| |

Received: 12 January 2021    Revised: 9 February 2022    Accepted: 16 February 2022

DOI: 10.1111/jbi.14370

RESEARCH ARTICLE

Biogeography and diversification of bare-­eyes, an endemic

Amazonian clade

Lincoln Carneiro1,2  | Tibério C. T. Burlamaqui1  | Alexandre Aleixo1,3  |

David C. Oren4 | José Maria Cardoso Da Silva5

1
Coord. de Zoologia. Museu Paraense
Emílio Goeldi, Pará, Brazil
2
Faculdade de Educação do Campo,
Universidade Federal do Pará, Cametá,
Brazil
3
Finnish Museum of Natural History,
University of Helsinki, Helsinki, Finland
4
Ministério da Ciência, Tecnologia e
Inovações do Brasil (MCTI), Brasilia, Brazil
5
Department of Geography and
Sustainable Development, University of
Miami, Miami, USA
Correspondence
Lincoln Carneiro, Coordenação de
Zoologia, Museu Paraense Emílio Goeldi,
Caixa Postal 399, CEP 66040-­170, Belém,
Pará, Brazil.
Email: lscarneiro@ufpa.br
Funding information
Fundação Amazônia Paraense de Amparo
à Pesquisa; Marion E. Kenworthy-­Sarah H;
Swift Action Fund
Handling Editor: Camila Ribas
Abstract
Aim: Biotic interchange, speciation and extinction processes drive biotas assembling.
However, the evolutionary outcomes of those mechanisms are complex and difficult
to discriminate. Here, we investigate how these processes affect avian diversification
in tropical forest regions and test the relative roles of vicariant speciation and biotic
interchange on the assemblage of Amazonian biota through the reconstruction of the
biogeographical history of bare-­eyes using molecular markers.
Location: Amazon.
Taxon: Phlegopsis (Aves: Thamnophilidae).
Methods: We carried out a phylogenetic reconstruction of Phlegopsis based on four
mtDNA and nuclear markers of 52 individuals from 21 localities representing all rec-
ognized taxa in the genus. We estimated phylogenetic relationships using both gene
tree and species tree methods, demographic history, gene flow and divergence time
to reconstruct the biogeographical history of the genus.
Results: Phylogenetic analyses recovered nine lineages delimited by some of the larg-
est Amazonian rivers. Molecular dating and biogeographical studies showed that (1)
most of the diversification in the genus occurred during the Quaternary; (2) vicariance
was the most critical biogeographical process driving the history of this group and (3)
two lineages are expanding their ranges, with one of them (P. n. nigromaculata) cross-
ing the boundaries of areas of endemism.
Main conclusions: Our results reinforce the notion that continental biotas are assem-
bled by alternating dispersal and vicariance events. In Phlegopsis, vicariance shaped
the distribution and differentiation of most lineages, but one event of post-­speciation
dispersal made two lineages sympatric in Western Amazonia. Dispersal events within
the Amazon are not random but are constrained by the characteristics of the spe-
cies that are expanding their ranges and the features of the places that receive such
species. Although most of the speciation events of Phlegopsis occurred during the
Quaternary, there is no reason to assume that such events were driven by climatic-­
vegetation changes associated with the Milankovitch cycles.

KEYWORDS
Amazon, dispersal, molecular systematics, neotropical region, quaternary, speciation

Journal of Biogeography. 2022;00:1–14. wileyonlinelibrary.com/journal/jbi © 2022 John Wiley & Sons Ltd.     1 |
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2      CARNEIRO et al.
1  |  I NTRO D U C TI O N
In the Amazon, there are nine biogeographical regions separated
by some of the longest and widest rivers in the region and take the
shape of large peninsulas with their tips pointing to the Amazon
River. Each one of these biogeographical regions has a unique biota
characterized by many endemic species. Therefore, these regions
can also be classified as areas of endemism (Borges & Silva, 2012;
Cracraft, 1985; da Silva et al., 2002). The species living in these areas
of endemism have different ages, evolutionary histories and habitat
requirements and have been assembled over time by tracking the
region's environmental changes (Bates, 2001; da Silva & Oren, 1996;
Haffer, 2008; Ribas et al., 2012).
Biotas are assembled due to three main biogeographical pro-
cesses: biotic interchange, speciation and extinction (Cracraft, 1994;
Ricklefs & Schluter, 1993). Biotic interchange adds species to a region,
while extinction reduces the number of species. In contrast, in situ
speciation adds endemic species to a region, distinguishing it from
other regions (da Silva et al., 2005). Although speciation has been con-
sidered as the primary factor shaping the composition of the biotas
of the Amazonian areas of endemism (Bates, 2001; Carneiro, Bravo,
et al., 2018; da Silva & Oren, 1996; Ribas et al., 2012), there is evi-
dence that biotic interchange between areas of endemism can also be
important (Antonelli et al., 2018; Bates, 2001; da Silva & Oren, 1996).
Among vertebrate clades restricted to the Amazon, related
species usually replace each other across the region's areas of en-
demism, with no range overlap between them. This distribution pat-
tern is generally interpreted as a result of the range fragmentation
of a widespread ancestor due to vicariant events followed by the
differentiation of the isolated populations into daughter species
(Cracraft,  1985; Haffer,  1969, 1974, 1987; Ribas et al.,  2012). In a
few groups, however, closely related species are sympatric. Because
sympatric speciation is rare among birds (Phillimore et al.,  2008),
these cases of sympatry are considered to be the result of post-­
speciation dispersal events (Chesser & Zink, 1994; Price et al., 2014;
Schweizer & Liu, 2018). Thus, studies on the transition between spa-
tial segregation (allopatry) to coexistence (sympatry) within clades
using phylogenetic approaches promise to reveal an underappreci-
ated mechanism of biotic assembly in Amazonia.
The genus Phlegopsis (bare-­eyes) is an excellent model to examine
the biogeographical processes behind the transition between allo-
patry and sympatry within the Amazon. There are three reasons for
this. First, the lineages of this genus show both allopatry and sympatry.
In general, the seven named lineages (ranked as subspecies) replace
one another across most Amazonian areas of endemism (Haffer, 1992;
Zimmer & Isler, 2020), but some lineages co-­occur in several localities
in western Amazonia due to their ability of them to live in both terra
firme and seasonally flooded (várzea) forests (Willis, 1982; Willis, 1984;
Zimmer & Isler, 2020). Second, Phlegopsis are forest birds with limited
dispersal propensity. They have rounded wings and rarely cross open
spaces, making them a reliable indicator of environmental changes
in the Amazon forests (Willis & Oniki,  1978). Finally, Phlegopsis are
specialized birds, making lineages' co-­occurrence less likely due to
interspecific competition (Willis & Oniki, 1978). In fact, Phlegopsis are
considered as ‘professional’ or ‘obligate’ army ant followers (Willis &
Oniki, 1978) that get most of their food by regularly following army-­
ants (primarily Eciton burchellii and Labidus praedator) in the forest
understorey to capture arthropods that attempt to flee ant swarms
(Willis & Oniki, 1978; Willis & Oniki, 1992). Because they are relatively
heavy and aggressive passerines (c. 50 g), Phlegopsis take the central
and best zones over the ant swarms, supplanting smaller bird species
or chasing them to peripheral zones (Willis, 1982).
In this paper, we test the hypothesis that speciation by vicariance
is more important than post-­speciation dispersal events to explain the
current geographical distribution of Phlegopsis and thus contribute to
the understanding of the processes driving bird diversification in trop-
ical forest regions. To do so, we use molecular markers to assess (a) the
phylogenetic relationships within the group, (b) the divergence ages of
these lineages and (c) the demographic history of these lineages.
2  |  M ATE R I A L S A N D M E TH O DS
2.1  |  Sampling and sequence analysis
We sampled 52 specimens representing all species and subspecies
recognized in Phlegopsis (Figure 1, Appendix S1). These species and
subspecies are as follows: P. e. erythroptera, P. e. ustulata; P. borbae;
P. n. nigromaculata, P. n. bowmani, P. n. confinis and P. n. paraensis. We
also included sequences of the five other Thamnophilidae genera
(Gymnopithys, Rhegmatorhina, Pithys, Phaenostictus and Willisornis) as
the outgroups, following Isler et al. (2014).
Total genomic DNA was extracted using the Sambrook and
Russell's  (1989) protocol from tissue and blood samples. We used
standard methods described elsewhere (Kocher et al.,  1989;
Prychitko & Moore,  1997; Slade et al.,  1993) to amplify and ob-
tain sequences for three mitochondrial coding genes and a nuclear
intron—­cytochrome b (Cyt B), cytochrome oxidase I (COI), NADH de-
hydrogenase subunit 2 (ND2) and beta-­fibrinogen intron 7 (BF7), for
primers details, see Appendix S2, Table S2.1.
Electropherograms were inspected, assembled in contigs
and edited in Geneious 9.1.2 (http://www.genei​ous.com, Kearse
et al.,  2012). Sequences were aligned with MAFFT v. 6 (Katoh
et al., 2002) using the default parameters and further inspected visu-
ally. The software PHASE (Stephens & Donnelly, 2003) was used to
estimate the gametic phases of FIB7, assuming a threshold of poste-
rior probability of 0.7. Unphased sequences with probabilities below
this threshold were also used in the analysis. Moreover, signs of past
recombination of the nuclear loci were tested using a PHI test (Bruen
et al., 2006) in Splits-­Tree4 (Huson & Bryant, 2006).
2.2  |  Phylogeny estimation
We estimated phylogenetic relationships through Bayesian Inference
(BI) using both MrBayes 3.2.1 (Ronquist & Huelsenbeck,  2003) and
CARNEIRO et al.       3|
A1
A2
70°W 60°W 50°W
A7
A6 P. n. paraensis
*/* A4
A5
A8 N
*/* A3
C1 H4, H5 0°
C4
0.92/77 C2 P. n. bowmani
C3
*/* B1
C5 H3 Negro B1
B2 A4, A5, A6,
*/* B3 P. n. confinis Japurá
B4
H1, H2 B2, B3 A7, A8
B5
*/90 E1 D1, D2, C4, C5
E2 P. n. nigromaculata A B4, B5
E3 Solimões D3, D4
D11 F1, F2,
0.59/67 D10 Xingu
A1, A2, A3
*/* D9 F3, F4, Tapájos
*/* D6 Tocantins
D8
D7 P. n. nigromaculata B
F5, F6, Madeira
D5 F7, F8 C1, C2, C3
D2
D1 D8, D9,
D4
D3 D10, D11
*/* J5
*/90 J4 J5
J3 P. borbae
J1
J2 G1, G2 D5, D6, D7
*/* G1 E2
P. e. ustulata B
*/* F7 G2 J1, J2, J3, J4
*/96 F1
F2 10°S
F8 E3 0 200 400 km
*/* F3 P. e. ustulata A E1
*/* F6
F5
F4
H4
H5
0.73/55 H2 P. e. erythroptera
H1 Atlantic
H3
*/* Oneillornis lunulatus Ocean
85/62 Oneillornis salvini
*/* */* Gymnopithys bicolor
*/* Gymnopithys rufigula
*/84 Gymnopithys leucaspis
*/* Rhegmatorhina melanosticta
*/* Rhegmatorhina hoffmannsi
Rhegmatorhina gymnops
Willisornis poecillinotus South
*/* Pithys albifrons America
90/76 Pithys castaneus
Phaenostictus mcleannani

F I G U R E 1  Sampling localities and molecular phylogeny of Phlegopsis based on mtDNA genes Cytb, COI, ND2 and a nuclear intron, bf7
(2865 bp). Bayesian and maximum likelihood analysis yield the same topology. Numbers on nodes are posterior probabilities/ML bootstrap.
*indicates maximum support values

Maximum Likelihood (ML) in RAxML 7.2.8 (Stamatakis, 2006). Three
independent runs conducted BI analysis with 107 generations, each
generation with four Markov chains, one cold and three heated, with
one sample every 1000 generations. Output parameters were visu-
alized using Tracer 1.6 (Drummond & Rambaut, 2007) to assess sta-
tionarity and convergence (Effective Sample Size –­ ESS values >200).
We discarded trees obtained before the chain reached stationarity to
estimate the topology and posterior probability of clades. We gener-
ated 1000 bootstrap pseudo-­replicates to evaluate the support for
ML. Both analyses used the unphased concatenated databank for all
genes with the best partition scheme and model of molecular evolu-
tion inferred by PartitionFinder 1.1.1 (Lanfear et al., 2012). The optimal
partition scheme and best-­fit models used on the BI are described in
detail in the supplementary material (Table S2.2, Appendix S2). This
concatenated phylogeny was used as a guide tree for further analysis
(Species tree, BioGeoBEARS and population genetics). Essentially, sup-
ported reciprocally monophyletic groups that were also geographically
structured were assumed to be hypothesized evolutionary units.
2.3  |  Species tree and molecular dating
We used *BEAST (Heled & Drummond,  2010), part of the BEAST
2.5 package (Bouckaert et al., 2019), to reconstruct a time-­calibrated
species tree, using all individuals of Phlegopsis lineages recovered by
our previous analyses. The partitions and models used on the spe-
cies tree are described in detail in the supplementary material (Table
S2.2, Appendix S2).
We used a Yule speciation prior and a relaxed uncorrelated lognor-
mal clock for all genes (Drummond et al., 2006). The molecular dat-
ing used a substitution rate of ND2 of 2.5% per million years (Smith &
Klicka, 2010) and estimated rates for the remaining markers. We spec-
ified a lognormal distribution and a relatively wide logarithmic stan-
dard deviation of 0.2 for each gene, thus encompassing alternative
substitution rates (e.g. Lerner et al., 2011). We did three independent
runs with 5 × 107 generations each, with parameters sampled every
5000 generations. The ESS values and the number of discarded sam-
ples were inferred with the help of TRACER 1.5 (Rambaut et al., 2014).
2.4  |  Biogeographical analysis
To estimate the biogeographical history of Phlegopsis, we used
‘BioGeoBEARS (Biogeography with Bayesian (and likelihood)
Evolutionary Analysis’ in R Scripts; Matzke, 2013; http://cran. r-­proje​
ct.org/web/packa​ges/BioGe​oBEAR​S/index.html). BioGeoBEARS
models probabilistic biogeographical scenarios onto a user-­defined
phylogeny. We ran six different analyses including the Dispersal–­
Extinction Cladogenesis Model (DEC), a likelihood version of the
Dispersal–­V icariance Analysis (‘DIVALIKE’), and a version of the
Bayesian inference of historical biogeography for discrete areas
(BAYAREALIKE), as well as ‘+J’ versions of these three models,
which include founder event speciation (Matzke,  2013). In these
analyses, we used our multilocus species tree to infer the ancestral
range probabilities by defining the eight Amazonian areas of ende-
mism where Phlegopsis is found as biogeographical units: IM = Imeri;
 |
4      CARNEIRO et al.
NP = Napo; JA = Jaú; IN = Inambari; RO = Rondônia; TA = Tapajos;
XI = Xingu; and BE = Belém (sensu Borges & Silva, 2012; da Silva
et al.,  2002). Although we have no molecular samples of P. n. ni-
gromaculata from Napo, phenotypic data (acoustic and morphologi-
cal) suggest a substantial similarity between the populations of P. n.
nigromaculata A living in Napo and Inambari (Carneiro et al., in prep).
We included this information in our biogeographical setting.
We set the maximum number of areas to eight. For the node pie
charts of ancestral biogeographical ranges, we accepted probability
values in which the most likely area was >5% (distributions with <5%
probability of occurrence combined are the white portions in the
pie charts; Figure  2). Finally, we compared the six different mod-
els for statistical fit via comparison of Log-­Likelihood (ln L), Akaike
Information Criterion (AIC), ΔAIC and Akaike weight (ωi) values
(Wagenmakers & Farrell, 2004).
2.5  |  Population genetics and
historical demography
We used DnaSP 5.10.01 (Librado & Rozas, 2009) to perform Tajima's
D (Tajima, 1989), Fu's FS (Fu, 1997) and the Ramos-­Onsins and Rozas'
R2 tests (Ramos-­Onsins & Rozas,  2002) under 1000 coalescent
simulations. We estimated the genealogical relationships among
haplotypes using median-­joining networks (Bandelt et al.,  1999)
as implemented in Haploviewer (http://www.cibiv.at/~greg/haplo​
viewer). For haplotype network, we removed the sequences and
parts of the fragment containing missing data. We used a Bayesian
Analysis of Population Structure (BAPS v 6.0.; Corander et al., 2008)
to estimate the level of geographical structure within P. nigromacu-
lata and P. erythroptera separately. The probabilities of genetic clus-
ters (from K = 1 to K = 10) for each group were estimated using the
mtDNA dataset only and mixture and admixture analyses. The pro-
gram was run 10 times for each value of K. The admixture analysis
was performed using 1000 iterations, a minimum of one individual
per population, 200 reference individuals for each population and
20 iterations of reference individuals.
We used the isolation–­migration model (Hey & Nielsen, 2004;
Nielsen & Wakeley, 2001) implemented in IMA2 (Hey, 2010) to esti-
mate levels of gene flow between neighbouring populations. IMA2
estimates were obtained only for reciprocally monophyletic pop-
ulation pairs in adjacent areas. IMA2 analyses employed the HKY
model (Hasegawa et al., 1985) for all markers; an inheritance scale
of 0.25 for the mtDNA and 1 for nDNA; a substitution rate for the
ND2 gene of 2.5% sequence divergence per million years per gen-
eration (estimating those of cytb, COI and BF7) and a 1.4 year gen-
eration time (Bird et al., 2020). We did several runs to establish the
best priors for effective population sizes, time of divergences and
migration parameters. Then, we performed three final runs with 105
5 6
generations as burn-­in, 10 trees sampled during 10 generations
and 20 chains. Finally, to test whether a model of isolation without
gene flow fit the data better than a model with gene flow, we used
Nielsen and Wakeley's approach (Nielsen & Wakeley, 2001) and the
likelihood-­ratio tests different models implemented in the IMA2 L
mode.
To analyse population size dynamics through time for both mi-
tochondrial and nuclear loci combined, we estimated extended
Bayesian skyline plots (EBSPs, Heled & Drummond, 2010) available
in the BEAST 2.5 package (Bouckaert et al., 2019). EBSP analyses in-
cluded lineages recovered by concatenated phylogeny. The best-­fit
substitution model for each marker, substitution rates, clock rates,
priors and the MCMC run strategies was the same described for the
phylogenetic analyses.
3  |  R E S U LT S
3.1  |  Sequence data and genetic diversity
We sequenced a total of 2861 bp (Table S2.3 in Appendix S2). The
nuclear locus showed no recombination (PHI test, p  =  0.534) and
higher intraspecific nucleotide diversity than that of the mtDNA
(Table S2.4 in Appendix S2). Phlegopsis lineages showed higher ge-
netic diversity for ND2 than other genes (HD and π; Table S2.4 in
Appendix S2).
3.2  |  Phylogenetic analyses
The concatenated tree supported that (1) Phlegopsis has nine well-­
defined lineages, (2) these lineages are reciprocally monophyletic
and (3) Phlegopsis are a sister group to the clade formed by the
genera Gymnopithys, Rhegmatorhina, Pithys, Phaenostictus and
Willisornis (Figure  1; Harvey et al.,  2020; Isler et al.,  2014). The
bare-­eyes can be grouped into two well-­supported clades: the first
one composed of P. e. erythroptera and P. e. ustulata (A and B line-
ages), and a second one comprising P. borbae, P. n. nigromaculata
(A and B lineages), P. n. bowmani, P. n. confinis and P. n. paraensis
(Figure 1). The first group is found in the western Amazon, with P. e
erythroptera occupying three areas of endemism (Imeri, Napo and
Jaú) and P. e ustulata (A and B) occupying one (Inambari) (Figure 1).
In the second group, P. borbae is restricted to one area of end-
emism (Rondônia), P. n. nigromaculata A is found in Inambari and
Napo, P. n. nigromaculata B is restricted to Rondônia. P. n. bowmani
is endemic to Tapajós, P. n. confinis is endemic to Xingu, and, fi-
nally, P. n. paraensis is restricted to Belém.
3.3  |  Species tree and divergence time estimates
The first divergence within Phlegopsis was between the ancestor
of P. erythroptera and P. ustulata and the ancestor of all other line-
ages around 1.6 Ma (time divergence estimate ranging from 0.75 Ma
to 3.02 Ma; Figure 2 and Figure S3.1). The next split separated the
ancestor of P. borbae from the ancestor of all subspecies of P. ni-
gromaculata clade around 1.2  Ma (0.51  Ma–­1.95  Ma). Then, P. n.
CARNEIRO et al. |
      5

ustulata diverged from P. n. erythroptera (0.8 Ma, 0.39 Ma–­1.04 Ma).
Finally, P. n. nigromaculata diverged from the ancestor of P. n. bowm-
ani–­P. n. confinis–­P. n. paraensis around 0.6  Ma (0.43–­0.86  Ma), P.
n. bowmani split from the ancestor of P. n. confinis–­P. n. paraensis at
0.45 Ma (0.34–­0.66 Ma), and P. n. confinis and P. n. paraensis diverged
at 0.4 Ma (0.19–­0.57 Ma).
possible combinations. However, these results are more realistic and
free from previous constraints that could bias biogeographical anal-
ysis. The DIVALIKE model suggests a scenario in which the lineages
of Phlegopsis result from genetic divergence due to the successive
subdivision of the populations of an immediate common ancestor
by vicariance with a few cases of sympatry between lineages due to
post-­speciation dispersal events (Figure 2).

3.4  |  Biogeographical analysis

Of the six biogeographical models evaluated, the best fit to our
dataset pertained to +J models (Appendix S3). All the +J models
show similar values (Table 1). Nevertheless, the +J versions of the
different models generated by BioGeoBEARS are doubtfully ap-
plied to non-­island groups and can lead to unrealistic results (Ree
& Sanmartín, 2018). Thus, we chose the DIVALIKE model, which is
the best fit for our data without the ‘+J' component (Figure 2). The
pie charts have multiple uncertainties that reflect the complexity of
the group's biogeographical pattern and the way we implemented
the analysis by allowing the software to search the probabilities for
all eight defined areas without restrictions. This approach gener-
ates less conclusive results mainly in the old nodes due to the many
3.5  |  Population genetics and
historical demography
The mtDNA or nuclear markers found no shared haplotypes among
the nine Phlegopsis lineages (Figure 3a). Gene flow analyses contrast-
ing only Phlegopsis lineages potentially in contact across riverine bar-
riers detected migration rates not statistically different from zero
(Table S2.5 in Appendix S2), indicating strong genetic isolation.
The P. n. nigromaculata clusters detected by BAPS were not the
same recovered by phylogenetic analyses. BAPS separated P. n. ni-
gromaculata into three lineages and not five, as the concatenated
tree. The BAPS analysis recovered an admixture event involving P. n.
nigromaculata A and P. n. bowmani (Figure 3b), as the migrations tests

NPIMJA P. e. erythroptera
IMJAIN
NPIMIN
NPIMJAIN
BioGeoBEARS IN P. e. ustulata A
Model: DIVALIKE
8 areas max.
Atlantic d (dispersal)=0.0713; IN P. e. ustulata B
e (extinction)=0;
Ocean

j (founder)=0;
LnL=−23.98
RO P. borbae

NPINROTAXIBE
ROTAXIBE INRO NPIN P. n. nigromaculata A
RO NPINRO NPRO

RO P. n. nigromaculata B
INROTAXIBE
Imeri NPINROTAXIBE NPROTAXIBE
Napo
Jaú Belém
TA P. n. bowmani

Inambari
Tapajós
Xingu TAXIBE XI P. n. confinis
Rondônia
XIBE
BE P. n. paraensis

1.5 1.0 0.5 0 Mya

F I G U R E 2  Biogeographical history for the Phlegopsis antbirds generated by BioGeoBEARS. The best-­fit model without J for our
reconstruction was DIVALIKE (ln L = −23.97, AIC = 51.96; see text for details). Colours represent the current distribution of taxa and
subclades. Node pie charts represent the likelihoods of ancestral states. Uncertainty in ancestral range reconstruction is shown where
distributions with <5% probability of occurrence are combined into white portions in pie charts
 |
6      CARNEIRO et al.

TA B L E 1  Models, parameters and scores from each of the analyses in BioGeoBEARS. Dispersal (d), extinction (e), founder (J), values of
log-­likelihood (ln L), Akaike information criterion (AIC), ΔAIC value and Akaike weight (ωi)

Rank Model Parameters d e j Ln L AIC ΔAIC ωi

1 DIVALIKE+J 3 0.0259 1.00e-­12 0.212 −21.16 48.33 0 5.57e-­01

2 BAYAREALIKE+J 3 0. 0165 1.00e-­07 0.318 −22.24 50.49 2.16 1.89e-­01
3 DEC + J 3 0.0215 1.00e-­12 0.367 −22.39 50.79 2.46 1.62e-­01
4 DIVALIKE 2 0.0712 1.00e-­12 0 −23.97 51.96 3.63 9.07e-­02
5 DEC 2 0.1155 3.44e-­01 0 −29.74 63.49 15.16 2.84e-­0 4
6 BAYAREALIKE 2 0.2238 1.8372 0 −31.93 67.87 19.54 3.18e-­05

(a)

(b)

F I G U R E 3  (a) Median-­joining haplotype networks estimated for each sequenced gene. Cyt b, 52 individuals, 453 bp; ND2, 49 individuals,
906 bp; COI, 52 individuals, 559 bp; and bf7, 52 individuals, 853 bp; (b) population clusters defined by the Bayesian analysis of population
structure (BAPS) are represented by thick black lines. Colours represent the populations recovered by phylogenetic analyses (see text for
details). Each bar corresponds to an individual (code and colours follow Figure 1)

were not statistically significant. This result may indicate retention
of ancestral polymorphism, but a contact at the southern edge of
the Amazon cannot be ruled out, as recovered by Weir et al. (2015)
and Cronemberger et al. (2020) and Dantas et al. (2021). Regarding
P. erythroptera, the results agreed with the phylogenetic analyses,
except for an additional separation within P. erythroptera (individual
H5, Figure 3b).
The EBSP analyses indicated increasing population sizes for
most lineages, except P. erythroptera (Figure  4). There is evidence
of gradual population growth in the last 50,000–­500,000 years,
with P. n. nigromaculata B and P. borbae exhibiting the sharpest in-
crease among all populations (Figure  4). P. erythroptera showed no
significant deviations from the null hypothesis of neutrality and con-
stant population size for any marker, while P. ustulata had significant
 CARNEIRO et al.

Phlegopsis nigromaculata paraensis Phlegopsis nigromaculata confinis Phlegopsis nigromaculata bowmani Phlegopsis nigromaculata A

3.5

3.0
4

3.0

2.5
2.5
3

2.0
2.0
2

1.5
2

1.5

1.0

Population size scalar

Population size scalar
Population size scalar
Population size scalar

1.0
1

0.5
0.5
0
0

0.0
0.0
0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.00 0.05 0.10 0.15 0.20 0.25 0.0 0.1 0.2 0.3 0.4

Time (M.y.) Time (M.y.) Time (M.y.) Time (M.y.)

Phlegopsis nigromaculata B Phlegopsis erythroptera erythroptera Phlegopsis borbae

Phlegopsis erythroptera ustulata A

6
4

2.5

5
4
3

2.0

4
3

3
1.5
2

2
1.0

Population size scalar

Population size scalar
Population size scalar

Population size scalar

1

1
0.5

0
0

0.0

0
0.0 0.2 0.4 0.6 0.8 1.0 1.2 0.0 0.5 1.0 1.5 2.0 0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
0.0 0.2 0.4 0.6 0.8 1.0 1.2
Time (M.y.) Time (M.y.) Time (M.y.)
Time (M.y.)

F I G U R E 4  Historical demographic inferred through extended Bayesian skyline plots based on mtDNA and nuclear sequence data. Dashed lines represent median values, while the solid lines
delimiting the grey area correspond to 95% confidence intervals. The X-­axis corresponds to time in million years before present. The Y-­axis represents Nₑτ in a logarithmic scale
|
      7
 |
8      CARNEIRO et al.
deviations only for ND2. P. borbae and all lineages classified under P.
nigromaculata, except P. nigromaculata A, showed expanding popula-
tions for at least one locus (Table S2.4 in Appendix S2). However, our
demographic and population results suggest a trend and should be
analysed with caution due to the relatively low number of localities
sampled from each population.
4  |  D I S C U S S I O N
We used genetic analyses at both phylogeographical and phyloge-
netic levels to reconstruct the biogeographical history of Phlegopsis.
Our results showed that (1) Phlegopsis comprises nine well-­marked
lineages associated with Amazonian areas of endemism; (2) most
of the diversification in this genus occurred during the Quaternary;
(3) vicariance is the most critical biogeographical mechanism driv-
ing the history of this group; (4) two lineages are expanding their
ranges, with one of them (P. n. nigromaculata A) crossing the bound-
aries of areas of endemism. Altogether, these four findings shed
light on some important and hitherto underappreciated aspects of
Amazonian biogeography.
4.1  |  Phlegopsis has nine well-­marked lineages
associated with areas of endemism
We found that Phlegopsis has at least nine genetically well-­marked
lineages with no evidence of gene flow between them, with two ex-
ceptions (P. erythroptera and P. n. nigromaculata A; Figure 2), each is
restricted to one area of endemism. This general pattern is similar to
several other forest groups endemic to the region (da Silva et al., 2002;
da Silva & Oren,  1996; Fernandes et al.,  2014; Ribas et al.,  2012;
Santana et al.,  2020) and reinforces the hypothesis advanced by
Wallace (1852) that the areas of endemism delimited by some of the
longest and widest of the region's rivers are a valid and useful frame-
work upon which biogeographical hypotheses can be proposed and
tested (Bates, 2001; Cracraft, 1985; da Silva et al., 2002; da Silva &
Garda, 2010; da Silva & Oren, 1996; Ribas et al., 2012). However, we
found that two individuals of P. erythroptera (H4 and H5) collected in
the same locality on the east bank of the middle-­upper Negro River
showed marked differences in mtDNA. This piece of information indi-
cates the possibility of gene flow across the river, an unexpected find-
ing for a rainforest understorey antbird (Burney & Brumfield, 2009;
Claramunt et al., 2012; Smith et al., 2014). The gene flow in erythrop-
tera (H4 and H5) may be related to changes in the main channel of the
Negro River (Cremon et al., 2016).
4.2  |  The origin and diversification of Phlegopsis
occurred during the Quaternary
Despite their genetic distinctness and lack of gene flow, the small
genetic distances between lineages, even within the mitochondrial
haplotype networks, indicated that diversification of crown bare-­
eyes is relatively recent, dating to less than ~2.0 million years ago
(Ma). However, the dates retrieved by us in the current study are
quite different from those recovered by previous studies for
Phlegopsis (Harvey et al., 2020; Silva et al., 2019). The dataset used
here is virtually the same used in Silva et al. (2019) and the difference
between the two estimates is undoubtedly related to the choice of
the markers used in the calibration of the molecular clock (less than
half of the Cytb in Silva et al. (2019) against the complete ND2 in the
present study). Our option here was to minimize potential problems
with missing data, which are known to impact the time estimation
(Zheng & Wiens, 2015).
Regarding the date estimation by Harvey et al.  (2020) for the
clade, the differences are likely related to the phylogenetic scale
of the two studies and to the different taxa included. The study by
Harvey et al. (2020) included only one individual of each recognized
species and, as a consequence, did not consider large genetic vari-
ation that exists within each taxon. In general, the ages retrieved
in our estimate for Phlegopsis are similar to those found by Ribas
et al.  (2018), for Rhegmatorhina, a phylogenetic and ecologically
close group to Phlegopsis, and to most of the dates proposed for pas-
serines in the Amazon basin (Silva et al., 2019).
The haplotype networks showed a structure in mitochondrial
DNA but not in the nuclear marker, consistent with their relative co-
alescent times (Hung et al., 2017; Zink & Barrowclough, 2008). Thus,
our results are consistent with those found in other Amazonian
clades (Hylopezus, Myrmothera, Psophia and Rhegmatorhina), in
which a nuclear marker was only capable of resolving the oldest
divergences (Carneiro, Bravo, et al., 2018; Ribas et al., 2012; Ribas
et al., 2018). The nuclear marker also indicated a recent divergence
among borbae and the ancestor of nigromaculata-­bowmani-­confinis-­
paraensis compared to the distance separating the ancestor of this
group from the ancestor of erythroptera-­ustulata. Phlegopsis lineages
are common monogamous understorey birds and are expected to
have a large effective population sizes (Ne), relative to bigger spe-
cies, thus further suggesting that nuclear loci would not be pre-
dicted to coalesce in Phlegopsis over this short time-­period (Ribas
et al., 2018; Willis & Oniki, 1978). Thus, estimating age and popula-
tion size using mitochondrial DNA is more appropriate than a single
or a few nuclear markers for recovering evolutionary relationships
within species complex at this taxonomic scale (Ribas et al., 2018).
Migration after divergence was not tested and if it occurred, it may
have affected the time estimates produced by the species tree anal-
ysis which would tend to be more recent. The *BEAST analysis does
not consider the possibility of migration after isolation, considering
all similarities among species as ancestral polymorphism (Heled &
Drummond, 2010).
Quaternary speciation in the Amazon is usually interpreted as
an outcome of the large-­scale climatic-­vegetational changes caused
by the Milankovitch cycles (Haffer, 1987; Haffer, 1993). That is the
foundation of the refuge model (Haffer, 1969), which has been the
dominant paradigm to explain avian diversification in the region in
the last decades (Silva et al.,  2019). However, the original refuge
CARNEIRO et al.
model is based on the assumption that the region's forests were re-
placed by open vegetations across the region during glacial periods
(Rocha & Kaefer,  2019; da Silva & Garda,  2010). According to the
model, speciation events, particularly those that occurred during the
Quaternary, would be directly related to climate and vegetational
changes caused by glacial cycles (Arruda et al., 2018; Haffer, 1969).
However, several studies have documented an intense geological
dynamic in the region during the Quaternary as a consequence of
neotectonics (Latrubesse & Rancy,  2000; Rossetti,  2014), changes
in sea level (Hoorn et al.,  2016; Irion & Kalliola,  2010) and fluvial
dynamics (Räsänen et al.,  1987; Rossetti,  2014). Furthermore, pa-
laeoriver dynamics that do not correspond to current river config-
urations could also be related to diversification events in Amazon
basin if they acted as semipermeable dispersal barriers through time
(Fernandes et al., 2014; Silva et al., 2019; Weir et al., 2015). Finally,
all palaeoecological data assembled to date have failed to show a
large-­scale replacement of forests by open vegetation across the
entire region during the glacial periods (e.g. Irion & Kalliola,  2010;
Kastner & Goni, 2003). In fact, such studies show only limited vege-
tation changes along the transition between the Amazon and other
ecological regions as well as around the existing Amazonian savanna
patches (Irion & Kalliola,  2010). In conclusion, there is no palaeo-
ecological evidence to assume that Quaternary speciation events in
the Amazon are necessarily a consequence of vegetation changes
caused by global climate changes.
4.3  |  Vicariance is the most important
biogeographical process factor driving the
history of Phlegopsis
Our results showed a complex biogeographical history for the lin-
eages of Phlegopsis that includes both vicariance and dispersal
processes, but that vicariance was the dominant one. Unlike other
biogeographical studies in Amazon basin (e.g. Carneiro, Bravo,
et al., 2018; Ferreira et al., 2017; Silva et al., 2019), we did not re-
strict the maximum number of areas because there is no evidence
to safely limit the distributions of ancestral nodes to a specific area
of endemism or group of areas of endemism. In fact, it is perfectly
plausible that the ancestor of Phlegopsis was distributed throughout
most of the current ranges of its descendant species. Furthermore,
maintaining the maximum number of areas does not restrict models
with fewer areas, but limiting the maximum number could prevent
the search for vicariant models that include more areas.
Vicariant events within Phlegopsis occurred mainly along the
boundaries of the eight areas of endemism, indicating that such
events can be associated with the largest and widest rivers of the
region. The vicariant event that separated the P. ustulata–­P. eryth-
roptera clade from all other lineages is associated with the Madeira,
while the divergence between P. ustulata and P. erythroptera is associ-
ated with the upper Amazon/Solimões River. In eastern Amazon, the
split between P. n. nigromaculata and P. n. bowmani–­P. n. confinis–­P.
n. paraensis is associated with the Tapajós, separating P. n. bowmani
|
      9
and P. n. confinis-­P. n. paraensis is linked to the Xingu, and the sep-
aration between P. n. confinis and P. n. paraensis with the Tocantins.
In addition to vicariant events between areas of endemism, we also
identified a split (separating P. borbae from P. n. nigromaculata–­P. n.
bowmani–­P. n. confinis–­P. n. paraensis) within the area of endemism
Rondônia. P. borbae and P. n. nigromaculata B are found together in a
few sites with the area of endemism Rondônia, but the extension of
this sympatry zone needs to be determined. In general, our results
indicate that the vicariant events that shaped the evolutionary his-
tory of Phlegopsis started along the Madeira drainage and advanced
progressively towards west and east. This west–­east pattern was
also identified for other groups of terrestrial vertebrates such as pri-
mates (Carneiro, Sampaio, et al., 2018; Lynch-­Alfaro et al., 2014), but
has been especially reported for birds (Azuaje-­Rodríguez et al., 2020;
Ferreira et al.,  2017; Ribas et al.,  2012; Santana et al.,  2020; Silva
et al., 2019).
The vicariant events within Rondônia are consistent with
the patterns found in other groups of vertebrates, such as birds
(Fernandes et al.,  2014; Ferreira et al.,  2017; Ribas et al.,  2018;
Santana et al.,  2020; Willis,  1969) and tamarins of the genus Mico
(Roosmalen et al.,  2000), which show several speciation events
within this area of endemism. These cases suggest that Rondônia is
a composite area of endemism, with a complex and dynamic biolog-
ical history that requires further investigation (Bates, 2001; da Silva
et al., 2005; da Silva & Oren, 1996; Ferreira et al., 2017). This area
of endemism is located in the contact zone between the old terrains
associated with the Pre-­C ambrian Brazilian plateau and the most re-
cent Tertiary and Quaternary terrains of western Amazon (da Silva
et al., 2005), suggesting that speciation events within the region are
driven by geological events (Silva et al., 2019). Recent studies show-
ing a particular geological dynamic and several drainage anomalies
within this area of endemism support this hypothesis (Hayakawa &
Rossetti, 2015; Latrubesse, 2002).
4.4  |  One lineage (nigromaculata) expanded its
range to other areas of endemism
Although vicariance was the dominant process shaping the cur-
rent distribution of the Phlegopsis lineages, our results support the
hypothesis that some lineages are expanding their ranges. EBSP
analyses suggest that P. n. bowmani and P. n. nigromaculata A and B
have expanded their ranges while the other lineages remained sta-
ble (Figure 4). P. n. bowmani is apparently expanding its range within
one area of endemism. In contrast, P. n. nigromaculata may have
dispersed first within Rondônia and became sympatric with borbae
(Willis, 1982). Then, it may have crossed the Madeira and colonized
most Inambari and Napo becoming sympatric with P. e. ustulata.
There are three general dispersal models to explain the range ex-
pansion of one lineage (review in Morrone, 2009): (1) jump disper-
sal, which are random movements of organisms across barriers that
allow the establishment of species in very distant areas, (2) diffusion,
defined as a gradual and fast range expansion through movements
 |
10      CARNEIRO et al.
of populations crossing adjacent habitats over several generations
without evolutionary changes, and (3) secular migration, which is
similar to diffusion, but slower and with evolutionary changes. Of
these three models, jump dispersal is unlikely to P. n. nigromaculata
because of its ecological traits. Between diffusion and secular mi-
gration models, our results support the latter. The main reason is
that populations of P. n. nigromaculata in western Amazon (lineage
A) show a slight but consistent genetic difference in relation to its
putative source population in Rondônia (lineage B).
Despite its limited dispersal potential, our results show that some
P. n. nigromaculata populations expanded their ranges in the last
150,000–­200,000 years (Figure 4). What were the underlying mecha-
nisms that could enable such expansion? Based on the current knowl-
edge in the ecology and behaviour of the lineages of Phlegopsis, we
suggest that the range expansion of P. n. nigromaculata across western
Amazon was enabled by two mechanisms: (1) the ability of P. n. nigro-
maculata to live in seasonally flooded várzea forests and (2) passive
dispersal across rivers due to fluvial dynamics (Bicudo et al.,  2019;
Pupim et al., 2019; Rossetti, 2014; Sousa-­Neves et al., 2013).
The ability to live in várzea forests is a recent adaptation within
bare-­eye antbirds because it is restricted to the clade P. n. nigromac-
ulata–­P. n. bowmani–­P. n. confinis–­P. n. paraensis. Across most of their
ranges, lineages of this clade inhabit both terra firme and season-
ally flooded (várzea) forests (Willis,  1984). However, in the western
Amazon, P. n. nigromaculata is found only in várzea forests and the tran-
sition of this forest to terra firme forests (Zimmer & Isler, 2020). In con-
trast, P. e. ustulata and P. e. erythroptera are associated mostly with terra
firme forests (Zimmer & Isler, 2020). Thus, P. n. nigromaculata is rarely
found in the same habitat as P. e. ustulata and P. e. erythroptera, even
though their ranges overlap. In the few localities where P. e. ustulata or
P. e. erythroptera meet with P. n. nigromaculata over army-­ant swarms,
P. n. nigromaculata occupies a subordinate position (Willis, 1982). Thus,
all evidence available suggests that P. n. nigromaculata expanded its
range across western Amazon by occupying a habitat that had never
been used by the lineages of Phlegopsis endemic to that large region.
This ecological plasticity could explain the fact that P. n. nigromaculata
lineages, particularly in the east, show a distribution pattern different
from that recovered for terra firme species (Ribas et al., 2012), and also
different from the patterns that have recently been recovered for sea-
sonally flooded forests species (Choueri et al., 2017; Thom et al., 2020).
Várzea forests are associated with white-­water rivers, which re-
ceive their names because they transport large quantities of sediments
generated in the Andes (Sioli, 1984). These rivers are very dynamic and
exhibit frequent lateral migration that transfers lands from one side of
the river to the other (Bicudo et al., 2019; Junk et al., 2011; Räsänen
et al., 1987). Because it is close to the Andes, western Amazon has the
largest density of white-­water rivers than any other Amazonian re-
gion (Junk et al., 2011). In addition, recent studies have demonstrated
that because rivers in western Amazon have high sediment loads, they
experience annual lateral migration rates that are higher than those
of rivers with lower sediment loads in other Amazonian drainages
(Constantine et al.,  2014). This geomorphological process, in turn,
can lead to the ‘passive dispersal’ of understorey birds with limited
dispersal ability across large rivers (Crouch et al., 2019). Therefore, P. n.
nigromaculata expanded its range across western Amazon by crossing
the large rivers of the region via ‘passive dispersal’ associated with the
fluvial dynamics of the white-­water rivers.
4.5  |  Lessons for Amazonian biogeography
In general, our results reinforce the notion that continental biotas are
assembled by dispersal events, followed by vicariance events, fol-
lowed by new dispersal events (Cracraft, 1994). Because the diversifi-
cation of Phlegopsis is recent, we were able to reveal some elements of
its biogeographical history. Similar to other studies (e.g. Bates, 2001;
da Silva & Oren, 1996; Ribas et al., 2012), we found that vicariance
was the most important event shaping the distribution and differ-
entiation within Phlegopsis. However, we have also identified that
secular migration can cause sympatry between closely related spe-
cies and thus increase the species diversity of areas of endemism over
time (da Silva et al., 2005; D'Horta et al., 2013; Soares et al., 2019;
Santana et al., 2020). Such dispersal events are not random, but they
are constrained by both the characteristics of the lineage that is ex-
panding its range as well as the characteristics of the places upon
which the lineage is expanding (Cracraft, 1994; Crouch et al., 2019). In
the case of Phlegopsis, the successful expansion of P. n. nigromaculata
westwards is a consequence of its ability to survive in várzea forests
as well as the influence of the region's intense fluvial dynamics that
enables ‘passive’ dispersal across large rivers. Although most of the
diversification of Phlegopsis occurred during the Quaternary, there
is no reason to assume that such processes were driven by climatic-­
vegetation changes associated with the Milankovitch cycles such as
proposed by the refuge model (Haffer,  1993). Because several of
the patterns that we described are also shared with other clades,
we believe that, complex palaeoecological history notwithstanding,
the biogeographical patterns of present-­day organisms can be organ-
ized out around a few general patterns that reveal the most general
chapters of the history of Amazonian biota during the Quaternary
(Bates, 2001; da Silva & Oren, 1996; Ribas et al., 2012).
AC K N OW L E D G E M E N T S
We thank the curator and curatorial assistants of the Museu
Paraense Emílio Goeldi collection for allowing us to sequence sam-
ples under their care. Specimens sequenced in this study were ob-
tained along several decades through collecting permits issued by
national environmental agency of Brazil. L.S.C. was supported by
FAPESPA fellowship during the study (FAPESPA grant #021/2016).
J. M. C. S. is supported by the University of Miami and the Swift
Action Fund. New collection permits from the Conselho Nacional de
Desenvolvimento Tecnológico e Científico—­CNPq and permission to
collect in protected areas from the Instituto Chico Mendes—­ICMBio
are also gratefully acknowledged.
C O N FL I C T O F I N T E R E S T
The authors declare no conflict of interest.
CARNEIRO et al.
DATA AVA I L A B I L I T Y S TAT E M E N T
All DNA sequences generated for this study are available from
GenBank: https://www.ncbi.nlm.nih.gov/genbank/. Additional in-
formation and datasets, including newick trees and scripts used in
ancestral range estimation are available from Dryad: https://doi.
org/10.5061/dryad.3bk3j9kmw.
ORCID
Lincoln Carneiro  https://orcid.org/0000-0002-7680-2291
Tibério C. T. Burlamaqui  https://orcid.org/0000-0002-0264-5780
Alexandre Aleixo  https://orcid.org/0000-0002-7816-9725
José Maria Cardoso Da Silva  https://orcid.org/0000-0002-7229-6694
REFERENCES
Antonelli, A., Zizka, A., Carvalho, F. A., Scharn, R., Bacon, C. D., Silvestro,
D., & Condamine, F. L. (2018). Amazonia is the primary source of neo-
tropical biodiversity. Proceedings of the National Academy of Sciences,
115(23), 6034–­6039. https://doi.org/10.1073/pnas.17138​19115
Arruda, D. M., Schaefer, C. E. G. R., Fonseca, R. S., Solar, R. R. C., &
Fernandes-­Filho, E. I. (2018). Vegetation cover of Brazil in the last
21 ka: New insights into the Amazonian refugia and Pleistocenic arc
hypotheses. Global Ecology and Biogeography, 27(1), 47–­56. https://
doi.org/10.1111/geb.12646
Azuaje-­Rodríguez, R. A., Weckstein, J. D., Dispoto, J. H., Patel, S.,
Cacioppo, J. A., Bates, J. M., Silva, S. M., & Aleixo, A. (2020). Molecular
systematics of the Amazonian endemic genus Hylexetastes (Aves:
Dendrocolaptidae): Taxonomic and conservation implications. Ibis,
162(1), 119–­136. https://doi.org/10.1111/ibi.12693
Bandelt, H.-­J., Forster, P., & Röhl, A. (1999). Median-­joining networks for
inferring intraspecific phylogenies. Molecular Biology and Evolution,
16(1), 37–­48. https://doi.org/10.1146/annur​ev.es.18.110187.002421
Bates, J. M. (2001). Avian diversification in Amazonia: Evidence for his-
torical complexity and a vicariance model for a basic pattern of di-
versification. In I. Viera, M. A. D'incão, J. M. C. Silva, & D. Oren
(Eds.), Diversidade Biológica e Cultural da Amazônia (pp. 119–­137).
Museu Paraense Emílio Goeldi.
Bicudo, T. C., Sacek, V., de Almeida, R. P., Bates, J. M., & Ribas, C. C.
(2019). Andean tectonics and mantle dynamics as a pervasive in-
fluence on Amazonian ecosystem. Scientific Reports, 9(1), 1–­11.
https://doi.org/10.1038/s4159​8-­019-­53465​-­y
Bird, J. P., Martin, R., Akçakaya, H. R., Gilroy, J., Burfield, I. J., Garnett,
S. T., Symes, A., Taylor, J., Şekercioğlu, Ç. H., & Butchart, S. H. M.
(2020). Generation lengths of the world's birds and their implica-
tions for extinction risk. Conservation Biology, 34(5), 1252–­1261.
https://doi.org/10.1111/cobi.13486
Borges, S. H., & Silva, J. M. C. (2012). A new area of endemism for
Amazonian birds in the Rio Negro Basin. The Wilson Journal of
Ornithology, 124(1), 15–­23. https://doi.org/10.1676/07-­103.1
Bouckaert, R., Vaughan, T. G., Barido-­S ottani, J., Duchêne, S.,
Fourment, M., Gavryushkina, A., Heled, J., Jones, G., Kühnert, D.,
De Maio, N., Matschiner, M., Mendes, F. K., Müller, N. F., Ogilvie,
H. A., Du Plessis, L., Popinga, A., Rambaut, A., Rasmussen, D.,
Siveroni, I., … Drummond, A. J. (2019). BEAST 2.5: An advanced
software platform for Bayesian evolutionary analysis. PLoS
Computational Biology, 15(4), 1–­28. https://doi.org/10.1371/journ​
al.​p cbi.1006650
Bruen, T. C., Philippe, H., & Bryant, D. (2006). A simple and robust sta-
tistical test for detecting the presence of recombination. Genetics,
172(4), 2665–­2681. https://doi.org/10.1534/genet​ics.​105.048975
Burney, C. W., & Brumfield, R. T. (2009). Ecology predicts levels of ge-
netic differentiation in neotropical birds. The American Naturalist,
174(3), 358–­368. https://doi.org/10.1086/603613
|
      11
Carneiro, J., Sampaio, I., Silva-­júnior, J. D. S., Farias, I., Hrbek, T., Pissinatti,
A., Silva, R., Martins-­junior, A., Boubli, J., Ferrari, S. F., & Schneider,
H. (2018). Phylogeny, molecular dating and zoogeographic his-
tory of the titi monkeys (Callicebus, Pitheciidae ) of eastern Brazil.
Molecular Phylogenetics and Evolution, 124, 10–­15. https://doi.
org/10.1016/j.ympev.2018.03.001
Carneiro, L., Bravo, G. A., Aristizábal, N., Cuervo, A. M., & Aleixo, A.
(2018). Molecular systematics and biogeography of lowland
antpittas (Aves, Grallariidae): The role of vicariance and disper-
sal in the diversification of a widespread neotropical lineage.
Molecular Phylogenetics and Evolution, 120, 375–­389. https://doi.
org/10.1016/j.ympev.2017.11.019
Chesser, R. T., & Zink, R. M. (1994). Modes of speciation in birds -­ a
test of Lynch'S method. Evolution, 48(2), 490–­497. https://doi.
org/10.2307/2410107
Choueri, É. L., Gubili, C., Borges, S. H., Thom, G., Sawakuchi, A. O.,
Soares, E. A. A., & Ribas, C. C. (2017). Phylogeography and pop-
ulation dynamics of antbirds (Thamnophilidae) from Amazonian
fluvial islands. Journal of Biogeography, 44, 2284–­2294. https://doi.
org/10.1111/jbi.13042
Claramunt, S., Derryberry, E. P., Remsen, J. V., Jr., & Brumfield, R. T.
(2012). High dispersal ability inhibits speciation in a continen-
tal radiation of passerine birds. Proceedings of the Royal Society B:
Biological Sciences, 279, 1567–­1574.
Constantine, J. A., Dunne, T., Ahmed, J., Legleiter, C., & Lazarus, E. D.
(2014). Sediment supply as a driver of river meandering and flood-
plain evolution in the Amazon Basin. Nature Geoscience, 7(12), 899–­
903. https://doi.org/10.1038/ngeo2282
Corander, J., Marttinen, P., Sirén, J., & Tang, J. (2008). Enhanced
Bayesian Modelling in BAPS Software for Learning Genetic
Structures of Populations. BMC Bioinformatics, 9, 539. https://doi.
org/10.1186/1471-­2105-­9-­539.
Cracraft, J. (1985). Historical biogeography and patterns of differenti-
ation within the south American avifauna: Areas of endemism.
Ornithological Monographs, 36, 49–­8 4.
Cracraft, J. (1994). Species diversity, biogeography, and the evolution of
biotas. Integrative and Comparative Biology, 34(1), 33–­47. https://
doi.org/10.1093/icb/34.1.33
Cremon, É. H., Rossetti, D. D. F., Sawakuchi, A. D. O., & Cohen, M. C. L.
(2016). The role of tectonics and climate in the late quaternary evo-
lution of a northern Amazonian river. Geomorphology, 271, 22–­39.
https://doi.org/10.1016/j.geomo​rph.2016.07.030
Cronemberger, Á. A., Aleixo, A., Mikkelsen, E. K., & Weir, J. T. (2020).
Postzygotic isolation drives genomic speciation between highly
cryptic Hypocnemis antbirds from Amazonia. Evolution, 74(11),
2512–­2525. https://doi.org/10.1111/evo.14103
Crouch, N. M. A., Capurucho, J. M. G., Hackett, S. J., & Bates, J. M. (2019).
Evaluating the contribution of dispersal to community structure in
neotropical passerine birds. Ecography, 42(2), 390–­399. https://doi.
org/10.1111/ecog.03927
Dantas, S. M., Weckstein, J. D., Bates, J., Oliveira, J. N., Catanach, T. A.,
& Aleixo, A. (2021). Multi-­character taxonomic review, systemat-
ics, and biogeography of the black-­c apped/tawny-­bellied screech
owl (Megascops atricapilla-­M. watsonii) complex (Aves: Strigidae).
Zootaxa, 4949(3), 401–­4 44.
da Silva, J. M. C., & Garda, A. (2010). Padrões e Processos Biogeográficos
na Amazônia. In C. J. B. C. Carvalho & E. A. B. Almeida (Eds.),
Biogeografia da América do Sul: Padrões e Processos. Roca.
da Silva, J. M. C., Novaes, F. C., & Oren., D. C. (2002). Differentiation of
Xiphocolaptes (Dendrocolaptidae) across the river Xingu, Brazilian
Amazonia: Recognition of a new phylogenetic species and biogeo-
graphic implications. Bulletin of the British Ornithologists' Club, 122,
185–­194.
da Silva, J. M. C., & Oren, D. C. (1996). Application of parsimony anal-
ysis of endemicity in Amazonian biogeography: An example with
 |
12      CARNEIRO et al.
primates. Biological Journal of the Linnean Society, 59(4), 427–­437.
https://doi.org/10.1006/bijl.1996.0073
da Silva, J. M. C., Rylands, A. B., Da Fonseca, G., & a B. (2005). The fate
of the Amazonian areas of endemism. Conservation Biology, 19(3),
689–­694. https://doi.org/10.1111/j.1523-­1739.2005.00705.x
D'Horta, F. M., Cuervo, A. M., Ribas, C. C., Brumfield, R. T., & Miyaki, C.
Y. (2013). Phylogeny and comparative phylogeography of Sclerurus
(Aves: Furnariidae) reveal constant and cryptic diversification in
an old radiation of rain forest understorey specialists. Journal of
Biogeography, 40(1), 37–­49. https://doi.org/10.1111/j.1365-­2699.​
2012.02760.x
Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006).
Relaxed phylogenetics and dating with confidence. PLoS Biology,
4(5), e88.
Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary
analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
Fernandes, A. M., Wink, M., Sardelli, C. H., & Aleixo, A. (2014). Multiple
speciation across the Andes and throughout Amazonia: The case
of the spot-­backed antbird species complex (Hylophylax naevius/​
Hylophylax naevioides). Journal of Biogeography, 41(6), 1094–­1104.
https://doi.org/10.1111/jbi.12277
Ferreira, M., Aleixo, A., Ribas, C. C., & Santos, M. P. D. (2017). Biogeography
of the neotropical genus Malacoptila (Aves: Bucconidae): The influ-
ence of the Andean orogeny, Amazonian drainage evolution and
palaeoclimate. Journal of Biogeography, 44(4), 748–­759. https://doi.
org/10.1111/jbi.12888
Fu, Y. X. (1997). Statistical tests of neutrality of mutations against pop-
ulation growth, hitchhiking and background selection. Genetics,
147(2), 915–­925.
Haffer, J. (1969). Speciation in Amazonian forest birds. Science, 165, 131–­137.
Haffer, J. (1974). Avian speciation in tropical South America (Vol. 14, pp.
1–­390). Nuttall Ornithol. Club.
Haffer, J. (1987). Biogeography of neotropical birds. In T. C. Whitmore
& G. T. Prance (Eds.), Biogeography and quaternary history in tropical
America (pp. 105–­150). Claredon Press.
Haffer, J. (1992). On the “river effect” in some forest birds of southern
Amazonia. Bol. Mus. Para. Emílio Goeldi. Série Zoologia, 8(1), 217–­246.
Haffer, J. (1993). Time's cycle and time's arrow in the history of Amazonia.
Biogeographica, 69, 15–­45.
Haffer, J. (2008). Hypotheses to explain the origin of species in Amazonia.
Brazilian Journal of Biology, 68(4), 917–­947.
Harvey, M. G., Bravo, G. A., Claramunt, S., Cuervo, A. M., Derryberry,
G. E., Battilana, J., Seeholzer, G. F., Shearer, M. J., O'Meara, B.
C., Faircloth, B. C., Edwards, S. V., Pérez-­Emán, J., Moyle, R. G.,
Sheldon, F. H., Aleixo, A., Smith, B. T., Chesser, R. T., Silveira, L. F.,
Cracraft, J., … Derryberry, E. P. (2020). The evolution of a tropi-
cal biodiversity hotspot. Science, 370, 1343–­1348. https://doi.
org/10.1126/scien​ce.aaz6970
Hasegawa, M., Kishino, H., &Yano, T. (1985). Dating of the human-­ape split-
ting by a molecular clock of mitochondrial DNA. Journal of Molecular
Evolution, 22(2), 160–­174. https://doi.org/10.1007/BF021​01694
Hayakawa, E. H., & Rossetti, D. F. (2015). Late quaternary dynamics in the
Madeira river basin, southern Amazonia (Brazil), as revealed by pa-
leomorphological analysis. Anais Da Academia Brasileira de Ciencias,
87(1), 29–­50. https://doi.org/10.1590/0001-­37652​01520​130506
Heled, J., & Drummond, A. J. (2010). Bayesian inference of species trees
from multilocus data. Molecular Biology and Evolution, 27(3), 570–­
580. https://doi.org/10.1093/molbe​v/msp274
Hey, J. (2010). Isolation with migration models for more than two popu-
lations. Molecular Biology and Evolution, 27(4), 905–­920. https://doi.
org/10.1093/molbe​v/msp296
Hey, J., & Nielsen, R. (2004). Multilocus methods for estimating
­population sizes, migration rates and divergence time, with appli-
cations to the divergence of Drosophila pseudoobscura and D. persi-
milis. Genetics, 167(2), 747–­760. https://doi.org/10.1534/genet​ics.​
103.024182
Hoorn, C., Bogotá-­A , G. R., Romero-­Baez, M., Lammertsma, E. I., Flantua,
S. G. A., Dantas, E. L., Dino, R., do Carmo, D. A., &Chemale JrF.
(2016). The Amazon at sea: Onset and stages of the Amazon River
from a marine record, with special reference to Neogene plant turn-
over in the drainage basin. Global and Planetary Change, 153, 51–­65.
https://doi.org/10.1016/j.glopl​acha.2017.02.005
Hung, C. M., Drovetski, S. V., & Zink, R. M. (2017). The roles of ecol-
ogy, behaviour and effective population size in the evolution of
a community. Molecular Ecology, 26(14), 3775–­3784. https://doi.
org/10.1111/mec.14152
Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks
in evolutionary studies. Molecular Biology and Evolution, 23(2), 254–­
267. https://doi.org/10.1093/molbe​v/msj030
Irion, G., & Kalliola, R. (2010). Long-­term landscape development pro-
cesses in Amazonia. In C. Hoorn & F. Wesselingh (Eds.), Amazonia:
Landscape and species evolution: A look into the past (pp. 185–­197).
Wiley-­Blackwell.
Isler, M. L., Bravo, G. A., & Brumfield, R. T. (2014). Systematics of the
obligate ant-­following clade of antbirds ( Aves: Passeriformes:
Thamnophilidae ). The Wilson Journal of Ornithology, 126(4), 635–­
648. https://doi.org/10.1676/13-­199.1
Junk, W. J., Piedade, M. T. F., Schöngart, J., Cohn-­Haft, M., Adeney, J. M.,
& Wittmann, F. (2011). A classification of major naturally-­occurring
amazonian lowland wetlands. Wetlands, 31(4), 623–­6 40. https://
doi.org/10.1007/s1315​7-­011-­0190-­7
Rocha, D. G. da, & Kaefer, I. L. (2019). What has become of the refugia
hypothesis to explain biological diversity in Amazonia? Ecology and
Evolution, 9(7), 4302–­4309. https://doi.org/10.1002/ece3.5051
Kastner, T. P., & Goni, M. A. (2003). Constancy in the vegetation of
the Amazon Basin during the late Pleistocene: Evidence from
the organic matter composition of Amazon deep sea fan sedi-
ments. Geology, 31(4), 291–­294. https://doi.org/10.1130/0091-­
7613(2003)031<0291:CITVO​T>2.0.CO;2
Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: a novel
method for rapid multiple sequence alignment based on fast Fourier
transform. Nucleic Acids Research, 30(14), 3059–­3 066. https://doi.
org/10.1093/nar/gkf436
Kearse, M., Moir, R., Wilson, A., Stones-­H avas, S., Cheung, M.,
Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C.,
Thierer, T., Ashton, B., Meintjes, P., & Drummond, A. (2012).
Geneious basic: An integrated and extendable desktop software
platform for the organization and analysis of sequence data.
Bioinformatics, 28(12), 1647–­1649. https://doi.org/10.1093/bioin​
forma​t ics/bts199
Kocher, T. D., Thomas, W. K., Meyer, A., Edwards, S. V., Paabo, S.,
Villablanca, F. X., & Wilson, A. C. (1989). Dynamics of mitochon-
drial DNA evolution in animals: Amplification and sequencing with
conserved primers. Proceedings of the National Academy of Sciences
of the United States of America, 86(16), 6196–­6200. https://doi.
org/10.1073/pnas.86.16.6196
Lanfear, R., Calcott, B., Ho, S. Y. W., & Guindon, S. (2012). PartitionFinder:
Combined selection of partitioning schemes and substitution mod-
els for phylogenetic analyses. Molecular Biology and Evolution, 29(6),
1695–­1701.
Latrubesse, E. M. (2002). Evidence of quaternary palaeohydrological
changes in middle Amazonia: The Aripuanã -­Roosevelt and Jiparaná
“fans”. Zeitschrift für Geomorphologie, 129, 61–­72.
Latrubesse, E. M., & Rancy, A. (2000). Neotectonic influence on tropi-
cal rivers of southwestern Amazon during the late quaternary: The
moa and Ipixuna river basins, Brazil. Quaternary International, 72(1),
67–­72. https://doi.org/10.1016/S1040​-­6182(00)00022​-­7
Lerner, H. R. L., Meyer, M., James, H. F., Hofreiter, M., & Fleischer, R.
C. (2011). Report multilocus resolution of phylogeny and times-
cale in the extant adaptive radiation of Hawaiian honeycreepers.
Current Biology, 21(21), 1838–­1844. https://doi.org/10.1016/​
j.cub.2011.09.039
CARNEIRO et al.
Librado, P., & Rozas, J. (2009). DnaSP v5: A software for comprehensive
analysis of DNA polymorphism data. Bioinformatics, 25(11), 1451–­
1452. https://doi.org/10.1093/bioin​forma​tics/btp187
Lynch-­Alfaro, J. W., Boubli, J. P., Paim, F. P., Ribas, C. C., Silva, M. N.,
Messias, M., Rohe, F., Merces, M. P., Silva, J. S., Jr., Silva, C. R.,
Pinho, G. M., Koshkarian, G., Nguyen, M. T., Harada, M. L., Rabelo,
R. M., Queiroz, H. L., Alfaro, M. E., & Farias, I. (2014). Biogeography
of squirrel monkeys ( genus Saimiri ): South-­Central Amazon ori-
gin and rapid pan-­Amazonian diversification of a lowland primate.
Molecular Phylogenetics and Evolution, 82(B), 436–­454. https://doi.
org/10.1016/j.ympev.2014.09.004
Matzke, N. J. (2013). Probabilistic historical biogeography: New models
for founder-­event speciation, imperfect detection, and fossils allow
improved accuracy and model-­testing. Frontiers in Biogeography, 5,
242–­248.
Morrone, J. J. (2009). Evolutionary biogeography: An integrative approach.
Columbia University Press.
Nielsen, R., & Wakeley, J. (2001). Distinguishing migration from isolation:
A Markov chain Monte Carlo approach. Genetics, 158(2), 885–­896.
Phillimore, A. B., Orme, C. D. L., Thomas, G. H., Blackburn, T. M.,
Bennett, P. M., Gaston, K. J., & Owens, I. P. F. (2008). Sympatric
speciation in birds is rare: Insights from range data and sim-
ulations. American Naturalist, 171(5), 646–­657. https://doi.
org/10.1086/587074
Price, T. D., Hooper, D. M., Buchanan, C. D., Johansson, U. S., Tietze,
D. T., Alström, P., Olsson, U., Ghosh-­Harihar, M., Ishtiaq, F., Gupta,
S. K., Martens, J., Harr, B., Singh, P., & Mohan, D. (2014). Niche
filling slows the diversification of Himalayan songbirds. Nature,
509(7499), 222–­225. https://doi.org/10.1038/natur​e13272
Prychitko, T. M., & Moore, W. S. (1997). The utility of DNA sequences
of an intron from the β-­fibrinogen gene in phylogenetic analysis of
woodpeckers (Aves: Picidae). Molecular Phylogenetics and Evolution,
8(2), 193–­204. https://doi.org/10.1006/mpev.1997.0420
Pupim, F. N., Sawakuchi, A. O., Almeida, R. P., Ribas, C. C., Kern,
A. K., Hartmann, G. A., Chiessi, C. M., Tamura, L. N., Mineli, T. D.,
Savian, J. F., Grohmann, C. H., Bertassoli, D. J., Stern, A. G., Cruz,
F. W., & Cracraft, J. (2019). Chronology of Terra Firme forma-
tion in Amazonian lowlands reveals a dynamic quaternary land-
scape. Quaternary Science Reviews, 210, 154–­163. https://doi.
org/10.1016/j.quasc​irev.2019.03.008
Rambaut, A., Suchard, M., Xie, D., & Drummond, A. (2014). Tracer v. 1.6.
Institute of Evolutionary Biology, University of Edinburgh. Available
online at: http://Beast.Bio.Ed.Ac.Uk/Tracer
Ramos-­Onsins, S. E., & Rozas, J. (2002). Statistical properties of new
neutrality tests against population growth. Molecular Biology
and Evolution, 19(12), 2092–­2100. https://doi.org/10.1093/oxfor​d​
jour​nals.​molbev.a004034
Räsänen, M. E., Salo, J. S., & Kalliola, R. J. (1987). Fluvial perturbance in
the western Amazon basin: Regulation by long-­term sub-­Andean
tectonics. Science, 238(4832), 1398–­1401. https://doi.org/10.1126/
scien​ce.238.4832.1398
Ree, R. H., & Sanmartín, I. (2018). Conceptual and statistical problems
with the DEC+J model of founder-­event speciation and its compar-
ison with DEC via model selection. Journal of Biogeography, 45(4),
741–­749. https://doi.org/10.1111/jbi.13173
Ribas, C., Aleixo, A., Nogueira, A. C. R., Miyaki, C. Y., & Cracraft, J.
(2012). A palaeobiogeographic model for biotic diversification
within Amazonia over the past three million years. Proceedings of
the Royal Society B: Biological Sciences, 279(1729), 681–­689. https://
doi.org/10.1098/rspb.2011.1120
Ribas, C. C., Aleixo, A., Gubili, C., D'Horta, F. M., Brumfield, R.
T., & Cracraft, J. (2018). Biogeography and diversification
of Rhegmatorhina (Aves: Thamnophilidae): Implications for
the evolution of Amazonian landscapes during the quater-
nary. Journal of Biogeography, 45(4), 917–­9 28. https://doi.
org/10.1111/jbi.13169
|
      13
Ricklefs, R. E., & Schluter, D. (1993). In R. E. Ricklefs & D. Schluter (Eds.),
Species diversity in ecological communities: Historical and geographi-
cal perspectives. University of Chicago Press.
Ronquist, F., & Huelsenbeck, J. P. (2003). Mrbayes 3: Bayesian phyloge-
netic inference under mixed models. Bioinformatics, 19, 1572–­1574.
Roosmalen, V. M., van Roosmalen, T., Mittermeier, R. A., & Rylands, A.
B. (2000). Two new species of marmoset, genus Callithrix Erxleben,
1777 (Callitrichidae, primates) from the Tapajós/Madeira interflu-
vium, south Central Amazonia, Bazil. Neotropical Primates, 8(2), 18.
Rossetti, D. F. (2014). The role of tectonics in the late quaternary evo-
lution of Brazil's Amazonian landscape. Earth-­Science Reviews, 139,
362–­389. https://doi.org/10.1016/j.earsc​irev.2014.08.009
Soares, L. M. D. S., Bates, J., Carneiro, L. S., Santos, M. P. D., & Aleixo,
A. (2019). Molecular systematics, biogeography and taxonomy of
forest-­falcons in the Micrastur ruficollis species complex (Aves:
Falconidae). Journal of Avian Biology, 50(4), 1–­14. https://doi.
org/10.1111/jav.01943
Sambrook, J., & Russell, D. W. (1989). Molecular cloning: a laboratory man-
ual (Vol. 3). Cold Spring Harbor Laboratory Press.
Santana, A., Silva, S. M., Batista, R., Sampaio, I., & Aleixo, A. (2020).
Molecular systematics, species limits, and diversification of the
genus Dendrocolaptes (Aves: Furnariidae): Insights on biotic ex-
changes between dry and humid forest types in the neotropics.
Journal of Zoological Systematics and Evolutionary Research, 00, 1–­17.
https://doi.org/10.1111/jzs.12408
Schweizer, M., & Liu, Y. (2018). Avian diversity and distributions and their
evolution through space and time. In D. Tietze (Ed.), Bird species.
Fascinating life sciences. Springer. https://doi.org/10.1007/978-­3-­
319-­91689​-­7_8
Silva, S. M., Townsend Peterson, A., Carneiro, L., Burlamaqui, T. C. T.,
Ribas, C. C., Sousa-­Neves, T., Miranda, L. S., Fernandes, A. M.,
D'Horta, F. M., Araújo-­Silva, L. E., Batista, R., Bandeira, C. H. M. M.,
Dantas, S. M., Ferreira, M., Martins, D. M., Oliveira, J., Rocha, T. C.,
Sardelli, C. H., Thom, G., & Aleixo, A. (2019). A dynamic continen-
tal moisture gradient drove Amazonian bird diversification. Science
Advances, 5(7), 1–­11. https://doi.org/10.1126/sciadv.aat5752
Sioli, H. (1984). Hydrochemistry and geology in the Brazilian Amazon re-
gion. Amazoniana, 1, 74–­83.
Slade, R. W., Moritz, C., Heidemann, A., & Hale, P. T. (1993). Rapid as-
sessment of single-­copy nuclear DNA variation in diverse species.
Molecular Ecology, 2, 359–­373.
Smith, B. T., & Klicka, J. (2010). The profound influence of the late
Pliocene Panamanian uplift on the exchange, diversification, and
distribution of New World birds. Ecography, 33, 333–­3 42. https://
doi.org/10.1111/j.1600-­0587.2009.06335.x
Smith, B. T., Mccormack, J. E., Cuervo, A. M., Hickerson, M. J., Aleixo, A.,
Cadena, C. D., Pérez-­Emán, J., Burney, C. W., Xie, X., Harvey, M. G.,
Faircloth, B. C., Glenn, T. C., Derryberry, E. P., Prejean, J., Fields, S.,
& Brumfield, R. T. (2014). The drivers of tropical speciation. Nature,
515, 406–­4 09. https://doi.org/10.1038/natur​e13687
Sousa-­Neves, T., Aleixo, A., & Sequeira, F. (2013). Cryptic patterns of
diversification of a widespread Amazonian woodcreeper species
complex (Aves: Dendrocolaptidae) inferred from multilocus phylo-
genetic analysis: Implications for historical biogeography and tax-
onomy. Molecular Phylogenetics and Evolution, 68, 410–­424.
Stamatakis, A. (2006). RAxML-­VI-­HPC: Maximum likelihood-­based
phylogenetic analyses with thousands of taxa and mixed models.
Bioinformatics, 22, 2688–­2690.
Stephens, M., & Donnelly, P. (2003). A comparison of bayesian meth-
ods for haplotype reconstruction from population genotype data.
American Journal of Human Genetics, 73(5), 1162–­1169. https://doi.
org/10.1086/379378
Tajima, F. (1989). Statistical method for testing the neutral mutation hy-
pothesis by DNA polymorphism. Genetics, 123, 585–­595.
Thom, G., Xue, A. T., Sawakuchi, A. O., Ribas, C. C., Hickerson, M. J.,
Aleixo, A., & Miyaki, C. (2020). Quaternary climate changes as
 |
14      CARNEIRO et al.

speciation drivers in the Amazon floodplains. Science. Advances, 6,

1–­11. https://doi.org/10.1126/sciadv.aax4718 B I O S K E TC H
Wagenmakers, E.-­J., & Farrell, S. (2004). AIC model selection using Akaike Lincoln S. Carneiro is interested in empirical biogeography of
weights. Psychonomic Bulletin & Review, 11(1), 192–­196. https://doi. Neotropical birds, with emphasis on investigation of the evolu-
org/10.3758/BF032​06482
tionary mechanisms behind diversification of species complexes
Wallace, A. R. (1852). On the monkeys of the Amazon. Proceedings of the
in widespread biomes. All authors share a common interest in
Zoological Society of London, 20, 107–­110.
Weir, J. T., Faccio, M. S., Pulido-­Santacruz, P., Barrera-­Guzman, A. O., general evolutionary biology and biogeography.
& Aleixo, A. (2015). Hybridization in headwater regions, and the
role of rivers as drivers of speciation in Amazonian birds. Evolution, Author contributions: L.S.C., A.A., D.O. and J.M.C.S. conceived
69(7), 1823–­1834. https://doi.org/10.1111/evo.12696
the research; L.S.C., A.A. and T.C.T.B obtained most of the speci-
Willis, E. O., & Oniki, Y. (1992). As aves e as formigas de correição. Boletim
Do Museu Paraense Emilio Goeldi. Serie Zoologia, 8, 123–­150. mens; T.C.T.B. generated the genetic data; L.S.C. and T.C.T.B.
Willis, E. O. (1969). On the behavior of five species of Rhegmatorhina, ant-­ analysed the data; L.S.C. and J.M.C.S led the writing, with other
following antbirds of the Amazon basin. The Wilson Bulletin, 81(4), authors contributing; and all authors read and approved the
363–­395.
manuscript.
Willis, E. O. (1982). The behavior of scale-­backed antbirds. The Wilson
Bulletin, 94(4), 447–­462.
Willis, E. O. (1984). Phlegopsis erythroptera (Gould, 1855) and relatives (Aves, S U P P O R T I N G I N FO R M AT I O N
Formicariidae) as army ant followers. Revista Brasileira de Zoologia, Additional supporting information may be found in the online
2(3), 165–­170. https://doi.org/10.1590/s0101​-­81751​98300​0300008
version of the article at the publisher’s website.
Willis, E. O., & Oniki, Y. (1978). Birds and Army ants. Annual Review of
Ecology and Systematics, 9(1), 243–­263. https://doi.org/10.1146/
annur​ev.es.09.110178.001331
Zheng, Y., & Wiens, J. J. (2015). Do missing data influence the ac- How to cite this article: Carneiro, L., Burlamaqui, T. C.,
curacy of divergence-­time estimation with BEAST? Molecular Aleixo, A., Oren, D. C. & Silva, J. M. (2022). Biogeography and
Phylogenetics and Evolution, 85, 41–­49. https://doi.org/10.1016/j. diversification of bare-­eyes, an endemic Amazonian clade.
ympev.2015.02.002
Journal of Biogeography, 00, 1–14. https://doi.org/10.1111/
Zimmer, K., & Isler, M. L. (2020). Black-­spotted bare-­eye (Phlegopsis
nigromaculata). In E. d. J. J. del Hoyo, A. Elliott, J. Sargatal, & D. jbi.14370
A. Christie (Eds.), Birds of the world. Cornell Lab of Ornithology.
https://doi.org/10.2173/bow.bsbey​e1.01
Zink, R. M., & Barrowclough, G. F. (2008). Mitochondrial DNA under
siege in avian phylogeography. Molecular Ecology, 17(9), 2107–­2121.
https://doi.org/10.1111/j.1365-­294X.2008.03737.x