A Molecular Phylogeny of Living Primates
Comparative genomic analyses of primates offer considerable potential to define and understand the processes that mold, shape, and transform the human genome. However, primate taxonomy is both complex and controversial, with marginal unifying consensus of the evolutionary hierarchy of extant primate species. Here we provide new genomic sequence (∼8 Mb) from 186 primates representing 61 (∼90%) of the described genera, and we include outgroup species from Dermoptera, Scandentia, and Lagomorpha. The resultant phylogeny is exceptionally robust and illuminates events in primate evolution from ancient to recent, clarifying numerous taxonomic controversies and providing new data on human evolution. Ongoing speciation, reticulate evolution, ancient relic lineages, unequal rates of evolution, and disparate distributions of insertions/deletions among the reconstructed primate lineages are uncovered. Our resolution of the primate phylogeny provides an essential evolutionary framework with far-reaching applications including: human selection and adaptation, global emergence of zoonotic diseases, mammalian comparative genomics, primate taxonomy, and conservation of endangered species.
Vyšlo v časopise:
A Molecular Phylogeny of Living Primates. PLoS Genet 7(3): e32767. doi:10.1371/journal.pgen.1001342
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001342
Souhrn
Comparative genomic analyses of primates offer considerable potential to define and understand the processes that mold, shape, and transform the human genome. However, primate taxonomy is both complex and controversial, with marginal unifying consensus of the evolutionary hierarchy of extant primate species. Here we provide new genomic sequence (∼8 Mb) from 186 primates representing 61 (∼90%) of the described genera, and we include outgroup species from Dermoptera, Scandentia, and Lagomorpha. The resultant phylogeny is exceptionally robust and illuminates events in primate evolution from ancient to recent, clarifying numerous taxonomic controversies and providing new data on human evolution. Ongoing speciation, reticulate evolution, ancient relic lineages, unequal rates of evolution, and disparate distributions of insertions/deletions among the reconstructed primate lineages are uncovered. Our resolution of the primate phylogeny provides an essential evolutionary framework with far-reaching applications including: human selection and adaptation, global emergence of zoonotic diseases, mammalian comparative genomics, primate taxonomy, and conservation of endangered species.
Zdroje
1. GoodmanM
PorterCA
CzelusniakJ
PageSL
SchneiderH
1998
Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence.
Molecular Phylogenetics and Evolution
9
585
598
2. GrovesCP
2001
Primate taxonomy.
Washington, DC
Smithsonian Institution Press
350
3. WilsonDE
ReederDM
2005
Mammal species of the world : a taxonomic and geographic reference.
Baltimore
Johns Hopkins University Press
2142
4. ChatterjeeHJ
HoSYW
BarnesI
GrovesC
2009
Estimating the phylogeny and divergence times of primates using a supermatrix approach.
BMC Evolutionary Biology
9
259
5. FabrePH
RodriguesA
DouzeryEJP
2009
Patterns of macroevolution among Primates inferred from a supermatrix of mitochondrial and nuclear DNA.
Molecular Phylogenetics and Evolution
53
808
825
6. Pecon-SlatteryJ
WilkersonAJP
MurphyWJ
O'BrienSJ
2004
Phylogenetic assessment of introns and SINEs within the Y chromosome using the cat family Felidae as a species tree.
Molecular Biology and Evolution
21
2299
2309
7. JohnsonWE
EizirikE
Pecon-SlatteryJ
MurphyWJ
AntunesA
2006
The Late Miocene radiation of modern Felidae: A genetic assessment.
Science
311
73
77
8. Eizirik EMW
SpringerMS
O'BrienSJ
2004
Molecular Phylogeny and Dating of Early Primate Divergences.
Ross CFKR
Anthropoid Origins: New Visions
New York
Kluwer Academic/Plenum
45
65
9. BajpaiS
KayRF
WilliamsBA
DasDP
KapurVV
2008
The oldest Asian record of Anthropoidea.
Proceedings of the National Academy of Sciences of the United States of America
105
11093
11098
10. KayRF
RossC
WilliamsBA
1997
Anthropoid origins.
Science
275
797
804
11. NowakRM
1999
Walker's mammals of the world.
Baltimore
Johns Hopkins University Press
1936
12. MurphyWJ
EizirikE
JohnsonWE
ZhangYP
RyderOA
2001
Molecular phylogenetics and the origins of placental mammals.
Nature
409
614
618
13. SchmitzJ
OhmeM
ZischlerH
2001
SINE insertions in cladistic analyses and the phylogenetic affiliations of Tarsius bancanus to other primates.
Genetics
157
777
784
14. MatsuiA
RakotondraparanyF
MunechikaI
HasegawaM
HoraiS
2009
Molecular phylogeny and evolution of prosimians based on complete sequences of mitochondrial DNAs.
Gene
441
53
66
15. ArnasonU
AdegokeJA
BodinK
BornEW
EsaYB
2002
Mammalian mitogenomic relationships and the root of the eutherian tree.
Proceedings of the National Academy of Sciences of the United States of America
99
8151
8156
16. JaneckaJE
MillerW
PringleTH
WiensF
ZitzmannA
2007
Molecular and genomic data identify the closest living relative of primates.
Science
318
792
794
17. KriegsJO
ChurakovG
JurkaJ
BrosiusJ
SchmitzJ
2007
Evolutionary history of 7SL RNA-derived SINEs in supraprimates.
Trends in Genetics
23
158
161
18. ChurakovG
KriegsJO
BaertschR
ZemannA
BrosiusJ
2009
Mosaic retroposon insertion patterns in placental mammals.
Genome Research
19
868
875
19. RoosC
SchmitzJ
ZischlerH
2004
Primate jumping genes elucidate strepsirrhine phylogeny.
Proceedings of the National Academy of Sciences of the United States of America
101
10650
10654
20. HorvathJE
WillardHF
2007
Primate comparative genomics: lemur biology and evolution.
Trends in Genetics
23
173
182
21. HorvathJE
WeisrockDW
EmbrySL
FiorentinoI
BalhoffJP
2008
Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar's lemurs.
Genome Research
18
489
499
22. MittermeierR
GanzhornJ
KonstantW
GlanderK
TattersallI
2008
Lemur Diversity in Madagascar.
International Journal of Primatology
29
1607
1656
23. TakaiM
AnayaF
ShigeharaN
SetoguchiT
2000
New fossil materials of the earliest new world monkey, Branisella boliviana, and the problem of platyrrhine origins.
American Journal of Physical Anthropology
111
263
281
24. TakaiM
AnayaF
1996
New specimens of the oldest fossil platyrrhine, Branisella boliviana, from Salla, Bolivia.
American Journal of Physical Anthropology
99
301
317
25. PouxC
ChevretP
HuchonD
de JongWW
DouzeryEJP
2006
Arrival and diversification of caviomorph rodents and platyrrhine primates in South America.
Systematic Biology
55
228
244
26. HodgsonJA
SternerKN
MatthewsLJ
BurrellAS
JaniRA
2009
Successive radiations, not stasis, in the South American primate fauna.
Proceedings of the National Academy of Sciences of the United States of America
106
5534
5539
27. OsterholzM
WalterL
RoosC
2008
Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups.
BMC Evolutionary Biology
8
58
28. OpazoJC
WildmanDE
PrychitkoT
JohnsonRM
GoodmanM
2006
Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates).
Molecular Phylogenetics and Evolution
40
274
280
29. SteiperME
RuvoloM
2003
New World monkey phylogeny based on X-linked G6PD DNA sequences.
Molecular Phylogenetics and Evolution
27
121
130
30. OsterholzM
WalterL
RoosC
2009
Retropositional events consolidate the branching order among New World monkey genera.
Molecular Phylogenetics and Evolution
50
507
513
31. Ankel-SimonsF
RasmussenDT
2008
Diurnality, Nocturnality, and the Evolution of Primate Visual Systems.
American Journal of Physical Anthropology
100
117
32. FordSM
DavisLC
1992
Systematics and body size: implications for feeding adaptations in New World monkeys.
American Journal of Physical Anthropology
88
415
468
33. CroppSJ
LarsonA
CheverudJM
1999
Historical biogeography of tamarins, genus Saguinus: The molecular phylogenetic evidence.
American Journal of Physical Anthropology
108
65
89
34. CanavezFC
MoreiraMAM
SimonF
ParhamP
SeuanezHN
1999
Phylogenetic relationships of the callitrichinae (Platyrrhini, Primates) based on beta(2)-microglobulin DNA sequences.
American Journal of Primatology
48
225
236
35. FordSM
1980
Callitrichids as phyletic dwarfs, and the place of Callitrichidae in Platyrrhini.
Primates
21
31
43
36. MoynihanM
1976
The New World primates : adaptive radiation and the evolution of social behavior, languages, and intelligence.
Princeton, N.J.
Princeton University Press
262
37. FleagleJG
1988
Primate adaptation and evolution.
San Diego
Academic Press
486
38. DelsonE
1992
Evolution of Old World Monkeys.
Jones SMR
PilbeamD
The Cambridge Encyclopedia of Human Evolution
Cambridge UK
Cambridge University Press
217
222
39. XingJ
WangH
ZhangY
RayDA
TosiAJ
2007
A mobile element-based evolutionary history of guenons (tribe Cercopithecini).
BMC Biology
5
5
40. TingN
TosiAJ
LiY
ZhangYP
DisotellTR
2008
Phylogenetic incongruence between nuclear and mitochondrial markers in the Asian colobines and the evolution of the langurs and leaf monkeys.
Molecular Phylogenetics and Evolution
46
466
474
41. PageSL
GoodmanM
2001
Catarrhine phylogeny: Noncoding DNA evidence for a diphyletic origin of the mangabeys and for a human-chimpanzee clade.
Molecular Phylogenetics and Evolution
18
14
25
42. PageSL
ChiuCH
GoodmanM
1999
Molecular phylogeny of old world monkeys (Cercopithecidae) as inferred from gamma-globin DNA sequences.
Molecular Phylogenetics and Evolution
13
348
359
43. MoulinS
Gerbault-SeureauM
DutrillauxB
RichardFA
2008
Phylogenomics of African guenons.
Chromosome Research
16
783
799
44. KaranthKP
SinghL
ColluraRV
StewartCB
2008
Molecular phylogeny and biogeography of langurs and leaf monkeys of South Asia (Primates : Colobinae).
Molecular Phylogenetics and Evolution
46
683
694
45. GrovesCP
1989
Cercopithecus and company: a primate radiation.
Science
244
860
861
46. KaranthKP
2008
Primate numts and reticulate evolution of capped and golden leaf monkeys (Primates: Colobinae).
Journal of biosciences
33
761
770
47. TosiAJ
MelnickDJ
DisotellTR
2004
Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini).
Journal of Human Evolution
46
223
237
48. TosiAJ
DisotellTR
MoralesJC
MelnickDJ
2003
Cercopithecine Y-chromosome data provide a test of competing morphological evolutionary hypotheses.
Molecular Phylogenetics and Evolution
27
510
521
49. ZieglerT
AbeggC
MeijaardE
Perwitasari-FarajallahD
WalterL
2007
Molecular phylogeny and evolutionary history of Southeast Asian macaques forming the M. silenus group.
Molecular Phylogenetics and Evolution
42
807
816
50. ElangoN
ThomasJW
YiSV
PrograNCS
2006
Variable molecular clocks in hominoids.
Proceedings of the National Academy of Sciences of the United States of America
103
1370
1375
51. SteiperME
2006
Population history, biogeography, and taxonomy of orangutans (Genus : Pongo) based on a population genetic meta-analysis of multiple loci.
Journal of Human Evolution
50
509
522
52. MullerS
HollatzM
WienbergJ
2003
Chromosomal phylogeny and evolution of gibbons (Hylobatidae).
Human Genetics
113
493
501
53. JauchA
WienbergJ
StanyonR
ArnoldN
TofanelliS
1992
Reconstruction of genomic rearrangements in great apes and gibbons by chromosome painting.
Proceedings of the National Academy of Sciences of the United States of America
89
8611
8615
54. MisceoD
CapozziO
RobertoR
Dell'OglioMP
RocchiM
2008
Tracking the complex flow of chromosome rearrangements from the Hominoidea Ancestor to extant Hylobates and Nomascus Gibbons by high-resolution synteny mapping.
Genome Research
18
1530
1537
55. RoosC
GeissmannT
2001
Molecular phylogeny of the major hylobatid divisions.
Molecular Phylogenetics and Evolution
19
486
494
56. ZhuLC
WangQ
TangP
ArakiH
TianDC
2009
Genomewide Association between Insertions/Deletions and the Nucleotide Diversity in Bacteria.
Molecular Biology and Evolution
26
2353
2361
57. TianDC
WangQ
ZhangPF
ArakiH
YangSH
2008
Single-nucleotide mutation rate increases close to insertions/deletions in eukaryotes.
Nature
455
105-U170
58. VolfovskyN
OleksykTK
CruzKC
TrueloveAL
StephensRM
2009
Genome and gene alterations by insertions and deletions in the evolution of human and chimpanzee chromosome 22.
BMC Genomics
10
51
59. ChenJQ
WuY
YangHW
BergelsonJ
KreitmanM
2009
Variation in the Ratio of Nucleotide Substitution and Indel Rates across Genomes in Mammals and Bacteria.
Molecular Biology and Evolution
26
1523
1531
60. Kehrer-SawatzkiH
CooperDN
2007
Understanding the recent evolution of the human genome: insights from human-chimpanzee genome comparisons.
Human Mutation
28
99
130
61. SchmitzJ
RoosC
ZischlerH
2005
Primate phylogeny: molecular evidence from retroposons.
Cytogenetic and Genome Research
108
26
37
62. TabuceR
MarivauxL
LebrunR
AdaciM
BensalahM
2009
Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence.
Proceedings of the Royal Society B-Biological Sciences
276
4087
4094
63. YoderAD
BurnsMM
ZehrS
DelefosseT
VeronG
2003
Single origin of Malagasy Carnivora from an African ancestor.
Nature
421
734
737
64. TeelingEC
ScallyM
KaoDJ
RomagnoliML
SpringerMS
2000
Molecular evidence regarding the origin of echolocation and flight in bats.
Nature
403
188
192
65. VentaPJ
BrouilletteJA
Yuzbasiyan-GurkanV
BrewerGJ
1996
Gene-specific universal mammalian sequence-tagged sites: application to the canine genome.
Biochemical Genetics
34
321
341
66. LyonsLA
LaughlinTF
CopelandNG
JenkinsNA
WomackJE
1997
Comparative anchor tagged sequences (CATS) for integrative mapping of mammalian genomes.
Nature Genetics
15
47
56
67. MoreiraMAM
2002
SRY evolution in Cebidae (Platyrrhini: Primates).
Journal of Molecular Evolution
55
92
103
68. FlynnJJ
NedbalMA
1998
Phylogeny of the Carnivora (Mammalia): Congruence vs incompatibility among multiple data sets.
Molecular Phylogenetics and Evolution
9
414
426
69. KatohK
TohH
2008
Recent developments in the MAFFT multiple sequence alignment program.
Brief Bioinform
9
286
298
70. KatohK
AsimenosG
TohH
2009
Multiple alignment of DNA sequences with MAFFT.
Methods in Molecular Biology
537
39
64
71. RambautA
2007
Se-Al. Sequence Alignment Editor.
Oxford
University of Oxford
72. TalaveraG
CastresanaJ
2007
Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.
Systematic Biology
56
564
577
73. PosadaD
CrandallKA
1998
MODELTEST: testing the model of DNA substitution.
Bioinformatics
14
817
818
74. SwoffordDL
2002
PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts
75. ZwicklDJ
2006
Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion.
Austin
The University of Texas
76. DrummondAJ
RambautA
2007
BEAST: Bayesian evolutionary analysis by sampling trees.
BMC Evolutionary Biology
7
214
77. DrummondAJ
HoSYW
PhillipsMJ
RambautA
2006
Relaxed phylogenetics and dating with confidence.
PLoS Biol
4
e88
doi:10.1371/journal.pbio.0040088
78. SeiffertER
SimonsEL
AttiaY
2003
Fossil evidence for an ancient divergence of lorises and galagos.
Nature
422
421
424
79. FranzenJL
GingerichPD
HabersetzerJ
HurumJH
von KoenigswaldW
2009
Complete primate skeleton from the Middle Eocene of Messel in Germany: morphology and paleobiology.
PLoS ONE
4
e5723
doi:10.1371/journal.pone.0005723
80. PouxC
DouzeryEJ
2004
Primate phylogeny, evolutionary rate variations, and divergence times: a contribution from the nuclear gene IRBP.
American Journal of Physical Anthropology
124
1
16
81. KayRF
FleagleJG
MitchellTRT
ColbertM
BownT
2008
The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina.
Journal of Human Evolution
54
323
382
82. SteiperME
YoungNM
SukarnaTY
2004
Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence.
Proceedings of the National Academy of Sciences of the United States of America
101
17021
17026
83. TosiAJ
DetwilerKM
DisotellTR
2005
X-chromosomal window into the evolutionary history of the guenons (Primates : Cercopithecini).
Molecular Phylogenetics and Evolution
36
58
66
84. VignaudP
DuringerP
MackayeHT
LikiusA
BlondelC
2002
Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad.
Nature
418
152
155
85. TavareS
MarshallCR
WillO
SoligoC
MartinRD
2002
Using the fossil record to estimate the age of the last common ancestor of extant primates.
Nature
416
726
729
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 3
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Whole-Exome Re-Sequencing in a Family Quartet Identifies Mutations As the Cause of a Novel Skeletal Dysplasia
- Origin-Dependent Inverted-Repeat Amplification: A Replication-Based Model for Generating Palindromic Amplicons
- FUS Transgenic Rats Develop the Phenotypes of Amyotrophic Lateral Sclerosis and Frontotemporal Lobar Degeneration
- Limited dCTP Availability Accounts for Mitochondrial DNA Depletion in Mitochondrial Neurogastrointestinal Encephalomyopathy (MNGIE)