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Current Biology 21, 1–7, November 8, 2011 ª2011 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2011.09.039
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Multilocus Resolution of Phylogeny
and Timescale in the Extant Adaptive
Radiation of Hawaiian Honeycreepers
Heather R.L. Lerner,
1,2,
*Matthias Meyer,
3
Helen F. James,
4,2
Michael Hofreiter,
5,3
and Robert C. Fleischer
1,2
1
Center for Conservation and Evolutionary Genetics,
Smithsonian Conservation Biology Institute,
National Zoological Park, PO Box 37012, MRC 5513,
Washington, DC 20013-7012, USA
2
Department of Biology, University of Maryland, College Park,
MD 20742, USA
3
Max Planck Institute for Evolutionary Anthropology
Deutscher Platz 6, 04103 Leipzig, Germany
4
Department of Vertebrate Zoology, National Museum of
Natural History, Smithsonian Institution, MRC 116,
Washington, DC 20013-7012, USA
5
Department of Biology, University of York, Wentworth Way,
Heslington, York YO10 5DD, UK
Summary
Evolutionary theory has gained tremendous insight from
studies of adaptive radiations. High rates of speciation,
morphological divergence, and hybridization, combined
with low sequence variability, however, have prevented
phylogenetic reconstruction for many radiations. The
Hawaiian honeycreepers are an exceptional adaptive radia-
tion, with high phenotypic diversity and speciation that
occurred within the geologically constrained setting of the
Hawaiian Islands. Here we analyze a new data set of 13
nuclear loci and pyrosequencing of mitochondrial genomes
that resolves the Hawaiian honeycreeper phylogeny. We
show that they are a sister taxon to Eurasian rosefinches
(Carpodacus) and probably came to Hawaii from Asia. We
use island ages to calibrate DNA substitution rates, which
vary substantially among gene regions, and calculate diver-
gence times, showing that the radiation began roughly when
the oldest of the current large Hawaiian Islands (Kauai and
Niihau) formed, w5.7 million years ago (mya). We show
that most of the lineages that gave rise to distinctive
morphologies diverged after Oahu emerged (4.0–3.7 mya)
but before the formation of Maui and adjacent islands
(2.4–1.9 mya). Thus, the formation of Oahu, and subsequent
cycles of colonization and speciation between Kauai and
Oahu, played key roles in generating the morphological
diversity of the extant honeycreepers.
Results
More than 3,700 km from any major landmass, the Hawaiian
Islands form the most remote archipelago in the world. Conse-
quently, evolution on the Hawaiian archipelago has been
predominantly driven by in situ speciation rather than repeated
colonization from continental sources, making the archipelago
an exceptional setting for studying fundamental evolutionary
processes including speciation and adaptation. The sequen-
tial ages of the islands, which formed by volcanism in a time
series [1, 2], coupled with speciation that often parallels island
formation, provide a means to estimate DNA substitution rates
in endemic Hawaiian lineages. Such estimates of molecular
substitution rates are critical to studies of evolution because
they provide the timeline from which rates of morphological
and behavioral change can be determined. These timescaled
data can also be used to investigate the role of life history traits
(e.g., metabolism, body size), population dynamics, and
cellular activities on evolutionary processes [3].
The Hawaiian honeycreepers (Fringillidae: Drepanidinae)
represent one of the most striking adaptive radiations of
vertebrates. These colorful songbirds have diversified in bill
morphology to an extent that they have not only convergently
evolved many of the bill morphologies found in mainland song-
birds but in addition evolved several bill forms unknown
anywhere else (e.g., akiapolaau, see Figure 1 and Figure 2
in [4]). Unfortunately, without a well-resolved phylogeny,
evolutionary insights from the Hawaiian honeycreeper radia-
tion are severely limited. Low levels of sequence divergence
among Hawaiian honeycreepers and rapid speciation have
thus far prevented adequate resolution of their phylogenetic
history (e.g., [5]). These limitations could likely be overcome
with a substantially larger data set (in terms of DNA base pairs),
as evidenced by an improvement in resolution from early
data sets using <1 kb [6, 7] of sequence to more recent
data sets of w2.5 kb [5]. Next-generation sequencing technol-
ogies that generate large amounts of sequence data and
recent barcoding methods that allow parallel processing of
multiple individuals in a single run [8] can efficiently and
cost-effectively generate phylogenetic data sets that are
orders of magnitude larger than those typically obtained with
traditional technology [9].
We sequenced complete mitochondrial genomes (w17 kb)
and 13 nuclear loci (8.2 kb) from 19 extant or recently extinct
Hawaiian honeycreeper taxa and 28 outgroup taxa (see Table
S1 available online) using 454 sequencing technology and
sample multiplexing [8, 10] as well as traditional sequencing
methods. Further details about DNA sequences are available
in the Supplemental Information. In addition to resolving the
phylogeny for the 19 extant Hawaiian honeycreepers and
related outgroups, we also calibrate evolutionary rates for all
regions or genes of the mitochondrial genome and 13 nuclear
loci, using Bayesian methods that provide greater accuracy
and resolution than in previous work. Two taxon sets were
analyzed: the ‘‘honeycreeper data set’’ included all 19 species
of recently extant Hawaiian honeycreepers and the common
rosefinch as the outgroup, and the ‘‘full taxon data set’’
included all Hawaiian honeycreepers as well as 28 outgroup
taxa (with the house sparrow as the outgroup) for a total of
47 taxa (Table S2). These data were intensively analyzed for
phylogenetic signal and to compute rates of DNA sequence
evolution.
Phylogenetic Analyses
We performed a variety of analyses using data from the two
taxon groups described above, and all produced similar topol-
ogies, although the best support was recovered with data
from whole mitochondrial genomes. As described below, all
*Correspondence: hlerner@gmail.com
Please cite this article in press as: Lerner et al., Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of
Hawaiian Honeycreepers, Current Biology (2011), doi:10.1016/j.cub.2011.09.039

analyses conclusively placed the Hawaiian honeycreepers
within the cardueline finch clade as sister to Eurasian rose-
finches (Carpodacus). The branching pattern within the large
clade of Hawaiian honeycreepers was fully resolved with mito-
chondrial data but lacked support from the nuclear intron data
at several midlevel nodes corresponding to the placement of
a clade of finch-like taxa (palila, Nihoa finch, and Laysan finch)
and to the placement of akiapolaau and anianiau (see details
below).
Bayesian analyses of the mitochondrial coding sequences
alone for all 47 taxa (i.e., the full taxon data set) produced
a topology (Figure 1A) that resolved the position of the honey-
creepers within the cardueline radiation and all of the internal
nodes within the radiation (all Bayesian posterior probabilities
[bpp] = 0.99–1.00). In Figure 1A, all post-burn-in trees are
shown with their estimated branch-lengths and topologies.
The fuzziness of the horizontal plane of the branches reflects
the variation in branch lengths among estimated trees. This
figure also shows that nearly all post-burn-in trees support
the topology shown in green, whereas only a few trees were
recovered that support an alternative topology in which the
Maui parrotbill and akiapolaau are not sister taxa (shown in
blue).
In order to reduce any effects of undetected selection on the
phylogenetic reconstruction, additional analyses were con-
ducted on a data set composed of mostly neutral
mitochondrial sites (i.e., third codon positions and control
region) for the honeycreeper data set. Maximum likelihood
and Bayesian analyses of this data set produced topologies
identical to that shown in Figure 1A (data not shown). An anal-
ysis of only neutral sites was not performed for the larger full
taxon data set because there was evidence of substitution
saturation for that data set at third codon positions. Those
sites were coded as purines or pyrmidines (RY-coded) for
analyses of the full taxon data set.
Figure 1B shows a species tree analysis of the combined
mitochondrial coding sequences and nuclear loci (22.4 kb
of aligned sequence in total) for the full taxon data set.
The species tree analysis jointly estimates the underlying
phylogeny for each locus and uses this information to estimate
the overall phylogeny for the species. Because trees found
after burn-in from a Bayesian analysis can vary both in
topology and branch lengths, typically, a single representative
tree is shown (e.g., the tree with the highest likelihood or
consensus tree) and uncertainty is shown as nodal support
values indicating the percent of trees in the set that share
the node in question. Although this quantitative approach is
easily interpretable, it obscures alternative topologies recov-
ered in the analysis. In order to retain information about alter-
native topologies as well as support, we present all topologies
recovered in the post-burn-in analysis for the Bayesian
species tree analysis of the mitochondrial coding sequences
House Sparrow
Blue Gray Tanager
Sayaca Tanager
Green Honeycreeper
Northern Cardinal
Red-winged Blackbird
Chaffinch
Hawfinch
Evening Grosbeak
Oriental Greenfinch
White-throated Canary
European Serin
Pine Siskin
Lesser Goldfinch
Orange Canary
European Goldfinch
Common Crossbill
House Finch
Purple Finch
Cassins Finch
Pine Grosbeak
Eurasian Bullfinch
Mongolian Finch
Black-Headed Mt. Finch
Asian Rosy Finch
Pallas’s Rosefinch
Long-tailed Rosefinch
Common Rosefinch
Poouli
Maui Creeper
Kauai Creeper
Akohekohe
Apapane
Iiwi
Palila
Nihoa Finch
Laysan Finch
Maui Parrotbill
Kauai Amakihi
Oahu Amakihi
Maui Amakihi
Hawaii Creeper
Hawaii Amakihi
Kauai Ak epa
Akepa
Anianiau
Akiapolaau
3
31
8
3
2
3
3
2
3
2
2
1
2
7
1
3
1
1
1
0.81
0.84
0.60
0.91
0.65
0.92
0.44
0.97
0.63
0.57
0.97
0.77
A B
Figure 1. Phylogeny for Hawaiian Honeycreepers and 28 Outgroup Taxa
(A) Cloudogram showing all trees resulting from a Bayesian analysis of whole mitogenomes (19,601 trees; 14,449 bps). Variation in timing of divergences is
shown as variation (i.e., fuzziness) along the x axis. Darker branches represent a greater proportion of corresponding trees. All nodes have support
values >0.99.
(B) Topologram showing all topologies resulting from Bayesian species tree estimation from 12 nuclear loci and whole mitochondrial genomes (22,389 bps;
1,200 trees). Numbers within circles indicate the number of indels supporting each branch. Darker branches represent a higher number of corresponding
topologies. Bayesian posterior probabilities <0.99 are indicated.
Current Biology Vol 21 No 21
2
Please cite this article in press as: Lerner et al., Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of
Hawaiian Honeycreepers, Current Biology (2011), doi:10.1016/j.cub.2011.09.039

and nuclear loci together (Figure 1B, 22.4 kb of aligned
sequence in total). For this data set, alternative topologies
were not visible when branch length variability was also shown
for every tree (see branch length variability on the horizontal
plane of Figure 1A), so instead, average branch lengths were
calculated and are presented here for each topology (using
DensiTree software, [11]). In this analysis, all nodes were
resolved with strong support with the exception of a few of
the internal nodes within the honeycreeper radiation. The
unresolved nodes correspond to the placement of a clade of
finch-like taxa (palila, Nihoa finch, and Laysan finch) and the
placement of akiapolaau and anianiau. These divergences
occur during a particularly rapid time of speciation within the
radiation, so it is not surprising that nuclear loci with slower
substitution rates and larger population sizes provide less
resolution than the mitochondrial data set (see discussion
below in Divergence Date Estimation).
Divergence Date Estimation
We assessed the age of the Hawaiian honeycreeper clade and
tempo of evolution within the radiation using a Bayesian time-
calibrated phylogeny estimated from the whole mitochondrial
genomes and using the three island-age calibration points and
the rationale from Fleischer et al. [7]. We confirm the assump-
tion that the divergence of the Maui and Kauai creepers
reflects the formation of the island of Oahu, because the
extinct Oahu and extant Maui creeper are sister taxa based
on previous mitochondrial DNA (mtDNA) analyses [12]. Our
age estimates (Figure 2) indicate that the ancestral colonists
arrived in the Hawaiian Islands sometime between the diver-
gence between Hawaiian honeycreepers and the common
rosefinch estimated at 7.2 mya (8.1–6.4 mya 95% highest
probability density [HPD]) and the earliest divergence within
the Hawaiian honeycreepers at 5.8 mya (6.3–5.2 95% HPD),
although these dates might be slightly overestimated because
they are generated from a gene tree analysis rather than
a species tree analysis [13]. Our calibration also resulted in
some novel insights into the pattern and timing of the Hawaiian
honeycreeper radiation. In particular, nearly all branches
leading to distinctive extant morphological lineages (morpho-
types) appear to have diverged between 5.8 and 2.4 mya,
a timeframe that overlaps with the formation of the island of
Oahu (4.0–3.7 mya) but occurs prior to the formation of the
Maui Nui island complex (i.e., Maui, Lanai, Molokai, and
Kahoolawe; 2.4–1.9 mya). This suggests that the formation of
the new island of Oahu, by providing a second major land
area well isolated from Kauai and Niihau, may have enabled
a higher rate of adaptation and speciation.
Evolutionary Rate Estimation
Evolutionary rates estimated from three separate mitochon-
drial and nuclear data sets (see below) in calibrated Bayesian
analyses show a broad distribution of locus-specific rates,
from 0.00035 substitutions per site per million years (s/s/my;
Rag 1) to 0.058 s/s/my (mitochondrial third codon positions).
Evolutionary rates in Figure 3A were estimated in the same
analysis from which the Hawaiian honeycreeper divergence
dates shown in Figure 2 were estimated, an analysis that
partitioned the mitochondrial genome according to functional
region (i.e., codon position, noncoding sequence, etc.). To
further explore mitochondrial rates of evolution by gene, we
conducted an analysis with a separate partition for each of
the 13 mitochondrial genes, the three domains of the control
region, RNA stems, and RNA loops (Figure 3B). Despite the
vastly different number of partitions used in analyses shown
in Figure 3A versus Figure 3B, evolutionary rate estimates for
partitions shared between these analyses (i.e., control region
domain II, RNA stems, and RNA loops) were identical or
differed by a value much less than the standard deviation.
Across the complete mtDNA genome, we found an average
rate of sequence divergence of 1.8% per million years, similar
to estimates from other studies for avian mtDNA (e.g., 1.1%–
2.1% for Passeriformes, [14]) and for the cytochrome-b gene
(2.1%, [15]). Rates of synonymous substitution (i.e., third
codon positions) were higher (5.8%, 5.2%–6.3% HPD) than
rates of nonsynonymous substitution and closer to rates
estimated from within-species comparisons [16]. We found
a 14-fold difference between the rates for the RNA stems
and domain III of the control region (Figure 3B), with some of
the slower rates found for genes that function in oxidative
energetics (i.e., the cytochrome c complex).
Evolutionary rates for all 13 nuclear loci (Figure 3C)
are lower than those of the mitochondrial regions, though
the fastest-evolving nuclear locus (beta-fibrinogen intron 7,
0.0019 s/s/my) is comparable to the slowest-evolving mito-
chondrial region (RNA stems, 0.0022 s/s/my). The nuclear
introns evolved at an average rate of 0.12% (0.07%–0.20%),
somewhat slower than the rate of 0.36% reported by Axelsson
et al. [16] from 33 turkey and chicken autosomal introns. We
use a younger calibration than the chicken-turkey split used
by Axelsson et al. (28 million years) and thus, our data may
be more applicable to recent divergences, such as those
within songbirds (i.e., Passeriformes, the majority of all extant
avian species). The Rag 1 exon evolved at a remarkably,
though not unexpectedly, slow rate of 0.04% per million years
(similar to 0.046%, calculated from [17]).
Discussion
Our results show clearly that next-generation DNA sequence
data sets hold tremendous promise for resolving the pattern,
process, and timing of island adaptive radiations. The higher
rate of substitution and smaller effective population size
of mitochondrial compared with nuclear DNA sequences
make whole mitochondrial genomes particularly useful for
resolving adaptive radiations, at least where mitochondrial
introgression is not prevalent [18]. For the Hawaiian honey-
creepers, species tree analyses show that the mitochondrial
signal agrees with the nuclear signal while providing higher
resolution because of the faster average substitution rate
compared with nuclear sites. For the mitochondrial genomes,
much of the signal derives from the large number of neutral or
noncoding sites, which are especially valuable when esti-
mating phylogenies of adaptive radiations because they are
more likely to reflect phylogenetic history than is DNA se-
quence from functional regions that may be confounded by
selection. Additionally, variance in mutation rate and branch
length variation among gene trees were not pronounced for
this group (as shown in Figure 3), although such variance has
been shown to be an important potential source of error in
estimating phylogenies for recent radiations [19, 20].
Although species tree estimation from the nuclear data
alone and the nuclear + mitogenomes produced a well-sup-
ported phylogeny, those analyses were unable to resolve all
nodes with high support. The mitochondrial sequences, on
the other hand, evolved on average w20 times faster than
the nuclear sequences (Figure 3) and produced a fully resolved
tree with high support. Including more alleles per taxon might
Phylogeny of the Hawaiian Honeycreeper Radiation
3
Please cite this article in press as: Lerner et al., Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of
Hawaiian Honeycreepers, Current Biology (2011), doi:10.1016/j.cub.2011.09.039

increase the power for phylogenetic resolution when using
the species tree method with nuclear sequences. Although
we are confident in the topology presented here, our future
research will explore nuclear allelic diversity within Hawaiian
honeycreeper taxa in order to more fully utilize modeling of
the coalescent process in phylogeny reconstruction.
A broader value of this study is the estimation of rates of
sequence evolution across the mitochondrial control region
Figure 2. Bayesian Divergence Date Estimates for Hawaiian Honeycreepers from Whole Mitochondrial Genomes Based on Three Island Age Calibration
Points [7]
Mean ages are shown above each node, with horizontal bars across nodes representing 95% highest probability density intervals. Shaded vertical bars
encompass the estimated subaerial to maximal shield-building dates for the recent Hawaiian Islands [1], where the gray bars indicate island ages used
as calibrations, and asterisks (*) identify constrained nodes. Lowercase letters identify divergence of a new morphological lineage before formation of
Oahu (a), during or after formation of Oahu (b), or before or during formation of Maui Nui (c). Distributions by island are listed to the right of each taxon where
closed circles denote historic and/or extant (and sometimes fossil) distributions, and open circles represent fossil distributions with no known historic or
extant populations. (1) The extant population occurs on Nihoa Island, but closely related extinct species mainly differing in size occurred on Kauai, Oahu, and
Hawaii Islands. (2) The extant population occurs on Laysan Island, but closely related extinct species mainly differing in sizes oc curred on Kauai and Hawaii
Islands. (3) A closely related species or subspecies occurred on Laysan Island. Photographs are by Jack Jeffrey.
Current Biology Vol 21 No 21
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Please cite this article in press as: Lerner et al., Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of
Hawaiian Honeycreepers, Current Biology (2011), doi:10.1016/j.cub.2011.09.039

and 13 nuclear loci using internal, minimal rate calibrations,
rather than external calibrations that may greatly precede the
formation of the clade being assessed (Figure S5). In the
past, a ‘‘2% rule’’ of avian mitochondrial divergence per million
years has often been applied, unfortunately somewhat indis-
criminately, in phylogenetics and phylogeography [21]. Our
rate estimates will allow researchers to select loci with appro-
priate rates of evolution for studies of avian phylogeny and
population genetics, as well as apply more precise substitu-
tion rates specific to the loci under study in order to estimate
the time frame for avian evolution. Our rate estimates for
several loci and functional regions (e.g., nonsynonymous sites)
are largely concordant with other published avian data sets
[14–17], suggesting broad applicability of our locus-specific
rates for population genetic and phylogenetic studies of avian
taxa. For instance, based on our estimates, studies that
require high rates of substitution could use ND2 and ATP6 in
addition to the more commonly used control region.
Knowledge of the outgroup relationships of an adaptive
radiation is essential to interpretations of evolutionary patterns
within the radiation; thus, we included a large set of outgroup
species in our analysis. This large taxon sampling also allowed
us to resolve previously unresolved relationships among out-
groups. Most previous studies have identified the cardueline
finches (Fringillidae: Carduelinae) as the likely source of the
honeycreeper radiation’s ancestor (summarized in [22]), but
the specific sister group within Carduelinae was unresolved.
Previous authors have pointed to crossbills (Loxia) and the
pine grosbeak (Pinicola enucleator) as modern ecological/
behavioral analogs for understanding how the continental car-
dueline ancestor of the Hawaiian honeycreepers may have
been able to colonize the remote Hawaiian Islands millions of
years ago [23, 24]. In contrast, all of our data sets and methods
of analysis (Figure 1;Figure S1) support a sister relationship
between Hawaiian honeycreepers and a clade of three rose-
finches (Carduelinae: Carpodacus), including the common
rosefinch.
Common rosefinches share an important life history trait
with crossbills and the pine grosbeak: they often move in large
mixed-sex groups to new wintering grounds outside their
typical range, a behavior termed an ‘‘irruption,’’ and they
may stay to breed in those new regions [25]. It is possible
that colonization by the ancestral species was aided by the
arrival of a large mixed-sex flock in the islands, representing
a sizable gene pool. Thus, a diverse initial gene pool may
have facilitated speciation and the evolution of extreme
morphological diversity in the honeycreeper radiation (for
another perspective see [4]). Assuming that rosefinches were
restricted in distribution to the Old World in the Miocene as
they are at present, it is likely that the ancestral stock leading
to Hawaiian honeycreepers arrived in Hawaii from the west.
Eurasian rosefinches and the other close outgroups share
the typical finch-like bill shapes of continental cardueline
finches, confirming that the Hawaiian honeycreepers evolved
their astonishing diversity of bill forms from an ancestor with
a finch-like bill and emphasizing the importance of conditions
Figure 3. Evolutionary Rates Estimated for Mitochondrial and Nuclear Genes, Introns, and Regions from Three Separate Bayesian Analyses
(A) Seven mitochondrial regions.
(B) Eighteen mitochondrial genes and regions.
(C) Thirteen nuclear loci. Any difference in average substitution rates for regions estimated in multiple analyses (e.g., RNA stems, RNA loops) lies within the
standard deviation for the estimates.
Phylogeny of the Hawaiian Honeycreeper Radiation
5
Please cite this article in press as: Lerner et al., Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of
Hawaiian Honeycreepers, Current Biology (2011), doi:10.1016/j.cub.2011.09.039

on the Hawaiian Islands in stimulating such a diverse radiation.
However, although all Eurasian rosefinch species resemble
one another in phenotype, particularly in bill morphology
[26], the oldest divergences in the honeycreeper radiation
lead to species that differ from rosefinches and other conti-
nental cardueline finches in bill morphology and feeding niche.
The recently extinct poouli had a superficially finch-like bill but
with a modified hard palate; it fed not on seeds but on snails
and other invertebrates [27]. The Kauai and Maui creepers
have straight thin bills and feed on arthropods; the Maui
creeper in particular is very warbler-like [24, 28]. The three
species of honeycreepers in our analysis that closely resemble
continental cardueline finches in their conical bills, cranial
osteology, and feeding habits (the palila, Nihoa finch, and
Laysan finch) are unexpectedly more recently diverged. That
the earliest diverging Hawaiian honeycreeper lineages lead
to taxa that differ in morphology and niche from continental
cardueline finches suggests that directional selection early in
the radiation favored adaptation to an invertebrate diet, an
evolutionary pattern also observed in the Galapagos finches
[24, 29]. Our phylogenetic results are consistent either with
a single evolutionary loss and subsequent gain of the finch-
like morphology and feeding niche or with the persistence of
a finch-like lineage with at least two gains of more thin-billed
and warbler-like morphologies. In either case, the resolved
molecular phylogeny reveals a more complex pattern of
morphological evolution than would be expected based on
classic papers about the radiation, which proposed phyloge-
netic patterns that minimized the morphological distance
between related taxa [23, 30].
The timing of the earliest divergence within the honey-
creepers corresponds closely to the emergence from the sea
of the islands of Niihau (5.7–5.3 mya) and Kauai (5.4–4.9 mya;
Figure 2). In this early time period before the formation of
Oahu, two divergences occurred, each separating a distinct
morphological lineage from the rest of the radiation (first the
poouli and second the Oahu and Maui creeper and relatives).
Biogeographically, the placement of poouli (a Maui taxon) as
an early divergence in Figure 2 suggests that the poouli or its
relatives formerly occurred on older islands. In the rich fossil
record of Hawaiian honeycreepers, the poouli occurs only on
Maui; however, it may be that extinct taxa, such as Xestospiza,
that occur on older islands are relatives of the poouli [24, 31].
DNA sequences from extinct subfossil honeycreepers might
resolve this issue.
Within the honeycreeper radiation, a burst of cladogenesis
accompanied by morphological diversification occurred
between 5.8 and 2.4 million years ago, a time period that
encompasses the formation of Oahu, yet precedes the forma-
tion of Maui Nui. During this time frame, six of ten major extant
morphological lineages evolved (nodes labeled ‘‘b’’ in Fig-
ure 2). That only two morphological lineages evolved after
this time frame emphasizes the importance of the formation
of Oahu, more so than Maui Nui, to the present-day morpho-
logical diversity of Hawaiian honeycreepers. This result is
surprising, given the larger size and greater ecological
complexity of Maui Nui as well as other work describing the
importance of Maui Nui for diversification in other Hawaiian
radiations [32]. For groups with more limited dispersal than
the Hawaiian honeycreepers, ecological conditions on Maui
Nui, and particularly the breakup of the Maui Nui complex of
volcanoes into several islands, probably played a greater
role in speciation. In contrast, repeated colonization and isola-
tion between Kauai and Oahu appears to be pivotal in spurring
cladogenesis of the Hawaiian honeycreepers. Oahu, as a newly
formed island initially without avian residents, likely provided
a blank slate allowing ecological and morphological differenti-
ation [33].
Supplemental Information
Supplemental Information includes two figures, five tables, and Supple-
mental Experimental Procedures and can be found with this article online
at doi:10.1016/j.cub.2011.09.039.
Acknowledgments
We would like to thank those who contributed tissues and the museum cura-
tors and collection managers (see Supplemental Information) who have
accommodated us. We thank Nancy Rotzel, Joshua Miller, Zachary
Sanford, and the Max Planck Institute for Evolutionary Anthropology for
assistance in the lab. Remco Bouckart, Joseph Heled, Matthew Kweskin,
and Michael Lerner provided technical support. Jack Jeffrey permitted
our use of his stunning Hawaiian honeycreeper photographs in Figure 2,
and H. Douglas Pratt provided the lovely cover art. Support for this research
was provided by National Science Foundation DEB-0643291, the Smithso-
nian Institution Center for Conservation and Evolutionary Genetics, the
Smithsonian Scholarly Studies Program, and the Max Planck Society.
Received: August 9, 2011
Revised: September 21, 2011
Accepted: September 21, 2011
Publication online: October 20, 2011
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Phylogeny of the Hawaiian Honeycreeper Radiation
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Please cite this article in press as: Lerner et al., Multilocus Resolution of Phylogeny and Timescale in the Extant Adaptive Radiation of
Hawaiian Honeycreepers, Current Biology (2011), doi:10.1016/j.cub.2011.09.039