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Evolutionary history of Coleoptera revealed by extensive sampling of genes and species

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Evolutionary history of Coleoptera revealed by extensive sampling of genes and species

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Beetles (Coleoptera) are the most diverse and species-rich group of insects, and a robust, time-calibrated phylogeny is fundamental to understanding macroevolutionary processes that underlie their diversity. Here we infer the phylogeny and divergence times of all major lineages of Coleoptera by analyzing 95 protein-coding genes in 373 beetle species, including ~67% of the currently recognized families. The subordinal relationships are strongly supported as Polyphaga (Adephaga (Archostemata, Myxophaga)). The series and superfamilies of Polyphaga are mostly monophyletic. The species-poor Nosodendridae is robustly recovered in a novel position sister to Staphyliniformia, Bostrichiformia, and Cucujiformia. Our divergence time analyses suggest that the crown group of extant beetles occurred ~297 million years ago (Mya) and that ~64% of families originated in the Cretaceous. Most of the herbivorous families experienced a significant increase in diversification rate during the Cretaceous, thus suggesting that the rise of angiosperms in the Cretaceous may have been an 'evolutionary impetus' driving the hyperdiversity of herbivorous beetles.
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ARTICLE
Evolutionary history of Coleoptera revealed by
extensive sampling of genes and species
Shao-Qian Zhang1, Li-Heng Che1, Yun Li1, Dan Liang1, Hong Pang1, Adam Ślipiński2& Peng Zhang1
Beetles (Coleoptera) are the most diverse and species-rich group of insects, and a robust,
time-calibrated phylogeny is fundamental to understanding macroevolutionary processes that
underlie their diversity. Here we infer the phylogeny and divergence times of all major
lineages of Coleoptera by analyzing 95 protein-coding genes in 373 beetle species, including
~67% of the currently recognized families. The subordinal relationships are strongly sup-
ported as Polyphaga (Adephaga (Archostemata, Myxophaga)). The series and superfamilies
of Polyphaga are mostly monophyletic. The species-poor Nosodendridae is robustly recov-
ered in a novel position sister to Staphyliniformia, Bostrichiformia, and Cucujiformia. Our
divergence time analyses suggest that the crown group of extant beetles occurred ~297
million years ago (Mya) and that ~64% of families originated in the Cretaceous. Most of the
herbivorous families experienced a signicant increase in diversication rate during the
Cretaceous, thus suggesting that the rise of angiosperms in the Cretaceous may have been
an evolutionary impetusdriving the hyperdiversity of herbivorous beetles.
DOI: 10.1038/s41467-017-02644-4 OPEN
1State Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-Sen University, Guangzhou, 510006, China.
2Australian National Insect Collection, CSIRO, GPO Box 1700, Canberra, ACT 2601, Australia. Correspondence and requests for materials should be
addressed to A.Ś. (email: Adam.Slipinski@csiro.au) or to P.Z. (email: alarzhang@gmail.com)
NATURE COMMUNICATIONS | (2018) 9:205 |DOI: 10.1038/s41467-017-02644-4 |www.nature.com/naturec ommunications 1
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Coleoptera, also known as beetles, are the most diverse and
species-rich insect group on Earth. With more than
380,000 described extant species1, beetles constitute ~25%
of all described animal species on this planet, and many species
remain to be described2. Beetles exhibit extraordinary morpho-
logical and ecological diversity and play important roles in nearly
all terrestrial and freshwater ecosystems3. To understand the
processes that have resulted in the extraordinary diversity of
beetles, a comprehensive time-calibrated phylogeny of extant
beetles is required. However, resolving the phylogeny of beetles
has proven to be a difcult challenge because of their exceptional
species richness, complicated morphological characteristics and
sparse molecular data. Therefore, deciphering the evolutionary
history of beetles is one of the most important and complicated
problems in insect biology.
Since the rst natural classication of beetles proposed by
Crowson4, many efforts have been made to rene the framework
based on morphological characters1,511. In recent years, many
researchers have attempted to resolve the beetle phylogeny on the
basis of molecular data1217. These studies have made great
progress; however, the resolution of the resulting phylogenies is
often poor, and many branches of the beetle tree-of-life remain
unresolved. For example, nine hypotheses regarding the rela-
tionships among four suborders of beetles (Fig. 1) have been
proposed in recent decades, but most of them did not receive
strong support11,16,1823. In addition, the relationships among the
series and superfamilies of Polyphaga have lacked consistently
strong nodal support, including the phylogenetic position of the
elusive Nosodendridae. These uncertainties have prevented the
development of a comprehensive time-calibrated phylogeny of
beetles, which is necessary to understand the macroevolutionary
processes that promoted the beetles extraordinary diversity.
Although early beetle fossils are rare, beetles are commonly
thought to have rst appeared in the Early Permian5,24. A recent
study has reported a fossil beetle from the Pennsylvanian (Car-
boniferous)25, thus suggesting an earlier origin of beetles,
although other researchers have suggested that the assessment of
this fossil should be re-evaluated26. On the other hand, molecular
studies have suggested that the age for crown Coleoptera ranged
from ~253 to 333 Mya (million years ago) and that the diver-
gences of most modern lineages occurred during the Late Triassic
to Cretaceous; however, the condence intervals of these age
estimates are large12,13,16,27.
It is well known that both taxon sampling and gene sampling
can affect the accuracy of phylogenetic reconstruction. In pre-
vious beetle phylogenetic studies, when the amount of sequence
was large (e.g., using ribosomal protein genes extracted from EST
data28, whole-mitochondrial genomes15,17, or transcriptome
data23,29), the taxon sampling was small, or when the taxon
sampling was large, the amount of sequence was small (e.g., three
genes: ~3000 nt12, four genes: 6600 nt14, and eight genes: 8377
nt16). Until recently, beetle molecular phylogenetics has mainly
relied on nuclear ribosomal DNA and mitochondrial gene
sequences. These data are either too conservative (lacking infor-
mation) or too heterogeneous in composition and evolutionary
rate (prone to systematic bias), and hence are insufcient for
resolving the higher level phylogeny of beetles. Compared with
nuclear ribosomal DNA and mitochondrial genes, nuclear
protein-coding (NPC) genes are more informative and less biased
in base composition, and they have been used to resolve many
problematic relationships in beetles16,30. However, because of the
deep evolutionary divergences in beetles and widely varying
evolutionary rates among taxa, NPC genes that can be amplied
across all beetles are still scarce (fewer than 10), thus resulting in
their relatively infrequent use in higher level beetle
phylogenetics16.
In this study, we dramatically increase the gene sampling by
including 95 recently developed31 nuclear protein-coding genes,
representing the largest source of data for beetle phylogenetics to
date. In addition, our broad taxon sampling includes 373 beetles
representing all recognized suborders, series, superfamilies and
124 of 186 families. Our results establish the phylogenetic rela-
tionships among major lineages and greatly improve robustness
throughout the entire phylogeny, especially in deep nodes. This
study provides a basis for a more accurate natural classication of
Coleoptera. Furthermore, we also estimate the divergence times
for the entire beetle phylogeny and study the tempo and pattern
of diversication of beetles. We nd that Coleoptera originated in
T1 T3T2
T4 T5
T7 T8
T6
T9
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Polyphaga
Myxophaga
Adephaga
Archostemata
Outgroups
Fig. 1 Nine proposed topologies among four suborders of Coleoptera. Topologies are derived from: T1, refs. 5,19; T2, ref. 11; T3, refs. 14,20; T4, ref. 12; T5, ref.
21; T6, ref. 22; T7, ref. 18; T8, refs. 17,23; T9 refs. 16,32
ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-017-02644-4
2NATURE COMMUNICATIONS | (2018) 9:205 |DOI: 10.1038/s41467-017-02644-4 |www.nature.com/naturecom munications
Content courtesy of Springer Nature, terms of use apply. Rights reserved
PP = 1.0 and BS 90
PP = 1.0 and 90 > BS 70
PP = 1.0 and BS < 70
1.0 > PP .095 and BS < 70
Trogossitidae Larinotus CSR058
Ptiliidae sp. CSR044
Chrysomelidae Dactylispa INB136
Brentidae Apion INB075
Nitidulidae Pallodes CSR122
Meloidae Epicauta INB093
Tenebrionidae Cryphaeus INB181
Monotomidae Monotomopsis CSR118
Pyrochroidae Morpholycus CSR130
Mycteridae Trichosalpingus CSR036
Brentidae Baryrhynchus INB044
Phloeostichidae Ropalobrachium CSR128
Rhipiphoridae Trigonodera CSR050
Tenebrionidae Ecnolagria CSR157
Murmidiidae Murmidius CSR078
Latridiidae Enicmus CSR028
Protocucujidae Ericmodes CSR129
Oedemeridae Pseudolycus CSR124
Tenebrionidae Tyrtaeus CSR156
Trogossitidae Rentonellum CSR059
Chrysomelidae Sominella INB138
Cerambycidae Strangalia INB066
Cryptophagidae Curelius INB192
Salpingidae Orphanotrophium CSR135
Brentidae Cylas INB199
Cucujidae Pediacus CSR087
Aderidae sp. INB206
Corylophidae Periptyctus CSR086
Tenebrionidae Adelium CSR149
Teredidae Teredolaemus CSR073
Cleridae Stenocallimerus INB190
Belidae Rhinotia CSR067
Chrysomelidae Altica INB141
Tenebrionidae Strongylium INB180
Ciidae Cis CSR080
Attelabidae Paratrachelophorus INB188
Chrysomelidae Anisodera INB137
Mycetophagidae Nototriphyllus CSR035
Cleridae Tenerus CSR083
Monotomidae Mimemodes CSR034
Coccinellidae Stethorus C54
Oedemeridae Ditylus INB033
Anamorphidae Papuella CSR095
Anthicidae Macratria CSR065
Chrysomelidae Cassida INB006
Euxestidae Hypodacnella CSR010
Anthicidae Trichananca CSR064
Coccinellidae Rhizobius C28
Boganiidae Paracucujus CSR006
Coccinellidae Ortalia C31
Erotylidae Episcapha INB023
Anthribidae Ozotomerus INB043
Erotylidae Episcaphula CSR101
Curculionidae Xylosandrus INB048
Coccinellidae Harmonia C10
Pythidae Anaplopus CSR131
Tenebrionidae Tanychilus CSR154
Bothrideridae Deretaphrus CSR072
Phalacridae sp. CSR040
Megalopodidae Temnaspis INB031
Curculionidae Dendroctonus
Attelabidae Byctiscus INB076
Phalacridae Olibrus INB122
Biphyllidae Althaesia CSR005
Ciidae Australocis CSR081
Erotylidae Cryptophilus CSR102
Nitidulidae Carpophilus INB196
Mycetophagidae Mycetophagus INB047
Curculionidae Episomus INB010
Zopheridae Bitoma CSR061
Cerylonidae Philothermus CSR011
Chrysomelidae Lilioceris INB135
Coccinellidae Sasajiscymnus C44
Silvanidae Uleiota CSR052
Zopheridae Monomma CSR060
Scraptiidae Scraptia INB205
Endomychidae Stenotarsus CSR098
Meloidae Zonitis CSR114
Silvanidae Psammoecus INB095
Cerambycidae Oberea INB067
Pyrochroidae Morpholycus CSR047
Tenebrionidae Cillibus CSR150
Cleridae Necrobia CSR084
Corylophidae Sericoderus CSR014
Anthicidae Anthicus CSR063
Salpingidae Orphanotrophium CSR051
Tenebrionidae Cteniopinus INB073
Bothrideridae Ascetoderes CSR074
Corylophidae Orthoperus INB209
Lymexylidae Atractocerus INB094
Silvanidae Psammoecus INB124
Nitidulidae Urophorus INB056
Silvanidae Silvanoprus CSR145
Passandridae Passandra CSR125
Anthicidae Lemodes CSR003
Melyridae Dasytes CSR115
Trogossitidae Parapeltis CSR159
Aderidae sp. CSR001
Chrysomelidae Chrysomela INB019
Endomychidae Holoparamecus CSR096
Acanthocnemidae Acanthocnemus CSR062
Rhipiphoridae Rhipidioides CSR133
Cleridae Allochotes INB191
Lymexylidae Melittomma CSR033
Melandryidae Melandryinae sp. INB203
Erotylidae Anadastus CSR100
Ciidae Cis CSR013
Endomychidae Cyclotoma CSR020
Cucujidae Platisus CSR016
Ischaliidae Ischalia INB049
Chrysomelidae Bruchidius INB144
Helotidae Neohelota INB004
Latridiidae Corticaria CSR029
Attelabidae Involvulus INB074
Cerambycidae Spondylis INB068
Monotomidae Rhizophagus CSR119
Teredidae Xylariophilus CSR071
Corylophidae Priamima CSR085
Tenebrionidae Cossyphus CSR153
Trogossitidae Leperina CSR160
Phalacridae Phalacrinus CSR126
Kateretidae Notobrachypterus CSR027
Alexiidae Sphaerosoma CSR002
Thanerocleridae Isoclerus CSR055
Brentidae Apion CSR075
Cryptophagidae Micrambina CSR015
Biphyllidae Biphyllus CSR068
Melandryidae Dircaeomorpha INB055
Coccinellidae Chnootriba C04
Tenebrionidae Chlorophila INB046
Discolomatidae Aphanocephalus CSR018
Prionoceridae Idgia INB040
Anthribidae Acorynus INB007
Salpingidae Euryplatus CSR134
Endomychidae Sinocymbachus INB005
Cleridae Cladiscus INB189
Erotylidae Thallis CSR099
Trictenotomidae Trictenotoma INB208
Cybocephalidae Cybocephalus CSR088
Chrysomelidae Trichochrysea INB139
Tenebrionidae Palorus CSR151
Tenebrionidae Platydema CSR155
Anthicidae Macratria INB050
Curculionidae Peribleptus INB185
Silvanidae Cryptamorpha CSR144
Coccinellidae Microfreudea C33
Zopheridae Zopherosis CSR163
Curculionidae Curculio INB184
Chrysomelidae Sagra INB134
Teredidae Xylariophilus CSR007
Chrysomelidae Oomorphoides INB142
Laemophloeidae Cryptolestes INB193
Cerambycidae Dorysthenes INB150
Melyridae Malachiinae sp. INB003
Mordellidae Hoshihananomia INB034
Endomychidae Encymon CSR097
Cerylonidae Ostomopsis CSR079
Sphindidae Aspidiphorus CSR053
Chrysomelidae Galerucinae sp. INB140
Tenebrionidae Tribolium
Propalticidae Propalticus CSR042
Nitidulidae Glischrochilus INB197
Archeocrypticidae Wattianus CSR066
Melyridae Carphurus CSR117
Monotomidae Thione INB207
Melyridae Dicranolaius CSR116
Curculionidae Platypodinae sp. INB045
Pyrochroidae Eupyrochroa INB027
Laemophloeidae Laemophloeus CSR110
Trogossitidae Thymalus INB024
Trogossitidae Ancyrona CSR158
Incertae sedis Rhizonium CSR105
Tenebrionidae Derispia INB072
Boridae Synercticus CSR069
Ulodidae Ulodes CSR161
Myraboliidae Myrabolia CSR037
Cleridae Xenorthrius INB012
Tenebrionidae Derispia CSR152
Tenebrionidae Cyphaleus CSR148
Latridiidae Melanophthalma CSR111
Salpingidae Ocholissa CSR136
Anthribidae Peribathys INB102
Nemonychidae Aragomacer CSR120
Oedemeridae Thelyphassa CSR123
Chrysomelidae Cryptocephalus INB143
Hobartiidae Hydnobioides CSR106
Coccinellidae Exochomus C25
Byturidae Haematoides INB039
Cerambycidae Xylotrechus INB069
Phloeostichidae Hymaea CSR127
Anthribidae Xylinada INB054
Ulodidae Meryx CSR162
Melyridae Carphurus INB131
Nitidulidae Brachypeplus CSR121
Pyrochroidae Pseudopyrochroa INB020
Attelabidae Phymatapoderus INB051
Chrysomelidae Chlamisus INB077
Tenebrionidae Amarygmus CSR147
Erotylidae Tetraphala INB029
Staphylinidae Staphylinus INB008
Elateridae Osslimus CSR092
Byrrhidae Notolioon CSR008
Scirtidae Pseudomicrocara CSR143
Nymphalidae Danaus
Dascillidae Metallidascillus INB200
Silphidae Nicrophorus INB022
Elateridae Ampedus INB161
Dermestidae Evorinea CSR090
Lampyridae Luciola INB061
Lampyridae Pristolycus INB060
Histeridae Saprinus CSR024
Psephenidae Sclerocyphon CSR043
Buprestidae Dicerca INB083
Byrrhidae Microchaetes CSR076
Scarabaeidae Rhyparus INB002
Ptilodactylidae Epilichas INB079
Callirhipidae Ennometes CSR009
Bombycidae Bombyx
Scarabaeidae Mimela INB145
Heteroceridae Heterocerus INB092
Carabidae Dischissus INB013
Hydrophilidae Anacaena INB105
Elmidae Graphelmis CSR093
Chrysopidae Dichochrysa IN54
Elateridae Hemicrepidius INB016
Noteridae Canthydrus INB115
Lycidae Libnetis YL0478
Elateridae Penia INB163
Lampyridae Pyrocoelia INB017
Geotrupidae Geotrupes INB097
Torridincolidae Satonius INB116
Hydraenidae Hydraena INB108
Apidae Apis
Rhagophthalmidae sp. INB128
Staphylinidae Scaphidium CSR054
Myrmeleontidae Myrmeleon IN53
Cupedidae Tenomerga INB118
Eulichadidae Eulichas INB025
Cantharidae Fissocantharis INB156
Bostrichidae Polycaon INB032
Psephenidae Mataeopsephus INB081
Dytiscidae Hyphydrus INB114
Haliplidae Peltodytes INB121
Eucinetidae Noteucinetus CSR021
Ptinidae Hedobia INB204
Ptilodactylidae Ptilodactyla INB015
Passalidae Aceraius INB096
Cantharidae Malthinus INB154
Elateridae Cardiotarsus INB210
Corydalidae Neochauliodes IN61
Dytiscidae Laccophilus INB111
Lycidae Dilophotes YL0454
Ptinidae Dorcatoma CSR046
Passalidae Ceracupes INB057
Staphylinidae Dianous INB175
Dryopidae Helichus CSR019
Histeridae Platysoma CSR023
Carabidae Omoglymmius INB120
Lampyridae Diaphanes INB158
Trogidae Omorgus CSR057
Derodontidae Derodontus CSR091
Cantharidae Lycocerus INB155
Scarabaeidae Anomala CSR141
Phengodidae Stenophrixothrix CSR041
Eucnemidae Otho INB035
Elateridae sp. INB164
Formicidae Atta
Limnichidae Byrrhinus CSR112
Staphylinidae Omaliinae sp. INB176
Scarabaeidae Allomyrina INB169
Staphylinidae Apatetica INB085
Artematopodidae Artematopus CSR004
Staphylinidae Scydmaeninae sp. CSR146
Trogidae Trox INB036
Scirtidae Elodes INB133
Lycidae Macrolycus YL0509
Hydrophilidae Berosus INB152
Bostrichidae Lyctus CSR070
Culicidae Anopheles
Buprestidae Trachys INB084
Hydrophilidae Helochares CSR108
Carabidae Lebia INB170
Jacobsoniidae Derolathrus CSR026
Staphylinidae Priochirus INB086
Throscidae Trixagus CSR056
Hydrophilidae Georissus INB106
Eucnemidae Anischia CSR022
Geotrupidae Australobolbus CSR137
Lycidae Lycostomus YL0616
Ascalaphidae Ascalohybris IN56
Scarabaeidae Onthophagus CSR142
Rhipiceridae Oligorhipis CSR049
Ptinidae Ptinus INB132
Dermestidae Dermestes CSR089
Lycidae Benibotarus YL0447
Dytiscidae Rhantus INB113
Carabidae Carabus INB100
Staphylinidae Megalopaederus INB030
Carabidae Pentagonica INB171
Scarabaeidae Protaetia INB104
Dryopidae Helichus INB194
Lucanidae Aegus INB148
Scirtidae Scirtinae sp. INB041
Scarabaeidae Copris INB146
Dytiscidae Agabus INB109
Elateridae Cebrio TH4
Lycidae Porrostoma CSR113
Dryopidae Pachyparnus INB166
Carabidae Elaphrus INB212
Hydrophilidae Sternolophus CSR107
Ptinidae Ptinus CSR045
Scarabaeidae Carneodon CSR139
Lampyridae Cyphonocerus INB062
Rhagophthalmidae Rhagophthalmus CSR132
Agyrtidae Pteroloma INB201
Leiodidae Agathidium CSR032
Nosodendridae Nosodendron CSR038
Artematopodidae Eurypogon INB202
Eucinetidae Noteucinetus CSR103
Elmidae Stetholus CSR094
Omethidae Drilonius INB127
Staphylinidae Tachinus INB088
Cantharidae Themus INB001
Staphylinidae Centrophthalmus INB091
Dermestidae Orphinus INB130
Cantharidae Ichthyurus INB065
Scarabaeidae Heteronyx CSR140
Limnichidae Cephalobyrrhus INB082
Elmidae Stenelmis INB038
Scarabaeidae Ectinohoplia INB147
Throscidae Trixagus INB125
Scarabaeidae Dasyvalgus INB149
Omethidae Drilonius INB129
Hydrophilidae Sphaeridium INB107
Cantharidae Themus INB063
Carabidae Pheropsophus INB168
Callirhipidae Simianus INB119
Psephenidae Schinostethus INB080
Jacobsoniidae Derolathrus CSR109
Silphidae Necrodes INB078
Elateridae Denticollis INB165
Cantharidae Prothemus INB064
Lycidae Platerodrilus YL0458
Carabidae Cicindela INB101
Buprestidae Coroebus INB018
Elateridae Melanotus INB211
Elateridae Denticollis INB162
Leiodidae Agyrtodes CSR030
Cantharidae Heteromastix CSR077
Lampyridae Vesta INB059
Carabidae Paussinae sp. TH2
Elateridae Agrypnus INB160
Eucnemidae Hemiopsida CSR104
Scarabaeidae Cheirotonus INB151
Byrrhidae Cytilus INB053
Dytiscidae Eretes INB112
Hydrophilidae Hydrophilus INB103
Hybosoridae Cyphopisthes CSR138
Staphylinidae Tachinus INB090
Clambidae Clambus CSR082
Staphylinidae Osorius INB087
Elateridae Pectocera INB159
Cantharidae Laemoglyptus INB153
Psephenidae Schinostethus INB052
Staphylinidae Scaphidium INB089
Glaphyridae Amphicoma INB011
Gyrinidae Orectochilus INB037
Lampyridae Drilaster INB157
Noteridae sp. CSR039
Drosophilidae Drosophila
Lucanidae Phalacrognathus INB098
Staphylinidae Staphylininae sp. INB174
Lampyridae Gorhamia TH3
Limnichidae Limnichus TH1
Hybosoridae Liparochrus CSR025
Dascillidae Dascillus INB028
Lucanidae Cyclommatus INB099
Carabidae Clivina INB167
Rhagophthalmidae Rhagophthalmus CSR048
Limnichidae Pelochares INB042
Hydrophilidae Oocyclus INB014
Leiodidae Cholevinae sp. CSR031
Chelonariidae Chelonarium CSR012
Cucujiformia
Cucujiformia
Adephaga
Dascilloidea
Buprestoidea
Byrrhoidea
Elateroidea
Hydrophiloidea
Scarabaeoidea
Bostrichoidea
Coccinelloidea
Curculionoidea
Chrysomeloidea
Cucujoidea
Cleroidea
Lymexyloidea
Tenebrinoidea
‘Scirtoidea’
‘Staphylinoidea’
Myxophaga
Archostemata
Outgroups
Polyphaga
‘Scirtoidea’
‘Derodontoidea’
‘Derodontoidea’
‘Derodontoidea’
‘Staphylinoidea’
Geadephaga
‘Hydradephaga’
Neuroptera
Megaloptera
Hymenoptera
Lepidoptera
Diptera
Coleoptera
Fig. 2 Cladogram of Coleoptera. The topology was inferred from the concatenated amino acid data set by ML (RAxML) and Bayesian inference (Exabayes).
Nodes with bootstrap values (BS) <70 and posterior probabilities (PP) <0.95 are not indicated by colored circles. Traditional taxonomic units that are not
monophyletic are indicated with quotation marks
NATURE COMMUNICATIONS | DOI: 10.1038/s41467-017-02644-4 ARTICLE
NATURE COMMUNICATIONS | (2018) 9:205 |DOI: 10.1038/s41467-017-02644-4 |www.nature.com/naturec ommunications 3
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the earliest Permian and that most extant lineages, especially
phytophagous beetles, diverged during the Cretaceous, thus
suggesting that the rise of angiosperms in the Cretaceous may
have played an important role in the hyperdiversication of
beetles. Our study provides a temporal perspective for under-
standing the evolutionary history of the Coleoptera and should
provide a cornerstone for the further study of systematics of this
extraordinarily diverse order.
Results
Higher level phylogenetic relationships of beetles. Our mole-
cular data included 95 nuclear protein-coding genes from 373
beetle species and 10 holometabolan outgroups (Supplementary
Data 1). The gene coverage for species ranged from 49.1 to 96.3%,
with an average of 78.6% (Supplementary Data 2). The con-
catenated supermatrix consisted of 23,802 amino acids (or 71,406
nucleotides). We estimated concatenated trees with both
nucleotide and deduced protein sequences by using two max-
imum likelihood (ML) methods (RAxML and IQ-TREE) and a
Bayesian approach (ExaBayes). The protein RAxML analysis
produced a well-resolved phylogeny (Supplementary Fig. 1).
Other ML and Bayesian analyses based on nucleotide or protein
sequences resulted in nearly identical phylogenies and similar
branch support, as shown in Fig. 2(Supplementary Figs. 26).
Gene tree-based coalescent analysis (ASTRAL) of our data
recovered a tree with lower nodal support that was also congruent
with the ML tree after collapsing of clades with <50% bootstrap
support (Supplementary Fig. 7). These congruent results indi-
cated that the resulting phylogeny was highly robust regardless of
the data set and tree-building method.
Our phylogenetic analyses achieved well-supported resolution
of relationships among all major lineages of beetles. In the ML
analyses, >85% of nodes were supported with standard bootstrap
values (RAxML) 70% or ultrafast bootstrap values (IQ-TREE)
95% (Supplementary Figs. 14). More than 95% of nodes have
posterior probabilities between 0.95 and 1 in the Bayesian
analyses (Supplementary Figs. 5and 6). For this discussion, we
use the protein RAxML tree as our preferred result (Fig. 2).
At the base of the Coleoptera tree, our phylogeny strongly
supported the relationships among suborders as Polyphaga
(Adephaga (Myxophaga, Archostemata)), a hypothesis recently
reported by McKenna et al.16 and Sharkey et al.32, albeit with
negligible to moderate support. The topology recovered in this
study with high support provided an opportunity to assess
relationships between suborders, which have been disputed for
decades. The approximately unbiased (AU) test analysis showed
that the three hypotheses with Polyphaga sister to the other three
suborders were signicantly better than the other hypotheses,
although these three hypotheses were not signicantly different
from one another (Table 1). It should be noted that our study
included only a single species of Archostemata and only one of
Myxophaga, which makes these taxa prone to long-branch
attraction (LBA). Therefore, the relationships among Adephaga,
Myxophaga, and Archostemata reported here should still be
considered as tentative and needed validation by future studies.
The Adephaga has been divided into two monophyletic groups
(the terrestrial Geadephaga and aquatic Hydradephaga) by many
molecular studies12,16,33; however, Hydradephaga is sometimes
recovered as paraphyletic14,17,34. In agreement with the latter, our
analyses recovered Hydradephaga as paraphyletic with the
aquatic Haliplidae and Gyrinidae forming a clade sister to all
other aquatic and terrestrial adephagans (Fig. 2). However, this
result had strong support only in the Bayesian analyses (BPP =
0.96; Supplementary Figs. 5and 6) and received negligible
support in the ML analyses (BS <50%; Supplementary Figs. 1and
2). Therefore, the phylogeny of Adephaga still remained
ambiguous. Given that our sampling of Hydradephaga was
insufcient, recovering internal relationships of Adephaga may
require sampling more aquatic adephagan families Amphizoidae,
Aspidytidae, Hygrobiidae, and Meruidae.
At the base of the strongly supported suborder Polyphaga, four
families occupied the basal nodes, forming two successive
branching clades sister to the remaining polyphagans (Fig. 2),
which is congruent with all recent studies12,14,16,28. In addition,
we corroborated the placement of Derodontidae as the sister
taxon to Clambidae + Eucinetidae with strong support (BS =98%,
BPP =1.0; Fig. 2), which had been only weakly supported
before16.
Series Elateriformia, which consists of the monophyletic
superfamilies Dascilloidea, Buprestoidea, Elateroidea, and
Byrrhoidea, was strongly recovered as the third branching lineage
of Polyphaga, and a similar result has only recently been
proposed from an analysis of beetle mitogenomes17.
Dascilloidea was strongly corroborated as the sister taxon to
the other superfamilies of Elateriformia (BS =100%; Fig. 2), in
agreement with recent studies14,16,35 but not with others12,17.
Buprestoidea was recovered as a sister to a clade of Byrrhoidea
and Elateroidea. However, the sisterhood between Byrrhoidea and
Elateroidea was only strongly supported in Bayesian analyses
(Supplementary Figs. 3and 4), similarly to the monophyly of
Byrrhoidea, in which moss-feeding Byrrhidae was only weakly
related to other byrrhoids (BS =40%; Supplementary Fig. 1).
Nosodendridae has previously been placed in various positions:
within Bostrichoidea7, within Derodontoidea11, associated with
Scirtoidea11,36, sister to Scarabaeiformia14, or grouped with
Elateriformia12,16. This family was robustly recovered in a novel
position in this study: as a sister clade to Staphyliniformia,
Bostrichiformia, and Cucujiformia (BS =100%; BPP =1.0; Fig. 2).
Table 1 Topology test for the nine proposed hypotheses among the four suborders of beetles
No. Topology Amino acid data Nucleotide data
Δln L AU test p-values Δln L AU test p-values
T9 (Polyphaga, (Adephaga, (Archostemata, Myxophaga))) 0 0.920 0 0.946
T8 (Polyphaga, (Myxophaga, (Adephaga, Archostemata))) 23.65 0.123 16.64 0.151
T7 (Polyphaga, (Archostemata, (Adephaga, Myxophaga))) 19.95 0.227 21.04 0.088
T1 (Archostemata, (Adephaga, (Myxophaga, Polyphaga))) 117.83 2e 05* 90.38 0.002*
T3 (Archostemata, (Myxophaga, (Adephaga, Polyphaga))) 109.62 0.001* 70.81 0.018*
T6 (Archostemata, (Polyphaga, (Myxophaga, Adephaga))) 59.96 0.036* 54.42 0.030*
T2 ((Archostemata, Adephaga), (Polyphaga, Myxophaga)) 118.50 4e 05* 93.51 1e 22*
T4 ((Archostemata, Myxophaga), (Adephaga, Polyphaga)) 92.38 5e 04* 64.45 0.007*
T5 ((Archostemata, Polyphaga), (Adephaga, Myxophaga)) 92.30 2e 05* 80.11 0.003*
*p-value <0.05 indicates statistical rejection
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CretaceousJurassicTriassicPermian CenozoicCarboniferous
300 250 200 150 100 50 0 (Mya)2575125175225275325
300 250 200 150 100 50 0 (Mya)2575125175225275325350
350
Archostemata
Polyphaga
“Core Polyphaga”
Cucujiformia
Phytophaga
Elateriformia
Mean divergence time and 95% CI (Mya)Mean divergence time and 95% CI (Mya)
Toussaint et al.27
McKenna et al.16
Hunt et al.12
Coleoptera
Adephaga
Polyphaga
Elateriformia
Bostrichiformia
Cucujiformia
This study
60
90
120
150
180
210
240
270
160
180
200
220
240
260
280
300
320
340
360
Dascilloidea
Elateroidea
Scarabaeoidea
Coccinelloidea
Curculionoidea
Cleroidea
Corylophidae
Dryopidae
Histeridae
Staphylinidae clade3
Byrrhidae
Attelabidae
Laemophloeidae
Incertae sedis Rhizonium
Trogossitidae clade2
Megalopodidae
Nosodendridae
Cupedidae
Anamorphidae
Scirtidae
Staphylinidae clade2
Limnichidae clade1
Elateridae Osslimus
Staphylinidae Centrophthalmus
Phloeostichidae
Sphindidae
Dascillidae
Throscidae
Omethidae
Teredidae
Acanthocnemidae
Trogossitidae clade1
Anthribidae
Rhipiceridae
Cerambycidae
Melandryidae Dircaeomorpha
Nemonychidae
Lycidae
Psephenidae
Geotrupidae
Limnichidae Cephalobyrrhus
Ptinidae
Endomychidae
Prionoceridae
Elateridae clade1
Ciidae
Rhagophthalmidae
Staphylinidae clade1
Byturidae
Propalticidae
Anthicidae Anthicus
Haliplidae
Salpingidae
Ischaliidae
Alexiidae
Monotomidae
Heteroceridae
Cleridae
Protocucujidae
Ripiphoridae Rhipidioides
Jacobsoniidae
Passandridae
Silphidae
Nitidulidae
Callirhipidae
Elateridae clade2
Myraboliidae
Eulichadidae
Elmidae
Boridae
Eucinetidae
Trogossitidae Leperina
Latridiidae
Derodontidae
Anthicidae Macratria
Pythidae
Coccinellidae
Hobartiidae
Trogossitidae Rentonellum
Chelonariidae
Cantharidae
Anthicidae clade1
Hybosoridae
Discolomatidae
Murmidiidae
Bostrichidae
Lampyridae
Ptiliidae
Ulodidae
Cryptophagidae
Zopheridae Zopherosis
Curculionidae
Phengodidae
Gyrinidae
Kateretidae
Melandryidae Melandryinae
Carabidae
Cybocephalidae
Phalacridae
Artematopodidae
Scarabaeidae
Lucanidae
Scraptiidae
Pyrochroidae
Eucnemidae
Silvanidae
Lymexylidae
Clambidae
Biphyllidae
Glaphyridae
Thanerocleridae
Trictenotomidae
Leiodidae
Ripiphoridae Trigonodera
Oedemeridae
Meloidae
Euxestidae
Noteridae
Bothrideridae
Brentidae
Passalidae
Boganiidae
Mycteridae
Trogidae
Hydraenidae
Belidae
Aderidae
Cerylonidae Philothermus
Mordellidae
Buprestidae
Helotidae
Dermestidae
Erotylidae
Mycetophagidae
Ptilodactylidae
Zopheridae clade1
Tenebrionidae
Torridincolidae
Chrysomelidae
Cucujidae
Agyrtidae
Staphylinidae Omaliinae
Hydrophilidae
Archeocrypticidae
Cerylonidae Ostomopsis
Dytiscidae
Melyridae
Tenebrionoidea
Lymexyloidea
Cleroidea
Cucujoidea
Curculionoidea
Chrysomeloidea
Coccinelloidea
Bostrichoidea
Staphylinoidea
Scarabaeoidea
Hydrophiloidea
Elateroidea
Byrroidea
Buprestoidea
Dascilloidea
Scirtoidea
+Derodontidae
Adephaga
Myxophaga
Nosodendridae
Jacobsoniidae
a
b
Fig. 3 New timescale for beetle evolution and comparison of divergence times. aTime-calibrated tree of beetles. The time tree was collapsed to family level
with outgroups removed (for detailed results, see Supplementary Fig. 8). Divergence times were estimated with MCMCTREE with 20 calibration points, on
the basis of the amino acid data set. Fossil constraints within Coleoptera are shown with black triangles. Horizontal bars represent 95% credibility intervals.
bComparison of divergence time estimates for twelve major nodes sharing across four beetle time trees. The circle represents the mean age, and the
whiskers mark the 95% credibility internals (Photo credits: Hong Pang, Yun Li, and Zhenhua Liu)
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In agreement with many previous studies1618,37,38, Hydro-
philoidea, Staphylinoidea (including Jacobsoniidae), and Scara-
baeoidea formed a well-supported clade (BS =94%; Fig. 2), thus
supporting a traditional monophyletic Haplogastra. Within this
clade, Staphylinoidea (including Jacobsoniidae) was closer to
Scarabaeoidea than to Hydrophiloidea with moderate support (BS
=78% and BPP =1.0; Supplementary Figs. 1and 5), inconsistent
with previous ndings that Staphyliniformia (Staphylinoidea +
Hydrophiloidea) was monophyletic or Hydrophiloidea was the
sister group of Scarabaeoidea8,16,37,39.Derolathrus (Jacobsoniidae),
which has previously been assigned to the superfamily Derodon-
toidea, was strongly recovered as sister to Hydraenidae + Ptiliidae
within Staphylinoidea (BS >90%; Fig. 2). The same or similar
placements were recovered on the basis of both morphological and
molecular data11,16, thus strongly suggesting that Derolathrus
(Jacobsoniidae) should be transferred to Staphylinoidea.
Bostrichiformia was strongly supported as the sister group of
the hyperdiverse series Cucujiformia in all of our analyses (BS =
100%; Fig. 2). Among the seven recognized superfamilies within
Cucujiformia, Coccinelloidea was sister to the remaining super-
families with moderate nodal support (BS =69%; Fig. 2). The
superfamily Cucujoidea (excluding Biphyllidae and Byturidae)
was a strongly supported clade (BS =93%; Fig. 2) and a sister
taxon to Phytophaga, which consists of the two highly supported
superfamilies Curculionoidea and Chrysomeloidea (Fig. 2). The
close relationships among Cucujoidea, Curculionoidea, and
Chrysomeloidea had maximal support in all analyses (BS =
100%; BPP =1.0; Fig. 2). Cleroidea was strongly recovered as
monophyletic (BS =100%; Fig. 2), when including Biphyllidae
and Byturidae, which were formerly placed in Cucujoidea but
recently transferred to Cleroidea12,40. The monophyly of
Lymexyloidea was moderately supported (BS =64%; Fig. 2), and
it was closely related to Tenebrionoidea with maximal support.
These two superfamilies jointly are sister to Cleroidea, with
moderate support (BS =72%; Fig. 2).
In summary, our beetle phylogeny corroborates many of the
deeper coleopteran nodes inferred by other studies but with
greater support. Relationships among the deepest branches in the
Polyphaga, for which previous studies have reported conicting
results, are now strongly supported. Our novel ndings include
the isolated position of Nosodendridae and a close relationship
between Scarabaeoidea and Staphylinoidea.
New timescale for beetle evolution. Before this study, only three
comprehensive family-level studies have been performed to esti-
mate divergence times for Coleoptera with newly generated
molecular data12,13,16. These three studies have suggested that the
last common ancestor of Coleoptera rst occurred in the Permian
period (253285 Mya). However, certain time estimates have
been criticized by Toussaint et al.27 because they conict with
current knowledge of the beetle fossil record. Using the data of
McKenna et al.16 but a different set of fossil calibration points,
Toussaint et al.27 have proposed a much older timescale for
Coleoptera for both deeper and shallower nodes. Their results
have indicated that the crown age of Coleoptera was ~333 Mya,
which is in the mid Carboniferous.
The extensive sampling of nuclear genes in our study provides
substantial new molecular data to estimate the divergence times
for extant beetles. Our divergence time analyses used a Bayesian
relaxed clock method (MCMCTREE) and 20 fossil calibration
points carefully selected from currently known Coleoptera fossils
(Supplementary Table 1). It should be pointed out that we used
some fossils to calibrate the crown groups of the superfamilies in
which they belong, even when the cited reference clearly places
the fossil in extant families. We have several considerations for
doing so: (1) poor fossil preservation of beetles often prevents
observation of the relevant characters, so it is possible to
erroneously place fossil taxa in extant families based on
incomplete morphological characters; (2) our taxon sampling
does not cover all beetle families and some families are
represented by only one species, the monophyly of some families
is not certain yet; (3) the monophyly of most superfamilies are
robust but the family-level relationships within each superfamily
is not robust. Therefore, it is more proper to use these fossils at
superfamily level but not family-level under the current situation
of both taxon sampling and phylogenetic robustness. We also ran
a time analysis using those fossils at family level to calibrate the
stem ages of relevant families. The resulting times were on
average 12% older than the times estimated by imposing fossils at
superfamily level. This result indicated that the divergence times
of beetle evolution are sensitive to the fossil calibration points, as
recently suggested by Toussaint et al.27. Because the use of fossils
in beetle divergence time analyses is still under debate16,27,we
tentatively used the divergence times estimated by imposing
fossils at superfamily level as our preferred time results. The full-
time tree for the 383 taxa sampled in this study is given in
Supplementary Fig. 8, and the family level time tree is
summarized in Fig. 3a. The 383-taxa time tree using fossils at
family level can be found in Supplementary Fig. 9.
Overall, our divergence times were notably more precise (i.e.,
smaller condence intervals) than those in the three previous
studies. The 95% condence intervals (CIs) for the 12 selected
nodes in the beetle tree (Fig. 3b) were ~50% narrower than
previous estimates. For example, the crown nodes of Coleoptera,
Adephaga, and Polyphaga in our study had 95% CIs ranging from
5.9 to 14.0 Mya, whereas McKenna et al.16 has reported CIs
ranging from 28.9 to 43.1 Mya (Supplementary Table 2). We
redid the time analyses using our 95 genes but the exact same age
constraints as used by McKenna et al.16 or Toussaint et al.27 and
still observed the increased precision of the dating results
(Supplementary Fig. 10). This result indicated that the greater
precision should be mainly attributed to the size of our data set
(71 kb), which exceeds those of previous studies (~8.4 kb at most)
by at least eightfold. A similar increase in precision of divergence
time estimations was also found for plethodontid salamanders by
using 95 nuclear genes41.
We estimated that the last common ancestor of extant beetles
occurred during the earliest Permian at 297 Mya (95% CI
291304), which is earlier than the Early Late Permian origin
(253285 Mya) estimated by Hunt et al.12 and McKenna et al.16
but later than that of Toussaint et al.27 (~333 Mya) (Fig. 3b). The
initial diversication of Polyphaga occurred at 280 (273287)
Mya, in the Early Permian, but the core Polyphaga(excluding
basal Scirtoidea and Derodontidae) occurred at 246 (240253)
Mya, which was shortly after the Permian-Triassic (PT) boundary
(Fig. 3a). Notably, the basal Polyphaga lineages are species-poor
(only ~1055 species), whereas the core Polyphagaincludes ~88%
of the described extant species of beetles (~340,000 species), and
the branch leading to core Polyphagawas long (24 million years
in duration) and spanned the PT boundary (Fig. 3a). These
results indicated that Polyphaga originated in the Permian and
survived through the End-Permian mass extinction.
In shallower nodes, such as the origin of many beetle
superfamilies, our time estimates are considerably younger than
those of Toussaint et al.27 and more consistent with the results of
the two earlier studies12,16 (Fig. 3b) and the results of other
researches focused on individual clades of beetles42,43. For
example, the crown age of Curculionoidea (weevils) estimated
in this study is 157 (156161) Mya, which is in the late Jurassic
period, in agreement with the Jurassic origin proposed by
Hunt et al.12 and McKenna et al.16,42. Toussaint et al.27 estimated
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Clade Rate ΔAICc
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
0.0645
0.0804
0.0810
0.0710
0.0203
0.0154
0.0678
0.0696
0.0785
0.0876
0.0165
0.0239
0.0657
0.0389
0.0642
Global rate 0.0484
54.24
27.78
28.83
30.98
23.05
21.09
17.96
8.79
11.84
8.57
8.3
7.02
6.28
8.36
5.44
0.015
0.04
0.064
0.088
Diversification rate
Torridincolidae(60)
Gyrinidae(882)
Haliplidae(218)
Carabidae(40350)
Noteridae(250)
Dytiscidae(4015)
Scirtidae(800)
Derodontidae(30)
Clambidae(170)
Eucinetidae(53)
Rhipiceridae(70)
Dascillidae(80)
Buprestidae(14700)
Byrrhidae(430)
Dryopidae(300)
Eulichadidae(30)
Ptilodactylidae(500)
Callirhipidae(150)
Chelonariidae(250)
Psephenidae(290)
LimnichidaeHeteroceridae(690)
Elmidae(1500)
Omethidae(33)
Artematopodidae(45)
Throscidae(150)
Eucnemidae(1500)
Cantharidae(5100)
Lissominae(150)
Lycidae(4600)
Elateridae1(4925)
Elateridae2(4925)
Lampyridae(2200)
Phengodidae(250)
Rhagophthalmidae(30)
Nosodendridae(50)
Histeridae(4300)
Hydrophilidae(3400)
Jacobsoniidae(20)
Ptiliidae(650)
Hydraenidae(1600)
StaphylinidaeSilphidae(56200)
Agyrtidae(70)
Leiodidae(3700)
Trogidae(300)
Lucanidae(1489)
Geotrupidae(920)
Passalidae(800)
Glaphyridae(204)
Hybosoridae(573)
Scarabaeidae(27000)
Dermestidae(1200)
Bostrichidae(570)
Ptinidae(2200)
Alexiidae(50)
Latridiidae(1000)
Anamorphidae(174)
Corylophidae(200)
Endomychidae(1606)
Coccinellidae(6000)
Chrysomelidae(32500)
Megalopodidae(350)
Cerambycidae(30079)
Nemonychidae(70)
Anthribidae(3900)
Belidae(375)
Attelabidae(2500)
Brentidae(4000)
Curculionidae(51000)
Boganiidae(11)
Erotylidae(3500)
Helotidae(107)
Sphindidae(59)
Protocucujidae(7)
Monotomidae(250)
Nitidulidae(4350)
Cybocephalidae(150)
Kateretidae(95)
Hobartiidae(6)
Cryptophagidae(600)
Silvanidae(500)
Cucujidae(44)
Phloeostichidae(14)
Myraboliidae(13)
Passandridae(109)
Phalacridae(640)
Propalticidae(30)
Laemophloeidae(430)
Rentoniinae(15)
Byturidae(24)
Biphyllidae(200)
Trogossitidae2Acanthocnemidae(301)
Thanerocleridae(30)
Cleridae(3400)
Trogossitidae1(300)
Prionoceridae(160)
Melyridae(6000)
Lymexylidae(70)
RipiphoridaeMordellidae(1900)
Zopheridae2(850)
Melandryidae2(210)
Ciidae(650)
Zopheridae1(850)
Melandryidae1(210)
Incertae sedis Rhizonium(1)
Mycetophagidae(130)
Archeocrypticidae(60)
Ulodidae(30)
Ischaliidae(34)
Aderidae(900)
Mycteridae(160)
Oedemeridae(500)
Trictenotomidae(13)
AnthicidaeMeloidae(6000)
Pyrochroidae(167)
Scraptiidae(500)
Pythidae(23)
Salpingidae(300)
BothrideridSeries(1250)
Cupedidae(31)
Boridae(4)
Tenebrionidae(20000)
60,00050,00040,00030,00020,00010,000
Number of species
7
10
15
5
8
6
3
1
9
11
12
4
13
14
2
CretaceousJurassicTriassicPermian Cenozoic
300 250 200 150 100 50 0 (mya)2575125175225275
300 250 200 150 100 50 0 (Mya)2575125175225275
Fig. 4 Diversication patterns of major beetle lineages inferred from MEDUSA analysis. Each terminal represents a monophyletic family-level taxon. The
number in parenthesis next to the taxon name indicates the number of validly described species within the taxon. The species richness of each taxon is also
indicated with histograms on the right. Branches are color coded to show the diversication rates. Clades with signicant diversication rate shifts
compared with the background rate are marked with circled numbers on the tree (red: rate increase; blue: rate decrease). Estimated net diversication
rates and differences in AICc scores are included in the lower left table
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this node to be 226.9 Mya (Late Triassic). In terms of the fossil
record, weevils rst appear unequivocally in the Late Jurassic
(Karatau, OxfordianKimmeridgian, 163.5152.1 Mya), which is
close to our time estimate.
In summary, our new timescale for beetle evolution suggests
that the crown Coleoptera originated in the earliest Permian. The
divergence among beetle series mainly occurred during the
Triassic, with most superfamilies appearing during the Jurassic,
and almost 64% of families appearing in the Cretaceous (stem
ages are used here because some families have only one species
sampled in this study). Even when we use the alternative
calibration scheme (using fossils at family level), there are still
46% of families that originated during the Cretaceous (Supple-
mentary Fig. 9). These age estimates corroborate many of the
dating results estimated by earlier studies, but with higher
precision (having smaller CIs).
Diversication tempo of beetles and its relationship with the
rise of angiosperms. What factors cause the extraordinary species
richness of beetles are still widely discussed. From a perspective of
morphology, the sclerotized forewings (elytra), which protect the
membranous ying hindwings, may be responsible for the
apparent success of beetles3. Moreover, other studies have also
emphasized the importance of complete metamorphosis, devel-
opment cycle and division of ecological niches to larvae and
adults as innovations of the extraordinary diversity of Holome-
tabola, including Coleoptera44,45. Another popular hypothesis
suggests that the striking diversity of beetles is largely driven by
co-radiations with owering plants42,46. However, Hunt et al.12
have argued that there is no apparent association between the
diversity of beetles and the diversication of angiosperms and
that the extreme diversity of beetles may be explained by their
long evolutionary history, high-lineage survival, and diversica-
tion in a wide range of niches.
On the basis of the new timescale of beetles, we calculated the
diversication pattern of beetles with both MEDUSA47 and
BAMM48. Both methods produced similar results of beetle
diversication. We estimated the global diversication rate for
Coleoptera to be 0.0484 lineages per million years (Myr)
(MEDUSA) or 0.0510 lineages per million years (BAMM) (Fig. 4,
Supplementary Fig. 11). The global diversication rate for
Coleoptera drops to ~0.045 lineages/Myr based on our alternative
time estimate (using fossils at family level). These rates are
apparently low compared with those of other organism groups
that experienced rapid radiation, such as neoavian birds (0.089
lineages/Myr)47 and angiosperms (0.077 lineages/Myr)49. Because
beetles originated in the lowermost Permian and have an
apparently low-diversication rate, we agree with Hunt et al.12
that the high-species richness of beetles as a whole should be
attributed to their long history and low-lineage extinction.
However, the MEDUSA analysis identied ten clades within
Coleoptera with signicantly higher diversication rates
(0.06420.0876 lineages/Myr) than the background diversication
rate, and they all belong to the suborder Polyphaga (Fig. 4). The
BAMM analysis also identied four rate-increase shifts that are
included within the MEDUSA results (Supplementary Fig. 11).
These clades include most species-rich groups of beetles, such as
Phytophaga, Scarabaeidae, Elateridae, and Tenebrionidae, which
constitute ~56.3% of extant species of beetles, thus indicating that
0
60,000
0
Described extant species
0 (Mya)20406080100120140160180200220240260280300
CretaceousJurassicTriassicPermian Cenozoic
0 (Mya)20406080100120140160180200220240260280300
CretaceousJurassicTriassicPermian Cenozoic
Net diversification rate
Staphylinidae
Carabidae
Curculionidae
Chrysomelidae
Cerambycidae
Scarabaeidae
Tenebrionidae
Buprestidae*
Herbivorous &
xylophagous
Predacious
Fungivorous &
saprophagous
Elateridae
Rate accelerating event
Rate slowdown event
ab
cd
Divergence events
0
10
20
30
40
50
60
0 (Mya)20406080100120140160180200220240260280300
CretaceousJurassicTriassicPermian Cenozoic
Family-level divergence events
0
10
20
30
40
0 (Mya)20406080100120140160180200220240260280300
CretaceousJurassicTriassicPermian Cenozoic
0.1
0.09
0.08
0.07
0.06
0.05
0.04
0.03
0.02
0.01 5000
10,000
15,000
20,000
25,000
30,000
35,000
40,000
45,000
50,000
55,000
Fig. 5 Diversication of beetles across the geological timescale. aTiming of the 15 signicant changes in net diversication rate identied by MEDUSA. The
dashed line denotes the background net diversication rate of Coleoptera. bOrigin times and the species richness of beetle families. We used stem age as
the origin time for a family when only one species is sampled for the family or when the taxon sampling did not cover the crown of the family. For non-
monophyletic families, the stem age of the oldest lineage of the family was used. The nine largest families with species numbers >10,000 are highlighted
with family names and feeding habits. For the Buprestidae (marked with an asterisk), we performed an additional time estimation, adding the
Schizopodidae sequences from McKenna et al.16 to calculate the stem age of this family. cNumber of divergence events within every 20 million year
interval calculated from the 383-taxon time tree. Note that the diversication rate of beetles experienced an upsurge beginning from the late Jurassic
(marked with a red line). dNumber of divergence events within every 20 million year interval calculated from the family-level time tree. A similar
diversication upsurge pattern was also detected in the late Jurassic
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more than half of beetle diversity can be attributed to fast
diversication rates in certain clades. In addition, both BAMM and
MEDUSA analyses detected two or ve clades with signicantly
lower diversication rates than the background rate (Fig. 4;
Supplementary Fig. 11), and they mainly belong to the species-
poor beetle groups. Moreover, 9 of 10 rate-accelerating events
detected by MEDUSA occurred in the Cretaceous, although all ve
rate slowdown events occurred much earlier (Fig. 5a). A similar
pattern was observed when we used the alternative timescale of
beetles: seven identical rate-increasing events were detected and ve
of them occurred in the Cretaceous, while all rates slowdown shifts
predated the Cretaceous (Supplementary Fig. 12). These results
suggested that the Cretaceous was an important period in shaping
the extreme diversity of beetles.
Flowering plants (angiosperms) diversied quickly during the
Cretaceous period and became the dominant group of plants50,51.
Interestingly, among the nine largest beetle families, which have
>10,000 described species, seven were estimated to originate in
the Cretaceous, and their diets are associated with plants (Fig. 5b).
Curculionidae, Chrysomelidae, Cerambycidae, and Buprestidae
are phytophagous, and more than three-quarters of species in
Scarabaeidae are phytophagous, whereas certain species in
Tenebrionidae and Elateridae are phytophagous, and many
others feed on decomposing plant materials and woody tissues.
In contrast, the other two species-rich families (Staphylinidae and
Carabidae) that are predominantly predacious were estimated to
originate in the Early Jurassic, long before the Cretaceous
(Fig. 5b). The coordination of diversication between angios-
perms and phytophagous beetles, but not with predacious beetles,
clearly shows that the extraordinary diversity of phytophagous
beetles can be attributed to co-evolution with angiosperms.
To show the diversication tempo of beetles through time, we
counted the number of divergence events of Coleoptera within
every interval of 20 million years from the Permian to the present,
on the basis of our 383-species time tree. We noticed that the
diversication rate of beetles experienced an upsurge in the late
Jurassic (~160 Mya) and reached the greatest speed in the
Cretaceous (Fig. 5c). This rate-elevating pattern remained stable
when we counted divergence events on the family-level time tree
(Fig. 5d). Although the oldest angiosperm fossils date from the
Valanginian to the Hauterivian in the Cretaceous52,53, the crown
age of the angiosperms has been estimated to be at least 160
Mya54,55. Therefore, the diversication rate pattern of beetles is
still consistent with the beetle-angiosperm co-evolution hypoth-
esis46. However, the accelerating diversication of beetles in the
late Jurassic also indicates that the rapid radiation of beetles
began before owering plants ourished.
Overall, no single explanation can explain the success of the
order Coleoptera. Perhaps, the Permian origin of the crown group
and a long period of evolution steadily increased the diversity of
beetles. Because lineage survival was high, beetle diversication
entered an exponentialphase in the late Jurassic. The subsequent
boom of owering plants in the Cretaceous provided new
ecological opportunities for phytophagous beetles, thus further
promoting the biodiversity of beetles. All these factors together
create the great diversity of extant beetles.
Methods
Taxon sampling. In this study, we used a Coleoptera classication that incorpo-
rated results from Ślipiński et al.1and Bouchard et al.10 with the exception of
Rhysodidae, which is considered to be a subfamily of Carabidae11, and added the
recently proposed superfamilies Coccinelloidea and eight recently elevated (or re-
elevated) families40,56. We sampled 371 coleopteran taxa representing the 4 extant
suborders, 7 series, 17 superfamilies and 124 of 186 families. Four neuropterid taxa,
including 3 families of Neuroptera and 1 family of Megaloptera, were used as
outgroups. Most of the missing families were species-poor lineages with limited
distribution. Additionally, we added 8 taxa with public genome data downloaded
from the Ensembl database (http://www.ensembl.org), including two beetles (Tri-
bolium castaneum and Dendronctonus ponderosae) and 6 other holometabolan
insects. Therefore, our nal taxon sampling included 383 species (373 beetles and
10 outgroups). We did not include Strepsiptera as an outgroup to beetles, because
among the 95 genes used in this study, only 44 (missing data >50%) could nd
orthologous sequences in the published Strepsiptera genome57. All specimens
derived from the Biological Museum of Sun Yet-Sen University, China and Aus-
tralian National Insect Collection, CSIRO, in Canberra, Australia were marked with
unique numbers. The detailed information of taxonomy, locality, collector/iden-
tier of specimens was provided in Supplementary Data 1.
DNA sequencing. Specimens were preserved in 95% ethanol and stored at 20°C.
DNA was extracted from the thorax muscles, legs or the entire specimen using a
TIANamp Genomic DNA kit (TIANGEN Inc., Beijing, China). Voucher specimens
have been deposited in the Biological Museum of Sun Yat-Sen University. Ninety-ve
nuclear protein-coding genes were amplied from DNA extracts by PCR using the
protocol and primers described in Che et al.31. The amplication products were
sequenced using a next-generation sequencing (NGS) strategy, as described by Feng
et al.58.Briey, all amplication products from a single specimen were pooled toge-
ther and puried. The specimen amplication product pools were then randomly
sheared to small fragments (200500bp), the ends were repaired, and a species-
specic barcode linker was added. All indexed amplication product pools were then
mixed together, and a sequencing library was constructed with the pooled DNA using
the TruSeq DNA Sample Preparation kit and sequenced on an Illumina HiSeq
2500 sequencer. Approximately 24 GB of 90-bp Illumina HiSeq paired-end reads were
obtained. These reads were bioinformatically sorted by barcode sequences and
assembled into consensus sequences using Trinity59. All assembled sequences were
checked for possible intron insertion by using a Python script provided by Che
et al.31.Thenal intron-removed sequences were further examined for frame shifts
and stop codons to ensure that they could be properly translated. GenBank accession
numbers for the new sequences are given in Supplementary Data 3.
Sequence alignment and data partition. All 95 genes were aligned using the
ClustalW algorithm implemented in MEGA v660 on the basis of the translated
amino acid sequences. Ambiguously aligned regions were trimmed using Gblock
v.0.91b61, with all gaps allowed (-b5 =a) and all other parameters at default set-
tings. Nucleotide alignments were performed according to the corresponding
protein alignments using a custom Python script. All 95 protein and nucleotide
alignments were concatenated. Binning genes into supergenesis a statistical
technique that can account for sampling error by increasing signal-to-noise ratio,
and it has been applied in phylogenetics recently6264. Because many genes in our
data set are short, we thus used data binning strategy to partition our data. The
protein data set was divided into 10 partitions according to the evolutionary rate of
each gene (measured as their overall mean P distances). ProtTest 365 was used to
identify the best-t models for the 10 partitions with the Bayesian information
criterion (BIC). We also did additional phylogenetic analyses using different par-
titioning schemes. The phylogenies inferred from unpartitioned and 95-gene-
partitioned data set are almost identical to that inferred from 10-bin-partitioned
data set, except several nodes with negligible supports (Supplementary Fig. 13).
This result showed that different partitioning schemes have little inuence to the
nal phylogenetic results. For the nucleotide data set, we used a Perl script
(Degen_v1_4.pl; http://www.phylotools.com) to degenerate nucleotides to IUPAC
ambiguity codes for the rst and third codon positions, an extension of RY coding,
which can reduce the effect of nucleotide compositional heterogeneity66. The
degenerated nucleotide data set makes synonymous changes largely invisible but
non-synonymous changes largely intact, which can be supported in RAxML and
IQ-TREE analyses. The resulting nucleotide data matrix was partitioned by codons
(three partitions dened), and the best-t models for every codon partition was
selected with PartitionFinder67.
Phylogenetic analyses. The protein and nucleotide data sets were analyzed with
both ML and Bayesian inference (BI) methods. The ML analyses were conducted
using RAxML v.8.068 and IQ-TREE69. Branch support in the RAxML analyses were
evaluated through a rapid bootstrap algorithm (-f a option) with 500 replicates. In
the IQ-TREE ML analyses, nodal support values were estimated using the
embedded ultrafast bootstrap approach (UFBoot), which is computational efcient
and relatively unbiased70.
Bayesian analyses were conducted using ExaBayes v1.4.171. Two Markov Chain
Monte Carlo (MCMC) runs were performed with one cold chain and three heated
chains (temperature set to 0.1) for 50 million generations, and sampling was
performed every 1000 generations. The average standard deviation of split
frequencies (ASDSFs) and potential scale reduction factor (PSRF) were <1% and
close to 1 across the two runs, respectively. The effective sample sizes (ESSs) were
>200 for all parameters after the rst 20% of generations were discarded.
The species tree analysis without gene concatenation was performed for the
protein data set using ASTRAL 4.7.672 under the coalescent model. For each gene,
the best ML tree and 200 bootstrapping trees were inferred by RAxML under the
best tting model selected by ProtTest. The species tree analysis was then
conducted using ASTRAL taking these 95 unrooted best ML trees and
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corresponding bootstrapping trees as input, under the multilocus bootstrapping
option with 200 replicates (-r=200).
The approximately unbiased (AU)73 test was used to evaluate the alternative
beetle phylogeny hypotheses, and site-wise log likelihoods of all alternative
topologies were calculated with RAxML using the -f g option. Then, the site log-
likelihood le was used as input to estimate the P-values for each alternative
hypothesis using the AU test implemented in the program CONSEL74.
Divergence time estimation. Divergence times were estimated by using
MCMCTREE in the PAML package75 with the uncorrelated rate model (clock =2).
The protein RAxML tree was used as the reference topology. Twenty fossils
(Supplementary Table 1), of which 13 were within the Coleoptera, were used to
calibrate the clock. Imposing maximum bounds is necessary when estimating deep
divergence times76. Because holometabolous insects are not known from before the
Pennsylvanian of the Carboniferous, we constrained the maximum age of the
Coleoptera-Neuropterida split to 323.2 Mya, the Mississippian-Pennsylvanian
boundary, which is a fairly conservative maximum bound for this node. To further
limit the effect of imposing an erroneous maximum constraint, we specied the tail
probability of this maximum bound as 2.5%; thus, the time estimation had a 2.5%
probability of being greater than the bound.
The ML estimates of the branch lengths for each of the 10 protein partitions
were calculated using CODEML (in PAML) under the WAG + F + Γmodel. To
specify the prior on the overall substitution rate, the root age (crown
Holometabola) was set to 345 Mya, according to a recent phylogenomic estimate23.
On the basis of the mean tree depth from the 10 protein partitions, the gamma-
Dirichlet prior for the overall substitution rate (rgene gamma) was set at G (1,
8.36), and the gamma-Dirichlet prior for the rate-drift parameter (sigma2 gamma)
was set at G (1, 4.5). The posterior time estimates were conducted by using a
MCMC algorithm. After the rst 100,000 iterations were discarded as burn-in, the
MCMC run was sampled every 100 iterations until it achieved 10,000 samples. Two
MCMC runs using different random seeds were compared to determine their
convergence with similar results, and effective sample sizes of every node age and
every parameter were >200, as determined in Tracer V1.477 software.
Diversication rate analyses. We used MEDUSA(Modeling Evolutionary
Diversication Using Stepwise AIC)47 and BAMM (Bayesian Analysis of Macro-
evolutionary Mixture)48 to investigate the tempo of diversication of the Coleop-
tera. MEDUSA was conducted on the ultrametric phylogenetic tree with the species
richness data. The time-calibrated Coleoptera tree generated by MCMCTREE was
pruned to a family-level chronogram so that each terminal reected a mono-
phyletic family (or possible equal). In some cases, families that were not mono-
phyletic were grouped together or split apart. The approximate numbers of
described species for terminals were obtained from Ślipiński et al.1. MEDUSA
sequentially adds rate shifts to the family-level chronogram until further additions
fail to have a distinct increase in model t (i.e., the improvement in AIC score is
lower than the threshold). The MEDUSA analysis was conducted in R using the
packages Geiger78 with the default settings, including the corrected AIC (AICc)
criterion and mixed model.
We also detected diversication rate shifts using BAMM v. 2.5. The 383-taxa
time-calibrated tree was used as input tree. To account for incomplete taxa
sampling, we used a non-random incomplete taxon sampling correction and
specied this sampling fractions by families. The family-specic sampling
probabilities were specied according to described species diversity obtained from
Ślipiński et al.1. The BAMM analysis was run for 60 million generations at a
temperature increment parameter of 0.01 and sampled event data every 1000
generations. We discarded the rst 10% generations as burn-in and examined the
effective sample size (ESS >200) of the log-likelihood and the number of shift events
for convergence with the CODA package79 in R. Finally, the best shift conguration
and the net diversication rates of clades were inferred with BAMMtools80.
Data availability. The raw sequences of the 95 genes, nucleotide and amino acid
alignments of 95 genes, phylogenetic trees, and time trees are available in gshare
(10.6084/m9.gshare.5306497). All new gene sequences have been deposited in
GenBank (for accession numbers, Supplementary Data 3). The raw Illumina
sequencing data generated in this paper can be downloaded from the NCBI
Sequence Read Archive under the BioProject Accession Number PRJNA419242.
Received: 5 May 2017 Accepted: 15 December 2017
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Acknowledgements
We thank all of our lab members for help in experiments and data analyses. We thank
Zhenhua Liu for kindly providing valuable beetle images. This work was supported by
the National Natural Science Foundation of China (grants No. 31672266 and 31372172
to P. Zhang) and the National Youth Talent Support Program (W02070133 to P. Zhang).
Author contributions
P.Z., D.L., and A.S. designed the project. Y.L., H.P., and A.S. carried out taxon sampling
and collection. S.-Q.Z. performed the DNA sequencing with the help of L.-H.C. and Y.L.
S.-Q.Z. and P.Z. analyzed the data. S.-Q.Z. and P.Z. wrote the paper.
Additional information
Supplementary Information accompanies this paper at https://doi.org/10.1038/s41467-
017-02644-4.
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... Up to date, the oldest beetle fossil was reported from the Permian (Kirejtshuk et al., 2014;Beutel et al., 2019a). Although many efforts have been made to explain this spectacular evolutionary radiation (Farrell, 1998;Hunt et al., 2007;Salem et al., 2020;Motyka et al., 2021), only a few attempts have been made to study the phylogeny of the entire Coleoptera (McKenna et al., 2015;Zhang et al., 2018;Beutel et al., 2019b;Cai et al., 2022). ...
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... Coleoptera comprises ~ 25% of all animal species identified with more than 380,000 currently identified species (Zhang et al. 2018). In Turkey, the number of species and subspecies of the Coleoptera is 11,910 and its percentage is 35.22% ...
... In three of the studies, Lymexylidae appeared to be nested within basal Tenebrionoidea, with various positions [12][13][14], although only a few gene fragments were sampled in these studies. Other studies, including three recent phylogenomic ones, suggested Lymexylidae as the sister group of (the remaining) Tenebrionoidea [15][16][17][18][19]. Wheeler [20] concluded that the maxillary palporgan is the strongest autapomorphy for this family, and considered its loss in Australymexylon Wheeler as secondary. ...
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... Beetles (Insecta: Coleoptera) are dominant worldwide, constituting nearly a quarter of all known fauna [1]. They form great biodiversity in different habitats and play significant roles in the functioning of the ecosystem [2]. They occur in all major habitats, except for the Polar and marine habitats, and are economically important as agricultural and household pests or predators [3]. ...
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