Phylogenetically patterned speciation rates and extinction risks change the loss of evolutionary history during extinctions

If we are to plan conservation strategies that minimize the loss of evolutionary history through human–caused extinctions, we must understand how this loss is related to phylogenetic patterns in current extinction risks and past speciation rates. Nee & May (1997, Science 278, 692–694) showed that for a randomly evolving clade (i) a single round of random extinction removed relatively little evolutionary history, and (ii) extinction management (choosing which taxa to sacrifice) offered only marginal improvement. However, both speciation rates and extinction risks vary across lineages within real clades. We simulated evolutionary trees with phylogenetically patterned speciation rates and extinction risks (closely related lineages having similar rates and risks) and then subjected them to several biologically informed models of extinction. Increasing speciation rate variation increases the extinction–management pay–off. When extinction risks vary among lineages but are uncorrelated with speciation rates, extinction removes more history (compared with random trees), but the difference is small. When extinction risks vary and are correlated with speciation rates, history loss can dramatically increase (negative correlation) or decrease (positive correlation) with speciation rate variation. The loss of evolutionary history via human–caused extinctions may therefore be more severe, yet more manageable, than first suggested.

[1]  S. Stanley,et al.  Macroevolution: Pattern and Process , 1980 .

[2]  Michael M. McKinney,et al.  Present and Future Taxonomic Selectivity in Bird and Mammal Extinctions , 1998 .

[3]  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.

[4]  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.

[5]  M. Mckinney Extinction Vulnerability and Selectivity: Combining Ecological and Paleontological Views , 1997 .

[6]  Paul H. Williams,et al.  What to protect?—Systematics and the agony of choice , 1991 .

[7]  K. Gaston,et al.  Evolutionary age and risk of extinction in the global avifauna , 1997, Evolutionary Ecology.

[8]  A. Hughes Differential human impact on the survival of genetically distinct avian lineages , 1999, Bird Conservation International.

[9]  R. Crozier Preserving the Information Content of Species: Genetic Diversity, Phylogeny, and Conservation Worth , 1997 .

[10]  W. Newmark,et al.  Extinction of mammal populations in Western North American national parks , 1995 .

[11]  R. Allen World conservation strategy. Living resource conservation for sustainable development. , 1980 .

[12]  J. L. Gittleman,et al.  Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia) , 1999, Biological reviews of the Cambridge Philosophical Society.

[13]  John H. Lawton,et al.  Population dynamic principles , 1994 .

[14]  C. Humphries,et al.  MEASURING BIODIVERSITY VALUE FOR CONSERVATION , 1995 .

[15]  Arne Ø. Mooers,et al.  Inferring Evolutionary Process from Phylogenetic Tree Shape , 1997, The Quarterly Review of Biology.

[16]  Peter L. Forey,et al.  Systematics and conservation evaluation , 1994 .

[17]  A. Ives,et al.  Reptile Extinctions on Land‐Bridge Islands: Life‐History Attributes and Vulnerability to Extinction , 1999, The American Naturalist.

[18]  Y. Gaudemer,et al.  Effects of mass extinctions on biodiversity , 1996, Nature.

[19]  I. Owens,et al.  Variation in extinction risk among birds: chance or evolutionary predisposition? , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  D. Raup Size of the Permo-Triassic Bottleneck and Its Evolutionary Implications , 1979, Science.

[21]  C. Krajewski Phylogeny and Diversity , 1991, Science.

[22]  Michael Taylor Diversity of life , 1994, Nature.

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

[24]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[25]  Brian Groombridge,et al.  1996 IUCN Red List of Threatened Animals , 1996 .

[26]  Robert M. May,et al.  Taxonomy as destiny , 1990, Nature.

[27]  S. Stanley A theory of evolution above the species level. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Diego P Vézquez,et al.  Biodiversity conservation: Does phylogeny matter? , 1998, Current Biology.

[29]  M. Slatkin,et al.  SEARCHING FOR EVOLUTIONARY PATTERNS IN THE SHAPE OF A PHYLOGENETIC TREE , 1993, Evolution; international journal of organic evolution.

[30]  G. Yule,et al.  A Mathematical Theory of Evolution Based on the Conclusions of Dr. J. C. Willis, F.R.S. , 1925 .

[31]  D. Faith Conservation evaluation and phylogenetic diversity , 1992 .

[32]  R M May,et al.  Extinction and the loss of evolutionary history. , 1997, Science.

[33]  C. Guyer,et al.  COMPARISONS OF OBSERVED PHYLOGENETIC TOPOLOGIES WITH NULL EXPECTATIONS AMONG THREE MONOPHYLETIC LINEAGES , 1991, Evolution; international journal of organic evolution.

[34]  Linda Partridge,et al.  These hierarchical views of life: phylogenies and metapopulations , 1991 .

[35]  K. Gaston,et al.  Birds, body size and the threat of extinction , 1995 .

[36]  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.

[37]  M. Benton,et al.  Diversification and extinction in the history of life. , 1995, Science.

[38]  C. Guyer,et al.  ADAPTIVE RADIATION AND THE TOPOLOGY OF LARGE PHYLOGENIES , 1993, Evolution; international journal of organic evolution.

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

[40]  D. Jablonski Background and Mass Extinctions: The Alternation of Macroevolutionary Regimes , 1986, Science.

[41]  Mark Kirkpatrick,et al.  SHAPE OF A PHYLOGENETIC TREE , 1993 .

[42]  Kevin J. Gaston,et al.  Do Conservationists and Molecular Biologists Value Differences between Organisms in the Same Way , 1994 .

[43]  S. Heard,et al.  Key evolutionary innovations and their ecological mechanisms , 1995 .

[44]  S. Heard,et al.  PATTERNS IN TREE BALANCE AMONG CLADISTIC, PHENETIC, AND RANDOMLY GENERATED PHYLOGENETIC TREES , 1992, Evolution; international journal of organic evolution.

[45]  S. Altschul,et al.  Equal animals , 1990, Nature.

[46]  S. Heard,et al.  PATTERNS IN PHYLOGENETIC TREE BALANCE WITH VARIABLE AND EVOLVING SPECIATION RATES , 1996, Evolution; international journal of organic evolution.

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

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

[49]  E. Vrba,et al.  Individuals, hierarchies and processes: towards a more complete evolutionary theory , 1984, Paleobiology.

[50]  D. Jablonski,et al.  Heritability at the Species Level: Analysis of Geographic Ranges of Cretaceous Mollusks , 1987, Science.

[51]  M. Benton,et al.  Evolutionary patterns from mass originations and mass extinctions. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.