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Background: Geographical and temporal patterns of diversification in bee hummingbirds (Mellisugini) were assessed with respect to the evolution of migration, critical for colonization of North America. We generated a dated multilocus phylogeny of the Mellisugini based on a dense sampling using Bayesian inference, maximum- likelihood and maximum parsimony methods, and reconstructed the ancestral states of distributional areas in a Bayesian framework and migratory behavior using maximum parsimony, maximum-likelihood and re-rooting methods. Results: All phylogenetic analyses confirmed monophyly of the Mellisugini and the inclusion of Atthis, Calothorax, Doricha, Eulidia, Mellisuga, Microstilbon, Myrmia, Tilmatura, and Thaumastura. Mellisugini consists of two clades: (1) South American species (including Tilmatura dupontii), and (2) species distributed in North and Central America and the Caribbean islands. The second clade consists of four subclades: Mexican (Calothorax, Doricha) and Caribbean (Archilochus, Calliphlox, Mellisuga) sheartails, Calypte, and Selasphorus (incl. Atthis). Coalescent-based dating places the origin of the Mellisugini in the mid-to-late Miocene, with crown ages of most subclades in the early Pliocene, and subsequent species splits in the Pleistocene. Bee hummingbirds reached western North America by the end of the Miocene and the ancestral mellisuginid (bee hummingbirds) was reconstructed as sedentary, with four independent gains of migratory behavior during the evolution of the Mellisugini. Conclusions: Early colonization of North America and subsequent evolution of migration best explained biogeographic and diversification patterns within the Mellisugini. The repeated evolution of long-distance migration by different lineages was critical for the colonization of North America, contributing to the radiation of bee hummingbirds. Comparative phylogeography is needed to test whether the repeated evolution of migration resulted from northward expansion of southern sedentary populations.
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R E S E A R C H A R T I C L E Open Access
The conquering of North America: dated
phylogenetic and biogeographic inference
of migratory behavior in bee
hummingbirds
Yuyini Licona-Vera and Juan Francisco Ornelas
*
Abstract
Background: Geographical and temporal patterns of diversification in bee hummingbirds (Mellisugini) were
assessed with respect to the evolution of migration, critical for colonization of North America. We generated a
dated multilocus phylogeny of the Mellisugini based on a dense sampling using Bayesian inference, maximum-
likelihood and maximum parsimony methods, and reconstructed the ancestral states of distributional areas in a
Bayesian framework and migratory behavior using maximum parsimony, maximum-likelihood and re-rooting
methods.
Results: All phylogenetic analyses confirmed monophyly of the Mellisugini and the inclusion of Atthis,Calothorax,
Doricha,Eulidia,Mellisuga,Microstilbon,Myrmia,Tilmatura, and Thaumastura. Mellisugini consists of two clades: (1)
South American species (including Tilmatura dupontii), and (2) species distributed in North and Central America
and the Caribbean islands. The second clade consists of four subclades: Mexican (Calothorax,Doricha)and
Caribbean (Archilochus,Calliphlox,Mellisuga)sheartails,Calypte, and Selasphorus (incl. Atthis). Coalescent-based
dating places the origin of the Mellisugini in the mid-to-late Miocene, with crown ages of most subclades in the
early Pliocene, and subsequent species splits in the Pleistocene. Bee hummingbirds reached western North
America by the end of the Miocene and the ancestral mellisuginid (bee hummingbirds) was reconstructed as
sedentary, with four independent gains of migratory behavior during the evolution of the Mellisugini.
Conclusions: Early colonization of North America and subsequent evolution of migration best explained
biogeographic and diversification patterns within the Mellisugini. The repeated evolution of long-distance
migration by different lineages was critical for the colonization of North America, contributing to the radiation of
bee hummingbirds. Comparative phylogeography is needed to test whether the repeated evolution of migration
resulted from northward expansion of southern sedentary populations.
Keywords: Bee hummingbirds, Biogeography, Mellisugini, Molecular phylogeny, Migration, North America
Background
Bird migration is one of the most extraordinary behaviors
found in nature. The voyage for migration involves a
fascinating suite of characters including navigational
systems, physiological specializations and the seasonal
timing of events [1, 2]. Our knowledge of several
ecological aspects of migration has become impressive
over time [3, 4]; however, much remains to be learned on
how long-distance seasonal migration repeatedly evolved
in a wide variety of bird lineages and about the selection
pressures underlying the evolution of migration [58]. In
particular, the origin and geographical directionality of
long-distance seasonal migration has been widely debated
in the literature (e.g., [7]), centered in two prominent ideas
originated on the examination of current distributions of
migratory species and their presumed sister species: the
southern-homeand the northern-homehypotheses. The
* Correspondence: francisco.ornelas@inecol.mx
Departamento de Biología Evolutiva, Instituto de Ecología, A.C., Carretera
Antigua a Coatepec No. 351, El Haya, Xalapa, 91070 Veracruz, Mexico
© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126
DOI 10.1186/s12862-017-0980-5
southern-homehypothesis posits that the breeding mi-
gratory species from the temperate regions are returning
to their tropical ancestral ranges during the winter,
whereas the northern-homehypothesis postulates that
the ancestral temperate range of migratory species be-
comes harsh for survival and depart to the novel tropics
during the winter, and then returning to their ancestral
home for breeding [6, 9]. In the southern-homehypoth-
esis, it is assumed that migration should evolve from
sedentary ancestors to migratory descendants in response
to ecological change or vice versa in the northern-home
hypothesis [10].
Escaping from intraspecific competition and the envir-
onmental seasonality with low food availability during
the breeding season has been interpreted as being cru-
cial for the evolution of migration [6, 1113]. However,
other factors such as increased harshness of climatic
conditions and variation in resource availability during
the non-breeding season, predation or parasitism would
also make species to shift their breeding ranges and
become migrants [6, 12]. Likely, migrant populations
originating from southern tropical regions might have
shifted their ranges northwards through long-distance
dispersal coupled with climatic cycles [14], assuming
competition in the tropical breeding ranges or the use of
seasonally abundant resources in temperate regions as
the driving forces for the northward expansion and
evolution of migration [2, 6, 9, 15]. Several authors have
envisioned scenarios for the transition from a sedentary to
a migratory species over evolutionary time [9, 11, 12, 16].
As a result of the differential effects of intraspecific and
interspecific competition, increasing seasonality of climate
or by certain patterns of climatic change during the
Tertiary and Pleistocene glaciations, Cox [11] proposed
that migration evolves from changing the initial sedentary
condition to that of a partial migrant, having with both
permanent sedentary populations and populations migrat-
ing into seasonally favorable adjacent areas. Partial mi-
grants then evolve further through extinction of sedentary
populations and expansion into derived forms with
separate or disjunct seasonal ranges. In contrast, Levey
and Stiles [16] developed a scenario where temporal and
spatial variation of resources, especially for fruit- and
nectar-feeding birds, led to altitudinal intra-tropical
migration, predisposing these birds to migrate out of
the tropics.
Despite the appeal of intraspecific competition and
variation in resource availability as being the first step
for the evolution of migration, these scenarios have
several shortcomings (reviewed in [6]) including those
that have shown how in a small fraction of recently-
expanded populations migratory behavior can increase
rapidly when favored by selection (e.g., [17, 18]). There-
fore, the repeated evolution of long-distance seasonal
migration within bird lineages linked to the occurrence
of relatively fast range expansions to take advantage of
abundant resources could be the result of selective
pressures occurring throughout several climatic cycles
affecting resource availability in seasonally changing
environments.
More recently, Somveille and collaborators [1922]
examined global spatial patterns in the diversity of
migratory birds, and found strong support for the
hypothesis that seasonality is the main force driving bird
migration worldwide (see also [23]). Whereas the previ-
ous studies attempt to explain the ecological mecha-
nisms driving the higher diversity of migratory species in
the Northern Hemisphere [22, 23], Rolland et al. [8]
used molecular phylogenies that included most extant
bird species to infer that sedentary behavior is ancestral
and that migratory behavior evolved independently
multiple times during the evolutionary history of birds.
They also found that seasonal migration increases
diversification via sedentary populations arising from mi-
gratory populations (asymmetrical speciation), in which
speciation of ancestral species into one sedentary and
one migratory species was more frequent in migratory
species than sedentary. Their results suggest that the
evolution of seasonal migration in birds has facilitated
diversification through the divergence of migratory
subpopulations that become sedentary, and illustrate
asymmetrical diversification as a mechanism by which
diversification rates are decoupled from species richness.
Hummingbirds (Trochilidae) are one of the largest
bird families, with ca. 338 species distributed in the
Americas [24]. The most recent molecular phylogeny
suggests that hummingbirds split from their sister group,
swifts and treeswifts, ca. 42 million years ago (MYA) in
Eurasia and that the age of the common ancestor of
hummingbirds in South America is ca. 22 MYA [25].
Given the gap between these two events and the absence
of relevant fossils in the Americas, McGuire et al. [25]
hypothesized that hummingbirds reached North America
by dispersal across Beringia. After that, hummingbirds
dispersed to the South American continent and may have
become extinct both in Europe and North America [25].
Hummingbirds have diversified into nine clades (Topazes,
Hermits, Mangoes, Brilliants, Coquettes, Patagona,
Mountain Gems, Bees, Emeralds), seven of which rapidly
diversified in South America in conjunction with the
Andean uplift. The common ancestor of the other two
clades, Bees and Mountain Gems, recolonized North
America ca. 12 MYA [25], before the formation of the
Central American land bridge and closure of the Isthmus
of Panama. While hummingbird diversification probably
increased in conjunction with the Andean uplift according
to divergence dating using substitution rate priors (rather
than fossil calibrations) [25], other divergence-dating
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 2 of 17
analyses using both fossil calibrations and substitution rate
priors retrieved older divergence splits between Bees and
Mountain Gems (2025 MYA; [26]), suggesting that
North American hummingbirds are not recent colonizers
and may have only become extinct in Europe [26, 27].
The beehummingbirds (Mellisugini tribe; [24]) com-
prise an assemblage of 16 genera and 36 small species
distributed throughout the Americas, from southern
Canada to South America [28]. Although some species
are geographically widespread (e.g., Archilochus spp.;
[28]), other have very restricted distributions such as the
smallest bird of the world (Mellisuga helenae) endemic
to Cuba. The most extensive molecular phylogeny of
hummingbirds to date [25], with at least one representa-
tive species for each genus in the Mellisugini, estimated
its relatively recent origin (ca. 5 MYA), revealed a high
rate of diversification (0.57 species/MYA), as compared
to other hummingbird clades. This phylogeny retrieved
Mellisugini as composed of two main clades: one clade in-
cluded species informally named woodstarsdistributed
in South America and Tilmatura dupontii with distribu-
tion in Central and North America, and the second clade
contained species arranged as in two subclades: (1)
Calypte,Selasphorus and Atthis species, and (2) shear-
tails(Doricha eliza and Calothorax lucifer), Archilochus
(A. colubris and A. alexandri), Calliphlox evelynae and
Mellisuga minima, in which phylogenetic relationships
between the sheartailsand the other species within the
subclade are not supported. Besides the high rate of diver-
sification, Mellisugini species are distinguished by the di-
morphic tail morphology, which in males the rectrices are
unusual in shape to produce sounds and acrobatic court-
ship displays during the breeding season (e.g., [2932]).
Mellisugini is the only group of hummingbirds with
long-distance seasonal migration and, therefore, an in-
teresting study group from a biogeographic perspective.
Most of the species in Canada and the USA are obligate,
long-distance seasonal migrants, which vacate their
entire breeding range to winter mainly in Mexico [28].
Several aspects of hummingbird long-distance seasonal
migration are particularly remarkable, with journeys
across the Gulf of Mexico by Archilochus colubris or
those of more than 6000 km by Selasphorus rufus,
breeding in western United States and Canada and
overwintering in Mexico [33]. However, the origin and
evolution of migratory behavior and the impact on
hummingbird diversification has not been studied. The
evolution of hummingbird migration is a complex
phenomenon to address because it is thought to evolve
rapidly in response to selection [9, 3436]. Previous
phylogenetic hypothesis [25] suggests that migratory
behavior is not evolutionarily constrained, as both sed-
entary and long-distance migratory species seem to have
evolved repeatedly within the Mellisugini. Understanding
the evolution of migratory behavior within the Mellisugini
is important, particularly because they are susceptible to
rapid evolutionary change, i.e. their high rate of net diver-
sification with species accumulation during their brief 5
MYA history [25], and because they can change their
migratory behavior to escape from increased harshness of
climatic conditions during the Pleistocene glacial cycles
[37], and from seasonal changes in the phenology and
availability of nectar floral resources by current global
climate changes [38]. Unfortunately, the lack of a wider
geographic sampling and the absence of some North
American representative species from previous phylogen-
etic analyses, has not allowed having a fully resolved
phylogeny of the group to understanding the evolution of
long-distance seasonal migration and timing of diversifica-
tion and colonization patterns.
The objectives of our study were to: (1) reconstruct
the phylogenetic relationships among bee hummingbirds
increasing both geographical and intraspecific sampling,
(2) estimate divergence times between species and
genera, and (3) reconstruct the ancestral range at each
divergence event, and subsequent temporal and
geographical shifts on migration in bee hummingbirds.
The suite of morphological and behavioral characters
coupled with the wide variety of environments where
they live, including the most xeric environments
tolerated within hummingbirds, have been linked to
their relatively rapid radiation with highest rate of
speciesaccumulation [25]. Thus, the Mellisugini present
a useful model for exploring hidden biodiversity due to
its wide distribution in both North and South American
continents and recent biogeographic origin, and for
understanding the potential impact of shifts between
sedentary and long-distance migratory behavior on
diversification of bee hummingbirds because migratory
and non-migratory species, and species with partial
migration (migratory and non-migratory populations)
occur only in the North American continent.
Methods
Sampling and laboratory methods
The data set included 116 samples of bee hummingbirds
from North America and the Caribbean Islands and 12
samples of bee hummingbirds from South America
(n= 16 samples), representing all 16 genera of bee hum-
mingbirds (32 of the 36 extant species, 89%). Tissue
samples were unavailable for four species: Chaetocercus
astreans (Colombia), C. berlepschi (Ecuador), C. heliodor
(Colombia, Venezuela and Ecuador), and Mellisuga
helenae (Cuba). Most of these species are endemic and
range-restricted; Chaetocercus berlepschi is threatened
by habitat loss [39, 40]. We include new sequence data for
60 individuals from the genera Archilochus,Atthis,
Calothorax,Doricha,Calypte,Selasphorus and Tilmatura
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 3 of 17
to supplement the data set in McGuire et al. [25] and Feo
et al. [31]. Additionally, we included a single individual of
each of 15 species of mountain gems and emeralds to be
used for sequence alignment and as outgroups. Samples
were obtained from vouchered tissue collections (see
Acknowledgements) and from our collecting efforts in
Mexico.
DNA was extracted from tissue or tail feathers with
the DNeasy Tissue extraction kit (Qiagen, Valencia, CA,
USA) using the standard protocol. We amplified and
sequenced six gene regions, two mitochondrial protein
coding genes1041 base pairs (bp) of nicotinamide
dehydrogenase subunit 2 (ND2) and 807 bp of nicotina-
mide dehydrogenase subunit 4 (ND4), and four nuclear
loci1085 bp of fibrinogen beta chain intron (FBG I7),
551 bp of adenylate kinase 1 intron 5 (AK1 I5), 577 bp
of ornithine decarboxylase 1 introns 6 and 7 intervening
exon (ODC1), and 635 bp of Z-linked muscle, skeletal,
receptor tyrosine kinase intron 3 (MUSK I3) using
specific primers (Additional file 1). Protocols for PCR
reactions and for sequencing the PCR products are
described elsewhere [41]. The products were read on a
310 automated DNA sequencer (Applied Biosystems) at
the INECOLs sequencing facility. Finally, assembled se-
quences were edited and checked for quality, pre-aligned
using MAFFT v7 (http://mafft.cbrc.jp/alignment/server/),
and then manually aligned using PhyDE [42]. Newly
generated sequences have been submitted to GenBank
(Accession nos. ND2: KX855335KX855393; ND4:
KX855394KX855450; AK1 I5: KX855451KX855509;
MUSK I3: KX855568KX855624; ODC1: KX855510
KX855567; FBG I7: KX855625KX855637; Additional
file 2). The alignments supporting the results of this article
are available in the Dryad Digital Repository (http://
dx.doi.org/10.5061/dryad.68fn0) as Licona-Vera and
Ornelas [43].
Phylogenetic reconstruction
The phylogeny was reconstructed using Bayesian infer-
ence (BI), maximum-likelihood (ML) and maximum parsi-
mony (MP). We performed BI comparative phylogenetic
analyses using MrBAYES v3.2.2 [44] and the CIPRES
Science Gateway [45] on the following data sets: (1) only
mitochondrial genes (unpartitioned mtDNA), (2) only
mitochondrial genes as two partitions (partitioned
mtDNA), (3) only nuclear genes (unpartitioned nuDNA),
(4) only nuclear genes as four partitions (partitioned
nuDNA), (5) combined loci data set with a single model
(concatenated), (6) each DNA region as one partition
(mtDNA + nuDNA), and (7) with a set partition-specific
DNA evolution models of each gene (6-partitions). We
used jMODELTEST v2.1.7 [46] to select an appropriate
model of nucleotide substitution for each locus and the
concatenated data set. GTR + I + G (ND2), TrN + I + G
(ND4), K80 + G (AK1 I5), HKY (MUSK I3), HKY (ODC1),
HKY + G (FBG I7), GTR + I + G (mtDNA data set),
GTR + G (nuDNA data set), and TrN + I + G
(concatenated) were selected as the best fitting models
and incorporated as prior information in the Bayesian
analyses. For each data set, two parallel Markov chain
Monte Carlo (MCMC) analyses were executed simultan-
eously for 30 million generations, sampling every 10,000
generations. Output parameters were visualized using
TRACER v1.6 (http://tree.bio.ed.ac.uk/software/tracer/). A
25% burn-in was used, and a majority rule consensus tree
was calculated and visualized in FIGTREE v1.4.3 (http://
tree.bio.ed.ac.uk/software/figtree/). We computed Bayes
factors with the harmonic means [47] to determine
whether applying partition-specific models for the com-
bined data sets significantly improved the explanation of
the data.
The ML analysis for the concatenated data set was run
using RAxML v8.2.9 [48] with a GTRGAMMA model
for each partition. Node support for the ML tree was
estimated with 1000 bootstrap replicates.
The MP analysis was run for the concatenated data set
in NONA v2.0 [49] using WINCLADA [50], with
nucleotide characters treated as equally weighted and
unordered. We ran 1000 iterations, holding 10 trees per
iteration with 10%of the nodes constrained, and all the
parameters set to default. Branch support was assessed
using bootstrap resampling, 1000 bootstrap-resampled
pseudo-replicate matrices were each analyzed using 100
random addition sequences (multi*100). Ten trees were
retained during TBR swapping after each search initi-
ation (hold/10).
Divergence time estimation
A Bayesian relaxed-clock analysis was performed in
BEAST v2.4.4 [51, 52] to assess species divergence times
using the six genes. We constrained Trochilidae and the
hummingbird clades used as outgroups (emeralds and
mountain gems) as monophyletic based on McGuire et
al. [25]. Divergence times were estimated using an
uncorrelated lognormal relaxed clock model across all
genes, with the trees linked and the substitution models
for each partition unlinked [53]. We calibrated our
divergence-dating analyses using a Yule speciation model
and three calibration strategies for divergence time esti-
mation: (1) incorporating a separate normally distributed
substitution rate calibration priors for ND2,ND4, AK1,
FGB, and ODC using the mean substitution rates
proposed by Lerner et al. [54] to model the tree prior,
allowing the substitution rate prior for MUSK I3 to be
calculated by BEAST because no substitution rate was
available; (2) using as secondary calibration the age of
the split between mountain gems and bee hummingbirds
(normal, mean 12.0 MYA, SD ± 1, range of 13.910.3
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 4 of 17
MYA) according to McGuire et al. [25] to calibrate the
root of the tree; and (3) using both strategies, secondary
calibration + substitution rates. This strategy was also
used for divergence time estimation using a reduced data
set, which includes one individual for each of the species
to contrast results of divergence time estimation from
single vs. multiple-individuals data sets.
Two independent chains of MCMC were run with
50 million generations, sampling every 5000 genera-
tions. Results were visualized in TRACER v1.6 (http://
tree.bio.ed.ac.uk/software/tracer/) to confirm appropri-
ate burn-in, adequate effective samples sizes (ESS > 200)
of the posterior distribution for all parameters, and to as-
sess convergence among runs by comparing likelihoods of
parameters. The three independent runs were combined
with LOGCOMBINER v2.4.4 [51, 52] and the resulting
maximum clade credibility tree and 95% highest posterior
(HPD) distributions of each estimated node annotated
using TREEANNOTATOR v2.4.4 [51, 52] and visualized
in FIGTREE v1.4.3 (http://tree.bio.ed.ac.uk/).
Ancestral areas of bee hummingbirds
We reconstructed ancestral geographic ranges using
Bayesian methods with BBM (Bayesian Binary MCMC)
analyses implemented in RASP v3.2.1 [55]. This method
determines the probability of each ancestral geographical
region for each node averaged over the collection of
trees derived from a Bayesian MCMC analysis [56, 57].
To reconstruct the ancestral areas, we loaded 6000 trees
from the Bayesian Inference analyses using MrBAYES.
The breeding distributions of each sample was obtained
from del Hoyo et al. [28] and crossed with the status and
distribution information compiled by the Cornell Labora-
tory of Ornithology as input (www.allaboutbirds.org/
guide). We coded each individual in the data set as occur-
ring in one or more of the following areas: A = western
North America, B = eastern North America, C = southeast-
ern Mexico and Central America, D = West Indies, and
E = South America (Additional file 3). These regions
were based on a modified map of the ecoregions
(http://maps.tnc.org/gis_data.html) proposed by Blair
and Sánchez-Ramírez [58]. The posterior probabilities
for nodes in the phylogeny with >0.90 were estimated
to incorporate information from most nodes of the
tree but minimizing phylogenetic noisefrom poorly
supported relationships. The maximum number of
areas in ancestral ranges was constrained to three,
Amazilia rutila assigned as outgroup using the
customoption, and the ancestral areas for nodes
visualized on the condensed tree. Analyses were run
for 50,000 iterations, sampling every 100 generations,
the first 25% of which were discarded as burn-in,
with the JC + gamma model of state transitions used
as input.
Evolution of migratory behavior
Ancestral state reconstruction was used to map migra-
tory behavior onto the resulting molecular phylogeny.
The evolution of migratory behavior was reconstructed
using maximum parsimony (MP) and maximum-
likelihood (ML) methods. We traced the evolution of
migratory behavior over the molecular phylogeny using
two topologies: one with all samples and the other with
one sample per species. The first topology corresponds
to the best estimate of Mellisugini phylogenetic relation-
ships using the 6-partitions data set (see Results), a
Bayesian 50% majority rule consensus tree of 132
samples of bee hummingbirds. We used the 18,000 post-
burnin trees from the BEAST analysis to account for the
phylogenetic uncertainty in the ancestral state recon-
struction. The second topology was a Bayesian 50%
majority rule consensus tree using one sample per spe-
cies (see Results). This tree was obtained from a BEAST
analysis using the same parameters and the 6-partitions
strategy described on methods section of phylogenetic
reconstruction.
For ancestral state reconstruction we used three
different coding schemes mainly based on information
in del Hoyo et al. [28] and Malpica and Ornelas ([37];
Additional files 3 and 4). In coding Scheme 1 species
that migrate seasonally between different latitudinal
geographical breeding and wintering ranges were coded
as migrants (i.e., obligate, long-distance migration; [59])
and non-migratory species were coded as sedentary. For
this coding scheme, we also considered as migratory
those species with partial migration, in which some indi-
viduals or populations are fully migratory across their
range and other individuals or populations are sedentary
(Selasphorus platycercus and Calothorax lucifer; [60]).
The migratory state does not include tropical humming-
bird species that may undertake altitudinal or short-
distance migration at the fringes of their northern ranges
in the northern temperate region (e.g., Amazilia violiceps,
Eugenes fulgens,Heliomaster constantii; [59]). In coding
Schemes 2 and 3, species with partial migration were
coded as sedentary or polymorphic, respectively, to test
the robustness of our conclusions to potential ambiguities
in character state coding [60]. Coding species with a sim-
ple binary codification (sedentary or migrant) and pruning
trees to species probably mask or confuse the ancestral
character reconstruction of species susceptible to rapid
evolutionary change of migratory behavior [3436]. Thus,
we conducted ancestral state reconstruction using the
data set with multiple individuals for a given species to
compare results with those obtained for species-level
analyses (single-individual data set). Also, insights might
be gained from sampling several individuals if these
provide the signal at the phylogenetic level of when the
shifts from migratory to sedentary (or vice versa) occurred
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 5 of 17
between populations in species with both sedentary and
migratory populations. Here, single individuals of C.
lucifer and S. platycercus with migratory and sedentary
populations were classified as either migrant or sedentary
based on data on Malpica and Ornelas [37] and because
samples of single individuals were collected during the
breeding season from known allopatric migratory or
sedentary populations. Species names, English names and
distributional range for the Mellisugini species used in this
study are provided in Additional file 5.
MP and ML based ancestral state reconstruction were
conducted in Mesquite v3.11 [61] using each of the
coding schemes of migratory behavior described above.
To account for topological uncertainty we used the
trace character over treesoption, which summarizes
the ancestral state reconstruction over a series of trees.
All reconstructions were integrated over the last 18,000
post burn-in of the Bayesian analysis and the ancestral
states were summarized using the Count trees with
uniquely best statesoption on the maximum credibility
tree using Mesquite. A reconstruction is regarded as
equivocal when there are two or more equally parsimo-
nious states inferred at a particular node. For the parsi-
mony ancestral character reconstructions character-state
changes were set as unordered, with other parameters as
default. In the ML approach, the character state for each
ancestral node was reconstructed using the Markov k-
state 1 parameter model (Mk1), which specifies an equal
probability of any state change and considers the rate of
change the only parameters. We conducted ancestral
state reconstruction with more than one method be-
cause each of the two methods described above suffers
from certain advantages and limitations [6266].
Ancestral states of migratory behavior in the Mellisugini
were also reconstructed using the re-rooting method of
Yang et al. [67] as implemented in PHYTOOLS v0.5 [68]
in R v3.3.0 [69]. This method re-roots the phylogeny at
every node and calculates the phylogenetically independ-
ent contrast for the root node, taking advantage of the fact
that this value is the maximum likelihood estimate for that
node [70, 71]. We used the Mk1 model for reconstruction
of the character state for each ancestral node, assuming
equal rate of evolution. Since the likelihood approach is
not applicable for polymorphic characters this reconstruc-
tion was performed using only the parsimony approach.
Results
Phylogeny
Bayesian analyses using the entire gene data set (nuDNA +
mtDNA) resulted in a well-supported phylogeny of the
Mellisugini tribe and close relatives (Fig. 1). The summary
of MP and ML bootstrap values and the Bayesian posterior
probabilities are presented on the branches of the BI 50%
majority-rule consensus tree (Fig. 1). Results of other
Bayesian analyses using partition or unpartitioned nuDNA
or mtDNA data sets are given in Additional file 6. Given
the stronger support between clades in the analyses
of the nuDNA + mtDNA data set and Bayes Factors,
we considered the MrBayes results of concatenated
mtDNA + nuDNA genes (with 6-partitions strategy)
to be our best estimate of phylogenetic relationships
in the Mellisugini. We rely on this tree in our ances-
tral state reconstructions and discussion of the evolu-
tion of migration and of biogeography. Changes to
previous phylogenetic topologies of the Mellisugini
(e.g. [25]) are indicated in Additional file 7.
Divergence dating and ancestral areas of bee
hummingbirds
The topology of the BEAST time-tree using the third
calibration strategy (secondary calibration + substitution
rates (Fig. 2) was concordant with those derived from
other reconstruction methods (Fig. 1, Additional file 6).
The BEAST analyses indicated the most recent common
ancestor (MRCA) for the Mellisugini originated approxi-
mately 9.93 MYA (95% HPD 11.947.92 MYA) in main-
land North America ~6 million years before the final
closure of the Isthmus of Panama (Fig. 2). The ancestor
originated in either western North America or southern
Mexico and Central America, with relatively high
support for nodes A (separating bee hummingbirds and
mountain gems) and B (separating South and North
American bee hummingbirds) yielded by the ancestral area
reconstruction (AC, 97% and 79%, respectively; Fig. 2). By
the end of the Miocene, the bee hummingbirds first
reached western North America (node C; A, 60%). Accord-
ingly, subsequent major nodes (nodes D, E, F, K, J) were
reconstructed as nearly 100% western North America (A).
Although it is uncertain where the ancestor of bee hum-
mingbirds was distributed in the region, the analysis sug-
gests that western North America was colonized during
the early diversification of the group with dispersals into
other regions of the Northern Hemisphere. The BEAST
analyses also showed a mid-to-late Miocene split separat-
ing South American woodstars from the other bee
hummingbirds (node B; Fig. 2), divergence of the Mexican
sheartails from other North American bee hummingbirds
in the late Miocene (node C), and that the diversification
of the South American woodstars (node L), Caribbean
sheartails (node H) and the split between the Calypte-
Selasphorus subclades (node E) occurred in the early
Pliocene (Fig. 2). Details of ages for other nodes of interest
are shown in Table 1.
Evolution of migratory behavior
The results of ancestral state reconstruction of long-
distance migratory behavior on the Bayesian 50%
majority-rule consensus tree of a reduced 32 bee
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 6 of 17
0.02 subst/site
1/100/100
1/100/-
1/61/100
1/100/99
1/100/100
1/94/99
0.75/56/95
1/100/100
1/95/99
1/100/99
0.97/88/96
1/93/98
1/100/100
1/100/100
0.92/58/91
0.99/75/93
1/100/100
1/100/100
1/100/100
1/100/100
1/100/100
0.57/51/94
1/100/100
1/100/98
1/100/100
1/84/96
0.99/50/-
1/100/99
1/100/100
1/100/100
1/100/100
1/94/100
1/100/99
0.92/59/93
1/100/100
1/94/97
0.83/-/82
Selasphorus platycercus
Atthis ellioti
Atthis heloisa
Selasphorus flammula
Selasphorus ardens
Selasphorus scintilla
Selasphorus calliope
Selasphorus sasin LSUMZB33988
Selasphorus sasin LSUMZB43116
Selasphorus sasin LSUMZB3117
Selasphorus sasin MVZ182025
Selasphorus sasin MVZ183552
Selasphorus sasin MVZ182072
Selasphorus rufus SRU01HGO
Selasphorus rufus SRU02HGO
Selasphorus rufus SRU04TLAX
Selasphorus rufus MVZ180196
Selasphorus sasin MVZ182183
Selasphorus rufus SRU06TLAX
Selasphorus rufus LSUMZB19586
Selasphorus sasin MVZ180632
Selasphorus rufus SRU03HGO
Selasphorus rufus SRU05TLAX
Selasphorus sasin MVZ180045
Selasphorus [platycercus] rufus LSUMNSB23428
Selasphorus platycercus CHIS200
Selasphorus platycercus CHIS201
Selasphorus platycercus CORO102
Selasphorus platycercus TLAX206
Selasphorus platycercus CHIS197
Selasphorus platycercus CHIS199
Selasphorus platycercus SWRS111
Selasphorus platycercus SWRS112
Selasphorus platycercus SWRS114
Selasphorus platycercus SWRS113
Selasphorus platycercus TLAX207
Atthis ellioti CJC272
Atthis ellioti CJC274
Atthis ellioti RAJ179
Atthis heloisa AHE02VER
Atthis heloisa AHE03HGO
Atthis heloisa FMNH343218
Atthis heloisa UNAMOVMP1041
Atthis heloisa AHE04PUE
Selasphorus flammula LSUMZB16222
Selasphorus flammula LSUMZB19794
Selasphorus flammula LSUMZB19847
Selasphorus flammula LSUMZB28246
Selasphorus flammula LSUMZB28253
Selasphorus flammula LSUMZB28260
Selasphorus flammula LSUMZB28313
Selasphorus flammula LSUMZB9952
Selasphorus flammula LSUMZB19883
Selasphorus flammula LSUMZB28269
Selasphorus ardens LSUMZB52914
Selasphorus ardens MBM18307
Selasphorus ardens LSUMZB52913
Selasphorus ardens LSUMZB52915
Selasphorus scintilla LSUMZB16266
Selasphorus calliope LSUMZB16854
Selasphorus calliope LSUMZB23775
Selasphorus calliope LSUMZB26272
Selasphorus calliope MVZ175821
Selasphorus calliope MVZ170138
Selasphorus calliope MVZ182182
1/100/99
1/77/97
1/100/99
Calypte anna LSUMZB24864
Calypte anna MNCN13108
Calypte anna MNCN13142
Calypte anna MNCN13036
Calypte anna MNCN13143
Calypte anna MNCN13153
Calypte costae CJC210
Calypte costae LSUMZB21595
Calypte costae CAC03BCS
Calypte costae CAC01BCS
Calypte costae CAC02BCS
Calliphlox evelynae LSUMZB59204
Calliphlox evelynae LSUMZB58890
Calliphlox evelynae YPM142568
Calliphlox evelynae YPM142569
Calliphlox evelynae YPM142570
Calliphlox lyrura YPM142566
Calliphlox lyrura YPM142567
Calliphlox lyrura YPM142564
Calliphlox lyrura YPM142562
Calliphlox lyrura YPM142565
Mellisuga minima MVZ183600
Mellisuga minima MVZ183602
Mellisuga minima STRIJAMM11
Archilochus colubris ACO04OAX
Archilochus colubris ACO05OAX
Archilochus colubris ACO02YUC
Archilochus colubris ACO03YUC
Archilochus colubris LSUMZB5270
Archilochus alexandri ARAO1CHI
Archilochus alexandri LSUMZB21848
Archilochus alexandri MNCN13145
Archilochus alexandri MNCN13151
Doricha eliza VER01LEN
Doricha eliza VER04XAL
Doricha eliza VER23LEN
Doricha eliza VER25LEN
Doricha eliza VER26ACT
Doricha eliza VER24LEN
Doricha eliza KU4435
Doricha eliza YUC09RLA
Doricha eliza YUC10RLA
Doricha eliza YUC18CHI
Doricha eliza UNAMB590
Doricha enicura DEN14COM
Doricha enicura RAJ182
Doricha enicura YPM142508
Doricha enicura DEN16COM
Calothorax pulcher CAL02VER
Calothorax pulcher PUE135
Calothorax pulcher CAP02OAX
Calothorax pulcher CAP04OAX
Calothorax pulcher CAP03OAX
Calothorax lucifer DF136
Calothorax lucifer LSUMZB43113
Calothorax lucifer YPM141067
Calothorax lucifer CAL07TLAX
Calothorax lucifer CAL11HGO
Calliphlox mitchellii LSUMZB12194
Calliphlox mitchellii LSUMZB2310
Calliphlox bryantae LSUMZB28180
Chaetocercus bombus LUMMZB5225
Chaetocercus mulsant LUMMZB6301
Microstilbon burmeisteri ZMC114932
Eulidia yarrellii WV022
Thaumastura cora LSUMZB14278
Thaumastura cora MSBBird33004
Myrmia micrura LSUMZB5233
Rhodopis vesper JOSE2
Rhodopis vesper LSUMZB14277
Myrtis fanny LSUMNZB3592
Calliphlox amethystina NMNHB10703
Tilmatura dupontii KU8188
Tilmatura dupontii PD1
Lampornis hemileucus LSUMZB16006
Lampornis castaneoventris LSUMZB28257
Lampornis calolaemus cinereicauda LSUMZB19791
Lampornis sybillae UWBM56159
Lampornis viridipallens LSUMZB19268
Lampornis amethystinus FMN343217
Lampornis clemenciae LSUMZB10119
Lampornis calolaemus LSUMZB28169
Heliomaster squamosus FMNH392806
Heliomaster furcifer LSUMZB6709
Heliomaster longirostris LSUMZB18268
Heliomaster constantii UWBM69186
Panterpe insignis LSUMZB16264
Lamprolaima rhami LSUMZB22001
Eugenes fulgens LSUMZB28291
Chlorostilbon swainsonii AMNHNKK1017
Chlorostilbon maugaeus LSUMZB11520
Chlorostilbon ricordii ANSP5570
Cynanthus latirostris LSUMZB33304
Chlorostilbon canivetii UWBM69030
Cynanthus sordidus LSUMZB22004
Cynanthus sordidus LSUMZB22005
Abeillia abeillei LSUMZB22002
Anthocephala floriceps JVLPi1253
Campylopterus rufus FMNH434025
Hylocharis leucotis LSUMZB22003
Amazilia cyanocephala LSUMZB19260
Amazilia beryllina FMNH394217
Amazilia candida UNAMPUE102
Amazilia rutila UWBM56002
Mountain
Gems
Emeralds
Selasphorus rufus/sasin
Calypte anna
Calypte costae
Calliphlox evelynae
Calliphlox lyrura
Mellisuga minima
Archilochus colubris
Archilochus alexandri
Doricha eliza
Doricha enicura
Calothorax lucifer/pulcher
South American
bee
hummingbirds
(Woodstars)
Mellisugini
Selasphorus
subclade
Mexican
Sheartails
subclade
Caribbean
Sheartails
subclade
Calypte
subclade
North American bee hummingbirds
Fig. 1 Phylogenetic 50% majority-rule consensus tree of the Mellisugini hummingbird from the Bayesian analysis of the combined NADH
dehydrogenase subunit 2 (ND2) and subunit 4 (ND4) mitochondrial protein coding genes, and fibrinogen beta chain intron (FBG I7), adenylate
kinase 1 intron 5 (AK1 I5), ornithine decarboxylase 1 introns 6 and 7 intervening exon (ODC1), and Z-linked muscle, skeletal, receptor tyrosine
kinase intron 3 (MUSK I3) nuclear loci. Partitioning considerably improved mean lnL values in the Bayesian analyses, with unpartitioned arithmetic
mean lnL = 35,190.36, compared with 34,147.09 for two partitions and 3341.47 for six partitions. Bayes factor comparison also indicated that
the 6-partitioned analysis provided better explanations than other data analyses: 2lnB (6-partitions/unpartitioned) = 3697.78, and 2lnB (6-partitions/2-
partitions) = 1611.24 significantly above the threshold value of 10. Bayesian posterior probabilities (PP) followed by bootstrap values (ML and MP,
respectively) are shown above the branches (only bootstrap values above 50 and PP values above 0.5 are shown for the main clades) for the
partitioned analyses. Note that the ID of the only sample of Selasphorus platycercus (LSUMNSB23428) included in the phylogeny presented by McGuire
et al. [25] is likely incorrect. Painting by Marco Pineda (courtesy of Juan Francisco Ornelas) showing Calothorax lucifer (male)
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 7 of 17
hummingbird species data set using only one individual
per species and the 6-partitions strategy (Additional file 8)
are shown in Fig. 3. The MP and ML reconstructions of
migratory behavior provided similar results with high
certainty in the bee hummingbirds, in which the phylo-
genetic position of migratory species indicates multiple
independent origin of long-distance migratory behavior
(Fig. 3ac). ML, MP, and the re-rooting method of Yang
Selasphorus platycercus
Atthis ellioti
Atthis heloisa
Selasphorus flammula
Selasphorus ardens/scintilla
Selasphorus calliope
Selasphorus rufus/sasin
Calypte anna
Calypte costae
Doricha eliza
Doricha enicura
Calothorax lucifer/pulcher
PLEPLIOMIOCENE
20 Ma 15 10 5 present
2.0 Ma
1
1
1
1
1
0.99
0.99
0.99
0.99
1
1
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
0.99
Mountain
Gems
Emeralds
South American
bee
hummingbirds
(Woodstars)
Calliphlox evelynae
Calliphlox lyrura
Mellisuga minima
Archilochus colubris
Archilochus alexandri
ABCDE
AC
AB
A
B
C
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
*
ab
AB
C
D
E
A
D
Selasphorus
subclade
Mexican
Sheartails
subclade
Caribbean
Sheartails
subclade
Calypte
subclade
North American bee hummin
g
birds
E
F
G
H
I
K
J
NA Selasphorus CA Selasphorus
L
Fig. 2 aBiogeographic regions used in the RASP analysis: A = western North America, B = eastern North America, C = southeastern Mexico and
Central America, D = West Indies, and E = South America. bChronogram of the Mellisugini lineages based on the third calibration method
(secondary calibration + substitution rates) with a Yule speciation model for the combined ND2 and ND4 mitochondrial genes and FBG I7,AK1 I5,
ODC1, and MUSK I3 nuclear loci data set. Purple bars indicate 95% Highest Posterior Density (HPD) intervals for selected nodes. The pink dotted
vertical lines denote the time span of the Pliocene. Results using Bayesian methods with BBM (Bayesian Binary MCMC) analyses implemented in
RASP [55] are drawn on this topology. The ancestral origin for each taxon, as delimited in (a), is shown on the terminal lineages. Pie charts at
nodes represent the probabilities of the ancestral distributions. These probabilities account for the phylogenetic uncertainty in the rest of the tree
and the biogeographic uncertainty at each node. Asterisks next to main nodes refer to posterior probability support for each node (* > 0.8
posterior probability). Painting by Marco Pineda (courtesy of Juan Francisco Ornelas) showing Calothorax pulcher (male)
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 8 of 17
Table 1 Divergence dates (MYA) of bee hummingbirds for various nodes estimated with a Bayesian uncorrelated lognormal relaxed-clock approach using a Yule speciation tree
prior as implemented in BEAST
Node Several-individuals Single-individual
Secondary calibration + substitution rates Secondary calibration Substitution rates Secondary calibration + substitution rates
PP Mean (95% HPD) PP Mean (95% HPD) PP Mean (95% HPD) PP Mean (95% HPD)
Node A: Bee hummingbirds/\Mountain Gems 1.0 14.08 (15.5412.51) 1.0 11.83 (13.799.85) 1.0 19.97 (24.8115.64) 0.99 12.49 (13.5811.37)
Node B: SA/NA bee hummingbirds 1.0 9.93 (11.947.92) 0.99 7.68 (9.815.60) 1.0 12.50 (16.049.11) 1.0 5.92 (6.595.24)
Node C: NA crown (Mex. sheartails/other) 1.0 8.03 (9.826.44) 0.99 6.32 (8.244.51) 1.0 9.56 (12.177.05) 1.0 4.98 (5.604.41)
Node D: Caribbean Sheartails/other 1.0 7.51 (9.145.95) 1.0 5.95 (7.834.27) 1.0 8.90 (11.316.59) 1.0 4.77 (5.364.23)
Node E: Calypte subclade/other 0.99 5.72 (7.204.31) 0.99 4.12 (5.622.73) 1.0 6.71 (9.084.87) 0.99 3.11 (3.612.62)
Node F: CA Selasphorus/NA Selasphorus 0.99 4.14 (5.273.04) 0.99 3.1 (4.291.97) 1.0 4.79 (9.084.87) 0.99 2.18 (2.611.80)
Node G: Mexican Sheartails crown 1.0 3.61 (5.112.39) 0.99 3.09 (4.661.70) 1.0 4.39 (6.172.71) 1.0 2.20 (2.761.69)
Node H: Caribbean sheartails crown 0.99 5.75 (7.354.21) 0.99 4.61 (6.213.13) 1.0 6.93 (9.284.86) 0.99 4.04 (4.613.44)
Node I: Calypte crown 0.99 3.09 (2.580.90) 0.99 2.56 (3.791.40) 1.0 3.46 (5.221.96) 0.99 2.14 (2.611.69)
Node J: CA Selasphorus crown 0.99 3.31 (4.422.29) 0.99 2.23 (3.211.33) 1.0 3.82 (5.122.57) 0.99 1.43 (1.771.10)
Node K: NA Selasphorus crown 0.99 3.66 (4.742.60) 0.99 2.64 (1.610.48) 1.0 4.24 (5.812.86) 0.99 1.16 (1.530.79)
Node L: South American crown 1.0 5.42 (7.043.81) 0.99 5.44 (7.383.67) 1.0 6.44 (8.724.32) 1.0 4.30 (4.943.65)
Posterior probabilities (PP) given for each node; estimates are given as mean ages (in millions of years) with 95% Highest Posterior Density (HPD) intervals in parentheses. The divergence time (mean 12.0 MYA, SD ± 1,
range of 13.910.3 MYA) between mountain gems and bee hummingbirds [25] was used for temporal calibration of the root node of the tree and the mean substitution rates proposed by Lerner et al. [54] to model
the tree prior. Node letters correspond to those in Figs 23.NA North America, SA South America, CA Central America
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 9 of 17
et al. [67] ancestral-state reconstructions supported a
sedentary ancestral mellisuginid (bee hummingbird) re-
gardless of the coding scheme used for migratory behavior
(Fig. 3ac). Because the results using the various coding
schemes were largely the same, we only present the results
based on one of the coding schemes for each of the ances-
tral state reconstructions: parsimony and species with
partial migration (C. lucifer and S. platycercus) coded as
polymorphic (Fig. 3a), and maximum likelihood and re-
rooting with C. lucifer and S. platycercus coded as migra-
tory (Fig. 3bc). Basal nodes of all North American
subclades (incl. Monophyly of Caribbean sheartails) were
reconstructed with strong support for the sedentary state
with MP, ML and re-rooting methods (Fig. 3ac), and
migratory behavior was gained four times during the evo-
lution of the Mellisugini: once in the Mexican sheartails
subclade (Calothorax lucifer) and the Caribbean sheartails
subclade (Archilochus species), and twice in the Selas-
phorus subclade (Selasphorus rufus,S. sasin and S.
calliope group and S. platycercus). Similar results were ob-
tained for the MP, ML and re-rooting ancestral state
reconstructions using the data set with several samples
(Fig. 3d), except that migratory behavior was been lost at
least once in S. platycercus (see also [37]).
Discussion
Phylogeny of bee hummingbirds
Our phylogenetic analyses recovered a monophyletic
South American clade sister to other bee hummingbirds
in Central America, the Caribbean islands and North
America. Despite this, the backbone of our tree topology
is not entirely consistent with that for previous studies
b
da
Sedentary
Migratory
Node Absent
Equivocal
c
Selasphorus platycercus
*
Atthis heloisa
Atthis ellioti
Selasphorus flammula
Selasphorus ardens
Selasphorus scintilla
Selasphorus calliope
Selasphorus rufus
Selasphorus sasin
Calypte anna
Calypte costae
Calliphlox evelynae
Calliphlox lyrura
Archilochus colubris
Archilochus alexandri
Mellisuga minima
Doricha eliza
Doricha enicura
Calothorax pulcher
Calothorax lucifer*
Calliphlox mitchellii
Calliphlox bryantae
Chaetocercus bombus
Chaetocercus mulsant
Microstilbon burmeisteri
Eulidia yarrellii
Thaumastura cora
Myrmia micrura
Rhodopis vesper
Myrtis fanny
Calliphlox amethystina
Tilmatura dupontii
Sedentary
Migratory
Node Absent
Equivocal
Sedentary
Migratory
3. Re-rooting method
1. Parsimony
Sedentary
Migratory
Node Absent
Equivocal
2. Maximum-likelihood
Sedentary
Migratory
Node Absent
Equivocal
Species node
South American
bee
hummingbirds
(Woodstars)
Selasphorus
subclade
Mexican
Sheartails
subclade
Caribbean
Sheartails
subclade
Calypte
subclade
North American bee hummin
g
birds
Selasphorus platycercus CHIS200
Selasphorus platycercus CHIS201
Selasphorus platycercus CORO102
Selasphorus platycercus TLAX206
Selasphorus platycercus CHIS197
Selasphorus platycercus CHIS199
Selasphorus platycercus SWRS111
Selasphorus platycercus SWRS112
Selasphorus platycercus SWRS114
Selasphorus platycercus SWRS113
Selasphorus platycercus TLAX207
Atthis ellioti CJC272
Atthis ellioti CJC274
Atthis ellioti RAJ179
Atthis heloisa AHE02VER
Atthis heloisa AHE03HGO
Atthis heloisa FMNH343218
Atthis heloisa UNAMOVMP1041
Atthis heloisa AHE04PUE
Selasphorus sasin LSUMZB33988
Selasphorus sasin LSUMZB43116
Selasphorus sasin LSUMZB3117
Selasphorus sasin MVZ182025
Selasphorus sasin MVZ183552
Selasphorus sasin MVZ182072
Selasphorus rufus SRU01HGO
Selasphorus rufus SRU02HGO
Selasphorus rufus SRU04TLAX
Selasphorus rufus MVZ180196
Selasphorus sasin MVZ182183
Selasphorus rufus SRU06TLAX
Selasphorus rufus LSUMZB19586
Selasphorus sasin MVZ180632
Selasphorus rufus SRU03HGO
Selasphorus rufus SRU05TLAX
Selasphorus sasin MVZ180045
Selasphorus [platycercus] rufus LSUMNSB23428
Selasphorus flammula LSUMZB16222
Selasphorus flammula LSUMZB19794
Selasphorus flammula LSUMZB19847
Selasphorus flammula LSUMZB28246
Selasphorus flammula LSUMZB28253
Selasphorus flammula LSUMZB28260
Selasphorus flammula LSUMZB28313
Selasphorus flammula LSUMZB9952
Selasphorus flammula LSUMZB19883
Selasphorus flammula LSUMZB28269
Selasphorus ardens LSUMZB52914
Selasphorus ardens MBM18307
Selasphorus ardens LSUMZB52913
Selasphorus ardens LSUMZB52915
Selasphorus scintilla LSUMZB16266
Selasphorus calliope LSUMZB16854
Selasphorus calliope LSUMZB23775
Selasphorus calliope LSUMZB26272
Selasphorus calliope MVZ175821
Selasphorus calliope MVZ170138
Selasphorus calliope MVZ182182
Calypte anna LSUMZB24864
Calypte anna MNCN13108
Calypte anna MNCN13142
Calypte anna MNCN13036
Calypte anna MNCN13143
Calypte anna MNCN13153
Calypte costae CJC210
Calypte costae LSUMZB21595
Calypte costae CAC03BCS
Calypte costae CAC01BCS
Calypte costae CAC02BCS
Calliphlox evelynae LSUMZB59204
Calliphlox evelynae LSUMZB58890
Calliphlox evelynae YPM142568
Calliphlox evelynae YPM142569
Calliphlox evelynae YPM142570
Calliphlox lyrura YPM142566
Calliphlox lyrura YPM142567
Calliphlox lyrura YPM142564
Calliphlox lyrura YPM142562
Calliphlox lyrura YPM142565
Mellisuga minima MVZ183600
Mellisuga minima MVZ183602
Mellisuga minima STRIJAMM11
Archilochus colubris ACO04OAX
Archilochus colubris ACO05OAX
Archilochus colubris ACO02YUC
Archilochus colubris ACO03YUC
Archilochus colubris LSUMZB5270
Archilochus alexandri ARAO1CHI
Archilochus alexandri LSUMZB21848
Archilochus alexandri MNCN13145
Archilochus alexandri MNCN13151
Doricha eliza VER01LEN
Doricha eliza VER04XAL
Doricha eliza VER23LEN
Doricha eliza VER25LEN
Doricha eliza VER26ACT
Doricha eliza VER24LEN
Doricha eliza KU4435
Doricha eliza YUC09RLA
Doricha eliza YUC10RLA
Doricha eliza YUC18CHI
Doricha eliza UNAMB590
Doricha enicura DEN14COM
Doricha enicura RAJ182
Doricha enicura YPM142508
Doricha enicura DEN16COM
Calothorax pulcher CAL02VER
Calothorax pulcher PUE135
Calothorax pulcher CAP02OAX
Calothorax pulcher CAP04OAX
Calothorax pulcher CAP03OAX
Calothorax lucifer DF136
Calothorax lucifer LSUMZB43113
Calothorax lucifer YPM141067
Calothorax lucifer CAL07TLAX
Calothorax lucifer CAL11HGO
Calliphlox mitchellii LSUMZB12194
Calliphlox mitchellii LSUMZB2310
Calliphlox bryantae LSUMZB28180
Chaetocercus bombus LUMMZB5225
Chaetocercus mulsant LUMMZB6301
Microstilbon burmeisteri ZMC114932
Eulidia yarrellii WV022
Thaumastura cora LSUMZB14278
Thaumastura cora MSBBird33004
Myrmia micrura LSUMZB5233
Rhodopis vesper JOSE2
Rhodopis vesper LSUMZB14277
Myrtis fanny LSUMNZB3592
Calliphlox amethystina NMNHB10703
Tilmatura dupontii KU8188
Tilmatura dupontii PD1
B
C
D
G
H
E
I
K
F
J
L
123
Selasphorus platycercus*
Atthis heloisa
Atthis ellioti
Selasphorus flammula
Selasphorus ardens
Selasphorus scintilla
Selasphorus calliope
Selasphorus rufus
Selasphorus sasin
Calypte anna
Calypte costae
Calliphlox evelynae
Calliphlox lyrura
Archilochus colubris
Archilochus alexandri
Mellisuga minima
Doricha eliza
Doricha enicura
Calothorax pulcher
Calothorax lucifer*
Calliphlox mitchellii
Calliphlox bryantae
Chaetocercus bombus
Chaetocercus mulsant
Microstilbon burmeisteri
Eulidia yarrellii
Thaumastura cora
Myrmia micrura
Rhodopis vesper
Myrtis fanny
Calliphlox amethystina
Tilmatura dupontii
Selasphorus platycercus*
Atthis heloisa
Atthis ellioti
Selasphorus flammula
Selasphorus ardens
Selasphorus scintilla
Selasphorus calliope
Selasphorus rufus
Selasphorus sasin
Calypte anna
Calypte costae
Calliphlox evelynae
Calliphlox lyrura
Archilochus colubris
Archilochus alexandri
Mellisuga minima
Doricha eliza
Doricha enicura
Calothorax pulcher
Calothorax lucifer*
Calliphlox mitchellii
Calliphlox bryantae
Chaetocercus bombus
Chaetocercus mulsant
Microstilbon burmeisteri
Eulidia yarrellii
Thaumastura cora
Myrmia micrura
Rhodopis vesper
Myrtis fanny
Calliphlox amethystina
Tilmatura dupontii
Sedentary
Migratory
B
C
L
G
I
K
J
F
E
D
H
B
C
L
G
I
K
J
F
E
D
H
B
C
L
G
I
K
J
F
E
D
H
321
Fig. 3 Ancestral state reconstructions across the set of 18,000 post burn-in BEAST trees for the Mellisugini based on parsimony in which species
with migratory and sedentary populations (Selasphorus platycercus and Calothorax lucifer) were coded as polymorphic (a) or migratory (b), and
estimation of ancestral states of migratory behavior carried out with the tree obtained from the Bayesian analysis under the ML criterion and the
MK1 model using all samples (c). Ancestral state reconstructions results obtained for the MP, ML and re-rooting methods using the data set with
several samples (d). Each square at the tips of the tree represents the state of each extant taxon and the pie charts at each node represent the
probability of the state of the common ancestor present at that node. Dark gray squares indicate fully migrant individuals and white squares
indicate sedentary individuals. Asterisks next to species names indicate species with migratory and sedentary populations. Painting by Marco
Pineda (courtesy of Juan Francisco Ornelas) showing Calothorax lucifer (female)
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 10 of 17
with fewer taxa and individual samples ([25, 72]; see
Additional file 7). According to our analyses, Mexican
sheartails split very soon after the split between South
American and North American bee hummingbirds, and
sister to remaining subclades. The Selasphorus subclade
is composed of two groups according to our results, the
North American Selasphorus (S. calliope,S. sasin,S. rufus)
and the Central American Selasphorus arranged by geog-
raphy, S. flammula,S. scintilla and S. ardens from Costa
Rica and Panama and S. platycercus,Atthis heloisa and A.
ellioti mainly from Mexico and Guatemala.
Our DNA sequence data set (including 162 samples
and 26 loci for each sample) contains 8.8% missing
data, and this incompleteness is unlikely to have nega-
tively impacted the accuracy of phylogenetic reconstruc-
tion because the number of characters in the analysis is
large [73, 74]. Perhaps adding more taxa and more
samples per taxon improved the accuracy of our phylo-
genetic reconstruction, in which monophyly of the
Caribbean sheartails (Archilochus,Mellisuga,Calliphlox)
is strongly supported. Lastly, our dense individual
sampling within S. platycercus indicated that this species
is nested within the group of Central American Selas-
phorus and Atthis species, the Selasphorus subclade, and
did leverage our phylogenetic and ancestral state recon-
structions from ID errors in single-individual species
representation of previous phylogenetic reconstructions.
Divergence dating and ancestral areas of bee
hummingbirds
According to our results, the crown age of the Mellisugini,
ca. 9.93 MYA using the several-individualsdata set and
the secondary calibration + substitution ratescalibration
strategy, is older than those estimated by McGuire et al.
[25] and Abrahamczyk and Renner [72], 5.3 and 7.226.71
MYA, respectively. When using the single-individuals
data set and the secondary calibration + substitution rates
calibration strategy, the crown age of the Mellisugini is
similar, ca. 6.595.24 MYA (Table 1). These obvious
differences across studies are likely due to the different
calibration strategies and taxon sampling employed.
McGuire et al. [25] included 27 species and 61 samples of
bee hummingbirds and Abrahamczyk and Renner [72] 25
species and 26 samples, whereas our study included 32
species and 132 samples. A discrepancy in age estimates is
observed in the comparison of the posterior mean age es-
timates between the single-individualspecies samples and
the several-individualsspecies samples (taxon sampling
variation) for the 6-partitions data sets (Table 1). In this
case, we know that all sampling and data conditions are
identical between the two analyses except for the density
of taxon sampling within species. The age estimates for
the Mellisugini (nodes BL) differ on average by about 2
MYA, with the all sampling consistently yielding older
ages leading to very different biogeographic conclusions.
Although the difference is greater for the deeper nodes in
the tree, the impact becomes minor as one moves to the
tips of the tree (Fig. 2, Table 1). Our results indicated that
different sampling strategies have yielded different
estimates and potential errors in molecular dating likely
due to sampling bias for recent evolutionary radiations. In
discussing age estimates in the subsequent discussion, we
refer primarily to the posterior mean point estimated
obtained with the several-individualsspecies samples for
the 6-partitions data set with more precision in divergence
time estimation of shallow nodes.
The early divergences within the Mellisugini are esti-
mated to have occurred after the mid-Miocene climatic
optimum (nodes B, C and D of Fig. 2; [75]), but the
majority of divergence events occurred much later, from
the Pliocene to the mid-late Pleistocene (Fig. 2). Based
on these results, we propose that the formation of the
mountain systems in Mexico and Central America from
mid-Miocene to the Pliocene was critical in providing
favorable habitats and climatic conditions for the
divergence of bee hummingbirds in the region. The bee
hummingbirds dispersed to North America in the mid-
Miocene, and then its history was probably marked by a
period of expansion to xeric environments and segrega-
tion into xeric and moist temperate forests directly
associated with a global decrease in temperature and
humidity during the Late Miocene [76] and desert
formation in North America [77]. Divergences of the
Mexican sheartails and the Calypte and Archilochus
species from their ancestors (Fig. 2) dated at 8.03, 5.72
and 5.76 MYA, respectively, coincides with the Miocene
peak in speciation rates in some plants characteristic of
xeric environments in Mexico, including Agave [78] and
cacti [79], through a region of the country similar to that
through which Calothorax is currently distributed and
feed upon. The radiation of the Mellisugini in Central
America, Caribbean islands and North America must
have been relatively rapid. During the Late Miocene, the
lineage would already be possibly occupying the main
mountain ranges in Central America, and occurring in
Mexico, in both montane and dry environments. The
divergences of Calothorax,Archilochus, and the NA
Selasphorus from their sedentary ancestors are dated at
3.09, 5.75, 4.14 MYA, respectively, suggesting that these
divergences occurred in the Pliocene. These divergences
also coincide with the second peak in speciation rates in
Agave sensu lato dated at 32.5 MYA influenced by
nectar feeding bats [78], and the transition from bee-
pollination to hummingbird-pollination in Mexico in the
Opuntia-Nopalea cacti clade dated at 5.73 MYA (95%
HPD 8.73.42 MYA; [80]). In contrast, divergence of
migratory S. platycercus from its sedentary ancestor is
dated at 1.54 MYA (95% HPD 2.270.93 MYA),
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 11 of 17
suggesting that the evolution of migration in S. platycer-
cus occurred in the Pleistocene as shown by ancestral
state reconstruction (Fig. 3).
The Late Miocene ages of hummingbird-dependent
plant clades in North America (95 MYA; [72] coincide
with the timings of divergence events of bee humming-
birds during the Pliocene and mid-late Pleistocene
(Table 1). Our interpretation is also supported by the
age of the oldest hummingbird-adapted group in North
America, Lonicera (Caprifoliaceae), with a stem age of
9.2 MYA and a crown age of 7.0 MYA [81], the age of
hummingbird-pollinated Psittacanthus mistletoes in
Mexico with a stem age of 9.68 MYA and a crown age
of 7.43 MYA [82, 83], and by the Pleistocene origin of
Penstemon in the Rocky Mountains with subsequent mi-
gration and radiation to the CascadeSierra Nevada cor-
dillera and then into southwestern North America and
throughout eastern North America [84]. Interestingly,
range expansions of bee hummingbirds in North Amer-
ica during the Pliocene seem to correspond to Pliocene
divergences within the hummingbird-pollinated Psitta-
canthus mistletoes apparently linked to habitat shifts
[82, 83]. For instance, the ages of the Calothorax shear-
tails, with a stem age of 3.6 MYA (95% HPD 5.112.39
MYA) and a crown age of 2.4 MYA (95% HPD 3.61
1.41 MYA), coincide with the timing of divergence
events of the Psittacanthus mistletoes they currently pol-
linate (P. auriculatus distributed in the xeric areas of
Oaxaca and P. calyculatus distributed in pine-oak forests
along the Trans-Mexican Volcanic Belt; [8587]), with a
stem age of 3.1 MYA and a crown age of 1.8 MYA [82,
83]. The ages of Calypte costae, with a stem age of 3.1
MYA (95% HPD 4.491.78 MYA) and a crown age of
1.7 MYA (95% HPD 2.580.91 MYA), coincide with the
timing of divergence events of the Psittacanthus mistle-
toes they currently pollinate in the Sonoran Desert, P.
sonorae, with a stem age of 4.8 MYA and a crown age of
0.3 MYA [82, 83].
Like the hummingbirds and their coevolved plants in
North America, the earliest divergence within the
Caribbean sheartails (5.7 MYA; Table 1) indicates that
they were also contemporaneous with lineages of
hummingbird-adapted flowers [72, 88]. Overall, the
results of our divergence-dating analysis seem to indicate
that the Pliocene range expansions of bee hummingbirds
are connected with the biogeography of their host plants
and provide interesting insights on how range expansions
into North America via habitat changes facilitated the evo-
lution of migration in this group.
Evolution of migratory behavior
Our study is the first to provide phylogenetic evidence
for the repeated evolution of long-distance migratory be-
havior in the radiation of the Mellisugini, with the crown
ancestors of the main clades and North American sub-
clades reconstructed as sedentary. Our results suggest
that long-distance seasonal migration arose independ-
ently four times in the Mellisugini: once in the Mexican
sheartails subclade (Calothorax lucifer) and the Carib-
bean sheartails subclade (Archilochus species), and twice
in the Selasphorus subclade (Selasphorus rufus,S. sasin
and S. calliope group and S. platycercus). Our study also
showed that migratory lineages are generally more
closely related to non-migratory lineages than to other
migratory lineages, and that long-distance seasonal mi-
gration arose at different times. For instance, the split
between migratory Archilochus species and sedentary
species endemic to the Caribbean islands (Mellisuga and
Calliphlox species) occurred at 5.7 MYA, whereas gen-
etic differentiation between migratory C. lucifer and S.
platycercus and their sedentary ancestors seem to have
started during the late Pleistocene.
Our ancestral area reconstruction appears to explain the
migration patterns of earliest Archilochus species, earliest
A. colubris breeding in eastern NA (USA and Canada) and
migrant to mainly eastern Mexico, Central America and
some Caribbean islands, and A. alexandri breeding in
western NA (USA and Canada) and migrant to western
Mexico. A phylogeographic approach accompanied with
paleodistributional modeling would be needed to test
whether the differences in migratory patterns between Ar-
chilochus sister species were influenced by Pleistocene cli-
mate change and their range shifts occurred earlier. Using
ecological niche modeling and phylogeographic data, Mal-
pica and Ornelas [37] showed first that S. platycercus is a
niche tracker and then that the climate conditions associ-
ated with modern obligate migrants in the USA were not
present during the LIG, which provides indirect evidence
for recent migratory behavior in S. platycercus on the tem-
poral scale of glacial cycles. Their study also revealed that
the evolution of migration within S. platycercus produced
no significant genetic structure using nuclear microsatel-
lites (nSSRs), migratory and sedentary groups of popula-
tions form an admixed population. The fact that they
detected no significant genetic differentiation between
migratory populations of S. platycercus and sedentary
populations of the species in central Mexico (platycercus
subspecies) is surprising because these hummingbirds in-
habit different breeding areas of the USA and Mexico, and
no evidence of sympatry at overwintering sites in Mexico
has been noted. However, phylogeographic analyses and
population genetic methods revealed that both migratory
populations in the USA and sedentary populations in
Mexico of the platycercus subspecies form one admixed
population, and that sedentary populations from southern
Mexico and Guatemala (guatemalae subspecies) diverged
earlier (0.75 MYA) and undertook independent evolution-
ary trajectories [37].
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 12 of 17
Several studies have explicitly outlined a similar frame-
work for addressing the evolution of bird migration
between North and Central America, in particular for
species with migratory populations in Canada and USA
and sedentary populations in Mexico and Central
America [10, 89]. For example, Milá et al. [90] examined
the evolution of migration in the chipping sparrow
(Spizella passerina) with sedentary populations in Mexico
and the southern USA and migratory populations in the
northern USA and Canada, and found evidence that
migration was driven by northern range expansion from
sedentary populations following glacial episodes.
Our study provides phylogenetic evidence for a seden-
tary origin for the Mellisugini, but certainly is not the
first to deal with this question in birds of the Northern
Hemisphere (e.g., [60, 8998]). Studies that have
reconstructed the ancestral state of migration in a
phylogenetic context have found either equivocal results
[93, 99, 100] or results in favor of a migratory [10, 60, 101]
or a sedentary ancestor [89, 92, 98, 102104]. Accord-
ing to a well-supported molecular phylogeny of Cath-
arus thrushes sensu lato (incl. Hylocichla mustelina),
long-distance seasonal migration is reconstructed as
the ancestral condition at most basal nodes when put-
ting character changes as close to the root of the tree
as possible (ACCTRAN resolving option), and north of
Mexico is reconstructed as the ancestral area with the
origin of the clade at 8 MYA, diversification of
Catharus from Hylocichla occurring at 6.9 MYA, and
further lineage divergence within Catharus starting in
the early Pliocene at 4.7 MYA [10]. Within Catharus,
migratory behavior was lost after the first speciation
event in the genus and was geographically and tempor-
ally correlated with Central American distributions and
the final closure of the Central American Seaway.
Subsequently, migratory behavior was re-gained twice
in Catharus and was geographically and temporally
correlated with a re-colonization of North America in
the late Pleistocene [10]. Counter to our results for the
Mellisugini, the ancestral wood-warbler (Parulidae) was
reconstructed as migratory using the well-supported
molecular phylogeny of Lovette et al. [97], with losses
of migration as prevalent as gains throughout the
evolutionary history of Parulidae [60]. These results
suggest that extant sedentary tropical radiations in the
Parulidae represent losses of long-distance seasonal mi-
gration and colonization of the tropics from temperate
regions [60]. However, many derived non-migratory
clades descended from non-migratory ancestors, sup-
porting the notion that the ancestor of the Parulidae
was a non-migrant [98]. Using a phylogenetic model of
the joint evolution of breeding and non-breeding,
wintering ranges to infer the biogeographic history in
the emberizoid passerine birds, Winger et al. [101]
found that seasonal migration between breeding ranges
in North America and winter ranges in the Neotropics
evolved primarily via shifts of winter ranges toward the
tropics from ancestral ranges in North America.
In the Mellisugini, it seems that migration evolved out
of the tropics through the northern extension of
ancestral tropical or subtropical breeding ranges into
temperate regions (southern home-theory; [6, 9]).
According to results of the Rolland et al.s [8] study that
included most extant bird species, we infer that seden-
tary behavior is ancestral and migratory behavior evolved
several times during the evolutionary history of the
Mellisugini. Testing increased diversification rates in the
Mellisugini with the evolution of migration is hampered
by the lack of statistical power (see [8] for further
discussion). Nonetheless, the divergence of a migratory
species into two migratory daughter species tend to be
less frequent that the divergence of a sedentary species
into two sedentary daughter species, consistent with the
findings of Rolland et al. [8] and predictions of Helbig
[5] and Claramunt et al. [105] that genetic differentiation
is reduced in migratory species with high dispersal
capacity. The results of Rolland et al.s [8] study suggest
that the mobility of migratory species promotes the
colonization of new areas and, if adapted to the new
habitat, populations can become sedentary and diverge
from the founding migratory species.
Several factors would have influenced the way bee hum-
mingbirds colonized the northern portion of North Amer-
ica in the mid-Pliocene. Following the first dispersal of
ancestral Archilochus hummingbirds from the Caribbean
islands to the northeast and northwest of North America,
either along the coastal slope or across the Gulf of
Mexico, it is possible that range changes in the Pleistocene
caused multiple populations to lose migration and stay
restricted to the Caribbean Islands with subsequent speci-
ation. Successful dispersal of North American Selasphorus
hummingbirds occurred from Central America and
southern Mexico to the northwest of the continent. The
evolution of migratory populations from ancestral seden-
tary populations in southern Mexico of S. platycercus
occurred later, likely due to Pleistocene climate changes
(see also [90]). These scenarios are consistent with the
idea that geographic isolation during the Late Pleistocene
account for intraspecific and sister-species-level diver-
gence largely based on habitat shifts influenced by climate
change (e.g., [102, 106108]), particularly shifts subse-
quent to the LGM produced distinct migratory pathways
and further genetic differentiation [93, 109]. Therefore, it
seems that divergence of a migratory species into two mi-
gratory daughter species is linked to a seemly rare event
of changing migratory trajectories widely documented in
some songbirds (e.g., [93, 109116]). Further study using
a comparative phylogeographic approach accompanied
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 13 of 17
with ecological niche modeling and more or faster mo-
lecular markers (e.g., SNPs, SSRs) should provide finer
resolution to the history of migration in the Mellisugini,
particularly for contrasts between shallow lineages with
sedentary and migratory species (e.g., Calothorax lucifer/
C. pulcher). For testing the effects of cyclical glacial
changes on producing seasonally unstable habitats, and
driving northward expansion and the evolution of sea-
sonal migration and contraction into southern sedentary
populations, and increased sampling of South American
woodstars, further study will be needed to test whether
the evolution of long-distance seasonal migration in North
American bee hummingbirds has facilitated diversification
in the Mellisugini through the divergence of migratory
subpopulations that become sedentary [8, 60].
We cannot eliminate the possibility that long-distance
migratory behavior evolved relatively early in the evolu-
tion of the Mellisugini. If this was the case, a migratory
ancestor lost migration multiple times. Under this hy-
pothesis colonization of North America and the Carib-
bean Islands would be more likely, despite that the
phylogenetic evidence of that migratory ancestor is now
lost, as temperate niches remained relatively open with
ephemeral resources with subsequent losses of migratory
at later times environments became less seasonal. If this
model were statistically supported, its results would sug-
gest that long-distance migratory behavior evolved once in
the base of the Mellisugini tree, with several subsequent
losses towards the end of the Pliocene. In coding SA bee
hummingbirds and mountain-gems as migratory as-
suming that a migratory ancestor lost migration mul-
tiple times, ancestral character state reconstruction
yielded equivocal results for the node of the Mellisu-
gini and further ancestral nodes within the tribe were
reconstructed as sedentary. When forcing only SA
bee hummingbirds to be migratory, both the node of
the Mellisugini and further ancestral nodes for main
clades within the tribe were reconstructed as seden-
tary (Results not shown).
Coxs [11] model predicts that migratory species will be
derived from sedentary species within the seasonal sub-
tropics, and that migratory behavior is a derived character
state. We believe that the Mellisugini lineage fits this
model in many ways, particularly because most migrant
species are closely related to the sedentary species found
in the seasonal highlands of Mexico and Central America.
An important result of our study is that long-distance mi-
gratory species do not form a monophyletic group. The
relationships between migrant and resident species within
the Mexican sheartails, Caribbean sheartails, and
Selasphorus subclades are more complex than we ex-
pected. Also, the repeated gains of migration occurred
during the Late Pliocene and this suggests that potential
responses, i.e. the temporal evolution of migratory
behavior, can be linked to historical, climatic and eco-
logical events on a phylogeny [7, 10]. However, we
cannot ignore the possibility that long-distance migra-
tory behavior in the Mellisugini was the ancestral
state with several drop-offs of migration. Given the high
degree of lability of the trait [3436] and assuming that
the phylogenetic signal of long-distance migratory behav-
ior in the Mellisugini is an artifact of phylogenetic inertia
in biogeographic range (including latitude and
temperature seasonality), these questions seem unanswer-
able, making long-distance seasonal migration non tract-
able over substantial evolutionary time until comparative
genomic data sets for migratory/sedentary closely related
species pairs and for migratory and non-migratory popu-
lations of species with partial migration become available.
Conclusions
Pliocenes mountain building in Mexico and Pleistocene
climate changes were the primary feature that structured
diversity in the Mellisugini. These results are consistent
with Coxs [12] idea that the Mexican Plateau and arid
southwestern United States have acted as staging
areas for the evolution of hummingbird migration.
Range expansions of early lineages of the Mellisugini seem
to be connected with the biogeography of their host plants
and provide interesting insights on how range expansions
into North America via habitat changes facilitated the evo-
lution of migration in this group. Recently evolved lineages
in all subclades of the Mellisugini appear to have under-
gone long-distance seasonal migration, albeit in different
directions. This history of repeated evolution of migration
within the Mellisugini allowed for divergence across com-
mon biogeographic regions spanned by North American
bee hummingbirds. It is likely that, without repeated evo-
lution of migration in different directions, diversification
of the Mellisugini would have decelerated towards the
present [25]. Thus, molecular patterns of diversification
within the Mellisugini reflect a dynamic history of
divergence, the main lineages during the Pliocene linked
to the formation of the mountain systems in Mexico and
Central America and further divergence by the evolu-
tion of seasonal migration during the Pleistocene.
Additional files
Additional file 1: Primers employed in this study. (DOC 39 kb)
Additional file 2: Species names, voucher information, locality, and
GenBank accession numbers for specimens sequenced in this study.
(DOC 102 kb)
Additional file 3: Species names, distributional codes and migratory
status for ancestral state reconstruction analyses of the Mellisugini
species used in this study. A = western North America, B = eastern
North America, C = eastern Mexico and Central America, D = West Indies,
E = South America; M = migratory, S = sedentary (binary character
codification). (DOC 169 kb)
Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 14 of 17
Additional file 4: Migratory status of the Mellisugini species for
ancestral state reconstruction analysis used in this study. M = migratory,
S = sedentary. (DOC 57 kb)
Additional file 5: Species names, English names and distributional
range for the Mellisugini species used in this study. (DOC 75 kb)
Additional file 6: Bayesian 50% majority rule consensus trees of 132
representatives of bee hummingbirds (32 of the 36 extant species, 89%),
15 of mountain gems and 15 of emeralds. The trees are based on data
sets of (a) only mitochondrial genes (unpartitioned mtDNA data set), (b)
only mitochondrial genes as two partitions (partitioned mtDNA data
set), (c) only nuclear genes (unpartitioned nuDNA data set), and (d)
only nuclear genes as four partitions (partitioned nuDNA data set).
Posterior probabilities (PP) > 0.5 are shown. (PDF 930 kb)
Additional file 7: Comparison of backbone tree topologies of the
Mellisugini. (a) McGuire et al. [25], (b) Abrahamczyk & Renner [72], and
(c) Bayesian 50% majority rule consensus tree of 32 bee hummingbird
species of this study in Additional file 7. Asterisks denote nodes with 1.0
posterior probability (PP) support. Numbers at nodes reflect posterior
probabilities less than 1.0. Support values for nodes of phylogeny in
(b) are not provided in Abrahamczyk & Renner [72]. (PDF 425 kb)
Additional file 8: Bayesian 50% majority rule consensus tree of 32 bee
hummingbird species and representatives of mountain gems and
emeralds used as outgroups. The tree is based on a combined data set
of all available fragments of ND2,ND4,AK1 I5,MUSK I3,ODC1 and FBG I7
and partition-specific DNA evolution models of each gene (6-partitions
data set). Posterior probabilities (PP) > 0.5 are shown. (PDF 404 kb)
Acknowledgements
We thank Cristina Bárcenas, Antonio Acini Vásquez, Andrés Ortíz-Rodríguez,
Clementina González, Flor Rodríguez-Gómez, Eduardo Ruiz-Sánchez, María
José Pérez-Crespo and Andreia Malpica for field and lab assistance; and
Cristina González-Rubio (CIBNOR), Borja Milá (MNCN-C SIC) and Rosa Alicia
Jiménez (MC: Escuela de Biología, USAC) for providing tissue samples
essential to this work. The samples collected in Mexico were conducted with
the permission of the Secretaría de Medio Ambiente y Recursos Naturales,
Instituto de Ecología, Dirección General de Vida Silvestre (permit numbers:
INE: SEMARNAP, D00-02/3269, INE SGPA/DGVS/02038/07, 01568/08, 02517/
09, 07701/11, 13528/14, 02577/15, 06448/16). Borja Milá provided useful
comments on previous versions of the manuscript. This work constitutes
partial fulfillment of Y.L.Vs doctorate in Biodiversity and Systematics at
INECOL.
Funding
This project was funded by the Departamento de Biología Evolutiva, Instituto
de Ecología, A.C. (INECOL) awarded to J.F.O. (20030/10563). Y.L.V. was
supported by a doctoral scholarship (262561) from CONACyT. The
publication costs were financed by the Dirección General of the INECOL
(20029/60813).
Availability of data and materials
Sequence reads can be accessed through GenBank under the Accession
Numbers KX855335KX855393 (ND2), KX855394KX855450 (ND4), KX855451
KX855509 (AK1 I5), KX855568KX855624 (MUSK I3), KX855510KX855567
(OCD1), KX855625KX855637 (FBG I7). The new sequence (FASTA) data
supporting the results of this article are available in the Dryad Digital
Repository (http://dx.doi.org/10.5061/dryad.68fn0) as Licona-Vera and Ornelas
[43].
Authorscontributions
The authors of this paper have a general interest in the evolutionary history
of hummingbirds. For this paper, YLV was involved in collecting most
samples and obtaining the molecular data, and together with JFO in
performing the phylogenetic and dating analyses, writing the manuscript
and interpreting the molecular and phylogenetic data. Both authors read
and approved the final manuscript.
Competing interests
The authors declare that they have no competing interests.
Consent for publication
No aspect of this study required written informed consent to participate.
Ethics approval and consent to participate
No aspect of this study required ethics approval.
Publishers Note
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Received: 28 January 2017 Accepted: 24 May 2017
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Licona-Vera and Ornelas BMC Evolutionary Biology (2017) 17:126 Page 17 of 17
... The same is true for other vertebrates, such as birds (e.g. babblers, white-eyes and bee hummingbirds: Cai et al. 2017;Licona-Vera and Ornelas 2017). ...
Article
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Lorisiformes are nocturnal primates from Africa and Asia with four genera, with two ( Arctocebus and Loris ), three ( Perodicticus ) and nine ( Nycticebus ) recognised species. Their cryptic lifestyle and lack of study have resulted in an underappreciation of the variation at the species and genus level. There are marked differences between the pygmy slow loris Nycticebus pygmaeus and the other Nycticebus species and, in the past, several authors have suggested that these may warrant recognition at the generic level. We here combine morphological, behavioural, karyotypical and genetic data to show that these contrasts are, indeed, significantly large and consistent. We propose Xanthonycticebus gen. nov. as a new genus name for the pygmy slow lorises and suggest a common name of pygmy lorises. Based on analysis of complete mitochondrial DNA sequences, we calculate the divergence of pygmy from slow lorises at 9.9–10.0%. The median date, calculated for the divergence between Xanthonycticebus and Nycticebus , is 10.5 Mya (range 4.9–21.0 Mya). Xanthonycticebus differs from Nycticebus by showing sympatry with other slow loris species, by habitually giving birth to twins, by showing seasonal body mass and whole body coat colour changes (absent in other species living at similar latitudes) and a multi-male, multi-female social system. Pygmy lorises are easily recognisable by the absence of hair on their ears and more protruding premaxilla. Xanthonycticebus is threatened by habitat loss and illegal trade despite legal protection across their range and all slow lorises are listed on appendix 1 of CITES. The suggested nomenclatural changes should not affect their legal status.
... For instance, synchronization of the flowering period with the movements and foraging activity of hummingbirds is important for the maintenance of ecological networks, given that plants provide nectar resources for hummingbirds (Junker et al., 2013;L opez-Segoviano et al., 2018;McKinney et al., 2012). In comparison to rangerestricted species, widely distributed hummingbird species facing broad environmental conditions that extend their geographical range might migrate tracking new floral nectar resources and colonizing new adequate habitat under future scenarios more readily than range-restricted species (Licona-Vera & Ornelas, 2017;Ornelas et al., 2015). ...
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Global climate change is associated with changes in precipitation patterns and an increase in extreme weather events, which might shift the geographic distribution of species. Despite the importance of this topic, information is lacking for many species, particularly tropical birds. Here, we developed species distribution models (SDMs) to evaluate future projections of the distribution of the widespread Buff-bellied Hummingbird (Amazilia yucatanensis) and for each of the recognized subspe-cies (A. y. yucatanensis, A. y. cerviniventris, A. y. chalconota), under climate change scenarios. Using SDMs we evaluate current and future projections of their potential distribution for four Representative Concentration Pathway (RCPs) for the years 2050 and 2070. We also calculated the subspecies climatic niche breadth to test the relationship between their area of distribution and climatic niche breadth and their niche overlap. Future climate-change models suggested a small increase in the potential distribution of the species and the subspecies A. y. yucatanensis, but the predicted potential geographic range decreased in A. y. chalconota and remained unaffected in A. y. cerviniventris. The climatic niche of A. y. cerviniventris contained part niche space of A. y. yucatanensis and part of A. y. chalconota, but the climatic niches of A. y. yucatanensis and A. y. chalconota did not overlap. Our study highlights the importance of correctly choosing the taxonomic unit to be analyzed because subspecies will respond in a different manner to future climate change; therefore, conservation actions must consider intrinsic requirements of subspecies and the environmental drivers that shape their distributions.
... 6.[p. 307] Phylogenetic analyses of nuclear and mitochondrial DNA sequences(McGuire et al. 2014, Licona-Vera andOrnelas 2017) have shown that Calliphlox as currently constituted is polyphyletic. These findings result in the following changes:Delete the genus heading, citation, and Notes for Calliphlox and replace them with the following heading, citation, and Notes:GenusPHILODICE Mulsant, Verreaux and Verreaux Philodice Mulsant, and J. and E. Verreaux, 1866, Mémoires de la Société Impériale des Sciences Naturelles de Cherbourg 12: 230. ...
... Or puisque les ancêtres de ces espèces migratrices sont d'origine tropicale, les scientifiques ont longtemps suggéré que la migration ait de fait évolué à partir des tropiques selon l'hypothèse SHT (ex. Outlaw et al. 2003, Licona-Vera & Ornelas 2017. Pourtant la migration a pu également apparaître en Amérique du Nord selon l'hypothèse NHT, chez des espèces sédentaires qui avaient déjà colonisées ces latitudes (à la suite de mouvements de dispersion). ...
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Si de nombreux animaux effectuent des migrations saisonnières, la migration des oiseaux demeure l’une des plus spectaculaires du règne animal et c’est d’abord parce qu’elle fascine les humains que cette migration est la plus étudiée depuis toujours. Mais malgré cet engouement précoce de la communauté scientifique, d’importantes interrogations persistent. Parmi celles-ci, les scénarios biogéographiques qui façonnent la distribution des espèces migratrices ou qui ont conduit des espèces ou des lignées entières à évoluer vers un comportement de migration saisonnière à longue distance restent peu compris.L'objectif de ma thèse était d’aborder ces questions à différents niveaux taxonomiques, afin d’étudier les implications écologiques et évolutives de la migration à longue distance chez les oiseaux. Plus précisément, (1) je me suis d’abord intéressé aux scénarios d’évolution biogéographique et des niches climatiques qui ont conduit à l’émergence de stratégies de migration géographique saisonnière à grande distance. (2) Resserrant le cadre taxonomique aux Charadriiformes, j’ai approfondi mes recherches sur la biogéographie de la migration en abordant la question du rôle de la migration dans les processus de diversification et la mise en place des gradients globaux de biodiversité. Pour mieux comprendre ces mécanismes évolutifs, j’ai également étudié (3) comment l’évolution de la coloration est reliée à l’évolution de stratégies de migration chez les Laridae et (4) l’influence de ces mouvements longues distances sur les autres évènements du cycle annuel chez une espèce d’oiseau marin de l’Arctique. (5) Enfin, à l’échelle intra-spécifique, je me suis penché sur la mise en place de nouvelles voies de migration chez deux de passereaux d’origine sibérienne pour explorer la question des rapides changements de distribution.Dans l'ensemble, les résultats de ces études montrent que les différentes facettes de l'écologie et l'évolution sont fortement intriquées pour comprendre l’évolution du comportement de migration longue distance. Ils montrent également l’importance de confronter plusieurs échelles taxonomiques et plusieurs facteurs, notamment temporels, pour appréhender l’histoire évolutive de ce comportement. Enfin, ils soulignent la difficulté de prévoir les changements de distribution des oiseaux migrateurs dans un contexte de changements globaux.
... colubris 1.5 mya, and S. sasin/ S.rufus 0.97 mya. Licona-Vera and Ornelas [53] used improved within-species sampling (previous studies included only a single representative of four [51] or six [52] of our focal species), and did not recover monophyletic groups for A. alexandri, S. sasin, or S. rufus. The latter study also estimated an older divergence date for a node within A. alexandri than the node separating C. anna and C. costae, albeit with overlapping 95% HPD intervals. ...
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Background: The study of speciation has expanded with the increasing availability and affordability of high-resolution genomic data. How the genome evolves throughout the process of divergence and which regions of the genome are responsible for causing and maintaining that divergence have been central questions in recent work. Here, we use three pairs of species from the recently diverged bee hummingbird clade to investigate differences in the genome at different stages of speciation, using divergence times as a proxy for the speciation continuum. Results: Population measures of relative differentiation between hybridizing species reveal that different chromosome types diverge at different stages of speciation. Using FST as our relative measure of differentiation we found that the sex chromosome shows signs of divergence early in speciation. Next, small autosomes (microchromosomes) accumulate highly diverged genomic regions, while the large autosomes (macrochromosomes) accumulate genomic regions of divergence at a later stage of speciation. Conclusions: Our finding that genomic windows of elevated FST accumulate on small autosomes earlier in speciation than on larger autosomes is counter to the prediction that FST increases with size of chromosome (i.e. with decreased recombination rate), and is not represented when weighted average FST per chromosome is compared with chromosome size. The results of this study suggest that multiple chromosome characteristics such as recombination rate and gene density combine to influence the genomic locations of signatures of divergence.
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The cold-climate hypothesis is the main and most supported explanation of the evolution of viviparity among reptiles. This hypothesis sustains that viviparity arose as a means to save eggs from an increased mortality in nests linked with low temperatures. In this sense, some authors have stated that viviparity could constitute an evolutionary constraint. However, the link between evolutionary constraints and the evolution of ecological niches has not been well studied. Here, we study the climatic niche evolution of a group of viviparous lizards from North America to test whether the diversification of the group is linked with Phylogenetic Niche Conservatism (PNC). We evaluated phylogenetic signals and trait evolution, besides a reconstruction of ancestral climate tolerances, and did not find PNC in the ecological niche of the species in the group. Surprisingly, we did not find conservatism in any bioclimatic variables associated with temperature; we only had evidence of conservatism in Precipitation Seasonality (Bio15) and Precipitation of Coldest Quarter (Bio19). Analysis of relative disparity through time (DTT) indicates high divergence around 4.0 MYA and 0.65 MYA that coincides with orogenic and glacial periods. There is no evidence that climatic niche differentiation was the main factor in the diversification of the studied group. Orogenic and glacial periods probably promote cycles of the availability of new territories and isolation, which could promote the rapid accumulation of ecological differences between the species of the group.
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The evolution of avian migration continues to be an intriguing research subject, even though relationships between migration and factors such as seasonality clearly exist. The question remains whether these relationships are evident within phylogenies containing both sedentary and migratory taxa. We explore the evolution of migration in the family Motacillidae by evaluating existing hypotheses for the evolution of migration in a comparative, phylogenetic framework at the interspecific level. Many hypotheses to explain the evolution of avian migration—such as the “evolutionary precursor” hypothesis (Levey and Stiles 1992, Chesser and Levey 1998) and the “stepping-stone” hypothesis (Cox 1968, 1985)—are based on New World migratory systems. The central components of these hypotheses should apply across biogeographic realms (i.e. the Old World), given that seasonality and habitat regimes are similar in the New and Old worlds. Using a molecular phylogeny containing most species in the Motacillidae, we investigated the potential interactions of seasonality and ecology with migratory and sedentary behavior. Our results suggest that habitat and migration are not correlated in the manner predicted by the evolutionary precursor hypothesis, but they also suggest the importance of increasing seasonality in explaining the patterns of the evolution of migration, an expected but previously unexamined evolutionary relationship. While understanding the limitations of applying generalizations to a complex evolutionary system such as migration, we have delineated here a broad methodology for testing hypotheses about the evolution of migration within a phylogenetic context. Pruebas Filogenéticas de Hipótesis sobre la Evolución de la Migración: Un Estudio de Caso en la Familia Motacillidae
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During the past century, numerous theoretical articles explored the evolution of seasonal migration in birds; many of these focused on environmental or social conditions that may have led to the origin of migration. More recent work has focused not on the origin of migration, but on changes in migratory behavior that have occurred in modern species and their immediate ancestors. We used a novel approach, a multistate ancestral state reconstruction of migration, to examine patterns of migratory evolution in the New World orioles (Icterus spp.). Both the multistate and binary reconstructions indicated repeated gains in migration. However, the multistate method revealed details of how migration may be gained that the standard binary-state reconstructions would not have shown. Our maximum-likelihood reconstruction, using branch lengths based on a molecular phylogeny, suggested multiple instances of rapid gain of migration. Furthermore, we found that every migratory species' migration type differed from that of its closest relatives. Surprisingly, no partially migratory species was closely related to a fully migratory species. These novel patterns involving gain of migration demonstrate the utility of multistate ancestral reconstruction for examining changes in migratory behavior in closely related birds. Reconstrucción de Estados Ancestrales de la Migración: Análisis con Múltiples Estados de Carácter Revelan Cambios Rápidos en los Orioles del Nuevo Mundo (Icterus spp.)
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The effects of seasonal migration on evolutionary change within lineages is poorly understood, in terms of both differentiation (cladogenesis) and specialization (anagenesis). Regarding differentiation, two contradictory hypotheses exist: Seasonal migration counters differentiation; or it can stimulate differentiation by exposing lineages to new environments. Regarding specialization, the morphological consequences of a migratory life history have not been well explored. We examined these issues by reconstructing morphological and molecular phylogenies of the genus Catharus (Turdidae), a group of forest-dwelling, New World thrushes traditionally considered to include a small “species flock” of Nearctic-Neotropic migrants. DNA sequence data (2,920–3,027 base pairs) do not support traditional taxonomy, and morphological characters conflicted with these data. Results suggest that long-distance seasonal migration arose independently four times in Catharus sensu lato (including Hylocichla mustelina). Correlated morphological evolution occurred among several characters in these lineages, and these shared traits may stem from ecological conditions in Nearctic forests. Migración Estacional, Especiación y Convergencia Morfológica en el Género Catharus (Turdidae)
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Aim The formation of the Trans‐Mexican Volcanic Belt (TMVB) played an important role in driving inter‐ and intraspecific diversification at high elevations. However, Pleistocene climate changes and ecological factors might also contribute to plant genetic structuring along the volcanic belt. Here, we analysed phylogeographical patterns of the parrot‐mistletoe Psittacanthus calyculatus to determine the relative contribution of these different factors. Location Trans‐Mexican Volcanic Belt. Methods Using nuclear and chloroplast DNA sequence data for 370 individuals, we investigate the genetic differentiation of 35 populations across the species range. We conducted phylogenetic, population and spatial genetic analyses of P. calyculatus sequences along with ecological niche modelling and Bayesian inference methods to gain insight into the structuring of genetic variation of these populations. Results Our analyses revealed population structure with three genetic groups corresponding to individuals from Oaxaca and those from the central‐eastern and western TMVB regions. A significant genetic signal of demographic expansion, an east‐to‐west expansion predicted by species distribution modelling, and approximate Bayesian computation analyses strongly supported a scenario of habitat isolation and invasion of TMVB by P. calyculatus during the late‐Pleistocene. Main conclusions The genetic differentiation of P. calyculatus may be explained by the combined effects of (1) geographical isolation linked to the effects of the glacial/interglacial cycles and environmental factors, driving genetic differentiation from congeners into more xeric vegetation and (2) the invasion of TMVB from east to west, suggesting a role for both colonization and glacial/interglacial cycles models.