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Climatic Shifts Drove Major Contractions in Avian Latitudinal Distributions Throughout the Cenozoic

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Climatic Shifts Drove Major Contractions in Avian Latitudinal Distributions Throughout the Cenozoic Climatic shifts drove major contractions in avian latitudinal distributions throughout the Cenozoic Erin E. Saupea,1,2, Alexander Farnsworthb, Daniel J. Luntb, Navjit Sagooc, Karen V. Phamd, and Daniel J. Fielde,1,2 aDepartment of Earth Sciences, University of Oxford, OX1 3AN Oxford, United Kingdom; bSchool of Geographical Sciences, University of Bristol, Clifton, BS8 1SS Bristol, United Kingdom; cDepartment of Meteorology, Stockholm University, 106 91 Stockholm, Sweden; dDivision of Geological and Planetary Sciences, Caltech, Pasadena, CA 91125; and eDepartment of Earth Sciences, University of Cambridge, CB2 3EQ Cambridge, United Kingdom Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved May 7, 2019 (received for review March 8, 2019) Many higher level avian clades are restricted to Earth’s lower lati- order avian historical biogeography invariably recover strong evi- tudes, leading to historical biogeographic reconstructions favoring a dence for an origin of most modern diversity on southern land- Gondwanan origin of crown birds and numerous deep subclades. masses (2, 6, 11). However, several such “tropical-restricted” clades (TRCs) are repre- The crown bird fossil record has unique potential to reveal sented by stem-lineage fossils well outside the ranges of their clos- where different groups of birds were formerly distributed in deep est living relatives, often on northern continents. To assess the time. Fossil evidence, for example, has long indicated that total- drivers of these geographic disjunctions, we combined ecological group representatives of clades restricted to relatively narrow niche modeling, paleoclimate models, and the early Cenozoic fossil geographic regions today were formerly found in different parts of record to examine the influence of climatic change on avian geo- – graphic distributions over the last ∼56 million years. By modeling the world (12 23). In particular, the Paleogene record of fossil the distribution of suitable habitable area through time, we illus- birds has yielded abundant evidence that many extant clades re- trate that most Paleogene fossil-bearing localities would have been stricted to southern landmasses had fossil stem-group represen- suitable for occupancy by extant TRC representatives when their tatives in the Northern Hemisphere (e.g., refs. 11–13, 15, 19, 21, stem-lineage fossils were deposited. Potentially suitable habitat and 24–38). Collectively, such biogeographic disjunctions between for these TRCs is inferred to have become progressively restricted early stem-group representatives and extant taxa cloud our ability ECOLOGY toward the tropics throughout the Cenozoic, culminating in rela- to infer ancestral ranges for the deepest crown bird subclades. The tively narrow circumtropical distributions in the present day. Our general sparseness and Northern Hemisphere bias of the avian results are consistent with coarse-scale niche conservatism at the fossil record, however, has limited attempts to incorporate bird clade level and support a scenario whereby climate change over fossils into large-scale hypotheses of avian biogeographic evolu- geological timescales has largely dictated the geographic distribu- tion. Even studies that have integrated phylogenetically con- tions of many major avian clades. The distinctive modern bias to- strained avian fossils into analytical reconstructions of ancestral ward high avian diversity at tropical latitudes for most hierarchical biogeography (6) have been criticized for effectively “swamping taxonomic levels may therefore represent a relatively recent phe- ” nomenon, overprinting a complex biogeographic history of dra- out information from the fossil record by virtue of the limited matic geographic range shifts driven by Earth’s changing climate, amount of fossil data compared with extant data in such analyses variable persistence, and intercontinental dispersal. Earth’scurrent (39). Thus, ancestral biogeographic reconstructions may have climatic trajectory portends a return to a megathermal state, which limited potential to reveal whether modern geographic distribu- may dramatically influence the geographic distributions of many tions of avian higher clades are truly reflective of their areas of range-restricted extant clades. Significance climate change | niche conservatism | latitudinal diversity gradient | ecological niche modeling | historical biogeography The fossil record reveals evidence of dramatic distributional shifts through time for many groups of organisms. One striking xtant avian biodiversity is represented by nearly 11,000 living example is the early fossil record of modern birds, which shows Especies, which inhabit virtually every conceivable subaerial that many bird groups currently restricted to the tropics were environment from the poles to the equator (1). However, despite formerly found at high latitudes in North America and Europe. the ubiquity of birds and their penchant for dispersal, extant Tracking potentially suitable habitat for these clades over the birdlife is unequally distributed across the Earth. In particular, last 56 million years reveals that cooling trends throughout this avian diversity—in terms of both species numbers and higher period may have largely dictated the geographic distributions taxonomic groups—is skewed toward tropical environments on of these “tropical” groups, complicating our understanding of the southern continents (i.e., those that formerly composed the where on Earth many of these lineages originated. Mesozoic supercontinent of Gondwana). This pattern led earlier avian historical biogeographic investi- Author contributions: E.E.S. and D.J.F. designed research; E.E.S. and D.J.F. performed re- search; A.F., D.J.L., and N.S. contributed new reagents/analytic tools; E.E.S. and K.V.P. gations to conclude that vicariance driven by Gondwanan analyzed data; and E.E.S. and D.J.F. wrote the paper. breakup, which was largely completed by the end of the Mesozoic, The authors declare no conflict of interest. played a predominant role in triggering deep phylogenetic and This article is a PNAS Direct Submission. geographic divergences within crown birds (e.g., ref. 2). However, Published under the PNAS license. recent phylogenetic divergence time studies suggest that most Data deposition: Data from this study have been deposited on the online data archive deep divergences within crown birds took place after the Creta- Zenodo (DOI: 10.5281/zenodo.2658119). – – – ceous Paleogene (K Pg) mass extinction (3 7), roughly 66.02 1E.E.S. and D.J.F. contributed equally to this work. million years ago (8). Although Australia, Antarctica, and South 2To whom correspondence may be addressed. Email: [email protected] or djf70@ America maintained connectivity into the Paleogene (9, 10), cam.ac.uk. Mesozoic Gondwanan vicariance appears to have played no role This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. in either the diversification or geographic expansion of the avian 1073/pnas.1903866116/-/DCSupplemental. crown group. Nonetheless, analytical reconstructions of higher Published online June 10, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1903866116 PNAS | June 25, 2019 | vol. 116 | no. 26 | 12895–12900 Downloaded by guest on September 25, 2021 origin or, instead, obscure a history of profound biogeographic fossil records: Ypresian (∼56 to 47.8 Ma), Priabonian (∼38 to shifts throughout their evolutionary history. 33.9 Ma), Rupelian (∼33.9 to 28.1 Ma), and Chattian (∼28.1 to The avian fossil record reveals information on where early rep- 23.03 Ma) (SI Appendix, Figs. S1–S20). We then evaluated resentatives of various lineages were found and, just as importantly, whether these paleo-projections correctly predicted pene- when in Earth history these birds lived. Paleontological evidence for contemporaneous fossil occurrences for each total clade (Fig. 2 major fluctuations in avian historical biogeographic patterns and SI Appendix, Figs. S21–S30). Of 19 Paleogene clade/locality therefore raises questions about the extent to which historical fac- occurrences investigated, only 4 were not predicted as highly tors, such as Cenozoic climatic change, may have been responsible suitable by our ecological models (Fig. 2 and SI Appendix, Figs. for driving historical shifts in avian geographic range, as has been S21–S30 and Table S2). Virtually all Ypresian-aged fossil local- demonstrated for ectothermic clades, such as turtles (40), and dis- ities were predicted as suitable, but more recent (Priabonian to missed as a factor influencing the demise of nonavian dinosaurs in Chattian) fossil occurrences were predicted with less fidelity (SI the Late Cretaceous (41). Here, we integrate both past and present Appendix, Table S2). Even so, all younger fossil occurrences avian distributional data and climate characterizations to model aside from one (Todidae) were predicted as suitable under at how habitable regions for 10 neornithine higher level clades (Fig. 1) least one paleo-plate and threshold model, and, when suitable have changed throughout the Cenozoic. We test whether we can habitat was not predicted by our ecological models, it was usually predict the presence of high-latitude Paleogene fossil occurrences of (∼60%) found within only 150 km of a clade-specific Paleogene these 10 clades, which are currently restricted to tropical and sub- fossil locality—potentially within levels of paleo-plate re- tropical latitudes, assuming climatic niche conservatism
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