervals for divergence dates. , 2008, Systematic biology.

[34]  Holger Scheib,et al.  Evolution of an Arsenal , 2008, Molecular & Cellular Proteomics.

[35]  J. Rage,et al.  A Diverse Snake Fauna from the Early Eocene of Vastan Lignite Mine, Gujarat, India , 2008 .

[36]  Luke J. Harmon,et al.  GEIGER: investigating evolutionary radiations , 2008, Bioinform..

[37]  I. Lovette,et al.  Exceptional among-lineage variation in diversification rates during the radiation of Australia's most diverse vertebrate clade , 2007, Proceedings of the Royal Society B: Biological Sciences.

[38]  J. Crampton,et al.  Rise and Fall of Species Occupancy in Cenozoic Fossil Mollusks , 2007, Science.

[39]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[40]  R. Ricklefs,et al.  Estimating diversification rates from phylogenetic information. , 2007, Trends in ecology & evolution.

[41]  M. Foote Symmetric waxing and waning of marine invertebrate genera , 2007, Paleobiology.

[42]  R. Ricklefs,et al.  Evolutionary diversification of clades of squamate reptiles , 2007, Journal of evolutionary biology.

[43]  Nancy Knowlton,et al.  Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. , 2007, Ecology letters.

[44]  Mark A McPeek,et al.  Clade Age and Not Diversification Rate Explains Species Richness among Animal Taxa , 2007, The American Naturalist.

[45]  A. Couloux,et al.  The phylogeny and classification of caenophidian snakes inferred from seven nuclear protein-coding genes. , 2007, Comptes rendus biologies.

[46]  Daniel L Rabosky,et al.  LASER: A Maximum Likelihood Toolkit for Detecting Temporal Shifts in Diversification Rates From Molecular Phylogenies , 2006, Evolutionary bioinformatics online.

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

[48]  B. Noonan,et al.  Dispersal and vicariance: the complex evolutionary history of boid snakes. , 2006, Molecular phylogenetics and evolution.

[49]  S. Ho,et al.  Relaxed Phylogenetics and Dating with Confidence , 2006, PLoS biology.

[50]  S. Hedges,et al.  Early evolution of the venom system in lizards and snakes , 2006, Nature.

[51]  B. Young,et al.  Widespread amphibian extinctions from epidemic disease driven by global warming , 2006, Nature.

[52]  C. Graham,et al.  Niche Conservatism: Integrating Evolution, Ecology, and Conservation Biology , 2005 .

[53]  D. Gower,et al.  The phylogenetic position of Anomochilidae (Reptilia: Serpentes): first evidence from DNA sequences , 2005 .

[54]  C. Orme,et al.  TESTING FOR LATITUDINAL BIAS IN DIVERSIFICATION RATES: AN EXAMPLE USING NEW WORLD BIRDS , 2005 .

[55]  J. Head,et al.  FIRST REPORT OF SNAKES (SERPENTES) FROM THE LATE MIDDLE EOCENE PONDAUNG FORMATION, MYANMAR , 2005 .

[56]  K. Gaston,et al.  Species‐energy relationships at the macroecological scale: a review of the mechanisms , 2005, Biological reviews of the Cambridge Philosophical Society.

[57]  J. D.,et al.  The phylogenetic position of Anomochilidae ( Reptilia : Serpentes ) : first evidence from DNA sequences , 2005 .

[58]  M. Donoghue,et al.  Historical biogeography, ecology and species richness. , 2004, Trends in ecology & evolution.

[59]  F. Burbrink,et al.  A molecular approach to discerning the phylogenetic placement of the enigmatic snake Xenophidion schaeferi among the Alethinophidia , 2004 .

[60]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[61]  F. Bokma TESTING FOR EQUAL RATES OF CLADOGENESIS IN DIVERSE TAXA , 2003, Evolution; international journal of organic evolution.

[62]  R. Kini,et al.  Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionary and toxinological implications , 2003 .

[63]  P. Stephens,et al.  Explaining Species Richness from Continents to Communities: The Time‐for‐Speciation Effect in Emydid Turtles , 2002, The American Naturalist.

[64]  S. Hedges,et al.  Higher-level relationships of snakes inferred from four nuclear and mitochondrial genes. , 2002, Comptes rendus biologies.

[65]  B. Rannala Identi(cid:142)ability of Parameters in MCMC Bayesian Inference of Phylogeny , 2002 .

[66]  D. Jablonski Survival without recovery after mass extinctions , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[68]  D. Schluter,et al.  Analysis of an evolutionary species–area relationship , 2000, Nature.

[69]  O. Rieppel,et al.  A fossil snake with limbs. , 2000, Science.

[70]  J. Holman Fossil snakes of North America : origin, evolution, distribution, paleoecology , 2000 .

[71]  J. Sepkoski,et al.  Evolutionary and preservational constraints on origins of biologic groups: divergence times of eutherian mammals. , 1999, Science.

[72]  H. Zaher Hemipenial morphology of the South American xenodontine snakes : with a proposal for a monophyletic Xenodontinae and a reappraisal of colubroid hemipenes. Bulletin of the AMNH ; no. 240 , 1999 .

[73]  S. J. Arnold,et al.  Snakes, the evolution of mystery in nature , 1998 .

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

[75]  K. Campbell,et al.  Rates of Evolution , 1987 .

[76]  David M. Raup,et al.  Mathematical models of cladogenesis , 1985, Paleobiology.

[77]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[78]  J. W. Valentine,et al.  Equilibrium Models of Evolutionary Species Diversity and the Number of Empty Niches , 1984, The American Naturalist.

[79]  F. Vuilleumier FAUNAL TURNOVER AND DEVELOPMENT OF FOSSIL AVIFAUNAS IN SOUTH AMERICA , 1984, Evolution; international journal of organic evolution.

[80]  M. Slatkin,et al.  The improbability of animal phyla with few species , 1983, Paleobiology.

[81]  J. Levinton A Theory of Diversity Equilibrium and Morphological Evolution , 1979, Science.

[82]  Stephen Jay Gould,et al.  The shape of evolution: a comparison of real and random clades , 1977, Paleobiology.

[83]  Explanation of large scale extinctions of lower vertebrates , 1976, Nature.

[84]  L. V. Valen GROUP SELECTION, SEX, AND FOSSILS. , 1975 .

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

[86]  A. G. Fischer LATITUDINAL VARIATIONS IN ORGANIC DIVERSITY , 1960 .

[87]  S. A. Barnett,et al.  The major features of evolution , 1955 .