Climatic shifts drove major contractions in avian latitudinal distributions throughout the Cenozoic

Significance The fossil record reveals evidence of dramatic distributional shifts through time for many groups of organisms. One striking example is the early fossil record of modern birds, which shows that many bird groups currently restricted to the tropics were formerly found at high latitudes in North America and Europe. Tracking potentially suitable habitat for these clades over the last 56 million years reveals that cooling trends throughout this period may have largely dictated the geographic distributions of these “tropical” groups, complicating our understanding of where on Earth many of these lineages originated. Many higher level avian clades are restricted to Earth’s lower latitudes, leading to historical biogeographic reconstructions favoring a Gondwanan origin of crown birds and numerous deep subclades. However, several such “tropical-restricted” clades (TRCs) are represented by stem-lineage fossils well outside the ranges of their closest living relatives, often on northern continents. To assess the drivers of these geographic disjunctions, we combined ecological niche modeling, paleoclimate models, and the early Cenozoic fossil record to examine the influence of climatic change on avian geographic distributions over the last ∼56 million years. By modeling the distribution of suitable habitable area through time, we illustrate that most Paleogene fossil-bearing localities would have been suitable for occupancy by extant TRC representatives when their stem-lineage fossils were deposited. Potentially suitable habitat for these TRCs is inferred to have become progressively restricted toward the tropics throughout the Cenozoic, culminating in relatively narrow circumtropical distributions in the present day. Our results are consistent with coarse-scale niche conservatism at the clade level and support a scenario whereby climate change over geological timescales has largely dictated the geographic distributions of many major avian clades. The distinctive modern bias toward high avian diversity at tropical latitudes for most hierarchical taxonomic levels may therefore represent a relatively recent phenomenon, overprinting a complex biogeographic history of dramatic geographic range shifts driven by Earth’s changing climate, variable persistence, and intercontinental dispersal. Earth’s current climatic trajectory portends a return to a megathermal state, which may dramatically influence the geographic distributions of many range-restricted extant clades.

[1]  C. Tambussi,et al.  A stem anseriform from the early Palaeocene of Antarctica provides new key evidence in the early evolution of waterfowl , 2019, Zoological Journal of the Linnean Society.

[2]  P. Valdes,et al.  Coupling of palaeontological and neontological reef coral data improves forecasts of biodiversity responses under global climatic change , 2019, Royal Society Open Science.

[3]  R. T. Brumfield,et al.  Evolutionary dynamics of hybridization and introgression following the recent colonization of Glossy Ibis (Aves: Plegadis falcinellus) into the New World , 2019, Molecular ecology.

[4]  J. Cracraft,et al.  Earth history and the passerine superradiation , 2019, Proceedings of the National Academy of Sciences.

[5]  D. Lunt,et al.  Ecological niche modelling does not support climatically-driven dinosaur diversity decline before the Cretaceous/Paleogene mass extinction , 2019, Nature Communications.

[6]  J. Diniz‐Filho,et al.  Climatic niche evolution in turtles is characterized by phylogenetic conservatism for both aquatic and terrestrial species , 2018, Journal of evolutionary biology.

[7]  Allison Y. Hsiang,et al.  A North American stem turaco, and the complex biogeographic history of modern birds , 2018, BMC Evolutionary Biology.

[8]  Brett R. Scheffers,et al.  Managing consequences of climate‐driven species redistribution requires integration of ecology, conservation and social science , 2018, Biological reviews of the Cambridge Philosophical Society.

[9]  P. Valdes,et al.  Eocene greenhouse climate revealed by coupled clumped isotope-Mg/Ca thermometry , 2018, Proceedings of the National Academy of Sciences.

[10]  D. Field Preliminary paleoecological insights from the Pliocene avifauna of Kanapoi, Kenya: Implications for the ecology of Australopithecus anamensis. , 2017, Journal of human evolution.

[11]  D. Ksepka,et al.  Early Paleocene landbird supports rapid phylogenetic and morphological diversification of crown birds after the K–Pg mass extinction , 2017, Proceedings of the National Academy of Sciences.

[12]  G. Mayr The early Eocene birds of the Messel fossil site: a 48 million‐year‐old bird community adds a temporal perspective to the evolution of tropical avifaunas , 2017, Biological reviews of the Cambridge Philosophical Society.

[13]  J. Cracraft,et al.  Conceptual and analytical worldviews shape differences about global avian biogeography , 2017 .

[14]  G. Mayr Avian higher level biogeography: Southern Hemispheric origins or Southern Hemispheric relicts? , 2017 .

[15]  Brett R. Scheffers,et al.  Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being , 2017, Science.

[16]  P. Valdes,et al.  Mid-latitude continental temperatures through the early Eocene in western Europe , 2017 .

[17]  S. Bowring,et al.  Direct high-precision U–Pb geochronology of the end-Cretaceous extinction and calibration of Paleocene astronomical timescales , 2016 .

[18]  P. Valdes,et al.  Modelling the climatic niche of turtles: a deep-time perspective , 2016, Proceedings of the Royal Society B: Biological Sciences.

[19]  Jeffrey P. Townsend,et al.  A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing , 2016, Nature.

[20]  P. Pearson,et al.  Changing atmospheric CO2 concentration was the primary driver of early Cenozoic climate , 2016, Nature.

[21]  I. Mayrose,et al.  Body sizes and diversification rates of lizards, snakes, amphisbaenians and the tuatara , 2016 .

[22]  Daniel J. Lunt,et al.  Palaeogeographic controls on climate and proxy interpretation , 2015 .

[23]  J. Cracraft,et al.  A new time tree reveals Earth history’s imprint on the evolution of modern birds , 2015, Science Advances.

[24]  D. Lunt,et al.  Atmospheric and oceanic impacts of Antarctic glaciation across the Eocene–Oligocene transition , 2015, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[25]  Colin W. Rundel,et al.  Interface to Geometry Engine - Open Source (GEOS) , 2015 .

[26]  J. Townsend,et al.  A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing , 2015, Nature.

[27]  M. Kageyama,et al.  Evaluation of CMIP5 palaeo-simulations to improve climate projections , 2015 .

[28]  P. Pearson,et al.  Descent toward the Icehouse: Eocene sea surface cooling inferred from GDGT distributions , 2015 .

[29]  Y. Yu,et al.  RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. , 2015, Molecular phylogenetics and evolution.

[30]  E. Matthysen,et al.  Niche conservatism among non-native vertebrates in Europe and North America , 2015 .

[31]  M. Gottfried The Lost World of Fossil Lake: Snapshots from Deep Time , 2015 .

[32]  Md. Shamsuzzoha Bayzid,et al.  Whole-genome analyses resolve early branches in the tree of life of modern birds , 2014, Science.

[33]  B. Lieberman,et al.  Macroevolutionary consequences of profound climate change on niche evolution in marine molluscs over the past three million years , 2014, Proceedings of the Royal Society B: Biological Sciences.

[34]  Herculano Alvarenga South American and Antarctic Continental Cenozoic Birds — Paleobiogeographic Affinities and Disparities , 2014 .

[35]  G. Mayr,et al.  Earliest and first Northern Hemispheric hoatzin fossils substantiate Old World origin of a “Neotropic endemic” , 2014, Naturwissenschaften.

[36]  Michael J. Landis,et al.  Bayesian analysis of biogeography when the number of areas is large. , 2013, Systematic biology.

[37]  P. Valdes,et al.  The Early Eocene equable climate problem: can perturbations of climate model parameters identify possible solutions? , 2013, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[38]  L. Grande The Lost World of Fossil Lake: Snapshots from Deep Time , 2013 .

[39]  M. White,et al.  Selecting thresholds for the prediction of species occurrence with presence‐only data , 2013 .

[40]  C. Tambussi,et al.  South American and Antarctic Continental Cenozoic Birds: Paleobiogeographic Affinities and Disparities , 2012 .

[41]  W. Jetz,et al.  The global diversity of birds in space and time , 2012, Nature.

[42]  A. Townsend Peterson,et al.  Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas , 2012 .

[43]  V. Barve,et al.  Variation in niche and distribution model performance: The need for a priori assessment of key causal factors , 2012 .

[44]  Maria Seton,et al.  Global continental and ocean basin reconstructions since 200 Ma , 2012 .

[45]  Daniel B. Thomas,et al.  Multiple cenozoic invasions of Africa by penguins (Aves, Sphenisciformes) , 2012, Proceedings of the Royal Society B: Biological Sciences.

[46]  D. Ksepka,et al.  Podargiform Affinities of the Enigmatic Fluvioviridavis platyrhamphus and the Early Diversification of Strisores (“Caprimulgiformes” + Apodiformes) , 2011, PloS one.

[47]  G. Mayr Two-phase extinction of “Southern Hemispheric” birds in the Cenozoic of Europe and the origin of the Neotropic avifauna , 2011 .

[48]  G. Mayr,et al.  Out of Africa: Fossils shed light on the origin of the hoatzin, an iconic Neotropic bird , 2011, Naturwissenschaften.

[49]  A. Peterson,et al.  The crucial role of the accessible area in ecological niche modeling and species distribution modeling , 2011 .

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

[51]  Paul J. Valdes,et al.  Optimal tuning of a GCM using modern and glacial constraints , 2010, Climate Dynamics.

[52]  J. D. Hoyo,et al.  Handbook of the Birds of the World , 2010 .

[53]  P. Valdes,et al.  Modelling the oxygen isotope distribution of ancient seawater using a coupled ocean–atmosphere GCM: Implications for reconstructing early Eocene climate , 2010 .

[54]  A. Tripati,et al.  Climate sensitivity to Arctic seaway restriction during the early Paleogene , 2009 .

[55]  Krister T. Smith A new lizard assemblage from the earliest eocene (Zone Wa0) of the bighorn basin, wyoming, USA: Biogeography during the warmest interval of the cenozoic , 2009 .

[56]  J. Cracraft Continental drift, paleoclimatology, and the evolution and biogeography of birds , 2009 .

[57]  D. Ksepka,et al.  Affinities of Palaeospiza bella and the Phylogeny and Biogeography of Mousebirds (Coliiformes) , 2009 .

[58]  Maria A. Gandolfo,et al.  Phylogenetic biome conservatism on a global scale , 2009, Nature.

[59]  A. Townsend Peterson,et al.  Rethinking receiver operating characteristic analysis applications in ecological niche modeling , 2008 .

[60]  G. Mayr,et al.  A TODY (ALCEDINIFORMES: TODIDAE) FROM THE EARLY OLIGOCENE OF GERMANY , 2007 .

[61]  T. Parsons,et al.  Diversification of Neoaves: integration of molecular sequence data and fossils , 2006, Biology Letters.

[62]  G. Dyke,et al.  Bird evolution in the Eocene: climate change in Europe and a Danish fossil fauna , 2006, Biological reviews of the Cambridge Philosophical Society.

[63]  R. Pearson,et al.  Predicting species distributions from small numbers of occurrence records: A test case using cryptic geckos in Madagascar , 2006 .

[64]  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.

[65]  B. A. Hawkins,et al.  Post‐Eocene climate change, niche conservatism, and the latitudinal diversity gradient of New World birds , 2006 .

[66]  E. Martin,et al.  Timing and Climatic Consequences of the Opening of Drake Passage , 2006, Science.

[67]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[68]  C. Hillenbrand,et al.  Drake Passage and Cenozoic climate: An open and shut case? , 2005 .

[69]  H. James PALEOGENE FOSSILS AND THE RADIATION OF MODERN BIRDS , 2005 .

[70]  G. Mayr The Palaeogene Old World potoo Paraprefica Mayr, 1999 (Aves, Nyctibiidae): Its osteology and affinities to the New World Preficinae Olson, 1987 , 2005 .

[71]  P. Valdes,et al.  Palaeo-digital elevation models for use as boundary conditions in coupled ocean–atmosphere GCM experiments: a Maastrichtian (late Cretaceous) example , 2004 .

[72]  Robert P. Anderson,et al.  Geographical distributions of spiny pocket mice in South America: insights from predictive models , 2002 .

[73]  G. Mayr A second skeleton of the early Oligocene trogonPrimotrogon wintersteiniMayr 1999 (Aves: Trogoniformes: Trogonidae) in an unusual state of preservation , 2001 .

[74]  A. Prinzing The niche of higher plants: evidence for phylogenetic conservatism , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[75]  J. Cracraft Avian evolution, Gondwana biogeography and the Cretaceous–Tertiary mass extinction event , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  G. Mayr Comments on the osteology of Masillapodargus longipes Mayr 1999 and Paraprefica major Mayr 1999, caprimulgiform birds from the Middle Eocene of Messel (Hessen, Germany) , 2001 .

[77]  C. Cox,et al.  Plate tectonics, seaways and climate in the historical biogeography of mammals. , 2000, Memorias do Instituto Oswaldo Cruz.

[78]  V. Sánchez‐Cordero,et al.  Conservatism of ecological niches in evolutionary time , 1999, Science.

[79]  J. Blondel,et al.  Evolution and history of the western Palaearctic avifauna. , 1998, Trends in ecology & evolution.

[80]  G. Mayr,et al.  The mousebirds (Aves: Coliiformes) from the Middle Eocene of Grube Messel (Hessen, Germany) , 1998 .

[81]  J. Meng,et al.  Faunal turnovers of Palaeogene mammals from the Mongolian Plateau , 1998, Nature.

[82]  Gerald Mayr Ein Archaeotrogon (Aves: Archaeotrogonidae) aus dem Mittel-Eozän der Grube Messel (Hessen, Deutschland)? , 1998, Journal für Ornithologie.

[83]  L. Grande Studies of paleoenvironments and historical biogeography in the Fossil Butte and Laney Members of the Green River Formation , 1994 .

[84]  J. Gauthier Fossil xenosaurid and anguid lizards from the early Eocene Wasatch Formation, Southeast Wyoming, and a revision of the Anguioidea , 1982 .

[85]  D. Gough Solar interior structure and luminosity variations , 1981 .

[86]  S. Webb A HISTORY OF SAVANNA VERTEBRATES IN THE NEW WORLD. Part II: South America and the Great Interchange , 1978 .

[87]  S. Webb,et al.  A History of Savanna Vertebrates in the New World. Part I: North America , 1977 .

[88]  D. Field,et al.  Genomic Signature of an Avian Lilliput Effect across the K‐Pg Extinction , 2018, Systematic biology.

[89]  P. Upchurch,et al.  The latitudinal biodiversity gradient through deep time. , 2014, Trends in ecology & evolution.

[90]  Primotrogon wintersteini A second skeleton of the early Oligocene trogon , 2009 .

[91]  Steven J. Phillips,et al.  Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. , 2009, Ecological applications : a publication of the Ecological Society of America.

[92]  C. Mourer-Chauviré,et al.  THE AVIFAUNA OF THE EOCENE AND OLIGOCENE PHOSPHORITES DU QUERCY (France): AN UPDATED LIST , 2006 .

[93]  Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/joc.1276 VERY HIGH RESOLUTION INTERPOLATED CLIMATE SURFACES FOR GLOBAL LAND AREAS , 2005 .

[94]  Chris D. Jones,et al.  Modelling vegetation and the carbon cycle as interactive elements of the climate system , 2002 .

[95]  W. Durka,et al.  The niche of higher plants: evidence , 2001 .

[96]  G. Mayr New or previously unrecorded avian taxa from the Middle Eocene of Messel (Hessen, Germany) , 2000 .

[97]  C. Mourer-Chauviré Les relations entre les avifaunes du Tertiaire inferieur d'Europe et d'Amerique du Sud , 1999 .

[98]  S. Olson The anseriform relationships of Anatalavis Olson and Parris (Anseranatidae), with a new species from the Lower Eocene London Clay , 1999 .

[99]  C. Janis Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events , 1993 .

[100]  S. Olson An early Eocene oilbird from the Green River Formation of Wyoming (Caprimulgiformes: Steatornithidae) , 1987 .

[101]  C. Mourer-Chauviré Les oiseaux fossiles des phosphorites du quercy (éocène supérieur a oligocène supérieur): Implications paléobiogéographiques , 1982 .

[102]  S. Olson Oligocene fossils bearing on the origins of the Todidae and the Momotidae (Aves: Coraciiformes) , 1976 .

[103]  G. Crosby Spread of the Cattle Egret in the Western Hemisphere , 1972 .

[104]  H. D. Macginitie The Eocene Green River flora of northwestern Colorado and northeastern Utah , 1969 .

[105]  C. V. Steenis The land-bridge theory in botany with particular reference to tropical plants , 1962 .