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Article history: The Thamnophilidae is a diverse radiation of insectivorous passerine birds that comprises nearly 220 spe-
Received 12 March 2012 cies and is mostly restricted to the lowlands and lower montane forests of the Neotropics. Current clas-
Accepted 18 June 2012 sification within Thamnophilidae relies primarily on morphological variation, but recent incorporation of
Available online xxxx
molecular and vocal data has promoted changes at various taxonomic levels. Here we demonstrate that
the genus Terenura is polyphyletic because Terenura callinota, T. humeralis, T. spodioptila, and T. sharpei are
Keywords: phylogenetically distant from the type species of the genus, Terenura maculata. More importantly, the
New subfamily
former four species are not particularly closely related to any other thamnophilids and represent a clade
New genus
Avian systematics
that is sister to all other members of the family. Because no genus name is available for this previously
Suboscines undetected lineage in the Thamnophilidae, we describe the genus Euchrepomis for callinota, humeralis,
Antwrens spodioptila, and sharpei, and erect the subfamily Euchrepomidinae. We discuss the taxonomic and evolu-
Antbirds tionary significance of this divergent lineage. This study highlights the importance of taxonomic coverage
and the inclusion of type taxa to redefine classifications to reflect accurately evolutionary relationships.
Ó 2012 Elsevier Inc. All rights reserved.
1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ympev.2012.06.016
Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016
2 G.A. Bravo et al. / Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx
Brazil, which had been placed in Formicivora by Sclater (1858). gene 2 – RAG2, 1152 bp) following the methods described in Groth
Cabanis and Heine did not provide a diagnosis or description of and Barrowclough (1999) and Barker et al. (2002). Additionally,
their new genus, but Terenura translates as ‘‘soft tail’’ in Greek (Jo- some sequences were obtained from previous publications of our
bling, 2010). The species Formicivora callinota (Sclater, 1855) was own work (Bravo et al., 2012; Brumfield and Edwards, 2007; Brum-
subsequently included in Terenura by Taczanowski and von Ber- field et al., 2007; Derryberry et al., 2011; Gómez et al., 2010; Moyle
lepsch (1885) without comment, but perhaps because Sclater et al., 2009). Analyses were conducted using a concatenated six-
noted in his original description of callinota that ‘‘it [callinota] must gene alignment containing 7025 bp.
be placed next to the Brazilian Formicivora maculata . . . with which We edited sequences using Sequencher 4.7 (Gene Codes Corpo-
it agrees in form and style of plumage.’’ This rationale apparently ration, Ann Arbor, MI) and checked that protein-coding sequences
led to the association of callinota with maculata. Subsequent classi- did not include stop codons or anomalous residues. We aligned se-
fications continued to place both in Terenura, along with three quences using the program MAFFT v. 6 (Katoh et al., 2002), and ob-
additional species described later, all noted as close relatives of cal- tained a concatenated dataset using Geneious Pro v5.5 (Drummond
linota and all described in Terenura: T. humeralis (Sclater and Salvin, et al., 2011). Newly obtained sequences were deposited in Gen-
1880), T. spodioptila (Sclater and Salvin, 1881), and T. sharpei (von Bank (Accession numbers JX213474–JX213578).
Berlepsch, 1901). The classification of Terenura as containing five
species remained stable until the addition of a sixth, newly discov- 2.2. Phylogenetic analyses
ered species: T. sicki (Texeira and Gonzaga, 1983). At least two phe-
notypic groups have been recognized within the genus based on We conducted ML analyses for six partition schemes under the
plumage differences: the ‘‘streaked-headed’’ group consisting of GTR + C model of nucleotide substitution using RAxML 7.2.7 (Sta-
T. maculata and T. sicki, and the ‘‘standard’’ Terenura consisting of matakis, 2006) on the Cipres Science Gateway V 3.1 (Miller et al.,
the remaining four species (Ridgely and Tudor, 1994). The 2010). We then calculated the Akaike Information Criterion (AIC)
‘‘streaked-headed’’ Terenura are restricted to the Atlantic Forest, for each partition and established that the most informative
whereas the ‘‘standard’’ Terenura are found through much of scheme is the fully partitioned dataset (16 partitions; each codon
Amazonia, the Guianan shield, and mid-elevations in the Andes position for each coding gene, and the nuclear intron for separate
and southern Central American mountains (Zimmer and Isler, partitions). To evaluate nodal support of the fully partitioned data-
2003). set, we conducted a rapid bootstrap analysis in RAxML using 1000
Here, we present results of morphological and DNA-based phy- bootstrap replicates under the GTR + C model of nucleotide substi-
logenetic analyses to test the monophyly of the genus Terenura and tution, following recommendations by the author in RAxML
assess its phylogenetic position within the family. We demonstrate manual.
that Terenura is polyphyletic and that a subset of its members, not Using the same partition strategy followed in the likelihood
including the type species T. maculata, represents the sister clade analysis (16 partitions), we also performed a Bayesian analysis as
to the rest of the Thamnophilidae. This subset of species must be implemented in Mr. Bayes 3.1.2 (Huelsenbeck and Ronquist,
placed in a separate genus for which no name is available, and they 2001) on the Cipres Science Portal (Miller et al., 2010). To deter-
deserve to be treated as a separate subfamily. We describe a new mine the best nucleotide substitution model for each partition,
genus for these species, place them in a new subfamily, and discuss we used PAUP (Swofford, 2003) to obtain likelihood values for
its phylogenetic, morphological, and evolutionary distinctiveness the 24 substitution models featured in MrModeltest 2.3 (Nylander,
among the Thamnophilidae. 2004). Based on comparison of AIC scores for each partition, we
determined that: the GTR + C + I model was the best fit for the first
codon position of ND2, cytb, and RAG1, and the second codon posi-
2. Materials and methods tion of ND2, ND3, and RAG1. GTR + C provided the best fit for the
third codon position of ND2, ND3, cytb, and RAG1, and for the nu-
2.1. Taxon sampling and laboratory procedures clear intron BF5. GTR + I was the best fit for the second codon posi-
tion of cytb and RAG2; SYM + C provided the best fit for the first
Our analysis is based on DNA sequences from 37 samples with codon position of ND3; HKY + C + I was the best fit for the first co-
physical voucher specimens housed in accessible scientific collec- don position of RAG2; and HKY + I was the best model for the third
tions (Peterson et al., 2007; Table 1). They represent 31 species codon position of RAG2. We conducted the analysis using 4 runs, 4
and 23 genera (14% and 48% of family, respectively), including chains, and 2 107 generations with a sample frequency of 1000, a
samples of nominate populations of Terenura maculata (3; type burn-in of 20%, and chain temperature of 1.75. The use of the
species), T. callinota (2), T. humeralis (2), T. sharpei (2), and T. spo- ‘‘compare’’ and ‘‘slide’’ functions of AWTY online (Wilgenbusch
dioptila (1). Samples of T. sicki were not available to us. For out- et al., 2004) were used to assess the performance of Bayesian phy-
groups we used sequences from Pipra spp. (Pipridae; LSUMZ B- logenetic inference.
18078/AMNH DOT-3872), Furnarius rufus (Furnariidae; AMNH
DOT-10431), Chamaeza campanisona (Formicariidae; UWBM 2.3. Ecomorphological analyses
KGB14), Hylopezus berlepschi (Grallariidae; FMNH 322345), Liosce-
les thoracicus (Rhinocryptidae; FMNH 390080/322412), Pittasoma We measured 10 ecomorphological variables (wing length, pri-
spp. (Conopophagidae; LSUMZ B-2285/B-11863), and Melanopareia mary 10 length, tail length, rectrix 1 width, secondary 1 length, bill
elegans (Melanopareiidae; LSUMZ B-5245/5246), length from nostril to tip, bill width at nostrils, bill depth at nos-
Total DNA was extracted from 25 mg of pectoral muscle using trils, tarsus length, hallux length) from 243 individuals (Appendix)
the Qiagen DNeasy kit, following the manufacturer’s protocol. representing antwrens in the genera, Epinecrophylla, Isleria, Myr-
Based on the methods described in Brumfield et al. (2007), we motherula, Microrhopias, Herpsilochmus, Formicivora, Stymphalornis,
amplified and sequenced three mitochondrial genes (nicotinamide Terenura, Stymphalornis, and Terenura. All measurements were ta-
dehydrogenase subunit 2 – ND2, 1041 bp; nicotinamide dehydro- ken to the nearest 0.01 mm with a Mitutoyo Digimatic Point Cali-
genase subunit 3 – ND3, 351 bp; cytochrome b – cytb, 1045 bp) per by G.A.B. Details of how they were taken can be found
and one autosomal nuclear intron (b-fibrinogen intron 5 – bF5, elsewhere (Baldwin et al., 1931; Derryberry et al., 2011). To assess
554 bp). We also amplified two coding nuclear genes (recombina- how diagnosable Terenura is with respect to all other antwrens in
tion activation gene 1 – RAG1, 2875 bp; recombination activation ecomorphological space, we conducted a discriminant function
Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016
G.A. Bravo et al. / Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx 3
Table 1
Ingroup taxa used in this study with tissue collection voucher number. Tissue collections: LSUMZ—Louisiana State University Museum of Natural Science, Baton Rouge; UWBM—
University of Washington Burke Museum, Seattle; USNM—United States National Museum of Natural History – Smithsonian Institution, Washington; AMNH—American Museum
of Natural History, New York City; FMNH—Field Museum of Natural History, Chicago; MPEG—Museu Paraense Emílio Goeldi, Belém, Brazil; IAvH—Instituto Alexander von
Humboldt, Villa de Leyva, Colombia.
analysis (DFA) using log-transformed measurements for all indi- (streaked-headed), whereas the other includes T. callinota, sharpei,
viduals in the data set and three grouping units: ‘‘streaked- humeralis, and spodioptila (standard). Both groups are also diagnos-
headed’’ Terenura, ‘‘standard’’ Terenura, and all other antwrens. able from other antwrens in morphologically similar genera
(Wilks’ lambda = 0.46, F20,462 = 10.82, P = 0.00). All T. maculata
specimens were correctly predicted as T. maculata, and all ‘‘stan-
3. Results
dard’’ Terenura specimens were correctly predicted as such.
Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016
4 G.A. Bravo et al. / Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx
Fig. 1. 50% Majority-rule Bayesian consensus tree topology of a subset of the Thamnophilidae showing that Terenura callinota, T. humeralis, T. spodioptila, and T. sharpei are not
closely related to T. maculata. Numbers at each node indicate posterior probability values (left) and bootstrap support values based on 1000 maximum-likelihood replicates
(right). Outgroups not shown.
four species are the only species in the Thamnophilidae with Diagnosis and definition. The degree of genetic differentiation
bright greenish backs and margins of the remiges; these are between Euchrepomidinae and the other subfamilies in the
gray in spodioptila, although the taxon meridionalis, currently Thamnophilidae is substantial. For instance, members of Euch-
treated as a subspecies of spodioptila, has distinctly olive mar- repomis differ in sequence divergence from any other genus in
gins of remiges (Snethlage, 1925). the family by no less than 13.4% in cytochrome b and 18.4% in
Etymology. Feminine generic name derived from the Greek ND2 (uncorrected p-distances). Also, their level of divergence
euchrôs (ruddy, bright-colored) and epômis (point of the shoul- in a slowly evolving nuclear gene such as RAG1 (2.0–2.9%) is
der). This refers to the bright yellow or bright orange-rufous similar to that exhibited in other subfamily-level comparisons
coloration of the lesser secondary coverts of males; a character in the Furnariides (e.g. 2.1–3.0% between Rhinocryptinae and
that, within Thamnophilidae, is unique to the members of the Scytalopodinae; and 2.7–2.9% among Sclerurinae, Dendrocolap-
genus. tinae, Furnariinae). Also, species of Euchrepomis possess several
morphological and behavioral distinctions. The presence of
brightly colored lesser coverts is unique in the family. Conspic-
3.4. New subfamily
uous fluffing or expansion of the brightly colored feathers of the
upperparts, including these bright feathers of the lesser upper-
Moyle et al. (2009) divided the Thamnophilidae into two sub-
wing coverts, is the principal component of apparently aggres-
families, Myrmornithinae for Myrmornis, Pygiptila, and Thamnistes,
sive or territorial interactions between males. Finally, no other
and Thamnophilinae for everything else except Terenura, and
thamnophilid group is so restricted to foraging in the canopy,
found that Terenura (here Euchrepomis) sharpei was sister to all
at the periphery of crowns of trees. Several other small ‘‘antw-
other thamnophilids. With more extensive taxon sampling, we
rens’’ in the genera Myrmotherula and Herpsilochmus, as well as
are compelled to recognize this new genus as a separate subfamily:
the two members of true Terenura, regularly forage in the can-
Euchrepomidinae, subfam. nov. opy, but all of these also range regularly into the subcanopy,
Type genus. Euchrepomis genus nov. which is rare for species in Euchrepomis.
Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016
G.A. Bravo et al. / Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx 5
Fig. 3. Examples of loudsongs of Terenura (A – maculata; B – sicki) and Euchrepomis (C – callinota; D – sharpei; E – humeralis; F – spodioptila). Both genera are characterized by
remarkably high similarity of loudsongs among all of their respective species. Recordings obtained from Isler and Whitney (2002).
Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016
6 G.A. Bravo et al. / Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx
membranous operculum, supporting observations by Salvin and Museum of Natural History (USNM); Instituto Alexander von Hum-
Godman. However, we could not observe any kind of covering on boldt (IAvH).
maculata either. Also, direct examination of specimens at MZUSP Epinecrophylla fulviventris (LSUMZ 163587, 163589, 178011); E.
revealed that tails of Terenura maculata specimens are softer than gutturalis (LSUMZ 53090, MPEG 66252, 66254, 66258); E. leu-
those of Euchrepomis specimens (M.A. Rego, personal communica- cophthalma (LSUMZ 52029, 137147, 150759, 172928); E. haemato-
tion), consistent with the meaning of the name Terenura. nota (LSUMZ 109932, 109934, 109938, 132702); E. fjeldsaai
Euchrepomis is the only genus in the family that exhibits con- (LSUMZ 83109); E. spodionota (LSUMZ 87968, 87969, 116881,
spicuous and contrasting orange-rufous or yellow rumps and 116883); E. ornata (LSUMZ 92379, 157127, MPEG 53893, 61345,
shoulders that are actively displayed during aggressive interac- 61346); E. erythrura (LSUMZ 78457, 83126, 87970, 116880); Isleria
tions between males. Although males of both species of Terenura guttata (LSUMZ 165714, MPEG 45899, 45900, 51034); I. hauxwelli
exhibit bright coloration in the upperparts, we have never ob- (LSUMZ 84823, 109924, 109926, 161753); Myrmotherula brachyura
served either of them actively fluffing or otherwise displaying (LSUMZ 102097, MZUSP 84846, 84847, 84848); M. obscura (LSUMZ
these feathers, even after considerable playback. Euchrepomis rep- 109908, 109916, 109917, 156501); M. ignota (LSUMZ 162115,
resents the only genus in the family entirely associated with the 164145, 178016, 178017); M. ambigua (MPEG 53081); M. sclateri
canopy and it is widely allopatric to Terenura. (LSUMZ 132665, MPEG 39992, 39995, 39997); M. surinamensis
Intrageneric similarity of loudsongs of both Terenura and Euch- (MPEG 20262, 20264, 21102, 21103); M. multostriata (LSUMZ
repomis is remarkably high. In contrast, loudsongs show only weak 115269, 115270, 116332, 137133); M. pacifica (LSUMZ 108320,
intergeneric similarity. Although both possess high-pitched trills 108321, 177733, ICN 31097, 31576); M. cherriei (ICN 37229,
(Fig. 3), the peak frequencies of Euchrepomis loudsongs (5.2– 37230); M. klagesi (LSUMZ 165771, B-25560, B-25561, MCH470/
6.6 kHz) are higher than those of Terenura (4.3–4.4 kHz), and paces 471); M. longicauda (LSUMZ 102100, 102101, 173982, 173983);
of Euchrepomis loudsongs (9–13 notes/s) are slower than those of M. gularis (LSUMZ 52761, MZUSP 81489, 81490, 81160); M. axillaris
Terenura (19–22 notes/s). Given the importance of vocalizations (MPEG 56945, LSUMZ 115305, 132726, 108334, 177734, 156522,
in the diversification of the family (Seddon, 2005), these differences 156519, 178447); M. schisticolor (LSUMZ 108330, 116897,
are not only relevant for diagnosing both genera, but suggest that 138712, 173985); M. sunensis (LSUMZ 83141, 83142, 83145,
these two genera have experienced distinct evolutionary histories. 83146); M. minor (MZUSP 5477, 28292, 60794, 70595); M. longipen-
Finally, this study represents another example of how tradi- nis (LSUMZ 109965, MPEG 35222, 53675, 59604); M. urosticta
tional taxonomy based on morphological similarities can be incon- (LSUMZ 113494, MZUSP 76217, 76218, 76219); M. iheringi (LSUMZ
gruent with DNA-based phylogenetic classifications (e.g. Bledsoe, 98334, MZUSP 76979, MPEG 60199, 60200); M. grisea (LSUMZ
1988; Raposo do Amaral et al., 2009). Although it had been previ- 90719, 90721, 179663, 179664); M. unicolor (LSUMZ 68022, MPEG
ously suggested that Terenura sensu lato represented two distinct 34454, MZUSP 2188, 67316, 79957); M. behni (LSUMZ 175410); M.
groups based on plumage differences (Ridgely and Tudor, 1994), menetriesii (LSUMZ 109978, 153368, 161758, MPEG 38067, 38212);
only complete sampling with the inclusion of the type species, T. M. assimilis (LSUMZ 109982, 119767, MPEG 56696, 56697); Herpsi-
maculata, allowed testing the evolutionary and taxonomic validity lochmus sellowi (MZUSP 80770, 83298, MPEG 54039, 54040,
of these groups. This highlights the importance of including sam- 57350); H. pileatus (MZUSP 76468, 76469, 76470, MPEG 54042,
ples of type taxa in both systematic and taxonomic studies. 54043); H. atricapillus (LSUMZ 124185, MZUSP 31766, 83300,
84393); H. motacilloides (LSUMZ 106002, 106003, 128513,
128514); H. parkeri (LSUMZ 116902, 116903, 116906, 116908); H.
Acknowledgments sticturus (MPEG 64995, 64996, 65342); H. dugandi (LSUMZ 92402,
128512); H. stictocephalus (MPEG 64992, 62993, 64994); H. gentryi
We are grateful to curators and collection managers of the Field (LSUMZ 172933, 172935, 172938, 172939); H. dorsimaculatus
Museum of Natural History (FMNH), United States National Mu- (LSUMZ 53111, MPEG 53110, 56389, 64711); H. roraimae (LSUMZ
seum of Natural History (USNM), University of Washington’s Burke 175411); H. pectoralis (LSUMZ 71677, MPEG 52474, MZUSP 2848,
Museum (UWBM), American Museum of Natural History (AMNH), 6836, 14256); H. longirostris (LSUMZ 150769, 150770, 150771,
Museu de Zoologia Universidade de São Paulo (MZUSP), Museu MPEG 55927); H. axillaris (LSUMZ 84851, 87989, 169888,
Paraense Emílio Goeldi (MPEG), Instituto Alexander von Humboldt 179675); H. rufimarginatus (LSUMZ 68025, 153373, MZUSP 25652,
(IAvH), and Instituto de Ciencias Naturales (ICN). A.M. Cuervo pro- 73351, 76222); H. sp. nov. 1 (LSUMZ B-25578, LSUMZ B-25579);
vided sequences for one specimen housed at Banco de Tejidos – H. sp. nov. 2 (LSUMZ 179661); Microrhopias quixensis (LSUMZ
Instituto Alexander von Humboldt (IAvH). N. Aristizábal assisted 119771, 132764, 163580, MPEG 56388); Formicivora iheringi
in obtaining sequences. This research was supported by grants (AMNH 243055, MZUSP 7639); F. grisea (LSUMZ 150778, 150780,
from the Frank Chapman Memorial Fund – AMNH, the American 175413, MPEG 53486); F. serrana (LSUMZ 65176, MZUSP 10385,
Ornithologists’ Union, the LSUMNS Big Day Fund, and LSU Biograds 25243); F. littoralis (MPEG 46318, 46320, 73507); F. melanogaster
to GAB, NSF grants DEB-0841729 and DBI-0400797 to RTB, and (LSUMZ 124196, MZUSP 81536, 83297, 84396); F. rufa (LSUMZ
DEB-1011435 to GAB. We thank N. David for his expertise in con- 124198, MZUSP 79625, 79626, 79627); F. grantsaui (MZUSP
structing new genus and subfamily names, and J.A. Chaves for his 76677, MPEG 60420, 60419); Stymphalornis acutirostris (MZUSP
great assistance designing and executing the antbird illustrations. 78797); S. sp. nov. (MZUSP 78797, 78788, 78790); Terenura macula-
This manuscript was greatly improved thanks to valuable com- ta (MZUSP 49910, 49912, 62534, USNM 515966); Euchrepomis cal-
ments provided by A.M. Cuervo and two anonymous reviewers. linota (LSUMZ 84862, 87995, 108346, 173966); E. humeralis (LSUMZ
119769, 132786, 170889, MPEG 63205); E. sharpei (LSUMZ 90722,
90723, 162682, 171313); E. spodioptila (MPEG 53109, IAvH 11286,
Appendix A USNM 625209).
Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016
G.A. Bravo et al. / Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx 7
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Please cite this article in press as: Bravo, G.A., et al. DNA sequence data reveal a subfamily-level divergence within Thamnophilidae (Aves: Passeriformes).
Mol. Phylogenet. Evol. (2012), http://dx.doi.org/10.1016/j.ympev.2012.06.016