Latitude, elevational climatic zonation and speciation in New World vertebrates

Many biodiversity hotspots are located in montane regions, especially in the tropics. A possible explanation for this pattern is that the narrow thermal tolerances of tropical species and greater climatic stratification of tropical mountains create more opportunities for climate-associated parapatric or allopatric speciation in the tropics relative to the temperate zone. However, it is unclear whether a general relationship exists among latitude, climatic zonation and the ecology of speciation. Recent taxon-specific studies obtained different results regarding the role of climate in speciation in tropical versus temperate areas. Here, we quantify overlap in the climatic distributions of 93 pairs of sister species of mammals, birds, amphibians and reptiles restricted to either the New World tropics or to the Northern temperate zone. We show that elevational ranges of tropical- and temperate-zone species do not differ from one another, yet the temperature range experienced by species in the temperate zone is greater than for those in the tropics. Moreover, tropical sister species tend to exhibit greater similarity in their climatic distributions than temperate sister species. This pattern suggests that evolutionary conservatism in the thermal niches of tropical taxa, coupled with the greater thermal zonation of tropical mountains, may result in increased opportunities for allopatric isolation, speciation and the accumulation of species in tropical montane regions. Our study exemplifies the power of combining phylogenetic and spatial datasets of global climatic variation to explore evolutionary (rather than purely ecological) explanations for the high biodiversity of tropical montane regions.

[1]  R. Wayne,et al.  Evaluating the divergence-with-gene-flow model in natural populations: the importance of ecotones in rainforest speculation , 2005 .

[2]  T. Kunz,et al.  Molecular phylogeny of New World Myotis (Chiroptera, Vespertilionidae) inferred from mitochondrial and nuclear DNA genes. , 2007, Molecular phylogenetics and evolution.

[3]  J. Wiens,et al.  LATITUDINAL VARIATION IN SPECIATION MECHANISMS IN FROGS , 2010, Evolution; international journal of organic evolution.

[4]  R. Baker,et al.  Systematics of Vampyressa and Related Genera of Phyllostomid Bats as Determined by Cytochrome-B Sequences , 2004 .

[5]  C. Rahbek,et al.  Geographic Range Size and Determinants of Avian Species Richness , 2002, Science.

[6]  Theodore Garland,et al.  Why tropical forest lizards are vulnerable to climate warming , 2009, Proceedings of the Royal Society B: Biological Sciences.

[7]  Simon A. Levin,et al.  Monographs in Population Biology , 2013 .

[8]  D. A. Nelson,et al.  Anomalous Variation in Mitochondrial Genomes of White-crowned (Zonotrichia leucophrys) and Golden-crowned (Z. atricapilla) Sparrows: Pseudogenes, Hybridization, or Incomplete Lineage Sorting? , 2001 .

[9]  D. Wake What Salamanders Have Taught Us About Evolution , 2009 .

[10]  J. Bickham,et al.  Molecular phylogeny of New World sheath‐tailed bats (Emballonuridae: Diclidurini) based on loci from the four genetic transmission systems in mammals , 2007 .

[11]  Carsten Rahbek,et al.  Predicting continental-scale patterns of bird species richness with spatially explicit models , 2007, Proceedings of the Royal Society B: Biological Sciences.

[12]  Steven L Chown,et al.  Macrophysiology for a changing world , 2008, Proceedings of the Royal Society B: Biological Sciences.

[13]  T. Castoe,et al.  Bayesian mixed models and the phylogeny of pitvipers (Viperidae: Serpentes). , 2006, Molecular phylogenetics and evolution.

[14]  R. A. Pyron,et al.  Neogene diversification and taxonomic stability in the snake tribe Lampropeltini (Serpentes: Colubridae). , 2009, Molecular phylogenetics and evolution.

[15]  J. Losos,et al.  Phylogenetic comparative methods and the geography of speciation , 2003 .

[16]  T. Price,et al.  Limits to Speciation Inferred from Times to Secondary Sympatry and Ages of Hybridizing Species along a Latitudinal Gradient , 2011, The American Naturalist.

[17]  Omar Torres‐Carvajal Phylogeny and biogeography of a large radiation of Andean lizards (Iguania, Stenocercus) , 2007 .

[18]  D. Schluter,et al.  Ice sheets promote speciation in boreal birds , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  B. Calcott Fitness Landscapes and the Origin of Species , 2005 .

[20]  J. Pramuk Phylogeny of South American Bufo (Anura: Bufonidae) inferred from combined evidence , 2006 .

[21]  K. Lohman,et al.  PHYLOGEOGRAPHY OF THE TAILED FROG (ASCAPHUS TRUEI): IMPLICATIONS FOR THE BIOGEOGRAPHY OF THE PACIFIC NORTHWEST , 2001, Evolution; international journal of organic evolution.

[22]  N. Dulvy,et al.  Global analysis of thermal tolerance and latitude in ectotherms , 2011, Proceedings of the Royal Society B: Biological Sciences.

[23]  R. G. Davies,et al.  Global hotspots of species richness are not congruent with endemism or threat , 2005, Nature.

[24]  T. Castoe,et al.  Higher-level phylogeny of Asian and American coralsnakes, their placement within the Elapidae (Squamata), and the systematic affinities of the enigmatic Asian coralsnake Hemibungarus calligaster (Wiegmann, 1834) , 2007 .

[25]  C. Cicero,et al.  The role of ecologic diversification in sibling speciation of Empidonax flycatchers (Tyrannidae): multigene evidence from mtDNA , 2002, Molecular ecology.

[26]  NEW MITOCHONDRIAL DNA DATA AFFIRM THE IMPORTANCE OF PLEISTOCENE SPECIATION IN NORTH AMERICAN BIRDS , 2004, Evolution; international journal of organic evolution.

[27]  D. Hillis,et al.  Evolutionary history of the genus Rhogeessa (Chiroptera: Vespertilionidae) as revealed by mitochondrial DNA sequences , 2008 .

[28]  D. Mulcahy Molecular systematics of neotropical cat-eyed snakes: a test of the monophyly of Leptodeirini (Colubridae: Dipsadinae) with implications for character evolution and biogeography , 2007 .

[29]  Kevin J. Gaston,et al.  Thermal tolerance, climatic variability and latitude , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  W. Wüster,et al.  A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). , 2008, Molecular phylogenetics and evolution.

[31]  C. Cadena TESTING THE ROLE OF INTERSPECIFIC COMPETITION IN THE EVOLUTIONARY ORIGIN OF ELEVATIONAL ZONATION: AN EXAMPLE WITH BUARREMON BRUSH-FINCHES (AVES, EMBERIZIDAE) IN THE NEOTROPICAL MOUNTAINS , 2007, Evolution; international journal of organic evolution.

[32]  J. Wiens,et al.  Niche Conservatism Drives Elevational Diversity Patterns in Appalachian Salamanders , 2010, The American Naturalist.

[33]  J. Cracraft,et al.  The assembly of montane biotas: linking Andean tectonics and climatic oscillations to independent regimes of diversification in Pionus parrots , 2007, Proceedings of the Royal Society B: Biological Sciences.

[34]  D. Schluter,et al.  The Latitudinal Gradient in Recent Speciation and Extinction Rates of Birds and Mammals , 2007, Science.

[35]  M. Feder Environmental Variability and Thermal Acclimation in Neotropical and Temperate Zone Salamanders , 1978, Physiological Zoology.

[36]  J. Losos,et al.  Mainland colonization by island lizards , 2005 .

[37]  R. Mittermeier,et al.  Biodiversity hotspots for conservation priorities , 2000, Nature.

[38]  J. T. Collins,et al.  Phylogeny-based delimitation of species boundaries and contact zones in the trilling chorus frogs (Pseudacris). , 2007, Molecular phylogenetics and evolution.

[39]  K. Gaston,et al.  Hemispheric Asymmetries in Biodiversity—A Serious Matter for Ecology , 2004, PLoS biology.

[40]  Paul R. Martin,et al.  Are mountain passes higher in the tropics? Janzen's hypothesis revisited. , 2006, Integrative and comparative biology.

[41]  J. García‐Moreno,et al.  MtDNA sequences support monophyly of Hemispingus tanagers. , 2001, Molecular phylogenetics and evolution.

[42]  B. Loiselle,et al.  Limits to elevational distributions in two species of emberizine finches: disentangling the role of interspecific competition, autoecology, and geographic variation in the environment , 2007 .

[43]  J. Diamond Distributional Ecology of New Guinea Birds , 1973, Science.

[44]  D. Janzen Why Mountain Passes are Higher in the Tropics , 1967, The American Naturalist.

[45]  Robert M. Zink,et al.  The Importance of Recent Ice Ages in Speciation: A Failed Paradigm , 1997 .

[46]  C. McCain Vertebrate range sizes indicate that mountains may be 'higher' in the tropics. , 2009, Ecology letters.

[47]  J. Wiens,et al.  Climatic zonation drives latitudinal variation in speciation mechanisms , 2007, Proceedings of the Royal Society B: Biological Sciences.

[48]  Jared L. Strasburg,et al.  Assembly of the eastern North American herpetofauna: new evidence from lizards and frogs , 2006, Biology Letters.

[49]  F. R. Santos,et al.  Molecular systematics of the genus Artibeus (Chiroptera: Phyllostomidae). , 2008, Molecular phylogenetics and evolution.

[50]  W. Jetz,et al.  Linking global turnover of species and environments , 2008, Proceedings of the National Academy of Sciences.

[51]  R. Lawson,et al.  Snake phylogeny: evidence from nuclear and mitochondrial genes. , 2002, Molecular phylogenetics and evolution.

[52]  Christopher J. Schneider,et al.  DIVERSIFICATION OF RAINFOREST FAUNAS: An Integrated Molecular Approach , 2000 .

[53]  G. Mittelbach,et al.  Is There a Latitudinal Gradient in the Importance of Biotic Interactions , 2009 .

[54]  J. Rodríguez-Robles,et al.  Molecular systematics of new world gopher, bull, and pinesnakes (Pituophis: Colubridae), a transcontinental species complex. , 2000, Molecular phylogenetics and evolution.

[55]  Y. Kumazawa,et al.  Molecular phylogenetic and dating analyses using mitochondrial DNA sequences of eyelid geckos (Squamata: Eublepharidae). , 2008, Gene.

[56]  A. J. Crawford,et al.  Cenozoic biogeography and evolution in direct-developing frogs of Central America (Leptodactylidae: Eleutherodactylus) as inferred from a phylogenetic analysis of nuclear and mitochondrial genes. , 2005, Molecular phylogenetics and evolution.

[57]  Molecular Phylogenetic Relationships Among the Wood Warblers ( Parulidae ) and Historical Biogeography in the Caribbean Basin , 2004 .

[58]  Mark V. Lomolino,et al.  Elevation gradients of species‐density: historical and prospective views , 2001 .

[59]  R. Baker,et al.  Systematics of the genera Carollia and Rhinophylla based on the cytochrome-B gene , 1999 .

[60]  J. Kerr,et al.  Quantifying the importance of regional and local filters for community trait structure in tropical and temperate zones. , 2011, Ecology.

[61]  Walter Jetz,et al.  Phylogenetic conservatism of environmental niches in mammals , 2011, Proceedings of the Royal Society B: Biological Sciences.

[62]  J. L. Parra,et al.  Very high resolution interpolated climate surfaces for global land areas , 2005 .

[63]  R. Lawson,et al.  Phylogenetic relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: how much DNA sequence is enough? , 2002, Molecular phylogenetics and evolution.

[64]  K. Burns,et al.  Molecular phylogenetics and biogeography of Neotropical tanagers in the genus Tangara. , 2004, Molecular phylogenetics and evolution.

[65]  J. Wiens,et al.  Accelerated rates of climatic-niche evolution underlie rapid species diversification. , 2010, Ecology letters.

[66]  Fredrica H. van Berkum,et al.  LATITUDINAL PATTERNS OF THE THERMAL SENSITIVITY OF SPRINT SPEED IN LIZARDS , 1988 .

[67]  Paul R. Martin,et al.  RAPID SYMPATRY EXPLAINS GREATER COLOR PATTERN DIVERGENCE IN HIGH LATITUDE BIRDS , 2010, Evolution; international journal of organic evolution.

[68]  C. McCain Global analysis of bird elevational diversity , 2009 .

[69]  W. Moore,et al.  Mitochondrial DNA phylogeny of the woodpecker genus Veniliornis (Picidae, Picinae) and related genera implies convergent evolution of plumage patterns , 2006 .

[70]  J. Terborgh Distribution on Environmental Gradients: Theory and a Preliminary Interpretation of Distributional Patterns in the Avifauna of the Cordillera Vilcabamba, Peru , 1971 .

[71]  J. Avise,et al.  Molecular Genetic Divergence between Avian Sibling Species: King and Clapper Rails, Long-Billed and Short-Billed Dowitchers, Boat-Tailed and Great-Tailed Grackles, and Tufted and Black-Crested Titmice , 1988 .

[72]  W. Moore,et al.  Molecular phylogeny of a cosmopolitan group of woodpeckers (genus Picoides) gased on COI and cyt b mitochondrial gene sequences. , 2002, Molecular phylogenetics and evolution.

[73]  Gregory K. Snyder,et al.  Temperature Adaptations in Amphibians , 1975, The American Naturalist.

[74]  A. Leaché,et al.  Phylogenetic relationships of horned lizards (Phrynosoma) based on nuclear and mitochondrial data: evidence for a misleading mitochondrial gene tree. , 2006, Molecular phylogenetics and evolution.

[75]  Charles W. Linkem,et al.  MITOCHONDRIAL INTROGRESSION AND INCOMPLETE LINEAGE SORTING THROUGH SPACE AND TIME: PHYLOGENETICS OF CROTAPHYTID LIZARDS , 2007, Evolution; international journal of organic evolution.

[76]  John-Arvid Grytnes,et al.  Niche conservatism as an emerging principle in ecology and conservation biology. , 2010, Ecology letters.

[77]  C. Graham,et al.  Evolutionary and Ecological Causes of the Latitudinal Diversity Gradient in Hylid Frogs: Treefrog Trees Unearth the Roots of High Tropical Diversity , 2006, The American Naturalist.

[78]  R. Baker,et al.  MOLECULAR EVIDENCE FOR EVOLUTION OF PISCIVORY IN NOCTILIO (CHIROPTERA: NOCTILIONIDAE) , 2001 .

[79]  E. Bonaccorso,et al.  Historical biogeography and speciation in the neotropical highlands: molecular phylogenetics of the jay genus Cyanolyca. , 2009, Molecular phylogenetics and evolution.

[80]  K. Gaston,et al.  Geographic range size and evolutionary age in birds , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[81]  A. Peterson,et al.  Phylogenetic Patterns in Montane Troglodytes Wrens , 1999 .

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

[83]  J. Klicka,et al.  Evolutionary patterns of morphometrics, allozymes and mitochondrial DNA in thrashers (Genus Toxostoma) , 1999 .

[84]  C. Graham,et al.  INTEGRATING PHYLOGENETICS AND ENVIRONMENTAL NICHE MODELS TO EXPLORE SPECIATION MECHANISMS IN DENDROBATID FROGS , 2004, Evolution; international journal of organic evolution.

[85]  S. Votier,et al.  What determines a species' geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). , 2010, The Journal of animal ecology.

[86]  L. Knowles,et al.  Tests of phenotypic and genetic concordance and their application to the conservation of Panamanian golden frogs (Anura, Bufonidae) , 2007, Molecular ecology.

[87]  D. Levey,et al.  Squeezed at the top: Interspecific aggression may constrain elevational ranges in tropical birds. , 2010, Ecology.

[88]  R. Chesser SYSTEMATICS, EVOLUTION, AND BIOGEOGRAPHY OF THE SOUTH AMERICAN OVENBIRD GENUS CINCLODES , 2004 .

[89]  R. Ricklefs,et al.  HISTORICAL BIOGEOGRAPHY OF THE NEW WORLD SOLITAIRES (MYADESTES SPP) , 2007 .

[90]  T. Papenfuss,et al.  Molecular phylogenetics, tRNA evolution, and historical biogeography in anguid lizards and related taxonomic families. , 1999, Molecular phylogenetics and evolution.

[91]  I. Lovette,et al.  ELEVATIONAL ZONATION AND THE PHYLOGENETIC RELATIONSHIPS OF THE HENICORHINA WOOD-WRENS , 2006 .

[92]  D. Hillis,et al.  Phylogeny of the New World true frogs (Rana). , 2005, Molecular phylogenetics and evolution.

[93]  Robert K. Colwell,et al.  The coincidence of rarity and richness and the potential signature of history in centres of endemism , 2004 .

[94]  J. Schulte,et al.  PHYLOGENETIC RELATIONSHIPS WITHIN IGUANIDAE INFERRED USING MOLECULAR AND MORPHOLOGICAL DATA AND A PHYLOGENETIC TAXONOMY OF IGUANIAN LIZARDS , 2003 .

[95]  J. Pérez-Emán,et al.  Molecular phylogenetics and biogeography of the Neotropical redstarts (Myioborus; Aves, Parulinae). , 2005, Molecular phylogenetics and evolution.

[96]  I. Lovette,et al.  Density-dependent diversification in North American wood warblers , 2008, Proceedings of the Royal Society B: Biological Sciences.

[97]  J. DaCosta,et al.  The Great American Interchange in birds: a phylogenetic perspective with the genus Trogon , 2008, Molecular ecology.

[98]  K. Zamudio,et al.  Horned lizard (Phrynosoma) phylogeny inferred from mitochondrial genes and morphological characters: understanding conflicts using multiple approaches. , 2004, Molecular phylogenetics and evolution.

[99]  J. L. Parra COLOR EVOLUTION IN THE HUMMINGBIRD GENUS COELIGENA , 2010, Evolution; international journal of organic evolution.

[100]  R. Jansson,et al.  The Fate of Clades in a World of Recurrent Climatic Change: Milankovitch Oscillations and Evolution , 2002 .

[101]  A. Purvis,et al.  A phylogenetic supertree of the bats (Mammalia: Chiroptera) , 2002, Biological reviews of the Cambridge Philosophical Society.

[102]  R. Huey Latitudinal Pattern of Between-Altitude Faunal Similarity: Mountains Might be "Higher" in the Tropics , 1978, The American Naturalist.

[103]  Paul R. Martin,et al.  Impacts of climate warming on terrestrial ectotherms across latitude , 2008, Proceedings of the National Academy of Sciences.