The DOI matches its Crossref record; 50 of the 50 references it cites were found in a registry or an index.
Anchored Hybrid Enrichment for Massively High-Throughput Phylogenomics
Abstract
The field of phylogenetics is on the cusp of a major revolution, enabled by new methods of data collection that leverage both genomic resources and recent advances in DNA sequencing. Previous phylogenetic work has required labor-intensive marker development coupled with single-locus polymerase chain reaction and DNA sequencing on clade-by-clade and locus-by-locus basis. Here, we present a new, cost-efficient, and rapid approach to obtaining data from hundreds of loci for potentially hundreds of individuals for deep and shallow phylogenetic studies. Specifically, we designed probes for target enrichment of >500 loci in highly conserved anchor regions of vertebrate genomes (flanked by less conserved regions) from five model species and tested enrichment efficiency in nonmodel species up to 508 million years divergent from the nearest model. We found that hybrid enrichment using conserved probes (anchored enrichment) can recover a large number of unlinked loci that are useful at a diversity of phylogenetic timescales. This new approach has the potential not only to expedite resolution of deep-scale portions of the Tree of Life but also to greatly accelerate resolution of the large number of shallow clades that remain unresolved. The combination of low cost (~1% of the cost of traditional Sanger sequencing and ~3.5% of the cost of high-throughput amplicon sequencing for projects on the scale of 500 loci × 100 individuals) and rapid data collection (~2 weeks of laboratory time) are expected to make this approach tractable even for researchers working on systems with limited or nonexistent genomic resources.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662
MrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 29,077
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849
MacClade 4.0: analysis of phylogeny and character evolution
(2001) · Choice Reviews Online · doi:10.5860/choice.39-2183 · Cited by 5,554
Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes
Siepel, A., Bejerano, G., Pedersen, J. S., Hinrichs, A. S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L. W., Richards, S., et al. (2005) · Genome Research · doi:10.1101/gr.3715005 · Cited by 3,971 · cited 3×
“Highly conserved regions of the genome have been discovered in insects, worms, and yeast as well as a diverse set of vertebrates (Glazov et al. 2005; Siepel et al. 2005; Stephen et al. 2008; Wang et al. 2009; Janes et al. 2010) and could easily be used in probe design as in the present study.”
BackgroundMrModeltest 2.2. Program Distributed by the Author
Nylander, J. A. A., Nylander, J., & Nylander, J. A. A. (2004) · Medical Entomology and Zoology · Cited by 2,648
Illumina Sequencing Library Preparation for Highly Multiplexed Target Capture and Sequencing
Meyer, M., & Kircher, M. (2010) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5448 · Cited by 2,231
The UCSC Genome Browser database: update 2011
Fujita, P. A., Rhead, B., Zweig, A. S., Hinrichs, A. S., Karolchik, D., Cline, M. S., Goldman, M., Barber, G. P., Clawson, H., Coelho, A., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkq963 · Cited by 1,811
Ultraconserved Elements in the Human Genome
Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W. J., Mattick, J. S., & Haussler, D. (2004) · Science · doi:10.1126/science.1098119 · Cited by 1,732
Gnirke, A., Melnikov, A., Maguire, J., Rogov, P., LeProust, E. M., Brockman, W., Fennell, T., Giannoukos, G., Fisher, S., Russ, C., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1523 · Cited by 1,433 · cited 1×
“sequence capture) uses oligonucleotides as baits that hybridize to genomic fragments containing the target sequence and allows target loci to be separated from nontarget regions of the genome (Albert et al. 2007; Gnirke et al. 2009).”
BackgroundFaircloth, B. C., McCormack, J. E., Crawford, N. G., Harvey, M. G., Brumfield, R. T., & Glenn, T. C. (2012) · Systematic Biology · doi:10.1093/sysbio/sys004 · Cited by 1,270
TimeTree: A public knowledge-base of divergence times among organisms
Hedges, S. B., Dudley, J., & Kumar, S. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl505 · Cited by 1,234
Target-enrichment strategies for next-generation sequencing
Mamanova, L., Coffey, A. J., Scott, C. E., Kozarewa, I., Turner, E. H., Kumar, A., Howard, E., Shendure, J., & Turner, D. J. (2010) · Nature Methods · doi:10.1038/nmeth.1419 · Cited by 1,219
Inferring Phylogeny Despite Incomplete Lineage Sorting
Maddison, W. P., & Knowles, L. L. (2006) · Systematic Biology · doi:10.1080/10635150500354928 · Cited by 1,142
Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform
Kircher, M., Sawyer, S., & Meyer, M. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr771 · Cited by 1,106
Increased Taxon Sampling Greatly Reduces Phylogenetic Error
Zwickl, D. J., & Hillis, D. M. (2002) · Systematic Biology · doi:10.1080/10635150290102339 · Cited by 939
Selecting the Best-Fit Model of Nucleotide Substitution
Posada, D., & Crandall, K. A. (2001) · Systematic Biology · doi:10.1080/10635150118469 · Cited by 937
Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits
Lutzoni, F., Kauff, F., Cox, C. J., McLaughlin, D., Celio, G., Dentinger, B., Padamsee, M., Hibbett, D., James, T. Y., Baloch, E., et al. (2004) · American Journal of Botany · doi:10.3732/ajb.91.10.1446 · Cited by 816
Direct selection of human genomic loci by microarray hybridization
Albert, T. J., Molla, M. N., Muzny, D. M., Nazareth, L., Wheeler, D., Song, X., Richmond, T. A., Middle, C. M., Rodesch, M. J., Packard, C. J., et al. (2007) · Nature Methods · doi:10.1038/nmeth1111 · Cited by 681
High-resolution species trees without concatenation
Edwards, S. V., Liu, L., & Pearl, D. K. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0607004104 · Cited by 588
Keeling, P. J., Burger, G., Durnford, D. G., Lang, B. F., Lee, R. W., Pearlman, R. E., Roger, A. J., & Gray, M. W. (2005) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2005.09.005 · Cited by 579
Genome 10K: A Proposal to Obtain Whole-Genome Sequence for 10 000 Vertebrate Species
Scientists, G. 1. C. O. (2009) · Journal of Heredity · doi:10.1093/jhered/esp086 · Cited by 547
Bayesian Estimation of Concordance among Gene Trees
Ane, C., Larget, B., Baum, D. A., Smith, S. D., & Rokas, A. (2006) · Molecular Biology and Evolution · doi:10.1093/molbev/msl170 · Cited by 489
Eukaryotic genome size databases
Gregory, T. R., Nicol, J. A., Tamm, H., Kullman, B., Kullman, K., Leitch, I. J., Murray, B. G., Kapraun, D. F., Greilhuber, J., & Bennett, M. D. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl828 · Cited by 432
(2005) · Choice Reviews Online · doi:10.5860/choice.42-4627 · Cited by 411
BEST: Bayesian estimation of species trees under the coalescent model
Liu, L. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn484 · Cited by 384
McCormack, J. E., Faircloth, B. C., Crawford, N. G., Gowaty, P. A., Brumfield, R. T., & Glenn, T. C. (2012) · Genome Research · doi:10.1101/gr.125864.111 · Cited by 377
Profiling Phylogenetic Informativeness
Townsend, J. P. (2007) · Systematic Biology · doi:10.1080/10635150701311362 · Cited by 328
Rokas, A., & Carroll, S. B. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040352 · Cited by 315
Mapping the Tree of Life: Progress and Prospects
Pace, N. R. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00033-09 · Cited by 286
The Accuracy of Species Tree Estimation under Simulation: A Comparison of Methods
Leaché, A. D., & Rannala, B. (2011) · Systematic Biology · doi:10.1093/sysbio/syq073 · Cited by 271
Estimating Species Trees from Unrooted Gene Trees
Liu, L., & Yu, L. (2011) · Systematic Biology · doi:10.1093/sysbio/syr027 · Cited by 252
Broadly Sampled Multigene Analyses Yield a Well-Resolved Eukaryotic Tree of Life
Parfrey, L. W., Grant, J., Tekle, Y. I., Lasek-Nesselquist, E., Morrison, H. G., Sogin, M. L., Patterson, D. J., & Katz, L. A. (2010) · Systematic Biology · doi:10.1093/sysbio/syq037 · Cited by 231
The eukaryotic tree of life: endosymbiosis takes its TOL
Lane, C. E., & Archibald, J. M. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2008.02.004 · Cited by 229
Creating a Buzz About Insect Genomes
Robinson, G. E., Hackett, K. J., Purcell-Miramontes, M., Brown, S. J., Evans, J. D., Goldsmith, M. R., Lawson, D., Okamuro, J., Robertson, H. M., & Schneider, D. J. (2011) · Science · doi:10.1126/science.331.6023.1386 · Cited by 206
The plant tree of life: an overview and some points of view
Palmer, J. D., Soltis, D. E., & Chase, M. W. (2004) · American Journal of Botany · doi:10.3732/ajb.91.10.1437 · Cited by 197
Huang, H., He, Q., Kubatko, L. S., & Knowles, L. L. (2010) · Systematic Biology · doi:10.1093/sysbio/syq047 · Cited by 156
Glazov, E. A., Pheasant, M., McGraw, E. A., Bejerano, G., & Mattick, J. S. (2005) · Genome Research · doi:10.1101/gr.3545105 · Cited by 124
Stephen, S. J., Pheasant, M., Makunin, I. V., & Mattick, J. S. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm268 · Cited by 119
(2004) · doi:10.1093/oso/9780195172348.001.0001 · Cited by 101
Taxon Sampling and the Optimal Rates of Evolution for Phylogenetic Inference
Townsend, J. P., & Leuenberger, C. (2011) · Systematic Biology · doi:10.1093/sysbio/syq097 · Cited by 99
DNA and Amphibian Life History
Goin, O. B., Goin, C. J., & Bachmann, K. (1968) · Copeia · doi:10.2307/1442021 · Cited by 97
Bashiardes, S., Veile, R. A., Helms, C. A., Mardis, E. R., Bowcock, A. M., & Lovett, M. (2004) · Nature Methods · doi:10.1038/nmeth0105-63 · Cited by 91
Repeat subtraction-mediated sequence capture from a complex genome
Fu, Y., Springer, N. M., Gerhardt, D. J., Ying, K., Yeh, C., Wu, W., Swanson-Wagner, R. A., D'Ascenzo, M. D., Millard, T., Freeberg, L., et al. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2010.04196.x · Cited by 81
Optimal Selection of Gene and Ingroup Taxon Sampling for Resolving Phylogenetic Relationships
Townsend, J. P., & López‐Giráldez, F. (2010) · Systematic Biology · doi:10.1093/sysbio/syq025 · Cited by 81
Townsend, J. P., López‐Giráldez, F., & Friedman, R. (2008) · Journal of Molecular Evolution · doi:10.1007/s00239-008-9142-0 · Cited by 68
Rapid progress on the vertebrate tree of life
Thomson, R. C., & Shaffer, H. B. (2010) · BMC Biology · doi:10.1186/1741-7007-8-19 · Cited by 44
Large Number of Ultraconserved Elements Were Already Present in the Jawed Vertebrate Ancestor
Wang, J., Lee, A., Kodzius, R., Brenner, S., & Venkatesh, B. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn278 · Cited by 38
Janes, D. E., Chapus, C., Gondo, Y., Clayton, D. F., Sinha, S., Blatti, C. A., Organ, C. L., Fujita, M. K., Balakrishnan, C. N., & Edwards, S. V. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq087 · Cited by 30
Assembling the Angiosperm Tree of Life: Progress and Future Prospects
Soltis, P. S., Moore, M. J., Burleigh, J. G., Bell, C. D., & Soltis, P. S. (2010) · Annals of the Missouri Botanical Garden · doi:10.3417/2009136 · Cited by 25
Cited by
A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing
Prum, R. O., Berv, J. S., Dornburg, A., Field, D. J., Townsend, J. P., Lemmon, E. M., & Lemmon, A. R. (2015) · Nature · doi:10.1038/nature15697 · Cited by 1,668
Self-citationA phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes
Pyron, R., Burbrink, F. T., & Wiens, J. J. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-93 · Cited by 1,641
Phylogenetic classification of bony fishes
Betancur-R, R., Wiley, E. O., Arratia, G., Acero, A., Bailly, N., Miya, M., Lecointre, G., & Ortí, G. (2017) · BMC Evolutionary Biology · doi:10.1186/s12862-017-0958-3 · Cited by 857
Selecting optimal partitioning schemes for phylogenomic datasets
Lanfear, R., Calcott, B., Kainer, D., Mayer, C., & Stamatakis, A. (2014) · BMC Evolutionary Biology · doi:10.1186/1471-2148-14-82 · Cited by 762
Johnson, M. G., Pokorny, L., Dodsworth, S., Botigué, L. R., Cowan, R. S., Devault, A., Eiserhardt, W. L., Epitawalage, N., Forest, F., Kim, J. T., et al. (2019) · Systematic Biology · doi:10.1093/sysbio/syy086 · Cited by 593
Metadata
- Authors
- Lemmon, A. R., Emme, S. A., & Lemmon, E. M.
- Venue
- Systematic Biology
- Publisher
- Oxford University Press (OUP)
- Published
- 2012-07-05
- Volume
- 61
- Issue
- 5
- Pages
- 727-744
- ISSN
- 1063-5157 (ISSN-L)
- 1076-836X
- OpenAlex
- W2066289589
- Cited by
- 833
- References
- 50
- FWCI
- 14.06
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.