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Megascops screech-owls are endemic to the New World and range from southern Canada to the southern cone of South America. The 21 currently recognized Megascops species occupy a wide range of habitats and elevations, from desert to humid montane forest, and from sea level to the Andean tree line. Species and subspecies diagnoses of Megascops are notoriously difficult due to subtle plumage differences among taxa with frequent plumage polymorphism. Using three mitochondrial and three nuclear genes we estimated a phylogeny for all but one Megascops species. Phylogenies were estimated with Maximum Likelihood and Bayesian Inference, and a Bayesian chronogram was reconstructed to assess the spatio-temporal context of Megascops diversification. Megascops was paraphyletic in the recovered tree topologies if the Puerto Rican endemic M. nudipes is included in the genus. However, the remaining taxa are monophyletic and form three major clades: (1) M. choliba, M. koepckeae, M. albogularis, M. clarkii, and M. trichopsis; (2) M. petersoni, M. marshalli, M. hoyi, M. ingens, and M. colombianus; and (3) M. asio, M. kennicottii, M. cooperi, M. barbarus, M. sanctaecatarinae, M. roboratus, M. watsonii, M. guatemalae, and M. vermiculatus. Megascops watsonii is paraphyletic with some individuals more closely related to M. atricapilla than to other members in that polytypic species. Also, allopatric populations of some other Megascops species were highly divergent, with levels of genetic differentiation greater than between some recognized species-pairs. Diversification within the genus took place during the last 8 million years, with a likely origin in Central America. The genus later expanded over much of the Americas and then diversified via multiple dispersal events from the Andes into the Neotropical lowlands.
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Molecular systematics of the new world screech-owls (Megascops: Aves,
Strigidae): biogeographic and taxonomic implications
q
Sidnei M. Dantas
a,
, Jason D. Weckstein
b,1
, John M. Bates
b
, Niels K. Krabbe
c
, Carlos Daniel Cadena
d
,
Mark B. Robbins
e
, Eugenio Valderrama
d
, Alexandre Aleixo
f
a
Curso de Pós-graduação em Zoologia, Universidade Federal do Pará/Museu Paraense Emilio Goeldi, Av. Perimetral, 1901, 66077-530 Belém, PA, Brazil
b
Integrative Research Center, Field Museum of Natural History, 1400 S Lake Shore Drive, Chicago, IL 60605, USA
c
Vertebrate Department of the Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark
d
Departamento de Ciencias Biológicas, Universidad de los Andes, Cra 1 N18A-12, Bogotá, Colombia
e
University of Kansas Biodiversity Research Institute, 1345 Jayhawk Boulevard, Lawrence, KS 66045, USA
f
Coordenação de Zoologia, Museu Paraense Emílio Goeldi, Campus de Pesquisa. Av. Perimetral, 1901, 66077-530 Belém, PA, Brazil
article info
Article history:
Received 26 May 2015
Revised 19 September 2015
Accepted 28 September 2015
Available online xxxx
Keywords:
Amazonia
Ancestral area reconstruction
Andes
Central America
Diversification
Neotropics
abstract
Megascops screech-owls are endemic to the New World and range from southern Canada to the southern
cone of South America. The 22 currently recognized Megascops species occupy a wide range of habitats
and elevations, from desert to humid montane forest, and from sea level to the Andean tree line.
Species and subspecies diagnoses of Megascops are notoriously difficult due to subtle plumage differences
among taxa with frequent plumage polymorphism. Using three mitochondrial and three nuclear genes
we estimated a phylogeny for all but one Megascops species. Phylogenies were estimated with
Maximum Likelihood and Bayesian Inference, and a Bayesian chronogram was reconstructed to assess
the spatio-temporal context of Megascops diversification. Megascops was paraphyletic in the recovered
tree topologies if the Puerto Rican endemic M. nudipes is included in the genus. However, the remaining
taxa are monophyletic and form three major clades: (1) M. choliba,M. koepckeae,M. albogularis,M. clarkii,
and M. trichopsis; (2) M. petersoni,M. marshalli,M. hoyi,M. ingens, and M. colombianus; and (3) M. asio,M.
kennicottii,M. cooperi,M. barbarus,M. sanctaecatarinae,M. roboratus,M. watsonii,M. atricapilla,M. guate-
malae, and M. vermiculatus.Megascops watsonii is paraphyletic with some individuals more closely related
to M. atricapilla than to other members in that polytypic species. Also, allopatric populations of some
other Megascops species were highly divergent, with levels of genetic differentiation greater than
between some recognized species-pairs. Diversification within the genus is hypothesized to have taken
place during the last 8 million years, with a likely origin in Central America. The genus later expanded
over much of the Americas and then diversified via multiple dispersal events from the Andes into the
Neotropical lowlands.
Ó2015 Elsevier Inc. All rights reserved.
1. Introduction
The New World screech-owl genus Megascops, recently split
from Otus based on vocal and molecular evidence (van der
Weyden, 1975; Marshall and King, 1988; Wink and Heidrich,
1999, 2000; Fuchs et al., 2008), currently includes 22 species
divided into ca. 63 taxa according to Marks et al. (1999), or 21 spe-
cies according to the American Ornithologists’ Union (Banks et al.,
2003; Remsen et al., 2015). Recognition of species limits and infer-
ences about relationships are notoriously difficult for this genus as
a result of considerable plumage similarity among taxa and poly-
morphism within taxa (Weske and Terborgh, 1981; Fitzpatrick
and O’Neill, 1986; Sick, 1997; Wink and Heidrich, 2000). For
instance, several subspecies described by Hekstra (1982) based
solely on plumage are not currently recognized, being instead con-
sidered as individual variation within recognized taxa (Marks et al.,
1999). In other cases, polytypic species such as Megascops guate-
malae are variably treated either as one polytypic species or as
many as four separate species with allopatric taxa distributed from
Mexico to the Bolivian Andes (Marks et al., 1999).
http://dx.doi.org/10.1016/j.ympev.2015.09.025
1055-7903/Ó2015 Elsevier Inc. All rights reserved.
q
This paper was edited by the Associate Editor Scott Edwards.
Corresponding author at: Coordenação de Zoologia, Museu Paraense Emílio
Goeldi, Campus de Pesquisa. Av. Perimetral, 1901, 66077-530 Belém, PA, Brazil.
E-mail address: smdantas@yahoo.com (S.M. Dantas).
1
Current addresses: Ornithology Department, Academy of Natural Sciences of
Drexel University, USA and Department of Biodiversity, Earth, and Environmental
Sciences, Drexel University, 1900 Benjamin Franklin Parkway, Philadelphia, PA 19103,
USA.
Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
Molecular Phylogenetics and Evolution
journal homepage: www.elsevier.com/locate/ympev
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
Previous phylogenetic hypotheses for Megascops (Heidrich et al.,
1995; Wink and Heidrich, 2000; Proudfoot et al., 2007; Wink et al.,
2009) all lacked extensive taxon sampling and only used partial
DNA sequences of one or two genes. Also, authors have elevated
forms of some polytypic taxa to species-level based on morpholog-
ical and/or vocal evidence. Thus, sampling multiple taxa and pop-
ulations in these polytypic species is important for resolving the
controversial taxonomy of Megascops and is critical for recon-
structing the evolutionary history of the group. Here, we present
the most complete phylogenetic data set for Megascops to date
based on broad taxon sampling covering all but one currently rec-
ognized species. The proposed phylogeny is used to discuss the his-
torical diversification and taxonomy of Megascops.
2. Material and methods
2.1. DNA extraction, amplification and sequencing
Our analyses included tissue samples from 44 individuals of 29
Megascops taxa (see Supplementary Material) belonging to all but
one species recognized by Marks et al. (1999) and an unnamed
taxon (see results). We were unable to find available tissues for
M. seductus. DNA was extracted using the DNeasy tissue extraction
kit (Qiagen, Valencia, California) or a phenol–chloroform protocol
(Sambrook and Russel, 2001). We obtained sequences of six differ-
ent genes including three mitochondrial genes (Cytochrome-b
[Cytb, 1035 bps], NADH dehydrogenase subunit 2 [ND2, 1040
bps] and Cytochrome c oxidase subunit 1 [COI, 379 bps]), one
nuclear intron (ß-fibrinogen Intron 5 [Bfib5, 560 bps]) and two Z-
linked introns (chromohelicase-DNA binding protein intron 18
[CHD, 349 bps] and muscle skeleton receptor tyrosine kinase
intron 4 [MUSK, 605 bps]). Primers used to amplify and sequence
each gene are listed in Table 1. For amplification and sequencing
of ND2 for this study we designed and used two internal primers:
L5758Mega (5
0
RRTGRGARATDGATGARAAGGC3
0
) and H5776Mega
(5
0
GGNTGRATRGGCYTRAACCARAC3
0
). Not all genes could be
sequenced for all individuals; Cytb was sequenced for all individu-
als; COI was sequenced for 43 individuals of all taxa; ND2 was
sequenced for 43 individuals of all taxa; Bfib5 was sequenced for
39 individuals of 26 taxa; MUSK was sequenced for 39 individuals
of 25 taxa, and CHD was sequenced for 34 individuals of 24 taxa
(see Supplementary Material).
MtDNA fragments were PCR-amplified using standard thermal
cycling conditions: denaturation at 94 °C, annealing between 46
and 56 °C, and extension at 72 °C, for 30 or 35 cycles. For the
nuclear genes, we used a touch-down PCR protocol in which the
annealing temperature was incrementally decreased from 58 °C
for five cycles to 54 °C for five cycles and 50 °C for 30 cycles. The
PCR products were run on a 1% agarose gel to verify whether
amplification was successful and of sufficient quantity for sequenc-
ing. PCR products were cleaned using either Exonuclease and
Shrimp Alkaline Phosphatase (ExoSap) enzymatic reactions (Uni-
ted States Biochemical), PEG 8000 20% NaCl 2.5 M, or GELase (Epi-
centre Technologies, Madison, WI). We cloned individual intron
sequences exhibiting length variant heterozygosity using the TOPO
TA cloning kit (Invitrogen), following the manufacturer’s protocol.
These cloned products were PCR amplified and then directly
sequenced to verify the sequence length of the variant haplotypes.
All PCR and cloned amplicons were cycle-sequenced using a Big-
Dye 3.1 Terminator kit (BigDye, Applied Biosystems, Foster City,
CA) with the same primers used for amplification. Cycle sequenc-
ing reactions were cleaned with ethanol EDTA precipitation, and
resuspended in Hi–Di formamide. Sequences were then visualized
through an ABI 3730 automated sequencer and aligned and recon-
ciled using Sequencher 3.1.1 (Gene Codes Corp, Ann Arbor, MI).
2.2. Phylogenetic analyses
Uncorrected genetic distances between lineages were calcu-
lated with MEGA 5 (Tamura et al., 2011), using the concatenated
mitochondrial data. We aligned sequences of all sampled individu-
als in Sequencher or Bioedit v. 7.1.3 (Tom Hall, Ibis Biosciences),
and concatenated them into one single dataset. Saturation was
evaluated with DAMBE (Xia and Xie, 2001). We used samples from
the following owl taxa as outgroups: Psiloscops (Otus)flammeolus,
Glaucidium peruanum,Otus megalotis,Lophostrix cristata and Asio
clamator (Fig. 1). The phylogeny was reconstructed using Maxi-
mum Likelihood (ML) as implemented in RAxML 7.0.3
(Stamatakis, 2006), as well as Bayesian Inference (BI) as imple-
mented in MrBayes 3.1.2 (Ronquist and Huelsenbeck, 2003).
The best-fit likelihood model of nucleotide substitution for each
gene was determined using MrModeltest 2.3 (Nylander, 2004),
based on Akaike’s information criterion (AIC). We tested different
partitioning schemes in BI: one partition (all data combined);
two partitions (mitochondrial genes combined and nuclear genes
combined); four partitions (mitochondrial genes separate and
nuclear genes combined; mitochondrial genes combined and
nuclear genes separate); and six partitions (all genes separate).
The selected partitioning scheme – i.e. the one with the best Bayes
factor value – had all mitochondrial genes separate and all nuclear
genes combined. We also analyzed mitochondrial and nuclear
datasets separately. For BI analysis we ran two parallel runs, with
four Markov chains and 10 million generations each, sampling the
chains every 500 generations. We discarded the first 5000 genera-
tions as burnin and used the remaining trees to create a 50%
majority-rule consensus tree and to calculate Bayesian posterior
probabilities (PP) as an assessment of nodal support.
2.3. Diversification timing and ancestral area reconstruction analyses
A Bayesian relaxed-clock analysis was performed in BEAST
v. 1.8.0 (Drummond et al., 2012) to assess species divergence times
Table 1
Primers used in the study.
Gene Primer References
Cytochrome-b (Cytb, 1035 bps) L14841 Kocher et al. (1989)
H16065 Helm-Bychowski and Cracraft (1993)
NADH dehydrogenase subunit 2 (ND2, 1040 bps) L5215 Hackett (1996)
H6313 Sorenson et al. (1999)
L5758Mega This study
H5776Mega This study
Cytochrome c oxidase subunit I (COI, 379 bps) L6625, H7005 Hafner et al. (1994)
Intron 5 of the nuclear b-fibrinogen gene (Bfib5, 560 bps) FIB5L, FIB5H Driskell and Christidis (2004)
Chromohelicase-DNA binding protein intron 18 (CHD, 349 bps) CHD-18F, CHD-18R Jacobsen et al. (2010)
Muscle skeleton receptor tyrosine kinase intron 4 (MUSK, 605 bps) MUSK-F, MUSK-R Kimball et al. (2009)
2S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
Fig. 1. Bayesian Inference phylogeny estimate based on a concatenation of all sequenced genes (Cytb, ND2, COI, BF5, CHD and MUSK). Node labels are BI/ML posterior
probability and bootstrap support values, respectively. Asterisks associated with nodes indicate that both BI and ML support values are equal to or above 95%. Nodes denoted
with a ‘‘–” indicate that they were not recovered by the ML analysis.
S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 3
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
using the COI, Cytb and ND2 genes. Only one individual per taxon
was used in the analysis. We linked the trees and clock (uncorre-
lated lognormal) models across all genes, but unlinked their substi-
tution models (Drummond et al., 2006). The mean (parameter ucld.
mean) for the clock rate was treated as an unknown parameter fol-
lowing a normal distribution (
l
= 1.105%;
r
= 0.34%) of substitu-
tions/site/branch/Ma. This prior was based on a widely used cytb
calibration rate of 0.01105 substitutions per million years (Weir
and Schluter, 2008). We used a Yule speciation process for the tree
prior. MCMC chains were run for 50 million generations sampling
every 5000 generations. Because ESSs parameter values associated
with some initial runs were below the recommend threshold, we
carried out multiple runs (up to 31) until values above 200 were
obtained for these parameters, combining all runs to estimate
the resulting chronogram. TRACER v. 1.5 was used to visualize
the posterior distributions for every parameter.
To reconstruct the ancestral history of the genus Megascops,we
carried out an ancestral area reconstruction analysis using BioGeo-
BEARS (BioGeography with Bayesian (and likelihood) Evolutionary
Analysis in R Scripts; Matzke, 2013;http://cran. rproject.org/
web/packages/BioGeoBEARS/index.html). This R package imple-
ments in a likelihood framework several ancestral area reconstruc-
tion models, such as LaGrange Dispersal-Extinction Cladogenesis
Model (DEC) (Ree and Smith, 2008), a likelihood version of DIVA
(DIVALIKE), and likelihood versions of range evolution models such
as BayArea and the Bayesian Binary Model (BBM) of RASP (Yu et al.,
2015). In BioGeoBEARS, founder event speciation can be added to
any of the previously described models, and left as a free parame-
ter estimated from the data, creating ‘‘DEC+J”, ‘‘DIVALIKE+J”, and
‘‘BAYAREA+J” models. We defined eight biogeographic areas based
on the distribution of Megascops taxa: (1) North America; (2) Cen-
tral America and trans-Andean South America; (3) Caribbean; (4)
Andes; (5) Tepuis; (6) Amazonia; (7) Atlantic Forest; and (8)
non-forested areas of cis-Andean South America. Our Bayesian
relaxed-clock tree was used to infer the ancestral area probability,
which was computed for each node and subsequently plotted on
the majority-rule chronogram. Finally, we compared the six differ-
ent models for statistical fit in two ways, using likelihood values
and Akaike Information Criterion (AIC), both implemented in the
BioGeoBEARS R package (Matzke, 2013). Only one individual of
each taxon was used in the analysis (Supplementary Material).
3. Results
3.1. Sequence divergence
Plots of uncorrected transition versus transversion divergence
did not indicate saturation among ingroup taxa. Uncorrected mito-
chondrial sequence divergence levels among all Megascops taxa
analyzed (Supplementary Material) ranged from 2.8% (between
M. watsonii usta and M. atricapilla to around 18% (between M.
nudipes and M. vermiculatus napensis). Divergence levels among
populations or individuals within M. vermiculatus (3.5–6.5%), M.
trichopsis (4.1%, not shown in the table), M. ingens (3.0%) and M.
watsonii (6.3%) were above the lowest divergence value between
recognized species.
3.2. Phylogenetic relationships
A four-partition scheme was selected as the best for the BI and
ML phylogenetic estimates using concatenated mitochondrial and
nuclear genes. For this partitioning scheme, each mitochondrial
gene had its own model applied to it and all nuclear genes were
treated as a single partition. Analysis of the mitochondrial and
nuclear concatenated (mit + nuc) data, and a separate analysis of
mtDNA data only (not shown) provided similar results, with a
few major discrepancies discussed below.
Megascops nudipes is sister to Psiloscops flammeolus (Fig. 1), ren-
dering the genus Megascops paraphyletic. The ML and BI nodal sup-
port values for the placement of M. nudipes outside the main
Megascops clade were high (Figs. 1 and 2). The remaining species
of the Megascops were divided into two major clades, both sup-
ported with significant BI values, but with just one of them recov-
ered and supported by the ML phylogeny (Fig. 1). One clade
includes M. choliba and M. koepckeae grouped as sisters with M.
albogularis. Members of this subclade are mainly South American
Fig. 2. Bayesian chronogram inferred from the mitochondrial genes sequenced (see text for details). Horizontal bars denote 95% posterior probability age intervals.
M. =Megascops.
4S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
(SA) species (except M. choliba, which is distributed as far north as
Costa Rica); this subclade in turn is sister to M. trichopsis and M.
clarkii, two Central American (CA) taxa. Megascops choliba duidae,
a Tepui endemic subspecies with a very different plumage from
other M. choliba subspecies, was nested well inside this species’
clade (samples LSUMZB-7413 and LSUMZB-7420 in Fig. 1). The
two M. trichopsis subspecies (FMNH 394215: M. t. trichopsis, from
Mexico and KUHNM 4931: M. t. mesoamericanus, from El Salvador)
differ by a 3.7% uncorrected p-distance based on mitochondrial
genes, surpassing the lowest level of divergence recovered herein
between currently recognized species (M. watsonii and M. atri-
capilla;Marks et al., 1999).
The second major clade contains the remaining Megascops spe-
cies divided into at least four subclades. The composition of these
subclades differs slightly between the mtDNA only and mtDNA
+ nuc analyses. One subclade includes five montane SA species:
M. ingens,M. colombianus,M. petersoni,M. hoyi, and M. marshalli.
With the exception of the basal node in the M. petersoni/hoyi/mar-
shalli clade, all support values in this clade were moderate to high
(Fig. 1). The M. ingens samples were divided into two groups, an
Ecuadorian and a Peruvian one (Fig. 1). Although they are consid-
ered the same subspecies (ingens), these samples differed geneti-
cally by 3.5% (uncorrected mitochondrial p-distance). The
position of another well-supported group within this sub-clade,
M. guatemalae/vermiculatus, is unresolved (Fig. 1); in contrast,
internal relationships in this clade are all well supported and
within-species divergences are relatively high. For example, two
samples of M. guatemalae (M. g. guatemalae and M. g. thompsoni)
from Mexico are 1.8% divergent from one another (uncorrected
mitochondrial p-distance) and are monophyletic with respect to
the M. vermiculatus group. Within M. vermiculatus, the Tepuian
(roraimae) and Andean (napensis) populations are sisters, with
the Panamanian sample (vermiculatus) sister to these two. Pairwise
uncorrected genetic distances between M. guatemalae and M. ver-
miculatus samples ranged from 8.4% to 9.4%, with distances within
M. vermiculatus ranging from 3.5% (roraimae–napensis) to 6.3% (ver-
miculatus–napensis).
The other groups contain the remaining SA, CA and North Amer-
ican (NA) species, including a well-supported South American
clade with M. roboratus,M. watsonii, and M. atricapilla (Fig. 1),
and an undescribed Megascops species from a population from
the Santa Marta Mountains (ICN 38770) reported as M. choliba by
Todd and Carriker (1922), but which does not fit with this or any
of the recognized species in this study. We refer to this individual
as ‘‘unnamed taxon”. Within this clade, M. watsonii is paraphyletic
with respect to M. atricapilla (Fig. 1). Megascops roboratus, an open
habitat to deciduous forest species from western Ecuador and Peru,
is the sister species to the M. watsonii/atricapilla clade, with the
unnamed taxon from the Santa Marta mountains coming out as
sister to this entire group, although with low statistical support,
perhaps because only Cytb sequences were available for this par-
ticular specimen.
A clade of North and Central American species including M. asio,
M. kennicotti,M. cooperi and M. barbarus, and the southern SA taxon
M. sanctaecatarinae is strongly supported by ML (ML boot-
strap = 100%) but not by BI (BI posterior probability = 85% analysis;
Fig. 1). This group was not well supported by the analysis of the
mtDNA only dataset (tree not shown), where neither Megascops
barbarus nor M. sanctaecatarinae were placed in this clade, leaving
the phylogenetic position of these species unresolved with respect
to one another.
Most relationships recovered by trees obtained exclusively with
the nuclear dataset (not shown) were similar to the ones based on
mitochondrial and both mitochondrial and nuclear datasets, with
some sister relationships receiving high support, such as P. flamme-
olus/M. nudipes,M. ingens/M. colombianus, and M. choliba/M. koepck-
eae. However, in the nuclear-only tree most clades, such as the M.
colombianus/ingens/hoyi/marshalli/petersoni group, were poorly
supported or unresolved. Similarly, Megascops trichopsis and M.
clarkii were not closely related to any species, whereas the CA
taxon M. vermiculatus vermiculatus fell into a CA/NA clade, that also
included M. sanctaecatarinae.
3.3. Diversification timing and ancestral area reconstructions
The split between Megascops nudipes/Psiloscops flammeolus and
the remaining Megascops was estimated to have occurred ca. 20
million years ago (mya) (height 95% HPD: 16.7–24.3 mya;
Fig. 2); 2). The first split in Megascops (excluding M. nudipes)
occurred in the Miocene, ca. 11.4 mya. Most splits in the genus
occurred during the Miocene and Pliocene, with a few occurring
more recently, during the Pleistocene (M. watsonii usta and
M. atricapilla;M. vermiculatus napensis and M. v. roraimae). The
chronogram topology was similar to those obtained in the
concatenated nuclear and mitochondrial BI/ML trees, except for
the position of M. sanctaecatarinae, which came out as sister to
the M. roboratus/watsonii/usta/atricapilla clade according to the
mitochondrial chronogram. Similarly, the chronogram recovered
M. barbarus as sister to the M. roboratus/watsonii/u-sta/atricapilla/
sanctaecatarinae/cooperi/kennicottii/asio/guatemalae/vermiculatus
clade. Both M. sanctaecatarinae and M. barbarus were related to
the M. cooperi/kennicottii/asio clade in the concatenated analyses.
The best ancestral area reconstruction model was DIVALIKE+J
(LnL=52.05; AIC = 110.1). The most likely ancestral area recon-
struction and the parameters and scores for each model (Table 2)
suggested that the core members of the genus Megascops were in
Central America during the Miocene (ca. 12.5 mya), after splitting
from a common ancestor with Megascops nudipes and Psiloscops
flammeolus (Fig. 2). Also in the Miocene, but after this split, there
was colonization of South America including the Andes
(7.5 mya), and Atlantic Forest and non-forested South America
areas. The Tepuis were colonized once from Andean ancestors
and North America was colonized from Central America. The anal-
ysis suggests Amazonian lowlands were colonized from Atlantic
Forest, and that at least one Andean/trans-andean species (M. rob-
oratus) derived from Atlantic Forest/Amazonian ancestors.
4. Discussion
4.1. Systematics and taxonomy of the genus Megascops
Our study provides a comprehensive phylogeny for all species
of the genus Megascops, except M. seductus, which is sometimes
treated as a subspecies of either M. asio or M. kennicottii and is geo-
graphically limited to a small range in southwestern Mexico. The
Puerto Rican endemic M. nudipes clearly is distantly related to
the other Megascops and its closest living relative among the spe-
cies included in this study appears to be Psiloscops (Otus)flammeo-
lus (Figs. 1–3), a western North American species with at least
Table 2
Models and parameters from each of the analyses conducted using BioGeoBEARS.
Dispersal (d), Extinction (e), Founder (j), values of Log-Likelihood (ln L) and Akaike
Information Criterion (AIC) scores from each model implemented.
Model dej ln LAIC
DEC 0.007 0 0 66.05 136.1
DEC+J 0.0021 0 0.0499 52.5 111
DIVALIKE 0.0092 0 0 61.7 127.4
DIVALIKE+J 0.0027 0 0.0467 52.05 110.1
BAYAREALIKE 0.0076 0.1244 0 78.47 160.9
BAYAREALIKE+J 0.0021 0 0.0568 54.85 115.7
S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 5
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
some populations wintering as far south as Central America (Marks
et al., 1999). Unfortunately, tissue from Margarobyas lawrencii of
Cuba, possibly a close relative of M. nudipes (Marshall and King,
1988, but see also Banks et al., 2003), was not available for this
study. The M. nudipes/P. flammeolus clade was recovered as the sis-
ter group to Megascops with high support. Thus, we suggest that
nudipes does not belong in the genus Megascops as currently
defined. One possibility would be to place nudipes into the genus
Psilocops or, alternatively, a more conservative approach might be
to resurrect the genus Gymnoglaux (Cabanis, 1855; see also Olson
and Suárez, 2008) for nudipes until data are available for Mar-
garobyas lawrencii.
Although relationships among many species and clades are
resolved in our reconstructions, the phylogenetic positions of some
groups remain unclear. For example, the basal relationships among
clades M. guatemalae/vermiculatus,M. barbarus/cooperi/kennicottii/
asio/sanctaecatarinae, and M. roboratus/watsonii/atricapilla are
poorly supported (Fig. 1). Similarly, basal relationships within the
well-supported M. petersoni/hoyi/marshalli/colombianus/ingens
clade are not well resolved (Fig. 1). The position of M. sanctaecatari-
nae, a southern SA species, is perhaps the most unexpected,
because it belongs in a clade including only NA and CA species
(M. asio,M. kennicottii,M. cooperi and M. barbarus). The mitochon-
drial tree (not shown) placed M. sanctaecatarinae within the
M. wat-sonii/atricapilla/roboratus/unnamed taxon clade, but with
low support, whereas M. barbarus was not included in the
M. asio/M. kennicotti/M. cooperi clade; therefore, the phylogenetic
affinities of M. sanctaecatarinae and M. barbarus reported herein
(Fig. 1) should be interpreted with caution until more data
become available. The relationships involving the remaining
species did not change in the mitochondrial-only tree compared
to the concatenated mitochondrial + nuclear analysis.
In contrast, our molecular data confirmed some hypothesized
relationships based on plumage and vocalizations. For example,
M. koepckeae and M. choliba are sister taxa, confirming the inde-
pendent species status of M. koepckeae as proposed by Fjeldså
et al. (2012). According to current taxonomy, the only paraphyletic
species recovered by the molecular data was M. watsonii, with
Fig. 3. Ancestral area reconstruction from BioGeoBEARS, derived from the Bayesian chronogram. The best-fit model was DIVALIKE+J. Most likely biogeographic areas are
shown in the circles, and the colors in the squares indicate the current species distribution. The map shows the location of the areas used. Combinations of two areas (for
example CAAN) are not shown on the map. We considered Mexico as Central America for this study.
6S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
populations from easternmost Amazonia grouping as sister to M.
atricapilla, an Atlantic Forest endemic. More detailed analyses deal-
ing with the phylogeography and species limits in the M. watsonii/
atricapilla clade will be published elsewhere (Dantas et al., unpub-
lished data). Other species, although monophyletic, showed con-
siderable genetic variation among populations, indicating long-
term isolation warranting consideration of species status. The
molecular data support not only the split between M. guatemalae
and M. vermiculatus (as adopted by Marks et al. (1999) but not
by Banks et al. (2003)), but high genetic divergences and reciprocal
monophyly among M. vermiculatus populations allow the recogni-
tion of three main groups, each corresponding to a named sub-
species. Average uncorrected p-distances among these clades
(6%) are substantially higher than between other currently recog-
nized species (e.g., M. watsonii and M. atricapilla), indicating that
they are probably best treated as distinct species. Although genetic
distance may not be sufficient to advocate for the split of species,
this case does provide ‘‘...corroborative evidence of species status”
(Johnson et al., 1999). The split of M. vermiculatus into three (M.
vermiculatus,M. roraimae, and M. napensis) separate species was
suggested by König and Weick (2008), who based their treatment
solely on morphological and vocal differences. Although tissues
were not available for M. v. pallidus (Hekstra, 1982) from northern
Venezuela, this taxon appears to be vocally distinct (18 recordings
from Zulia and Aragua compared with 12 recordings of roraimae
from Suriname, Guyana, and Sierra de Lema, Bolívar, Venezuela)
and could well deserve recognition as a separate species (Krabbe,
unpublished data).
Two Eastern Andean slope populations of M. ingens from Ecua-
dor and Peru, regarded as belonging to the same taxon (M. ingens
ingens), are divergent by 3.0% (uncorrected p-distance), and the
central Mexican (trichopsis) and El Salvadorian (mesoamericanus)
subspecies of M. trichopsis are divergent by 4.1% (uncorrected p-
distance), which suggests that multiple species-level taxa are
involved in each of these groups. Molecular studies with better
geographic and population level sampling coupled with morpho-
logical and vocal characters would help to confirm whether this
variation in M. vermiculatus,M. ingens and M. trichopsis is consis-
tent with recognizing these subspecies as species-level taxa. In
both cases, these divergences may fall across biogeographic breaks
that are established for other taxa (e.g., Winger and Bates, 2015).
The unnamed taxon (ICN 38770) comes from a population of
Megascops originally identified as M. choliba by Todd and Carriker
(1922), although these authors noted that it was very distinct in
plumage from that species, and could be an undescribed taxon.
The sequenced specimen did not fall within M. choliba or any other
Megascops clade, and its lowest uncorrected genetic distance to
other groups in this study (6.1%, between it and M. w. usta)is
higher than that recovered between other recognized Megascops
species. These results support the recognition of this population
as a distinctive species, which will be described elsewhere (Krabbe,
unpublished data).
4.2. Historical biogeography
According to the dating analyses, the first split within Megascops
(except M. nudipes) took place in the late Miocene, ca. 11 mya, sep-
arating the widespread M. choliba/koepckeae/albogu-laris/clarkii/tri
chopsis clade from the remaining species (Fig. 2). The ancestral area
reconstructions suggest a CA/Andes ancestral distribution for the
ancestor of all ‘‘true” Megascops species (Fig. 3). The fact that the
genus is more speciose in CA and the Andes is consistent with these
areas being inferred as the centers of origin for Megascops.
According to the dating and ancestral area reconstruction anal-
yses, the trans-Andean/NA clade M. clarkii/trichopsis split from the
widespread SA M. choliba/koepckeae/albogularis clade around
10 mya, with the ancestor of all these species most likely dis-
tributed in the Andes, CA and trans-Andean SA (Fig. 3). Also, SA
was colonized independently by Megascops at least three times,
and NA was colonized independently at least twice (Fig. 3). The
timing of these events span the last 9 mya, before the estimated
end of the Andean uplift (Gregory-Wodzicki, 2000) and after the
more recent estimates for the uplift of the Panama isthmus
(Farris et al., 2011; Montes et al., 2015). Most CA Megascops species
occupy montane habitats, and thus dispersal to the northern Andes
is feasible for these lineages. Other vertebrate groups from SA have
crossed into CA after the end of the uplift of the northern Andes,
including capuchin monkeys (Cebus sp.; Alfaro et al., 2012) and
Dendrocincla woodcreepers (Weir and Price, 2011), and thus per-
meability must not have been so limited in that area (see also
Smith et al., 2014). Closure of the Panama isthmus has long been
thought to have occurred at 3.5 mya (Coates and Obando, 1996),
but it has recently been suggested that the geological closure of
the isthmus likely occurred much earlier, by the middle Miocene
(13 to 15 Ma; Farris et al., 2011; Montes et al., 2015). Thus, CA col-
onization events in many avian taxa, such as the core tanagers
(Sedano and Burns, 2009), doves (Johnson and Weckstein, 2011),
even theoretically low-dispersal species such as Sclerurus(d’Horta
et al., 2013), and Megascops may have taken place either before
or after the final closure of the isthmus, depending on the age esti-
mated for this event according to different authors (Coates and
Obando, 1996; Farris et al., 2011; Montes et al., 2015).
The reconstruction suggesting that the Amazon forest species
(M. watsonii) and one Andean/trans-andean species (M. roboratus)
were derived from Atlantic Forest ancestors should be interpreted
with caution. The model implemented by BioGeoBEARS suggests
that M. watsonii usta had Atlantic Forest ancestors, whereas M. w.
watsonii had Amazonian ancestors. The tree used in the BioGeo-
BEARS analysis has M. sanctaecatarinae, a southern Atlantic Forest
species, separating earliest in the M. sanctaecatarinae/M. robora-
tus/M. watsonii/M. atricapilla clade, which might have caused this
result. The position of M. sanctaecatarinae in the phylogeny was
not well resolved by this study, so using this topology for the bio-
geographic analysis could have biased the reconstruction.
Megascops diversification in the Andes took place during the last
9 million years, with most species originating in the Miocene/Plio-
cene (during the last 5–7.5 million years). Most of the species that
diverged at this time inhabited the central and southern Andes,
with only three species found north of Ecuador. The uplift of the
Andes is believed to have had a very important role in the
diversification of the Neotropical avifauna, by producing a series
of isolated areas/habitats, where populations could evolve inde-
pendently (Sedano and Burns, 2009; Chaves et al., 2010; Weir
and Price, 2011; McGuire et al., 2014). Overall, our data are consis-
tent with the hypothesis that the Andean uplift occurred from
south to north (e.g. Garzione et al., 2008), with the ages associated
with nodes of the more central and southern species being older
than those of the northernmost ones, as observed in an Andean
Megascops clade containing M. ingens,M. colombianus,M. petersoni,
M. clarkii, and M. hoyi.Bonaccorso et al. (2011) found a similar pat-
tern in some southern clades of Aulacorhynchus toucanets. How-
ever, M. albogularis, occurring in the central/northern Andes, has
an old origin (ca. 8.7 mya), with M. koepckeae and M. vermiculatus
napensis, both from the central Andes, having a relatively recent
origin (ca. 2–1 mya). However, Megascops v. napensis is derived
from a more recent colonization of the Andes by a CA group. A
similar pattern is also found in other avian taxa, such as the
Drymophila caudata antbird superspecies (Isler et al., 2012) and
Andigena toucans (Lutz et al., 2013). Orogeny of the Andes seems
to have played an important role in the diversification of
Megascops, and this process seems to have occurred in many
geographic directions and habitats.
S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 7
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
Cis-Andean SA was colonized at least three times, probably by
Andean ancestors in all instances, during the last 5 my (Fig. 3).
Only one Megascops lineage diversified extensively in the Cis-
Andean lowlands (M. watsonii/atricapilla). The first splitting event
(dating to about 3.5 mya) isolated Guianan shield populations of
M. watsonii from the remaining ones in the M. watsonii/atricapilla
clade and could be related to the formation of the Amazon and
Negro rivers in the Amazonian lowlands. This is consistent with
the timing suggested for the origin of the modern trans-
continental Amazon River (ca. 2.5 mya; Ribas et al., 2012; d’Horta
et al., 2013). Populations outside the Guianan Shield later split into
three clades, including western and eastern Amazonian clades and
an Atlantic Forest clade. These splitting events, plus the separation
of eastern Amazonian and Atlantic Forest taxa, occurred during the
last 1–2 my, a similar time range estimated for the splits of eastern
Amazonian populations of Psophia (Ribas et al., 2012), some Scleru-
rus species (d’Horta et al., 2013), and Thamnophilus aethiops (Thom
and Aleixo, 2015). A more detailed account of the relationships and
biogeographical history of these Amazonian and Atlantic Forest
Megascops species complexes will be presented elsewhere.
4.3. Conclusions
The present study clarifies the taxonomic status of some Megas-
cops taxa and species groups, such as M. koepckeae,M. guatemalae,
M. vermiculatus, and an undescribed species from the Santa Marta
Mountains in Colombia. Nonetheless, broader geographic and pop-
ulation level sampling of species with some degree of differentia-
tion within them, such as M. watsonii,M. ingens and M. trichopsis,
will clarify the taxonomy and species limits of these taxa. Addi-
tional sampling might also help reconstruct the phylogenetic posi-
tion of species in the NA and CA M. asio,M. kennicottii,M. barbarus
and M. cooperi species complexes.
From a biogeographical perspective, our data support a complex
scenario of diversification in the Neotropics, with an origin in the
highlands of Central America or the Andes and multiple invasions
and recolonizations involving all major sectors and biomes of SA
and CA.
Acknowledgments
We are grateful to the following institutions which made this
work possible through tissue loans: Field Museum of Natural His-
tory (FMNH – Dave Willard); American Museum of Natural History
(AMNH – Paul Sweet, Thomas Trombone); Academy of Natural
Sciences of Philadelphia (ANSP – Nate Rice); National Museum of
Natural History (NMNH – James Dean); Museu de Zoologia da
Universidade de São Paulo (MZUSP – Luis Fabio Silveira); Univer-
sity of Kansas Biodiversity Research Institute; University of
Nevada, Las Vegas (John Klicka); Louisiana State University
Museum of Natural Science (LSUMNS – Donna Dittmann and J.V.
Remsen, Jr.); and Zoological Museum, University of Copenhagen
(ZMUC – Jon Fjeldså). The Instituto de Ciencias Naturales – Univer-
sidad Nacional de Colombia (ICN – F. Gary Stiles) provided the
unnamed taxon sample. During data collection and analyses SMD
was supported by a doctoral fellowship from ‘‘Conselho Nacional
de Desenvolvimento Científico e Tecnológico” (CNPq
#142211/2009-5) and a ‘‘sandwich” PhD scholarship from ‘‘Coorde
nação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES)/
Fulbright Brazil (#BEX 3424-10-3). The laboratory work was con-
ducted in the Pritzker laboratory at the Field Museum of Natural
History (FMNH) and the Molecular Biology Laboratory at the
Museu Paraense Emilio Goeldi (MPEG). Field and laboratory work
related to this paper were generously funded in part by CNPq –
Brazil (grants #310593/2009-3; ‘‘INCT em Biodiversidade e Uso
da Terra da Amazônia” #574008/2008-0; #563236/2010-8; and
#471342/2011-4) FAPESPA – Brazil (ICAAF 023/2011 and ICAAF
010/2012), and the United States National Science Foundation
DEB-1503804 (1120054) to JDW, JMB, and AA. AA was also sup-
ported by a CNPq research productivity fellowship
(#310880/2012-2). We thank J. Fjeldså for useful remarks on an
early draft of the manuscript, and L. Carneiro for his help with Bio-
GeoBEARS analysis.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.ympev.2015.09.
025.
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S.M. Dantas et al. / Molecular Phylogenetics and Evolution xxx (2015) xxx–xxx 9
Please cite this article in press as: Dantas, S.M., et al. Molecular systematics of the new world screech-owls (Megascops: Aves, Strigidae): biogeographic and
taxonomic implications. Mol. Phylogenet. Evol. (2015), http://dx.doi.org/10.1016/j.ympev.2015.09.025
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