Earth history and the passerine superradiation
Edited by Michael E. Alfaro, University of California, Los Angeles, CA, and accepted by Editorial Board Member David Jablonski February 26, 2019 (received for review August 9, 2018)
Significance
Our understanding of the factors that affected the diversification of passerines, the most diverse and widespread bird order (Passeriformes), is limited. Here, we reconstruct passerine evolutionary history and produce the most comprehensive time-calibrated phylogenetic hypothesis of the group using extensive sampling of the genome, complete sampling of all passerine families, and a number of vetted fossil calibration points. Our phylogenetic results refine our knowledge of passerine diversity and yield divergence dates that are consistent with the fossil record, and our macroevolutionary analyses suggest that singular events in Earth history, such as increases in Cenozoic global temperature or the colonization of new continents, were not the primary forces driving passerine diversification.
Abstract
Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation.
Data Availability
Data deposition: Raw sequencing reads and ultraconserved element (UCE) nucleotide sequences are available from the National Center for Biotechnology Information (NCBI) Sequence Read Archive and Genbank as part of BioProjects PRJNA304409 and PRJNA480834. NCBI BioSample accession numbers are available in Dataset S1. The PHYLUCE computer code used in this study is available from https://github.com/faircloth-lab/phyluce. Other custom computer code, DNA alignments, analysis inputs, and analysis outputs are available from the Dryad Digital Repository database, datadryad.org/ (doi: https://doi.org/10.5061/dryad.2vd01gr).
Acknowledgments
We thank the curators, staff, and field collectors at the institutions listed in Dataset S1 for tissue samples used in this project; without their hard work, this study would not have been possible. We also thank Van Remsen for comments on earlier drafts, and we thank our three reviewers and the editor for their comments, which improved this manuscript. This study was supported by setup funds from Louisiana State University (to B.C.F.) and by funds from the National Science Foundation: Grant DEB-1655624 (to B.C.F. and R.T.B.), Grant DEB-1655736 (to B.T.S., D.T.K., and R.T.C.), Grants DEB-1655559 and DEB-1541312 (to F.K.B.), Grant DEB-1655683 (to R.T.K. and E.L.B.), Grants DEB-1241181 and DEB-1557053 (to R.G.M.), Grant DEB-1146265 (to R.T.B., A.A., R.T.C., and F.H.S.), Grant DEB-1241066 (to J.C.), and Grant DEB-1146423 (to E.P.D.). M.J.B., N.D.W., T.C.G., R.T.B., E.L.B., and B.C.F. were supported by grants from the Smithsonian Grand Challenges Consortia. G.A.B. and L.F.S. were supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (Grants 2012-23852-0 and 56378-0). L.F.S. and A.A. were supported by the Conselho Nacional de Pesquisas (Grants 302291/2015-6 and 306843/2016-1). P.A. was supported by the Swedish Research Foundation (Grant 2015-04402) and Jornvall Foundation. Portions of this research were conducted with high-performance computing resources provided by Louisiana State University (www.hpc.lsu.edu). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.
Supporting Information
Appendix (PDF)
- Download
- 707.55 KB
Dataset_S01 (XLSX)
- Download
- 43.15 KB
Dataset_S02 (TXT)
- Download
- 743.04 KB
Dataset_S03 (XLSX)
- Download
- 20.65 KB
References
1
A Feduccia, Explosive evolution in tertiary birds and mammals. Science 267, 637–638 (1995).
2
ED Jarvis, et al., Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014).
3
RO Prum, et al., A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).
4
S Claramunt, J Cracraft, A new time tree reveals Earth history’s imprint on the evolution of modern birds. Sci Adv 1, e1501005 (2015).
5
RG Moyle, et al., Tectonic collision and uplift of Wallacea triggered the global songbird radiation. Nat Commun 7, 12709 (2016).
6
W Jetz, GH Thomas, JB Joy, K Hartmann, AO Mooers, The global diversity of birds in space and time. Nature 491, 444–448 (2012).
7
G Mayr Avian Evolution (Wiley, Chichester, UK, 2017).
8
DJ Field, et al., Early evolution of modern birds structured by global forest collapse at the end-Cretaceous mass extinction. Curr Biol 28, 1825–1831.e2 (2018).
9
FK Barker, A Cibois, P Schikler, J Feinstein, J Cracraft, Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci USA 101, 11040–11045 (2004).
10
DJ Field, AY Hsiang, A North American stem turaco, and the complex biogeographic history of modern birds. BMC Evol Biol 18, 102 (2018).
11
CG Sibley, Jr B Monroe Distribution and Taxonomy of the Birds of the World (Yale Univ Press, New Haven, CT, 1990).
12
E Dickinson, L Christidis The Howard & Moore Complete Checklist of the Birds of the World, eds E Dickinson, L Christidis (Aves Press, 4th Ed, Eastbourne, UK) Vol 2 (2014).
13
CG Sibley, J Ahlquist Phylogeny and Classification of the Birds of the World (Yale Univ Press, New Haven, CT, 1990).
14
FK Barker, GF Barrowclough, JG Groth, A phylogenetic hypothesis for passerine birds: Taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc Biol Sci 269, 295–308 (2002).
15
PGP Ericson, et al., A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens. Proc Biol Sci 269, 235–241 (2002).
16
SJ Hackett, et al., A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008).
17
FK Barker, Mitogenomic data resolve basal relationships among passeriform and passeridan birds. Mol Phylogenet Evol 79, 313–324 (2014).
18
J Cracraft, Avian higher-level relationships and classification: Passeriforms. The Howard & Moore Complete Checklist of the Birds of the World, eds E Dickinson, L Christidis (Aves Press, 4th Ed, Eastbourne, UK) Vol 2, xvii–xlv (2014).
19
AP Selvatti, LP Gonzaga, CADM Russo, A Paleogene origin for crown passerines and the diversification of the Oscines in the New World. Mol Phylogenet Evol 88, 1–15 (2015).
20
GC Gibb, et al., New Zealand passerines help clarify the diversification of major songbird lineages during the Oligocene. Genome Biol Evol 7, 2983–2995 (2015).
21
WE Boles, The world’s oldest songbird. Nature 374, 21–22 (1995).
22
JA Clarke, CP Tambussi, JI Noriega, GM Erickson, RA Ketcham, Definitive fossil evidence for the extant avian radiation in the Cretaceous. Nature 433, 305–308 (2005).
23
RG Moyle, RT Chesser, RO Prum, P Schikler, J Cracraft, Phylogeny and evolutionary history of Old World suboscine birds (Aves: Eurylaimides). Am Mus Novit 3544, 1–22 (2006).
24
KA Jønsson, P-H Fabre, RE Ricklefs, J Fjeldså, Major global radiation of corvoid birds originated in the proto-Papuan archipelago. Proc Natl Acad Sci USA 108, 2328–2333 (2011).
25
JI Ohlson, M Irestedt, PG Ericson, J Fjeldså, Phylogeny and classification of the New World suboscines (Aves, Passeriformes). Zootaxa 3613, 1–35 (2013).
26
DM Hooper, TD Price, Chromosomal inversion differences correlate with range overlap in passerine birds. Nat Ecol Evol 1, 1526–1534 (2017).
27
TD Price, et al., Niche filling slows the diversification of Himalayan songbirds. Nature 509, 222–225 (2014).
28
JF Parham, et al., Best practices for justifying fossil calibrations. Syst Biol 61, 346–359 (2012).
29
H Stehlin, Remarques sur les faunules de mammifères des couches éocènes et oligocènes du Bassin de Paris. Bulletin de la Société Géologique de France 9, 488–520. French (1909).
30
A Cooper, RA Cooper, The Oligocene bottleneck and New Zealand biota: Genetic record of a past environmental crisis. Proc Biol Sci 261, 293–302 (1995).
31
J Meng, MC McKenna, Faunal turnovers of Palaeogene mammals from the Mongolian Plateau. Nature 394, 364–367 (1998).
32
CA Landis, et al., The Waipounamu erosion surface: Questioning the antiquity of the New Zealand land surface and terrestrial fauna and flora. Geol Mag 145, 173–197 (2008).
33
PO Title, DL Rabosky, Do macrophylogenies yield stable macroevolutionary inferences? An example from squamate reptiles. Syst Biol 66, 843–856 (2017).
34
C Hoorn, et al., Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927–931 (2010).
35
BT Smith, et al., The drivers of tropical speciation. Nature 515, 406–409 (2014).
36
Y-J Feng, et al., Phylogenomics reveals rapid, simultaneous diversification of three major clades of Gondwanan frogs at the Cretaceous-Paleogene boundary. Proc Natl Acad Sci USA 114, E5864–E5870 (2017).
37
P Alström, et al., Discovery of a relict lineage and monotypic family of passerine birds. Biol Lett 10, 20131067 (2014).
38
J Fjeldså, D Zuccon, M Irestedt, US Johansson, PGP Ericson, Sapayoa aenigma: A New World representative of ‘Old World suboscines’. Proc Biol Sci 270, S238–S241 (2003).
39
RT Chesser, Molecular systematics of New World suboscine birds. Mol Phylogenet Evol 32, 11–24 (2004).
40
J del Hoyo, N Collar HBW and BirdLife International Illustrated Checklist of the Birds of the World. Passerines (Lynx Edicions, Barcelona) Vol 2 (2016).
41
FB Gill, D Donsker, IOC World Bird List (v. 8.1). Available at https://doi.org/10.14344/IOC.ML.8.1. Accessed February 27, 2018. (2018).
42
PGP Ericson, S Klopfstein, M Irestedt, JMT Nguyen, JAA Nylander, Dating the diversification of the major lineages of Passeriformes (Aves). BMC Evol Biol 14, 8 (2014).
43
JS Berv, DJ Field, Genomic signature of an avian Lilliput effect across the K-Pg extinction. Syst Biol 67, 1–13 (2018).
44
J Cracraft, Continental drift, paleoclimatology, and the evolution and biogeography of birds. J Zool 169, 455–545 (1973).
45
SL Olson, Oligocene fossils bearing on the origins of the Todidae and the Momotidae (Aves: Coraciiformes). Smithson Contrib to Paleobiol 27, 111–119 (1976).
46
ZX Li, CM Powell, An outline of the palaeogeographic evolution of the Australasian region since the beginning of the Neoproterozoic. Earth Sci Rev 53, 237–277 (2001).
47
HD Scher, EE Martin, Timing and climatic consequences of the opening of Drake Passage. Science 312, 428–430 (2006).
48
RH Ree, I Sanmartín, Conceptual and statistical problems with the DEC+J model of founder-event speciation and its comparison with DEC via model selection. J Biogeogr 45, 741–749 (2018).
49
J Cracraft, S Claramunt, Conceptual and analytical worldviews shape differences about global avian biogeography. J Biogeogr 44, 958–960 (2017).
50
CR Marshall, Five palaeobiological laws needed to understand the evolution of the living biota. Nat Ecol Evol 1, 0165 (2017).
51
G Mayr, A Manegold, New specimens of the earliest European passeriform bird. Acta Palaeontol Pol 51, 315–323 (2006).
52
G Mayr Paleogene Fossil Birds (Springer, Berlin, 2009).
53
I Sanmartín, H Enghoff, F Ronquist, Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biol J Linn Soc Lond 73, 345–390 (2001).
54
J Zachos, M Pagani, L Sloan, E Thomas, K Billups, Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686–693 (2001).
55
M Irestedt, JI Ohlson, D Zuccon, M Källersjö, PGP Ericson, Nuclear DNA from old collections of avian study skins reveals the evolutionary history of the Old World suboscines (Aves, Passeriformes). Zool Scr 35, 567–580 (2006).
56
AP Selvatti, A Galvão, AG Pereira, L Pedreira Gonzaga, CA Russo, An African origin of the Eurylaimides (Passeriformes) and the successful diversification of the ground-foraging pittas (Pittidae). Mol Biol Evol 34, 483–499 (2017).
57
P-O Antoine, et al., First record of Paleogene Elephantoidea (Mammalia, Proboscidea) from the Bugti Hills of Pakistan. J Vertebr Paleontol 23, 977–980 (2003).
58
J Kappelman, et al., Oligocene mammals from Ethiopia and faunal exchange between Afro-Arabia and Eurasia. Nature 426, 549–552 (2003).
59
JX Samuels, LB Albright, TJ Fremd, The last fossil primate in North America, new material of the enigmatic Ekgmowechashala from the Arikareean of Oregon. Am J Phys Anthropol 158, 43–54 (2015).
60
G Mayr, Two-phase extinction of “Southern Hemispheric” birds in the Cenozoic of Europe and the origin of the Neotropic avifauna. Palaeobiodivers Palaeoenviron 91, 325–333 (2011).
61
A Manegold, Passerine diversity in the late Oligocene of Germany: Earliest evidence for the sympatric coexistence of suboscines and oscines. Ibis 150, 377–387 (2008).
62
C Mourer-Chauvire, M Hugueney, P Jonet, Discovery of passeriformes in the Upper Oligocene of France. C R Acad Sci II 309, 843–849 (1989).
63
R Hall, Southeast Asia’s changing palaeogeography. Blumea J Plant Taxon Plant Geogr 54, 148–161 (2009).
64
J Fuchs, J Fjeldså, RCK Bowie, G Voelker, E Pasquet, The African warbler genus Hyliota as a lost lineage in the Oscine songbird tree: Molecular support for an African origin of the Passerida. Mol Phylogenet Evol 39, 186–197 (2006).
65
KA Jønsson, J Fjeldså, Determining biogeographical patterns of dispersal and diversification in oscine passerine birds in Australia, Southeast Asia and Africa. J Biogeogr 33, 1155–1165 (2006).
66
KJ Mitchell, et al., Ancient mitochondrial genomes clarify the evolutionary history of New Zealand’s enigmatic acanthisittid wrens. Mol Phylogenet Evol 102, 295–304 (2016).
67
TH Worthy, AJD Tennyson, RP Scofield, An early Miocene diversity of parrots (Aves, Strigopidae, Nestorinae) from New Zealand. J Vertebr Paleontol 31, 1102–1116 (2011).
68
B Kass, A Raftery, Bayes factors. J Am Stat Assoc 90, 773–795 (1995).
69
CAE Strömberg, Evolution of grasses and grassland ecosystems. Annu Rev Earth Planet Sci 39, 517–544 (2011).
70
DA Duchêne, X Hua, L Bromham, Phylogenetic estimates of diversification rate are affected by molecular rate variation. J Evol Biol 30, 1884–1897 (2017).
71
JE McCormack, et al., Ultraconserved elements are novel phylogenomic markers that resolve placental mammal phylogeny when combined with species-tree analysis. Genome Res 22, 746–754 (2012).
72
JD Manthey, LC Campillo, KJ Burns, RG Moyle, Comparison of target-capture and restriction-site associated DNA sequencing for phylogenomics: A test in cardinalid tanagers (Aves, genus: Piranga). Syst Biol 65, 640–650 (2016).
73
LC Campillo, CH Oliveros, FH Sheldon, RG Moyle, Genomic data resolve gene tree discordance in spiderhunters (Nectariniidae, Arachnothera). Mol Phylogenet Evol 120, 151–157 (2018).
74
G Zhang, et al., Comparative genomics reveals insights into avian genome evolution and adaptation. Science; Avian Genome Consortium 346, 1311–1320 (2014).
75
BC Faircloth, Tutorial III: Harvesting UCE Loci from Genomes. Available at https://phyluce.readthedocs.io/en/latest/tutorial-three.html. Accessed August 6, 2018. (2018).
76
TC Glenn, et al., Adapterama I: Universal stubs and primers for thousands of dual-indexed Illumina libraries (iTru & iNext). bioRxiv:10.1101/049114. (2016).
77
MG Grabherr, et al., Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29, 644–652 (2011).
78
S Nurk, et al., Assembling genomes and mini-metagenomes from highly chimeric reads. Research in Computational Molecular Biology. RECOMB 2013, Lecture Notes in Computer Science, eds Deng M, Jiang R, Sun F, Zhang X (Springer, Berlin), Vol 7821, pp 158–170. (2013).
79
BC Faircloth, PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32, 786–788 (2016).
80
BC Faircloth, Tutorial I: UCE Phylogenomics. Available at https://phyluce.readthedocs.io/en/latest/tutorial-one.html. Accessed August 6, 2018. (2018).
81
AM Kozlov, AJ Aberer, A Stamatakis, ExaML version 3: A tool for phylogenomic analyses on supercomputers. Bioinformatics 31, 2577–2579 (2015).
82
A Stamatakis, RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
83
J Chifman, L Kubatko, Quartet inference from SNP data under the coalescent model. Bioinformatics 30, 3317–3324 (2014).
84
J Chifman, L Kubatko, Identifiability of the unrooted species tree topology under the coalescent model with time-reversible substitution processes, site-specific rate variation, and invariable sites. J Theor Biol 374, 35–47 (2015).
85
P Vachaspati, T Warnow, ASTRID: Accurate species TRees from internode distances. BMC Genomics 16, S3 (2015).
86
S Mirarab, T Warnow, ASTRAL-II: Coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44–i52 (2015).
87
L Liu, L Yu, DK Pearl, SV Edwards, Estimating species phylogenies using coalescence times among sequences. Syst Biol 58, 468–477 (2009).
88
TK Seo, Calculating bootstrap probabilities of phylogeny using multilocus sequence data. Mol Biol Evol 25, 960–971 (2008).
89
SYW Ho, MJ Phillips, Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times. Syst Biol 58, 367–380 (2009).
90
AJ Drummond, MA Suchard, D Xie, A Rambaut, Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29, 1969–1973 (2012).
91
M dos Reis, Z Yang, Approximate likelihood calculation on a phylogeny for Bayesian estimation of divergence times. Mol Biol Evol 28, 2161–2172 (2011).
92
SA Smith, JW Brown, JF Walker, So many genes, so little time: A practical approach to divergence-time estimation in the genomic era. PLoS One 13, e0197433 (2018).
93
A Rambaut, AJ Drummond, Tracer v.1.6. Available at tree.bio.ed.ac.uk/software/tracer/. Accessed April 25, 2017. (2014).
94
JW Brown, SA Smith, The past sure is tense: On interpreting phylogenetic divergence time estimates. Syst Biol 67, 340–353 (2018).
95
NJ Matzke, BioGeoBEARS: BioGeography with Bayesian (and likelihood) evolutionary analysis in R scripts. PhD dissertation (University of California, Berkeley, CA). (2013).
96
JR Clark, et al., A comparative study in ancestral range reconstruction methods: Retracing the uncertain histories of insular lineages. Syst Biol 57, 693–707 (2008).
97
RH Ree, SA Smith, Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 57, 4–14 (2008).
98
NJ Matzke, Model selection in historical biogeography reveals that founder-event speciation is a crucial process in Island Clades. Syst Biol 63, 951–970 (2014).
99
J Hansen, M Sato, G Russell, P Kharecha, Climate sensitivity, sea level and atmospheric carbon dioxide. Philos Trans A Math Phys Eng Sci 371, 20120294 (2013).
100
T Stadler, Mammalian phylogeny reveals recent diversification rate shifts. Proc Natl Acad Sci USA 108, 6187–6192 (2011).
101
S Höhna, The time-dependent reconstructed evolutionary process with a key-role for mass-extinction events. J Theor Biol 380, 321–331 (2015).
102
S Höhna, et al., RevBayes: Bayesian phylogenetic inference using graphical models and an interactive model-specification language. Syst Biol 65, 726–736 (2016).
103
S Höhna, et al., Statistical phylogenetic inference using RevBayes. Available at https://raw.githubusercontent.com/revbayes/revbayes_tutorial/master/tutorial_TeX/RB_Manual.pdf. Accessed January 16, 2017. (2017).
104
; R Development Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna). Version 3.3.2. Available at www.r-project.org. Accessed February 1, 2017. (2008).
105
DL Rabosky, Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS One 9, e89543 (2014).
106
CH Oliveros, et al., Data from: “Earth history and the passerine superradiation.” Dryad Digital Repository. https://doi.org/10.5061/dryad.2vd01gr. Deposited March 7, 2019. (2019).
Information & Authors
Information
Published in
Cover image: Pictured is a green-headed tanager (Tangara seledon) in Itatiaia National Park, Brazil. Carl H. Oliveros et al. analyzed the DNA of 137 passerine families as well as fossil and geological records and found that passerine diversification began around 47 million years ago in Australia and did not strongly correlate with changing global temperatures or the colonization of new continents. The findings suggest that passerine diversification likely resulted from complex mechanisms that included several climatological and geological events. See the article by Oliveros et al. on pages 7916–7925. Image courtesy of Daniel J. Field.
Classifications
Copyright
Copyright © 2019 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Data Availability
Data deposition: Raw sequencing reads and ultraconserved element (UCE) nucleotide sequences are available from the National Center for Biotechnology Information (NCBI) Sequence Read Archive and Genbank as part of BioProjects PRJNA304409 and PRJNA480834. NCBI BioSample accession numbers are available in Dataset S1. The PHYLUCE computer code used in this study is available from https://github.com/faircloth-lab/phyluce. Other custom computer code, DNA alignments, analysis inputs, and analysis outputs are available from the Dryad Digital Repository database, datadryad.org/ (doi: https://doi.org/10.5061/dryad.2vd01gr).
Submission history
Published online: April 1, 2019
Published in issue: April 16, 2019
Keywords
Acknowledgments
We thank the curators, staff, and field collectors at the institutions listed in Dataset S1 for tissue samples used in this project; without their hard work, this study would not have been possible. We also thank Van Remsen for comments on earlier drafts, and we thank our three reviewers and the editor for their comments, which improved this manuscript. This study was supported by setup funds from Louisiana State University (to B.C.F.) and by funds from the National Science Foundation: Grant DEB-1655624 (to B.C.F. and R.T.B.), Grant DEB-1655736 (to B.T.S., D.T.K., and R.T.C.), Grants DEB-1655559 and DEB-1541312 (to F.K.B.), Grant DEB-1655683 (to R.T.K. and E.L.B.), Grants DEB-1241181 and DEB-1557053 (to R.G.M.), Grant DEB-1146265 (to R.T.B., A.A., R.T.C., and F.H.S.), Grant DEB-1241066 (to J.C.), and Grant DEB-1146423 (to E.P.D.). M.J.B., N.D.W., T.C.G., R.T.B., E.L.B., and B.C.F. were supported by grants from the Smithsonian Grand Challenges Consortia. G.A.B. and L.F.S. were supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (Grants 2012-23852-0 and 56378-0). L.F.S. and A.A. were supported by the Conselho Nacional de Pesquisas (Grants 302291/2015-6 and 306843/2016-1). P.A. was supported by the Swedish Research Foundation (Grant 2015-04402) and Jornvall Foundation. Portions of this research were conducted with high-performance computing resources provided by Louisiana State University (www.hpc.lsu.edu). Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government.
Notes
This article is a PNAS Direct Submission. M.E.A. is a guest editor invited by the Editorial Board.
Authors
Competing Interests
The authors declare no conflict of interest.
Metrics & Citations
Metrics
Citation statements
Altmetrics
Citations
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.
Cited by
Loading...
View Options
View options
PDF format
Download this article as a PDF file
DOWNLOAD PDFLogin options
Check if you have access through your login credentials or your institution to get full access on this article.
Personal login Institutional LoginRecommend to a librarian
Recommend PNAS to a LibrarianPurchase options
Purchase this article to access the full text.