Molecular Phylogenetics and Evolution 130 (2019) 346–356

Contents lists available at ScienceDirect

Molecular Phylogenetics and Evolution
journal homepage: www.elsevier.com/locate/ympev

Near-complete phylogeny and taxonomic revision of the world’s babblers(Aves: Passeriformes)

T

Tianlong Caia,b,c, Alice Ciboisd, Per Alströma,e,f, Robert G. Moyleg, Jonathan D. Kennedyc,
Shimiao Shaoh, Ruiying Zhangb,i, Martin Irestedtj, Per G.P. Ericsonj, Magnus Gelangk,⁎
Yanhua Qua,b, Fumin Leia,b, , Jon Fjeldsåc
a

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
College of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, ChinacCenter for Macroecology, Evolution and Climate, Natural History Museum of Denmark, Zoological Museum, Universitetsparken 15, DK-2100 Copenhagen, DenmarkdNatural History Museum of Geneva, CP 6434, CH 1211 Geneva 6, SwitzerlandeDepartment of Ecology and Genetics, Animal Ecology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, 752 36 Uppsala, Swedenf
Swedish Species Information Centre, Swedish University of Agricultural Sciences, Box 7007, Uppsala SE-750 07, Swedeng
Department of Ecology and Evolutionary Biology and Biodiversity Institute, University of Kansas, Lawrence, KS 66045, USAhState Forestry Administration Key Laboratory of Biodiversity Conservation in Southwest China, Southwest Forestry University, Kunming 650224, ChinaiCenter for Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, Chinaj
Department of Bioinformatics and Genetics, Swedish Museum of Natural History, PO Box 50007, Stockholm SE-10405, SwedenkGothenburg Natural History Museum, Box 7283, 402 35 Göteborg, Swedenb

ARTICLE INFOABSTRACT

Keywords:
Babblers
Passeriformes
Phylogeny
Supertree
Taxonomy
Rogue taxa
Temporal banding

The babblers are a diverse group of passerine birds comprising 452 species. The group was long regarded as a“scrap basket” in taxonomic classification schemes. Although several studies have assessed the phylogenetic
relationships for subsets of babblers during the past two decades, a comprehensive phylogeny of this group has
been lacking. In this study, we used five mitochondrial and seven nuclear loci to generate a dated phylogeny forbabblers. This phylogeny includes 402 species (ca. 89% of the overall clade) from 75 genera (97%) and all fivecurrently recognized families, providing a robust basis for taxonomic revision. Our phylogeny supports sevenmajor clades and reveals several non-monophyletic genera. Divergence time estimates indicate that the sevenmajor clades diverged around the same time (18–20 million years ago, Ma) in the early Miocene. We use thephylogeny in a consistent way to propose a new taxonomy, with seven families and 64 genera of babblers, and a
new linear sequence of names.

1. Introduction
The babblers are a diverse group of oscine passerine birds, which
includes more than 450 species in five families (Gill and Donsker,
2018). Species in the group are mainly distributed in Southeast Asiaand the Afrotropics, with a few species occurring in the Palearctic, andonly one species (Wrentit Chamaea fasciata) having colonized the New
World (del Hoyo et al., 2007; Gill and Donsker, 2018). Most babblers
are resident, but some of the northern breeders are long-distance migrants. The group inhabits a wide diversity of habitats, including tropical, subtropical and temperate forests, woodlands, thickets, marshlands and arid habitats, with species occurring from sea level to above
the tree limit (del Hoyo et al., 2007). The species display great variationin body size (ca. 6–156 g), bill shape, plumage color, vocalizations,⁎social behaviour and ecology (del Hoyo et al., 2007). Their great diversity in morphology and ecology, as well as high levels of sympatry,suggest that they are an ideal group for assessing biogeography,
adaptive radiation theory and mechanisms of species coexistence(Moyle et al., 2012). The first step towards understanding these processes is to develop a robust phylogeny for the group. However, to dateno comprehensive species-level phylogeny of babblers exists.
The babblers have a chequered taxonomic history, and the group
was long regarded as a “scrap basket” for genera that did not fit wellinto other families (Mayr and Amadon, 1951). Delacour (1946, 1950)
proposed the first pre-molecular classification of babblers based on
plumage colour and bill shape. Delacour’s lists placed most babblers in
the family Timaliidae, which included six tribes: Pellorneini, Pomatorhinini, Timaliini, Chamaeini, Turdoidini and Picathartini, and was

Corresponding author at: Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
E-mail address: leifm@ioz.ac.cn (F. Lei).

https://doi.org/10.1016/j.ympev.2018.10.010
Received 1 May 2018; Received in revised form 4 October 2018; Accepted 9 October 2018
Available online 12 October 20181055-7903/ © 2018 Elsevier Inc. All rights reserved.

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Table 1
Name, number of sequences, length of sequence and best substitution model for each locus included in the study.
Loci

Abbreviation

Taxa

Length (bp)Model (Beast)

Cytochrome b
NADH dehydrogenase subunit 2
NADH dehydrogenase subunit 3
Cytochrome c oxidase subunit I
ATP synthase subunit 6
Fibrinogen beta chain intron 5
Glyceraldehyde-3-phosphodehydrogenase intron 11
Muscle skeletal receptor tyrosine kinase intro 3
Myoglobin intron 2
Ornithine decarboxylase intron 6 and 7
Recombination activating protein 1
Transforming growth factor beta 2 intron 5

Cytb
ND2
ND3
COI
ATP6
FIB-5
GAPDH-11
MUSK-3
MB-2
ODC-6/7
RAG1
TGFB2-5

329
320
267
206
71
176
196
155
205
198
139
279

1143
1041
351
651
684
571
344
575
647
612
961
601

GTR+I+ΓGTR+I+ΓGTR+I+ΓGTR+I+ΓGTR+I+Γ
GTR+Γ
GTR+Γ
GTR+Γ
GTR+Γ
GTR+I+ΓGTR+I+Γ
GTR+Γ

considered to be most closely related to the Old World warblers (traditional Sylviidae). This classic taxonomy of babblers remained in use
until Sibley and Ahlquist (1990) provided a new classification based on
DNA-DNA hybridization data. These data and the taxonomy of Sibley
and Monroe (1990) led to the removal of the genera Garritornis, Pomatostomus and Picathartes from babblers, and suggested that Sylvia wasembedded within the babbler group. They suggested dividing thebabblers into the subfamilies Sylviinae (with tribes Timaliini, Chamaeini and Sylviini) and Garrulacinae, both of which were placed in thefamily Sylviidae. The white-eyes (Zosterops) were placed in a seperatefamily Zosteropidae that was sister to the babblers (Sibley and Ahlquist,
1990).
Subsequent studies have attempted to clarify the phylogeny ofbabblers using DNA sequence data. Cibois (2003) published the firstassessment of phylogenetic relationships among babblers using a broad
representation of species with data for three mitochondrial genes. Thisphylogeny revealed that shrike babblers Pteruthius spp. and Greychested Kakamega Kakamega poliothorax were not members of thebabblers, while suggesting that Sylvia and Zosterops belonged in thisgroup. Several other studies also supported the close relationships of
Sylvia and Zosterops to babblers (Alström et al., 2006; Barker et al.,2004). Subsequent studies showed that several taxa previously placedin this group should be removed from the babbler assemblage, whereas
others have been shown to belong to this group (Alström et al., 2013;
Gelang et al., 2009; Moyle et al., 2012). Gelang et al. (2009) considered
Sylviidae as a separate family, and the white-eyes and “core babblers”
as the family Timaliidae (including subfamilies Timaliinae, Pellorneinae, Leiothrichinae and Zosteropinae). With the first comprehensive
sampling of babblers including 183 species (ca. 40% of the overall
species), Moyle et al. (2012) proposed three families of babbler assemblages: Sylviidae, Zosteropidae and Timaliidae (with the subfamilies Timaliinae, Pellorneinae and Leiothrichinae). Using one mitochondrial and six nuclear genes with comprehensive sampling of thesuperfamily Sylvioidea, Fregin et al. (2012) and Alström et al. (2013)
considered five primary clades at the rank of family for the babbler
assemblage: Sylviidae, Zosteropidae, Timaliidae, Pellorneidae andLeiothrichidae. This taxonomy was gradually recognized by recent
taxonomic lists (Dickinson and Christidis, 2014; Gill and Donsker,
2018). However, some phylogenetic relationships and generic names
continue to differ.
In this study, we use a multi-locus dataset combining published andnewly generated sequences to reconstruct a time-calibrated phylogeny
for 89% of the world’s babbler species. Our results reveal some novel
relationships and non-monophyly for some genera. Based on thiscomprehensive tree, we propose a revised classification in which we
strive to circumscribe families and genera in a consistent way based ondivergence times.

2. Methods
2.1. Taxon sampling and sequences
Taxonomic arrangements above the species level follow the Howardand Moore Complete Checklist of the Birds of the World (4th edition)(Dickinson and Christidis, 2014) with the exclusion of Elachura formosa,Madanga ruficollis and Leonardina woodi because the latest molecularevidence suggests they are not babblers (Alström et al., 2014, 2015;
Oliveros et al., 2012). We include 47 taxa considered as subspecies inthe Howard and Moore Checklist (Dickinson and Christidis, 2014) but
recognized as species in the IOC world birds list 8.1 (Gill and Donsker,
2018). In total, we analyzed 402 species out of a total of 452 babbler
species (Gill and Donsker, 2018). Additionally, we included 108 species
representing closely related family groups (Aegithalidae, bushtits;
Phylloscopidae, leaf warblers; Cettiidae, bush warblers) and Paroidea(tits and remizids) as outgroups (Alström et al., 2013; Fregin et al.,2012). We generated 179 new DNA sequences for babblers(MK068915–MK069083), and combined these with published sequences (Cibois, 2003; Cibois et al., 2018; Gelang et al., 2009; Liu et al.,2016; Luo et al., 2009; Moyle et al., 2012, 2009; Voelker and Light,
2011; Warren et al., 2006) to produce a supermatrix consisting of 12loci (five mitochondrial; six nuclear introns; one nuclear coding gene;
Tables 1 and Table S1).
We extracted DNA from ethanol-preserved tissue or blood samples
using a DNEasy Blood and Tissue Kit (Qiagen) following the manufacturer’s protocol. DNA from toepads of museum specimens were extracted using a well-established ancient-DNA extraction protocol(Irestedt et al., 2016, 2006). The Polymerase Chain Reaction (PCR)
amplification was performed for the fresh tissue samples using the
published primers Table S2) (Friesen et al., 1999; Irestedt et al., 2001;
Kimball et al., 2009; Sorenson et al., 1999). For toepad samples of
Zosterops, a number of new primers were designed to amplify smaller
fragments of mitochondrial genes (approximate 200–300 bp). The PCR
conditions were set as follows: denaturation at 94 °C for 3 min, followed
by 35–40 cycles (94 °C for 30 s, annealing temperature (Table S2) for
30 s, and 72 °C for 45 s), and a final 5 min at 72 °C. All PCR products
were purified using a QIAquick PCR purification kit (Qiagen) and sequenced using the ABI 3730xl Analyzer.
In addition, we used de novo assembly to generate new sequences for
16 toepad samples. The preparation of paired-end genome libraries forIllumina high-throughput sequencing followed the protocol publishedby Meyer and Kircher (2010), except that no further fragmentation wasneeded of the DNA derived from museum skins as this is already fragmented through natural degradation. To reduce clonality each library
was amplified with four different indexes. Four species with four indexes were each pooled, and each pool was then run on a single Illumina Hiseq X lane. The sequencing reads were processed using a custom
designed workflow that is available at https://github.com/mozesblom.
The workflow removes PCR duplicates, adapter contamination, low347

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quality bases, low-complexity reads and merges overlapping read-pairs.
Both adapter and quality trimming was done using TRIMMOMATIC(v.0.3221), PCR duplicates were removed with SuperDeduper(v.1.422), reads were merged with PEAR (v.0.9.623) and overall
quality and length distribution of sequence reads were inspected priorand post the clean-up workflow using FASTQC (v.0.11.524).
Published DNA sequences were downloaded from GenBank andselected in the following way. First, we downloaded all available sequences of ingroup and outgroup taxa using family names as key words
to search for each gene. After aligning sequences in MUSCLE 3.8.31(Edgar, 2004) using default settings, we conducted 100 rapid bootstrap
searches to obtain the Maximum Likelihood (ML) tree using RAxML
8.2.4 (Stamatakis, 2014). Next, we selected the best candidates (thelongest sequences from the clade including most sequences of thatspecies) based on the ML tree and geographical location of the sample.
If available, we selected sequences from the same individual (searcheduntil to June 2017).

between Liocichla steerii (endemic to Taiwan Island) and L. ripponi(mainland Asia). The second calibration was derived from the earliest
appearance of a diversity of oscine passerine fossils on the Northern
Hemisphere (Europe) from the late Oligocene (∼26–25 Ma); thesefossil remains have not been assigned to specific extant families(Manegold, 2008) but morphological details are shared with several
deep lineages of the large Passerida radiation (Elminia, Remiz, Regulus,
Bombycilla and Hypocolius; J.F., unpublished). Since phylogenetic studies with a broader sampling place the start of the radiation of sylvioid
birds shortly after the basal Passerida radiation, we set the minimum
age of the most recent common ancestor (MRCA) of Sylvoidea andParoidea as 25 Ma with 5% and 95% quantiles of 25.5–37.6 Ma under
the lognormal distribution.
Divergence time was estimated in BEAST 1.8.4 (Drummond andRambaut, 2007) using the relaxed molecular clock model based on thefull partition strategy and the best substitution model for each locus
chosen by Partitionfinder 2 under BIC option (Table 1) (Lanfear et al.,2012). We implemented the best ML tree as a starting tree, and applied
the Yule speciation tree prior. In addition, we also employed the substitution rate of mitochondrial genes (2.1%/Ma) (Weir and Schluter,2008) with a relaxed-clock to estimate the divergence time. These
analyses were run for 200 million generations in total and was sampled
every 1000 generations. TRACER v1.6 (Rambaut et al., 2014) was used
to examine the effective sample size (ESS) to evaluate the convergenceof MCMC chains. Finally, we discarded the first 80,000 trees as ‘burnin’
and used the remaining 120,000 trees to produce a maximum clade
credibility (MCC) tree.

2.2. Phylogenetic analyses
Before alignment, all protein-coding sequences were translated toamino acids to check for stop codons using the online tool EMBOSSTranseq (Li et al., 2015). Then, sequences were aligned for each locus
individually using MUSCLE 3.8.31 (Edgar, 2004). Ambiguous regions in
nucler introns were removed in Gblocks 0.9b (Talavera and Castresana,2007), resulting in 4–18% of sequences being removed. A ML tree wasreconstructed for each locus using 10,000 ultrafast bootstrap (Hoang
et al., 2017) under the best model estimated by ModelFinder (-m MFP)
(Kalyaanamoorthy et al., 2017) with Bayesian Information Criterion(BIC) option in IQ-TREE (Nguyen et al., 2014). These analyses allowed
us to have an initial quality check of the sequences, enabling us todetect any spurious sequences.
Phylogenetic relationships were inferred using the concatenatedalignment of 12 loci in the IQ-TREE 1.6.1 (Nguyen et al., 2014). We
considered three partitioning schemes: (1) “unpartitioned”: all lociwere combined as one partition; (2) “full”: each locus was regarded as apartition; and (3) “PF”: the optimal partitioning scheme suggested byPartitionfinder 2 (Lanfear et al., 2012) according to the BIC under the“greedy” search algorithm. The best substitution model for each partition was chosen by ModelFinder (-m MFP) (Kalyaanamoorthy et al.,2017) according to the BIC option in IQ-TREE. Nodal support was assessed using 10,000 ultrafast bootstrap replicates (Hoang et al., 2017).
Our DNA matrix contained some taxa represented by some missing
or short sequences, which often proved difficult to place with any
confidence in the phylogeny, and which we refer to as rogue taxa
(Aberer et al., 2013; Moyle et al., 2012). To improve resolution of thephylogeny, we identified rogue taxa using 1000 RAxML (Stamatakis,2014) fast bootstrap trees in RogueNaRok (Aberer et al., 2013). Somerogue taxa were removed from the complete data matrix (Data-1) toproduce a pruned data matrix (Data-2). Then, using the reduced data
matrix, we repeated ML tree searches following the same settings as for
Data-1.

2.4. Temporal banding for consistent families and genera
Temporal banding is an approach to assess the consistency oftaxonomic ranks and provides a practical solution to temporal inconsistencies (Avise and Johns, 1999; Holt and Jønsson, 2014). This approach identifies temporally consistent taxonomic ranks by splitting a
dated phylogeny at specified points in time, such that the descendenttaxa of the independent lineages form taxonomic units of comparable
age (Holt and Jønsson, 2014; Jønsson et al., 2016). To do this, Jønsson
et al. (2016) provided a “least disruption” approach to revise taxonomic
ranks, which tested all possible splitting points for the MCC tree andthen compared these to current taxonomic families and genera. The
best cut-off points would result in the fewest changes of the originaltaxonomy (with highest percentage consistency). In this study, we used
the R script provided by Jønsson et al. (2016) to delimit consistentfamilies and genera of babblers, providing a basis for taxonomic revisions. We used this approach pragmatically rather than strictly, and we
explicitly tried to be conservative and to propose a minimal number ofchanges.
3. Results
Our DNA supermatrix consisted of 2538 sequences from 402 babbler species (89%) in 75 out of 77 recognized genera (missing genera:
Rukia and Megazosterops), including five mitochondrial and seven nuclear loci (mean = 6.3 loci/taxon) (Table 1). The final complete data
matrix (Data-1) included a total of 8181 bp including five mitochondrial genes and seven nuclear genes, of which 4000 sites were parsimony informative. Based on the analysis of rogue taxa, we removed 42
rogue taxa (81% represented by Zosterops) from Data-1 to produce a
pruned data matrix (Data-2). Different partition strategies produced
congruent phylogenetic trees with differences in support values at somenodes. Generally, tree inference using the “full partition” data producedon average higher support values than other partition schemes. Thus, inthe following we present only the results from the analyses under “fullpartition”.

2.3. Divergence times
We used two calibration points to estimate divergence time ofbabblers. The first calibration was derived from the separation of
Taiwan Island from mainland Asia in the early Pliocene. The mountainsof Taiwan were progressively uplifted since the late Miocene–early
Pliocene (∼6–5 million years ago, Ma) (Huang et al., 2000; Sibuet andHsu, 2004) due to the northward movement of the Luzon Shelf. Several
phylogenetic analyses calibrated by fossil and substitution rate of
mtDNA have suggested that the divergence between mainland andTaiwan Island pairs of birds occurred around 5–1.5 Ma (Cai et al., 2018;
Qu et al., 2015; Wu et al., 2011). Thus, we used a normal prior with 5%
and 95% quantiles age of 1.5–6 Ma to calibrate the node splitting
348

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Fig. 1. Maximum likelihood phylogeny derived from 12 loci with rogue taxa removed from the matrix (Data-2). Bootstrap values are indicated at the nodes.

3.1. Phylogenetic analysis

our phylogeny. Clades A and B were strongly supported as sisters (together forming the Sylviidae), and formed the sister clade to the others.
Clades C (Zosteropidae), D (Timaliidae), E (Pellorneidae), F (Alcippe;
part of Leiothrichidae) and G (Leiothrichidae sensu stricto) were sequential sisters. The position of the Alcippe clade (F) as sister to Leiothrichidae (G) received higher BS value in the analysis of Data-2 than in
the analysis of Data-1 (BS: 94% and 56%, respectively).

Phylogenetic analyses of the two different DNA matrices (Data-1
and Data-2) reconstructed very similar topologies (Figs. 1 and S1). As
expected, trees with rogue taxa removed (Data-2) produced on average
higher bootstrap support (BS) values than the complete DNA matrix(Data-1). Seven well supported primary clades (A–G) were identified in349

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Tree inferences using newly generated sequences revealed thephylogenetic positions of some taxa previously not studied (Fig. S1).
Most taxa with new sequences were placed in the corresponding genera
defined by Dickinson and Christidis (2014). For example, a total of 11
newly sequenced Zosterops were placed in the Zosterops clade. Stachyris
nonggangensis was strongly supported as sister to S. humei and S. roberti.
Schoeniparus variegaticeps was sister to S. castaneceps, and Alcippe pyrrhoptera was sister to A. brunneicauda. Mixornis flavicollis was close to M.
gularis and M. bornensis. Spelaeornis kinneari and S. oatesi were closely
related to S. reptatus and S. longicaudatus. Pomatorhinus melanurus was
sister to P. horsfieldii. Garrulax bieti was sister to G. lunulatus, and G.
woodi, koslowi and waddelli were close to G. lanceolatus. Trochalopteronmelanostigma and T. peninsulae were sisters, both of which were close to
T. formosum. Turdoides rufescens was sister to T. affinis and T. striata.
Argya altirostris was closely related to A. caudata and A. huttoni. We
found Tephrozosterops stalkeri to be strongly supported as sister to Zosterops. Garrulax calva and G. lugubris formed a well-supported sisterclade to the Pomatorhinus clade.

Leiothrichidae. However, individual gene trees showed various relationships of Alcippe, and the support for a sister position to Leiothrichidae derives from the transforming growth factor beta 2 (TGFB2)
gene (Moyle et al., 2012). Our phylogeny with all 10 species of Alcippeincluded placed Alcippe as sister to Leiothrichidae, but the support values were not unanimously high (BS = 56%, posterior probability(PP) = 0.99). In the analyses without the rogue taxa, the support values
for this position were significantly improved (BS = 94%, PP = 1.00).
Thus, the phylogenetic position of Alcippe seems to be largely affectedby the rogue taxa. This may be assessed in the future using morecomprehensive data for these rogue taxa.
4.2. Divergence times
Our phylogeny using a fossil and a biogeographic event as a calibration implies that babblers originated in the late Oligocene to early
Miocene, at approximately 23.5 Ma (28–20 Ma). The dates are slightly
younger than the time from a previous study estimated by a large DNA
matrix and multiple fossil calibrations of modern birds at 30.5 Ma(36–25 Ma) (Claramunt and Cracraft, 2015). The earlier study did notuse calibrations within the Sylvioidea, thus it is not surprising that theircalibrations produced a broader range of divergence times than our
phylogeny. Our estimated divergence times for babblers are well matched with the divergence times in previous studies of the same group(Moyle et al., 2012; Price et al., 2014). Using two secondary calibrations, Moyle et al. (2012) estimated that the split of Zosteropidae and“core babblers” occurred at approximately 18 Ma (21–16.1 Ma), consistent with our estimate of that split at 20.4 Ma (24.6–17.4 Ma). Priceet al. (2014) used fossil and biogeographic data to calibrate the phylogeny for the Himalayan passerines. They concluded that the MRCA of
the core babblers (Timaliidae, Pellorneidae and Leiothrichidae) occurred at 20.9 Ma, which is closely similar to our results (19.2 Ma).
However, our calibrations suggested a much older divergence time
between Sylvia and Timalia (21.9 Ma; 18.6–26.4 Ma) than found by
Moyle et al. (2016), which derived calibrations from Prum et al. (2015)
and Jarvis et al. (2014) and indicated the split time between Sylvia andTimalia at 13.5 Ma (12–15.5 Ma). In addition, our estimated times are
consistent with calibrations using the evolutionary rate of mitochondrial genes, i.e., the Old World warblers (Voelker and Light, 2011) and
Alcippe morrisonia complex (Qu et al., 2015).

3.2. Divergence times
ESSs of all parameters were higher than 200 after 5 million generations. The two calibration methods obtained very similar divergencetimes. However, the tree based on the mitochondrial clock rate reported
higher 95% highest posterior densities (HPD) than the tree based on
fossil and biogeographic event calibrations (Figs. 2 and 3, S2). Thus, thelatter is presented as our main result (Figs. 2 and 3). According to thisanalysis, babblers split from their close extant relatives in the late
Oligocene–early Miocene (23.5 Ma, 95% HPD 28–20 Ma). The MRCA ofbabblers was estimated to have occurred at 21.9 Ma (95% HPD
26.4–18.6). Soon thereafter, the seven primary lineages diverged fromeach other within a relatively short period (up to 18 Ma, 95% HPD
21.5–15 Ma).
3.3. Temporal banding to delimit consistent families and genera
The temporal banding analyses (Fig. S3, Table S3) suggested classifying the babblers into 6 families (with the most recent split at
18.1 Ma) and 50 genera (most recent split at 10.8 Ma), of which 94% of
the families and 60% of the genera were unchanged from the current
taxonomic list (Dickinson and Christidis, 2014). The revised genera ofbabblers were well matched with the taxonomy of Dickinson andChristidis (2014). In addition, temporal banding also suggested that
Sylviidae should be considered as two families represented by clade A
and clade B, respectively.

4.3. Phylogenetic conclusions and taxonomic revisions
Based on our results, we propose a revised classification of thebabbler radiation where we aim to break up in monophyletic units all
currently defined taxa (del Hoyo et al., 2007; Dickinson and Christidis,
2014; Gill and Donsker, 2018) that were found to be poly- or paraphyletic based on the molecular data. We also used divergence times
from the time-calibrated tree to circumscribe genera. Our temporal
banding analysis suggests recognition of 50 genera using a cut-off limitof 10.8 Ma, of which 60% of the genera were consistent with current
taxonomy (Dickinson and Christidis, 2014). Analyzing a supermatrix
tree for corvoid birds, Jønsson and Fjeldså (2006) also found that a cutoff limit of 10 Ma for recognizing genera was generally in good agreement with traditional classification, and ongoing analysis of otherpasserine groups (J.F. et al., in progress) suggests that this cut-off levelalso causes little conflict with traditional classification of most otherpasserines, except for the most rapidly diversifying groups of New
World nine-primaried oscines (Barker et al., 2015). We therefore strive
to apply this cut-off level (ca. 10 Ma) for the babbler genera, and only a
few currently recognised genera older than this threshold were identified. The main avian taxonomic references (Bock, 1994; Deignan, 1964;
Richmond, 1992; Sharpe, 1881, 1883; Wolters, 1975–1982) were used
when resurrection of names previously treated as junior synonyms wasnecessary. The taxonomic names that we recommend can be found in
Table S4, and for families and genera in Figs. 2 and 3.

4. Discussion
4.1. Effects of rogue taxa in phylogenic inference
In this study, we used newly generated and previously publishedDNA sequences from 12 loci to construct a phylogeny comprising 89%
of the world’s babbler species. In the analyses of the complete dataset(Data-1), 80% of the nodes received BS ≥ 95%. However, some deep
nodes were poorly supported. This lack of resolution could be due tosome rogue taxa with incomplete sequence data. Some previous studies
have confirmed this assumption, because the support values for many
nodes increase after removing rogue taxa (Aberer et al., 2013; Moyleet al., 2012; Shakya and Sheldon, 2017). This also seems true for thisstudy, because after removal of the 42 rogue taxa (Data-2), 90% of thenodes received BS ≥ 95%.
Support for the relationship of the genus Alcippe (Clade F) appears
to be dependent on the sampling scheme. Gelang et al. (2009) included
only one species of Alcippe, and found strong support for placing it assister to Pellorneidae. In contrast, Moyle et al. (2012) recovered a cladewith seven Alcippe in a strongly supported sister position to350

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Fig. 2. Divergence time estimates of the babbler radiation based on the complete supermatrix (Data-1) estimated in BEAST using two calibrations. Bars on nodes
indicate 95% highest posterior density of age estimates. Posterior probabilities are only shown at the deeper nodes. Family names are those recommend based on thepresent study. Illustrations of birds by J.F.

4.3.1. Family Sylviidae
The Sylviidae includes the type genus Sylvia, with representatives in
the western part of the Palearctic and in the Afrotropics, the two
Afrotropical genera Parophasma and Lioptilus, and the Palearctic genus
Curruca, as well as an assemblage of Oriental taxa, such as fulvettas(e.g. Fulvetta, Lioparus), parrotbills (e.g. Paradoxornis) and allies, andthe only babbler found in the New World, the Wrentit Chamaea fasciata(del Hoyo et al., 2007; Dickinson and Christidis, 2014). According toour results, the Sylviidae as currently circumscribed are divided into
two large clades (A and B) that diverged in the early Miocene (19.5 Ma;
95% HPD 23–16.1 Ma), similar in time to the other families of babblers.
We therefore suggest the name Sylviidae be restricted to the westernclade (A) that includes the genera Sylvia, Curruca, Parophasma and
Lioptilus, whereas we propose to reinstall the family group nameParadoxornithidae for the eastern clade B. Within the Sylviidae, we
propose the recognition of only two genera corresponding to the twomain clades that diverged around the 10 Ma limit: the genus Sylvia
Scopoli, 1769 (type species S. atricapilla), and the genus Curruca
Bechstein, 1802 (type species C. curruca). This change necessitates that
Parophasma Reichenow, 1905 and Lioptilus Bonaparte, 1850 be treatedas junior synomyns of Sylvia.
Parrotbills have been the subject of several recent phylogenetic
studies (Liu et al., 2016; Yeung et al., 2006, 2011) suggesting that thegenus Paradoxornis Gould, 1836 was paraphyletic, notably by the inclusion of Conostoma. Penhallurick (2010) proposed a complete revision of the group, in which the parrotbills were divided into eight
genera, based on morphological, call and song characters that were also
consistent with the clades obtained in phylogenetic studies. The genus
Paradoxornis as defined by Penhallurick and Robson (2009) contained
three species: the type species P. flavirostris, and P. guttaticollis and P.
heudei. The characters used to group these three species were their large
size, a strongly graduated tail, and a short and strong bill, with a deep,351

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Fig. 3. Detailed phylogeny of babblers based on BEAST analysis using the complete supermatrix (Data-1). Numbers at nodes refer to Bayesian posterior probability/
ML bootstrap support. Family names correspond to Fig. 2. Asterisks indicate 100% bootstrap support and 1.0 posterior probability. Species names with an asterisk (*)
indicate newly sequenced species. Species names in blue color are the generic names that we recommend.

S-shaped curve of the cutting edge of the upper mandible (del Hoyo
et al., 2007). The three species formed a clade in Liu et al. (2016) and
Yeung et al. (2011), but they are paraphyletic in our larger phylogeny.
In all studies, P. flavirostris and P. guttaticollis were sisters, but P. heudei
was sister to a clade including P. flavirostris/P. guttaticollis and the groupformed by Conostoma aemodium and the newly resurrected genera
Psittiparus and Cholornis [see Penhallurick (2010) for a correction on theuse of Hemirhynchus Hodgson, 1843 in Penhallurick and Robson(2009)]. The estimated divergence between P. heudei and the rest of theclade is close to the 10 Ma threshold, so two taxonomic approaches are
possible. The first option corresponds to the finer split at the genus
level, following the propositions of Penhallurick and Robson (2009)
based on morphological and vocal characters. In this case, the species
heudei should be removed from Paradoxornis and the genus Calamornis,
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Fig. 3. (continued)

Gould 1874 resurrected for this taxon. The alternative option favours abroader genus definition for Paradoxornis Gould, 1836, that includes allof the species in this clade (heudei, flavirostris, guttaticollis, gularis, bakeri, ruficeps, aemodium, paradoxa, unicolor), in which case the genericnames Psittiparus Hellmayr, 1903, Cholornis J. Verreaux, 1870, andConostoma Hodgson, 1842 would become junior synonyms. We favour
this second option in which the taxonomy of the group is not inflatedcompared with other babbler families. Similarly, the second primary
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clade of parrotbills should be treated as a single genus, Suthora
Hodgson, 1837 and the names Chleuasicus Blyth, 1845, Neosuthora
Hellmayr, 1911, and Sinosuthora Penhallurick and Robson, 2009 betreated as junior synonyms. Chleuasicus Blyth, 1845 was resurrected by
Penhallurick and Robson (2009) for the species atrosuperciliaris, Neosuthora Hellmayr, 1911 for the species davidiana, and Sinosuthora
Penhallurick and Robson (2009) was created to provide a name for the
five-species clade of small parrotbills with greyish to rufous brownfringes to the flight feathers and no lateral crown-stripes (conspicillata,
zappeyi, brunnea, alphonsiana, webbiana); przewalskii, although not sequenced by Yeung et al. (2011), was also included into Sinosuthora.
We do not propose additional changes for the remaining genera
within Paradoxornithidae, although the case of Chamaea fasciata is
worth mentioning. Chamaea fasciata is sister to the (now redefined)genus Paradoxornis, with a divergence close to the 10 Ma threshold.
However, the ecology and morphology of this New World endemic
differ from the typical parrotbills and it has been isolated for a longtime from its Asian sister-group. We therefore retain this monotypic
genus.

large Zosterops clade, and this monotypic genus could be retained toreflect the unique morphology of this taxon. Lastly, phylogenetic relationships are still uncertain for two small genera not yet sampled(Rukia and Megazosterops).
4.3.3. Family Timaliidae
The Timaliidae, as presently circumscribed, represents a group of
Asian birds with diverse morphology and ecology, distributed acrossthe entire Oriental region east to Wallace’s line (del Hoyo et al., 2007).
We first propose to merge the two monospecific genera Dumetia Blyth,1849 and Rhopocichla Oates, 1889 into the senior Dumetia. The divergence between the two taxa is below the 10 Ma threshold and theirmorphological differences are within the range of differences foundwithin other babbler genera. Second, we propose a revision for two
species previously classified as laughingthrushes in the Leiothrichidae:
Garrulax lugubris and G. calva. The first has a small range restricted tosouth Thailand, Peninsular Malaysia and Sumatra, and the second is
endemic to north Borneo. Both are medium-sized blackish birds, similarby size and shape to laughingthrushes, but with a unique head pattern:a wattle and patch of blue orbital and postocular skin in G. lugubris, anda featherless yellowish crown with a blue submoustachial area in G.
calva (as seen also in some other Timaliidae species), and red bill (as intwo species of Pomatorhinus). These two rare birds have never been thesubject of molecular analyses until our data showed that they are unrelated to the true laughingthrushes and instead belong to the family
Timaliidae. They were sister taxa with strong support, and diverged
from the clade that comprises all Pomatorhinus species earlier than
10 Ma. The striking morphology of these two species and their phylogenetic divergence from other babblers support their placement in theirown genus: we suggest to resurrect Melanocichla Sharpe, 1883, namedwith lugubris as type species, for these two closely related species.
Moyle et al. (2012) showed that the genus Sphenocichla GodwinAusten & Walden, 1875 was embedded within Stachyris Hodgson, 1844,a result followed by Dickinson and Christidis (2014). We confirmed thisresult with sampling the two taxa that composed this genus (S. humei
and S. roberti, the latter being a recent split). With the inclusion of these
two species, the genus Stachyris is monophyletic, although with low
support. Because of the absence of robust support for the nodes within
the Stachyris clade, we favour a conservative approach and suggest no
further divisions within the genus. Finally, we do not propose additional modifications for the remaining genera within this family.

4.3.2. Family Zosteropidae
Several studies already suggested that Yuhina was paraphyletic(Cibois et al., 2002; Moyle et al., 2012; Zhang et al., 2007), and ourcomprehensive analysis, which is the first one to include almost all of
the species, confirms this result and identifies three sequential sister
lineages. The type species of Yuhina Hodgson, 1836 (Y. gularis) belongs
to the largest clade, with six species. The genus Staphida Gould, 1871
can be resurrected for the clade formed by its type species torqueola andthe two species castaniceps and everetti. Finally, the species diademata issister to all other Zosteropidae and requires its own genus. As far as canbe determined, there is no available generic or subgeneric name associated with this species. Therefore, we propose a new generic name:Parayuhina gen. nov.
Type species: Parayuhina diademata (Verreaux, 1869) comb. nov.
Diagnosis: 14–18 cm in length, 15–29 g; mostly greyish-brownplumage with a darker brown erectable crest, prominent white supercilium/nuchal collar from above the eye across the nape, contrastingly
blackish basal parts of primaries and secondaries, and white underwing-coverts; shallowly forked tail; and pale yellowish/orange legs.
Differs from Staphida in lacking broad white tips to the outer tailfeathers, and from Yuhina by its larger size, slightly forked tail andabsence of streaks on head or flanks. Sexes similar.
Etymology: This feminine name is based on the name previously
used for a group of crested babblers, Yuhina, that proved to be paraphyletic based on phylogenetic results. This name was itself based on
the Nepalese word for these birds, “Yuhin” (Richmond, 1992). We add
the prefix Para, from Ancient Greek παρά “near”, to remind the fact that
this taxon does not form a monophyletic group with the other yuhinas.
Remarks: A monospecific genus. Occurs in forested mountainous
areas of central and south China, north-east Myanmar and northVietnam.
The white-eyes form a large clade, with a long internode leading to
an exceptionally rapid island diversification, comprising more than 100
species. We refrain from merging all species into a single genus becauseof the morphological diversity within this group, although diversification within the clade was rapid and occurred within less than 10 Ma.
Several genera might not be monophyletic (Dasycrotapha, Heleia,
Zosterornis), but the nodes are not well supported and further decisions
on this group must await a more comprehensive analysis. In particular,
the position of Apalopteron familiare, embedded within Heleia, is delicate, because if this result is confirmed the name of the entire clade
should be changed to the senior name Apalopteron Bonaparte, 1854 (vs.
Heleia Hartlaub, 1865). However, this topology was not supported by
our ML trees. We confirmed the inclusion of Chlorocharis Sharpe, 1888(one species: emiliae) within Zosterops Vigors & Horsfield, 1827 (Limet al., 2018; Moyle et al., 2009). Tephrozosterops stalkeri is sister to the

4.3.4. Family Pellorneidae
Gelang et al. (2009) found Turdinus macrodactylus sister to Graminicola, whereas our analyses supported Graminicola as sister to the restof Pellorneidae, and our MCC and ML trees using Data-1 recovered
Turdinus as sister to the others (except Graminicola), but with low
support in the ML tree. Despite the uncertainty of the position of Turdinus macrodactylus, both studies confirmed with good support thepolyphyly of Turdinus as defined by Dickinson and Christidis (2014) (aswell as the genus Napothera as defined by Gill and Donsker (2018)). We
suggest to restrict the genus Turdinus to its type species macrodactylus(T. atrigularis, not sampled yet, might also stay in this genus), and toresurrect the name Gypsophila Oates, 1883 (type Turdinus crispifrons,
Blyth) for the clade composed of T. crassa, T. brevicaudata and T. crispifrons (T. calcicola and T. rufipectus, not sampled yet but morphologically similar, are likely also part of this group). Richmond (1992) andZimmer (1926) gave “March” as publication date for Oates’ Handbook toBirds of British Burma, whereas Sharpe’s Catalogue of the Birds in the
British Museum was published in July 1883 (Sherborn, 1934). Thissuggests that Gypsophila Oates, 1883 has priority over Corythocichla
Sharpe, 1883 (indeed Gypsophila Oates was used by Sharpe (1903) in
his hand-list rather than his own name).
We confirmed the position of Napothera epilepidota as sister to thefour species placed in Rimator, with a divergence close to 10 Ma. We
suggest to place all five species found in this clade (N. epilepidota, R.
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Acknowledgements

malacoptila, R. albostriata, R. pasquieri and Jabouilleia danjoui), as well as
J. naungmungensis (not sampled here but confirmed in this clade byRenner et al. (2018)) in Napothera Gray, 1842 (type species epilepidota),with Rimator Blyth, 1847, and Jabouilleia Delacour, 1927, as juniorsynonyms. The last species classified in Turdinus (marmoratus), with aunique scaled pattern and a large size, might be left as it is until it has
been analysed phylogenetically.
Pellorneum Swainson, 1832, as currently defined, is also polyphyletic. Because the type species (ruficeps) forms a clade with P. capistratum, one option could be to move the species albiventre to thegenus Trichastoma Blyth, 1842. However, the limits between these two
closely related genera have often been debated (Deignan, 1964;
Delacour, 1946), and several species have not been sampled yet in
genetic studies (Pellorneum nigrocapitatum, P. fuscocapillus, P. palustre
and Trichastoma buettikoferi). Although the divergence between the twogenera is older than 10 Ma, we suggest to merge all species within thesenior name Pellorneum, in agreement with Eaton et al. (2016). This
group would then unite all species with similar ground-foraging
ecology and adaptations. We propose no modifications for Schoeniparus,
Malacopteron, Malacocincla, Gampsorhynchus, Laticilla, Illadopsis, Kenopia or Ptilocichla.

We thank a lot of colleagues and collaborators who have sharedsamples with us for this study: Guangxi University, China (Fang Zhou
and Lijiang Yu); Kunming Institute of Zoology, Chinese Academy of
Sciences, China (Xiaojun Yang); Museum of the Institute of Zoology,
Chinese Academy of Sciences, China (Peng He); Museum of theKunming Institute of Zoology, Chinese Academy of Sciences, China(Luming Liu); American Museum of Natural History, USA (Paul Sweet
and Thomas J. Trombone); Zoological Museum, University of
Copenhagen, Denmark (Jan Bolding Kristensen); and Museum fürNaturkunde der Humboldt-Universität, Berlin (Pascal Eckhoff, Sylke
Frahnert). Many thanks to Sen Li and Alexander Flórez-Rodríguez for
their kind help in phylogenetic reconstruction, to Manuel Ruedi forsuggesting the new genus name Parayuhina, and to Edward Dickinson
and Steven Gregory for bibliographic information regarding the genus
Gypsophila. We also thank two anonymous reviewers for their insightful comments that improved the manuscript. This work was supported by the National Natural Science Foundation of China (No.
31630069 to F.L. and T.C.); the China Scholarship Council (No. 20167988 to T.C.); the Swedish Research Council (No. 2015-04402 to P.A.,
No. 621-2014-5113 to M.I. and No. 621-2013-5161 to P.E.); the US
National Science Foundation (DEB-1241181 to R.G.M.); the Danish
National Research Foundation (DNRF96 to J.D.K. and J.F.); andJornvall Foundation and Mark and Mo Constantine (to P.A.).

4.3.5. Family Leiothrichidae and the genus Alcippe
The taxonomic revision within Leiothrichidae has been treated inanother paper (Cibois et al., 2018). However, the comprehensive phylogeny presented here highlighted the particularity of the genus Alcippe,
whose position relative to Leiothrichidae and Pellorneidae is notunanimously strongly supported in our analyses (see Section 4.1), andalso varies among other studies (Gelang et al., 2009; Moyle et al.,2012). Because the divergence between these three clades occurred
early during the Miocene, we suggest the genus Alcippe Blyth, 1844 beplaced in a separate family. The family name Alcippidae is however
preoccupied by Alcippidae Hancock, 1849, which refers to a family of
marine invertebrates, now a synonym of Trypetesidae Stebbing, 1910
(Truesdale, 1993). To avoid homonymy in family-group names, as
stated in Art. 29.6 of the International Code of Zoological Nomenclature
4th edition (International Commission on Zoological Nomenclature,1999), we propose a new family name based on the entire name of thetype genus:
Alcippeidae fam. nov.
Type genus: Alcippe Blyth, 1844
Diagnosis: A group of small birds, 12.5–16.5 cm in length,13.2–18.3 g, with brown or olive-grey upperparts, wings and tail, buffywhite underparts, brown or grey crown, nape and ear-coverts, and often
white eye-ring and blackish lateral crownstripes. Sexes similar. The
species in Alcippeidae are smaller than those in the Leiothrichidae(laughingthrushes and allies), with duller plumage. They are more arboreal in habits than the Pellorneidae, which have stronger legs.
Etymology: In the Greek mythology, Alcippe is the daughter of Ares
and Aglauros.
Remarks: Occur in forests and scrub of the Oriental region (mainlySoutheast Asia).

Declaration of interest
None.
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://doi.org/10.1016/j.ympev.2018.10.010.
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