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Non-sister Sri Lankan white-eyes (genus Zosterops) are a result of independent colonizations

Authors:
  • Indian Institute of Science Education and Research Tirupati
  • University of Minnesota

Abstract and Figures

Co-occurrence of closely related taxa on islands could be attributed to sympatric speciation or multiple colonization. Sympatric speciation is considered to be rare in small islands, however multiple colonizations are known to be common in both oceanic and continental islands. In this study we investigated the phylogenetic relatedness and means of origin of the two sympatrically co-occurring Zosterops white-eyes, the endemic Zosterops ceylonensis and its widespread regional congener Z. palpebrosus, in the island of Sri Lanka. Sri Lanka is a continental island in the Indian continental shelf of the Northern Indian Ocean. Our multivariate morphometric analyses confirmed the phenotypic distinctness of the two species. Maximum Likelihood and Bayesian phylogenetic analyses with ~2000bp from two mitochondrial (ND2 and ND3) and one nuclear (TGF) gene indicated that they are phylogenetically distinct, and not sister to each other. The two subspecies of the peninsula India; Z. p. egregius of Sri Lanka and India and Z. p. nilgiriensis of Western Ghats (India) clustered within the Z. palpebrosus clade having a common ancestor. In contrast, the divergence of the endemic Z. ceylonensis appears to be much deeper and is basal to the other Zosterops white-eyes. Therefore we conclude that the two Zosterops species originated in the island through independent colonizations from different ancestral lineages, and not through island speciation or multiple colonization from the same continental ancestral population. Despite high endemism, Sri Lankan biodiversity is long considered to be a subset of southern India. This study on a speciose group with high dispersal ability and rapid diversification rate provide evidence for the contribution of multiple colonizations in shaping Sri Lanka’s biodiversity. It also highlights the complex biogeographic patterns of the South Asian region, reflected even in highly vagile groups such as birds.
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RESEARCH ARTICLE
Non-sister Sri Lankan white-eyes (genus
Zosterops) are a result of independent
colonizations
Nelum Wickramasinghe
1,2
, V. V. Robin
2¤
, Uma Ramakrishnan
2
, Sushma Reddy
3
, Sampath
S. Seneviratne
1
*
1Avian Evolution Node, Department of Zoology and Environment Sciences, Faculty of Science, University of
Colombo, Colombo, Sri Lanka, 2National Center for Biological Sciences, Tata Institute of Fundamental
Research, Bangalore, India, 3Biology Department, Loyola University Chicago, Chicago, Illinois, United
States of America
¤Current address: Department of Biology, Indian Institute of Science Education and Research, Tirupati,
Andhra Pradesh, India
*sam@sci.cmb.ac.lk
Abstract
Co-occurrence of closely related taxa on islands could be attributed to sympatric speciation
or multiple colonization. Sympatric speciation is considered to be rare in small islands,
however multiple colonizations are known to be common in both oceanic and continental
islands. In this study we investigated the phylogenetic relatedness and means of origin of
the two sympatrically co-occurring Zosterops white-eyes, the endemic Zosterops ceylonen-
sis and its widespread regional congener Z.palpebrosus, in the island of Sri Lanka. Sri
Lanka is a continental island in the Indian continental shelf of the Northern Indian Ocean.
Our multivariate morphometric analyses confirmed the phenotypic distinctness of the two
species. Maximum Likelihood and Bayesian phylogenetic analyses with ~2000bp from two
mitochondrial (ND2 and ND3) and one nuclear (TGF) gene indicated that they are phyloge-
netically distinct, and not sister to each other. The two subspecies of the peninsula India; Z.
p.egregius of Sri Lanka and India and Z.p.nilgiriensis of Western Ghats (India) clustered
within the Z.palpebrosus clade having a common ancestor. In contrast, the divergence of
the endemic Z.ceylonensis appears to be much deeper and is basal to the other Zosterops
white-eyes. Therefore we conclude that the two Zosterops species originated in the island
through independent colonizations from different ancestral lineages, and not through island
speciation or multiple colonization from the same continental ancestral population. Despite
high endemism, Sri Lankan biodiversity is long considered to be a subset of southern India.
This study on a speciose group with high dispersal ability and rapid diversification rate pro-
vide evidence for the contribution of multiple colonizations in shaping Sri Lanka’s biodiver-
sity. It also highlights the complex biogeographic patterns of the South Asian region,
reflected even in highly vagile groups such as birds.
PLOS ONE | https://doi.org/10.1371/journal.pone.0181441 August 9, 2017 1 / 16
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OPEN ACCESS
Citation: Wickramasinghe N, Robin VV,
Ramakrishnan U, Reddy S, Seneviratne SS (2017)
Non-sister Sri Lankan white-eyes (genus
Zosterops) are a result of independent
colonizations. PLoS ONE 12(8): e0181441. https://
doi.org/10.1371/journal.pone.0181441
Editor: Tzen-Yuh Chiang, National Cheng Kung
University, TAIWAN
Received: December 23, 2016
Accepted: July 2, 2017
Published: August 9, 2017
Copyright: ©2017 Wickramasinghe et al. This is an
open access article distributed under the terms of
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files. The DNA sequences are deposited in NCBI
Genbank and the accession numbers are given in
the paper.
Funding: Major funding is provided by the National
Research Council of Sri Lanka (Grant number: 14-
072) to S.S.S. (NRC URL—http://www.nrc.gov.lk/)
and an Outstanding Scientist Award – Department
of Atomic Energy, India to U.R. (DAE URL—http://
dae.nic.in/). The funders had no role in study
Introduction
Speciation is the evolutionary process by which biological populations diverge into distinct
species through reproductive isolation [13]. ‘Allopatric speciation’ occurs when populations
are reproductively isolated due to a geographic barrier [4]. Genetic differences get accumulated
within the isolated populations overtime and cause these geographically separated populations
to become distinct species through reproductive isolation. On the other hand in ‘sympatric
speciation’, reproductive isolation is non-geographic and the newly diverged species will share
the same geographic location [4,5]. Even though allopatric speciation is common and widely
accepted, sympatric speciation is considered to be rare in nature and a topic of debate [611].
Islands provide a unique opportunity to understand the evolutionary processes behind
diversification and speciation [1214]. For example, the patterns of speciation in birds were
largely elucidated using studies of island birds [1416]. Even though islands can harbor sister
species, there is little evidence for sympatric speciation producing such species assemblages [4,
17] especially in small islands. Madeiran storm-petrel [6,10] and Atlantic finches [11] are few
such examples. Large islands (e.g. Madagascar) often have a greater diversity of terrain and
ecological niches that may allow more intra-island diversification ([1820] but see [21]). This
diversity provides enough barriers for isolation, which results in intra-island allopatric specia-
tion. Small islands, however, usually do not carry such diversity in niches. Therefore when
related species are found in small islands, they tend to be results of ‘multiple colonizations’ [17,
22,23].
Multiple colonization is a result of an island getting colonized more than once (twice—dou-
ble colonization; more than twice—multiple colonization) by a foreign population. If there is
sufficient time passed between such colonizations, they could diversify into separate species
and co-exist in the island [15,24,25]. Such multiple colonizations can be seen across narrow
water gaps in oceanic and continental islands [18,26]. When these colonizations take place from
the same ancestral population it results in species from a paraphyletic group co-occurring in
islands (Fig 1). Ripley in 1949 suggested several such examples of probable double colonizations
of birds into Sri Lanka from India including two species of barbets (the endemic Megalaima
rubricapilla and the widespread M.haemacephala) two species of hill-mynahs (the endemic Gra-
cula ptilogneys and the widespread G.religiosa) and two species of white-eyes (the endemic Zos-
terops ceylonensis and the widespread Z.palpebrosus) [25]. However, when colonization takes
place from mainland populations with different ancestors (non-related populations) through
independent colonization events, it could result in non-sister likely polyphyletic groups co-
occurring in islands [17,2729] (see Fig 1).
Sri Lanka is a continental island situated on the same shallow continental shelf with India
[30]. During Pleistocene glaciations, genetic mixing between Sri Lanka and the mainland
(India) was possible through faunal exchange over the Palk Strait land bridge that emerged as
a result of reduced sea level [31]. Sri Lankan biota is considered closely related to that of South-
ern India [32]. Together with the Western Ghats (of India) it is also considered a single biodi-
versity hotspot suggesting a single biogeographic community of species [32]. However,
historical [33] as well as modern authors [34] recognize Sri Lankan biota as a distinct unit.
Modern analyses using relatively less vagile groups such as freshwater crabs, freshwater fish,
tree frogs and reptiles [34] had shown that Sri Lanka has its own endemism.
White-eyes are canopy-dwelling, small passerine birds belonging to the family Zosteropidae
[35]. As the name implies, many have conspicuous white-colour eye rings, olive-green upper
parts, yellow throats, and yellow or greyish-white bellies [35]. The family comprises of ~100
species belonging to 14 genera, of which the most speciose genus, Zosterops consists of typical
white-eyes with ~75 species [35]. Fifty out of the 75 of these Zosterops white-eyes are island
Patterns of colonization in Sri Lankan white-eyes
PLOS ONE | https://doi.org/10.1371/journal.pone.0181441 August 9, 2017 2 / 16
design, data collection and analysis, decision to
publish, or preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
Fig 1. Three explanations for the co-occurrence of closely related taxa on an island. a.) Sympatric
speciation/ intra-island diversification. The ancestor (A) from the mainland colonized the island. Later it got
Patterns of colonization in Sri Lankan white-eyes
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endemics indicating a high level of island endemism [35]. Many inhabit tropical islands in the
Indian Ocean, western Pacific Ocean, and the Gulf of Guinea. They show high dispersal poten-
tial hence have the ability to colonize islands [28,36,37]. Sympatric occurrence of multiple
species of white-eyes on islands is largely attributed to multiple colonizations as in the case of
Mascarene Islands, Lord Howe Island and Norfolk Island white-eyes [17,2729]. It is sug-
gested that dispersal of white-eyes took place from Asia to Africa [38], and from Asia or Aus-
tralia into the central pacific [28,36].
The Zosteropidae radiation took place ~2 Mya [36] and within this short period of time a
rapid diversification of the Zosterops has taken place showing the highest rate of diversification
among all vertebrates [36,39]. As a result the white-eyes have been referred to as ‘great specia-
tors’ in birds [28,36,40,41]. They have been extensively used as models in bird speciation and
evolutionary studies especially on islands [21,37,4244].
The two species found in Sri Lanka are the endemic Z.ceylonensis (Ceylon White-eye or
Hill White-eye) and its widespread congener Z.palpebrosus (Oriental White-eye) [4547]. Z.
p.egregious in Sri Lanka is a subspecies that has a widespread distribution throughout the ori-
ental region including lowlands of India and Lakshadweep islands [35,47,48] (Fig 2). Z.ceylo-
nensis is confined to the hills of Sri Lanka mainly above 1000m, common in high elevation
evergreen forests, adjacent tea plantations and home gardens (Fig 2). Mees [48] stated that
phenotypically Z.ceylonensis is much closer to Z.p.nilgiriensis (subspecies confined to the Nil-
giri and Palani hills of the southern Western Ghats) than to other Z.palpebrosus and consid-
ered Z.p.nilgiriensis a link between Z.palpebrosus and Z.ceylonensis [48]. As previously
mentioned, Ripley [25] suggested that the Zosterops white-eye species pair in Sri Lanka owe
their origin to a double colonization from the same ancestral population in India.
The three possible scenarios that could explain the origin of the two white-eye species in
Sri Lanka are through intra-island speciation (sympatric), double colonization from related
mainland population in different time periods and independent colonization from different
ancestral populations (Fig 1). In order to investigate the probable means of speciation, we per-
formed phylogenetic analyses using gene sequence data to investigate their probable origin
and colonization histories. Aim of our study was to answer three specific questions: 1.) are the
two commonly known forms of white-eyes in Sri Lanka, Z.ceylonensis and Z.palpebrosus phe-
notypically and phylogenetically distinct? 2.) if so, are they phylogenetically sister to each
other? and 3.) did Z.ceylonensis and Z.palpebrosus originate through sympatric speciation,
double colonization from the same ancestral population or independent colonization from dif-
ferent (unrelated) populations?
Methods
Field sampling
The Department of Wildlife Conservation of Sri Lanka (Permit No: WL/3/2/19/13) reviewed
the ethical, conservation and legal standing of this study and provided the permit to carry out
the research. The Forest Department of Sri Lanka (Permit No: R&E/RES/NFSRC/14) allowed
access to certain protected areas. The Forest Departments of Kerala (Permit No: Wl10-1647/
2011) provided permits to carry out this study in Western Ghats of India.
isolated and diverged into another species (B), resulting in two sister taxa (A and B). b.) Double colonization
from same ancestral population (AB’), resulting in paraphyletic taxa (A and B). c.) Independent colonization
from different ancestral populations (A and B), resulting in polyphyletic taxa.
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Adult white-eyes were sampled using 12m mist nets of 16mm mesh size [49], with the help
of call playbacks (as in [50]). In Sri Lanka, a total of 70 birds were captured in a ~200km tran-
sect along an elevational gradient spanning from the sea level (0m) at Colombo (6˚ 55’ 37.48"N
and 79˚ 51’ 40.47"E) to 2367m at mount Piduruthalagala (7˚ 00’ 03"N and 80˚ 46’ 26"E) the
highest peak in the island. In India, sampling was carried out in two locations in the Anaimalai
Hills of the Western Ghats mountain range (Fig 3). A total of 10 birds were captured from
Munnar (10˚ 05’ 21"N and 77˚ 03’ 35"E; 1800m-2500m) and from Periyar (9˚ 28’ N and77˚ 10’
E; 800 m-1000m). From each captured bird ~10μl of blood was collected from the brachial
vein of the wing [51] and stored in Queen’s Lysis Buffer [52] and birds were released back to
their original habitat.
Phenotypic measurements
Fifteen morphological characters were measured using a dial caliper (±0.01mm) from each
bird as in previous studies [50,53] (S1 Fig). The measurements that could vary with the
Fig 2. The two white-eye species in Sri Lanka. (A) Distribution of Z.palpebrosus and Z.ceylonensis.Z.palpebrosus has a widespread distribution
throughout the oriental region and in Sri Lanka. The endemic Z.ceylonensis is confined to the hills of Sri Lanka. (B) Z.palpebrosus (Oriental white-eye) and
(C) Z.ceylonensis (Ceylon white-eye) distribution in Sri Lanka. (D) Z.palpebrosus and (E) Z.ceylonensis.
https://doi.org/10.1371/journal.pone.0181441.g002
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measurer were taken three times to reduce measurement error. NW took the measurements
from all birds in this study.
Genetic data
Genomic DNA was extracted using standard Phenol-Chloroform method (as in [50,54]). The
entire second and third subunits of mitochondrial nicotinamide adenine dinucleotide dehy-
drogenase (ND2 and ND3) and fifth intron of the nuclear gene transcription growth factor
(TGFβ2) were amplified by polymerase chain reaction (PCR) and sequenced using Sanger
Fig 3. Sampling locations in Sri Lanka and in India. In Sri Lanka sampling spanned along an elevational gradient, from the sea level (0m) to the peak of
the highest mountain, Piduruthalagala (2360m). In India sampling was carried out in Munnar (1800m-2500m) and in Periyar (800 -1000m).
https://doi.org/10.1371/journal.pone.0181441.g003
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sequencing method. The thermo cycling profile was as below: denaturation at 95˚C for 5 min,
followed by 35 cycles of denaturation at 94˚C for 35s, annealing at 55˚C for 35s, extension at
72˚C for 45s, and a final extension step of 72˚C for 15min. ND2 was PCR amplified using
primers L5216 and H6313 [55], L5758 and H5766 [56], with the last two as internal sequencing
primers. ND3 was amplified with the primers L10755 and H11151 [57] and TGFβ2 with
TGF5-TGF6 [58]. Molecular work was done at the Molecular Ecology and Evolution labora-
tory at the Department of Zoology, University of Colombo and at the National Centre for Bio-
logical Sciences (NCBS), Bangalore. The Sequencing Facility at NCBS carried out Sanger
sequencing for all the samples.
Data analysis
Phenotypic analysis. Discriminant Function Analysis (DFA) was performed on the phe-
notypic data to determine whether there is a distinct phenotypic clusters, corresponding the
existing species of the white-eyes of Sri Lanka, in the dataset. To avoid collinear variables, sig-
nificant principal components (PCs) that resulted from a principal component analysis were
selected using eigenvalues and scree plots [59]. Two canonical plots were derived (JMP ver. 8,
SAS Inst., Cary, NC), one with the reduced set of variables (which had the highest contribution
to the selected PCs) and the second using the selected PCs.
Phylogenetic analysis. We used Geneious version 7.1.6 [60] to examine the trace files for
quality, to edit sequences, de novo assemble and multiple align sequences across taxa using
ClustalW algorithm [61]. We examined appropriate models of evolution and the best way to
partition gene regions using PartitionFinderver 1.1.0 [62]. The optimal partitioning scheme
had 4 partitions: 1
st
codon position ND2 and ND3, 2
nd
codon position ND2 and ND3, 3
rd
codon position ND2 and ND3, and TGF. Phylogenetic trees were built through Maximum
likelihood (ML) approach using RAxML ver. 8.1.22 [63] and Bayesian approach using
MrBayes ver 3.2.5 [64].
For ML, we conducted tree searches rapid bootstrap of 1000 replicates and there after a
thorough ML search of 10 runs using a separate GTR+G+I evolutionary model for each parti-
tion. Invariant sites were not included in the model. We conducted a Bayesian analysis by run-
ning the MCMC chain for 20,000,000 generations, sampling every 1000 steps, with 25% of the
samples discarded as burnin. We assessed the convergence using the standard deviation of
split frequencies below 0.01 and checking for stationarity using Tracer ver. 1.6 [65].
Divergence dating
We used BEAST ver. 2.4.4 [66] to estimate divergence times within Zosteropidae. We assigned
HKY model for each gene, with 4 categories estimate shape for gamma. We used a second calibra-
tion of Zosteropidae + Zosteronis (formerly Stachyris) from Philippines cited in Moyle et al [36]—
5.01 Ma (4.46–5.57 Ma). We assumed a Yule speciation process for the tree model and a relaxed
clock lognormal distribution for the molecular clock model, and linked clock and tree models.
We set calibration as a normal distribution with mean 5.01 and sigma of 0.555 and ran MCMC
chains for 20 million generations, sampling every 500
th
generation and discarding the first 25% as
burnin. We used Tracer ver. 1.6 [65] to examine parameters and to ensure stationarity.
Results
Phenotypic analysis
Based on the eigenvalues (S2 Table) and scree plot (S2 Fig) first three PCs were selected for the
DFA. The canonical plots separated Z.ceylonensis and Z.paplebrosus into two phenotypically
Patterns of colonization in Sri Lankan white-eyes
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distinct clusters with 87% accuracy (Fig 4). Opening of the eye ring and total culmen signifi-
cantly contributed to the phenotypic distinctness of the two species (Fig 4).
Phylogenetic analysis
The concatenated and partitioned ML and Bayesian trees showed similar topologies. In both
analyses, there are several short internodes and polytomies, however, the clades of significance
to Sri Lankan birds were well supported (Fig 5). Z.ceylonensis did not cluster with sympatric
Z.palpebrosus but is resolved as the basal lineage to all its congeners in the clade of Zosterops.
This relationship received high ML bootstrap support (100%) and Bayesian posterior probabil-
ity (1.0). Zosterops palpebrosus is not monophyletic, Z.p.unicus (Flores Island) groups with
Australasian species while the southern Asian sub species are in a separate clade that is sister to
Western Indian Ocean (African) species with strong support (90% ML bootstrap/ 1.0 Bayesian
PP). The Sri Lanka population of Z.palpebrosus (currently in the widespread subspecies (egre-
gius) is sister to the Western Ghats population (Z.p.nilgiriensis) with strong support (100/
1.0). Individual gene trees of ND2 and ND3 show similar patterns to the concatenated analyses
Fig 4. Canonical plots derived from the multivariate analysis. (A) Canonical plot of phenotypic variation of
the Z.ceylonensis and Z.palpebrosus populations with the morphological features that significantly contributed
to the three reduced variables (PC1-PC3). Z.ceylonensis and Z.palpebrosus are two phenotypically distinct
clusters that differentiate along the horizontal axis. Eye ring opening and total culmen contributed significantly to
differentiating the species along this axis. (B) Canonical plot of phenotypic variation of the Z.ceylonensis and Z.
palpebrosus populations with PC1, PC2 and PC3. Z.ceylonensis and Z.palpebrosus are two phenotypically
distinct clusters for which PC1 contributed significantly.
https://doi.org/10.1371/journal.pone.0181441.g004
Patterns of colonization in Sri Lankan white-eyes
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Fig 5. Phylogenetic affinities of white-eyes. Phylogenetic relationships of Zosterops white-eyes using maximum
likelihood (ML) analyses of the concatenated, partitioned dataset of 3 genes (ND2, ND3, TGF). The topology of ML
Patterns of colonization in Sri Lankan white-eyes
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in both ML and Bayesian approaches, however, the topology using TGF5 is less resolved, per-
haps due to insufficient informative sites.
Divergence dating
Results from the BEAST dating analyses (Fig 6) shows that Z.ceylonensisis much older diver-
gence that split from its congeners around 1.79MYA (95% HPD: 1.31–2.32). Zosterops palpeb-
rosus in Sri Lanka, on the other hand, is a more recent split that diverged 0.19MYA (95%
HPD: 0.10–0.31) from its sister population.
Discussion
Phenotypic distinctness of Z.ceylonensis and Z.palpebrosus in Sri
Lanka
Differences in phenotype (mainly plumage and vocalization), which had been the basis for sep-
arating the two species, is known for Z.ceylonensis and Z.palpebrosus in Sri Lanka [35,4547].
With an unbiased character based approach, here we showed that the two species are distinct
phenotypic clusters (Fig 4). Mees [48] suggested that Z.ceylonensis is morphologically closer to
Z.p.nilgiriensis than any other Z.palpebrosus [48], our study did not investigate morphological
similarities of Z.ceylonensis and Z.p.nilgiriensis, however our phylogenetic analysis showed a
separate origin for these two lineages.
Are Z.ceylonensis and Z.palpebrosus in Sri Lanka phylogenetically
distinct?
All individuals identified as Z.ceylonensis grouped together as a monophyletic group. Simi-
larly, all individuals of Z.palpebrosus from Sri Lanka form a distinct group. Therefore Z.ceylo-
nensis and Z.palpebrosus formed two distinct clades (Fig 5). There is concordance between
morphometric and phylogenetic divergence across these two species (Figs 46), hence we con-
clude that they are phenotypically and phylogenetically distinct lineages and true species for
Sri Lanka.
Are Zosterops white-eyes in Sri Lanka sister to each other?
Our analysis shows that these two lineages of Sri Lankan white-eyes are not each other’s closest
relatives. Similar to other studies of white-eyes [28,36], the genus Zosterops likely diversified
very rapidly as implied by the extremely short internodes throughout much of the tree (this
study and in [28,36]). Nevertheless, we can draw conclusions based on strong nodal support
values regarding the placement of the Sri Lankan lineages. Z.ceylonensis is not closely related
to the Z.palpebrosus, which is the most geographically proximate species found throughout
southern Asia and in Sri Lanka, but rather is sister to the entire Zosterops clade (Figs 5and 6).
There is strong support for this relationship in our phylogeny but given that many other
named species of Zosterops are yet to be sampled genetically, additional data will shed more
light into this relationship.
Furthermore there is strong support for the placement of Sri Lankan Z.p.egregious as sister
to the Western Ghats Z.p.nilgiriensis (Fig 5). However Z.palpebrosus appears to be polyphyletic
and Bayesian analyses were highly similar (outgroups not shown). Symbols at nodes indicate ML bootstrap
support (open circles show >70%, solid circles show >90%); all nodes with circles had Bayesian posterior
probabilities values of 0.95 or greater. Illustrations of white-eyes are by J. Smit [67] (public domain).
https://doi.org/10.1371/journal.pone.0181441.g005
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Fig 6. Divergence times of Zosterops.The blue colour bars indicate 95% HPD (Highest Posterior Density) intervals. Divergence time estimates show that
Z.ceylonensis diverged around 1.79 MYA and Z.palpebrosus in Sri Lanka diverged around 0.19 MYA.
https://doi.org/10.1371/journal.pone.0181441.g006
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with at least one subspecies (Z.p.unicus) not grouping with the remaining populations from
Asia. We only have a limited number of populations included from southern Asia to the analy-
sis, but within this sampling, the southern populations from Sri Lanka and Western Ghats are
more closely related than populations within the rest of Indian subcontinent. Z.palpebrosus is
sister to a clade from western Indian Ocean islands and Africa with strong support, but the
directionality of colonization is unclear given the short internodes of other congeners (Figs 5
and 6) [28].
Did Z.ceylonensis and Z.palpebrosus in Sri Lanka originate through
sympatric speciation, double colonization from same population or
independent colonization from different populations?
Ripley (1949) suggested the double ‘invasion’ (colonization) hypothesis to explain the origins
of the white-eye species pair in Sri Lanka and assumed Z.ceylonensis as the species that may
have arrived first to the island [25]. Our results, especially the dated phylogeny confirms the
early arrival of Z.ceylonensis (Fig 6). Moreover our phylogenetic analysis indicates that the Sri
Lankan Z.palpebrosus show strong affinities to the Indian Z.palpebrosus. However Z.ceylonen-
sis does not show affinities to any of the extant south Asian clades. Therefore the Sri Lankan
white-eyes must have colonized from different ancestral source in different time windows.
Conclusions
Here we showed that Z.ceylonensis and Z.palpebrosus in Sri Lanka are phenotypically and
genetically distinct entities, and that they are not sister to each other. Z.palpebrosus is sister to
the Western Indian Ocean Zosterops clade and within, Z.p.egregius in Sri Lanka is sister to Z.p.
nilgiriensis of Western Ghats. Our results suggest that the two Zosterops species originated in the
island through independent colonizations from different ancestral lineages and not through
island speciation or double colonization from the same continental ancestral population. We
also confirm that Z.ceylonensis is an ancient lineage which originated first and Z.palpebrosus
later. While the origin of Z.ceylonensis is still unclear, our results imply that Z.ceylonensis could
be the ancestor to all Zosterops white-eyes. However, due to the fact that many of the Zosterops
have not been sampled, identity of the ancestral Zosterops cannot be confirmed. This study pro-
vides vital information on the patterns of speciation and the generation of endemism in the
island of Sri Lanka. It stresses that Sri Lanka fauna may not entirely be a subset of the Indian
faunal assemblage, even with groups that show high dispersal ability such as birds. The patterns
of colonization can get complicated in continental islands with a history of complex geological
affinities with neighboring landmasses.
Supporting information
S1 Fig. Morphometric measurements used for the morphometric analysis. 1. weight 2. head
length 3. head width 4. Total culmen 5. Exposed culmen 6. bill height 7. bill width 8. thickness
of the eye-ring; eye ring (a) 9. opening of the ring; eye ring (b) 10. diameter of the eye-ring; eye
ring (c) 11. eye ring width 12. flattened wing length 13. tarsus (right) length 14. first claw
length 15. tail length.
(TIF)
S2 Fig. Scree plot. This plots the eigen values associated with each PC. At PC4 the slope of the
curve levels off, hence only PC1, PC2 and PC3 were used for the analysis.
(TIF)
Patterns of colonization in Sri Lankan white-eyes
PLOS ONE | https://doi.org/10.1371/journal.pone.0181441 August 9, 2017 12 / 16
S1 Table. Sample ID or band number, tissue source and collection locality for each species
used in the phylogenetic study with GenBank accession numbers for each gene sequence.
Footnote.
FMNH, The Field Museum of Natural History; KUNHM, University of Kansas Natural His-
tory Museum; LSUMNS, Louisiana State University Museum of Natural Science; USNM,
National Museum of Natural History; UWBM, University of Washington Burke Museum;
AMNH, American Museum of Natural History; CMNH, Cleveland Museum of Natural His-
tory.
(DOCX)
S2 Table. Eigen values for each variable in each principal component (PC) resulted from
the principal component analysis.
(DOCX)
Acknowledgments
We thank Prof. Preethi Udagama and Saminda Fernando, Department of Zoology, University
of Colombo for the assistance provided during all steps of the project implementation; C. K.
Vishnudas for extensive field assistance in the Western Ghats; Sequencing facility at the
National Center for Biological Sciences, Bangalore India for performing Sanger Sequencing;
Avian Evolution Node lab members at the Department of Zoology, University of Colombo
and Lab 3 members at the National Center for Biological Sciences for the help during labora-
tory work; S.P. Vijay Kumar and Naveen Namboothri for discussions; Krishnapriya Tamma
for comments on the manuscript; The Department of Wildlife Conservation of Sri Lanka (Per-
mit No: WL/3/2/19/13), Forest Department of Sri Lanka (Permit No: R&E/RES/NFSRC/14)
and Forest Departments of Kerala (Permit No: Wl10-1647/2011) for providing permits to
carry out the field components of this study. Major funding is provided by the National
Research Council of Sri Lanka research grant (Grant number: 14–072) to SS. Three anony-
mous reviewers and Prof. Tzen-Yuh Chiang the academic editor of PLOS-one provided
insightful comments on the earlier versions of this manuscript.
Author Contributions
Conceptualization: V. V. Robin, Sampath S. Seneviratne.
Data curation: Nelum Wickramasinghe.
Formal analysis: Nelum Wickramasinghe, Sushma Reddy.
Funding acquisition: Uma Ramakrishnan, Sampath S. Seneviratne.
Investigation: Nelum Wickramasinghe, V. V. Robin, Uma Ramakrishnan, Sampath S.
Seneviratne.
Methodology: Nelum Wickramasinghe, V. V. Robin, Sushma Reddy, Sampath S. Seneviratne.
Project administration: Uma Ramakrishnan, Sampath S. Seneviratne.
Resources: V. V. Robin, Uma Ramakrishnan, Sushma Reddy, Sampath S. Seneviratne.
Software: Sushma Reddy.
Supervision: Uma Ramakrishnan, Sampath S. Seneviratne.
Validation: Sushma Reddy.
Visualization: Sushma Reddy.
Patterns of colonization in Sri Lankan white-eyes
PLOS ONE | https://doi.org/10.1371/journal.pone.0181441 August 9, 2017 13 / 16
Writing – original draft: Nelum Wickramasinghe, V. V. Robin, Sushma Reddy, Sampath S.
Seneviratne.
Writing – review & editing: Nelum Wickramasinghe, V. V. Robin, Uma Ramakrishnan, Sus-
hma Reddy, Sampath S. Seneviratne.
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... In Zosterops, however, traditional methods that rely on morphological tools to infer how species are related to one another have proven to be unreliable, as plumage features of ecologically distinct and geographically disjunct Zosterops species are often indistinguishable (Mees, 1957;Mayr, 1965). Although a more recent application of genetic methods has helped disentangle the white-eye radiation to some extent, most studies have concentrated on Afrotropical, Melanesian, and Indian Ocean members of the genus (Slikas et al., 2000;Warren et al., 2006;Moyle et al., 2009;Cox et al., 2014;Linck et al., 2016;Wickramasinghe et al., 2017;Manthey et al., 2020;Martins et al., 2020). There continues to be a dearth of knowledge on this radiation across the core of its Asian distribution due to limited sampling and lack of genetic data. ...
... Apart from incomplete geographic sampling, the lack of resolution of the white-eye radiation has largely been a consequence of sparse genomic sampling: most phylogenetic studies of white-eyes have been restricted to one or a few genetic markers, resulting in trees that are plagued by unresolved polytomies, hampering useful evolutionary inference (Slikas et al., 2000;Warren et al., 2006;Moyle et al., 2009;Oatley et al., 2012;Á .S and Joseph, 2013;Cox et al., 2014;Husemann et al., 2016;Linck et al., 2016;Round et al., 2017;Wickramasinghe et al., 2017;Shakya et al., 2018;Cai et al., 2019;Lim et al., 2019;O'Connell et al., 2019;Martins et al., 2020). Disentangling relationships within rapid and recent radiations, such as white-eyes, requires overcoming the challenges of heterogeneous gene trees due to biological factors such as incomplete lineage sorting (Edwards et al., 2005;Song et al., 2012). ...
... The evolutionary history of Zosterops has received a fair amount of scientific attention, but mostly by means of single mitochondrial or few nuclear loci, therefore resulting in trees plagued by unresolved polytomies (e.g. Figure 2-figure supplement 3; Degnan and Moritz, 1992;Degnan, 1993;Slikas et al., 2000;Warren et al., 2006;Moyle et al., 2009;Oatley et al., 2012;Á .S and Joseph, 2013;Cox et al., 2014;Husemann et al., 2016;Linck et al., 2016;Round et al., 2017;Wickramasinghe et al., 2017;Shakya et al., 2018;Cai et al., 2019;Lim et al., 2019;O'Connell et al., 2019). Using more than 700 genome-wide loci with a dense species sampling, our study produced an improved phylogeny of Zosterops and reveals the existence of three discrete main clades characterized by an Indo-African, Asiatic, and Australasian core of distribution, respectively ( Figure 2). ...
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Archipelagoes serve as important 'natural laboratories' which facilitate the study of island radiations and contribute to the understanding of evolutionary processes. The white-eye genus Zosterops is a classical example of a 'great speciator', comprising c. 100 species from across the Old World, most of them insular. We achieved an extensive geographic DNA sampling of Zosterops by using historical specimens and recently collected samples. Using over 700 genome-wide loci in conjunction with coalescent species tree methods and gene flow detection approaches, we untangled the reticulated evolutionary history of Zosterops , which comprises three main clades centered in Indo-Africa, Asia, and Australasia, respectively. Genetic introgression between species permeates the Zosterops phylogeny, regardless of how distantly related species are. Crucially, we identified the Indonesian archipelago, and specifically Borneo, as the major centre of diversity and the only area where all three main clades overlap, attesting to the evolutionary importance of this region.
... In Zosterops , however, traditional methods that rely on morphological tools to infer how species are related to one another have proven to be unreliable, as plumage features of ecologically distinct and geographically disjunctZosterops species are often indistinguishable (Mees 1957;Mayr 1965). Although a more recent application of genetic methods has helped disentangle the white-eye radiation to some extent, most studies have concentrated on Melanesian and Indian Ocean members of the genus (Slikas et al. 2000;Warren et al. 2006;Moyle et al. 2009;Cox et al. 2014;Linck et al. 2016;Wickramasinghe et al. 2017;Manthey et al. 2020). There continues to be a dearth of knowledge on this radiation across the core of its Asian distribution due to limited sampling and lack of genetic data. ...
... Apart from incomplete geographic sampling, the lack of resolution of the white-eye radiation has largely been a consequence of sparse genomic sampling: most phylogenetic studies of white-eyes have been restricted to one or a few genetic markers, resulting in trees that are plagued by unresolved polytomies, hampering useful evolutionary inference (Slikas et al. 2000;Warren et al. 2006;Moyle et al. 2009;Oatley et al. 2012;Nyári and Joseph 2013;Cox et al. 2014;Husemann et al. 2016;Linck et al. 2016;Round et al. 2017;Wickramasinghe et al. 2017;Shakya et al. 2018;Cai et al. 2019;Lim et al. 2019;O'Connell et al. 2019). Disentangling relationships within rapid and recent radiations, such as white-eyes, requires overcoming the challenges of heterogenous gene trees due to biological factors such as incomplete lineage sorting (Edwards et al. 2005;Song et al. 2012). ...
... Given white-eyes' model status in speciation research, the evolutionary history of Zosterops has been addressed by a fair amount of research, but most studies have utilized single mitochondrial or few nuclear loci, resulting in trees that are plagued by unresolved polytomies (e.g., Fig. S2; (Slikas et al. 2000;Warren et al. 2006;Moyle et al. 2009;Oatley et al. 2012;Nyári and Joseph 2013;Cox et al. 2014;Husemann et al. 2016;Linck et al. 2016;Round et al. 2017;Wickramasinghe et al. 2017;Shakya et al. 2018;Cai et al. 2019;Lim et al. 2019;O'Connell et al. 2019). Using more than 700 genome-wide loci with a dense species sampling, our study produced a greatly improved phylogeny of Zosterops and reveals the existence of three discrete main clades characterized by an Indo-African, Asiatic and Australasian core of distribution, respectively (Fig. 2). ...
... ND2, ND3 and COI are widely used genes, allowing for comparisons with a large amount of published material to elucidate the evolutionary history of our target species. ND2 and ND3 sequences were concatenated and analysed separately to COI sequences, due to a much wider sample of Zosterops ND2 and ND3 genes being available on GenBank Wickramasinghe et al., 2017). Moyle et al. (2009) ...
... Myr) by Moyle et al. (2009), was used as a point calibration. This calibration was set as a normal distribution with mean 5.01 and sigma 0.555 (Wickramasinghe et al., 2017). Rates of evolution were set at 0.029 (lower bound: 0.024, upper bound: 0.033) and 0.024 (lower bound: 0.019, upper bound: 0.029) for ND2 and ND3, respectively, representing the number of substitutions per site per million years, derived from estimates produced by Lerner et al. (2011) for honeycreepers, following Linck et al. (2016). ...
... A Relaxed Clock Log Normal clock model was found to have the highest marginal likelihood and was selected for use (Baele et al., 2012(Baele et al., , 2013. A Yule speciation process was assumed for the tree model, following Wickramasinghe et al. (2017). We ran 10 independent MCMC chains for 100 million generations, sampling every 20 000 generations. ...
Article
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Research in the Indo-Pacific region has contributed massively to the understanding of speciation. White-eyes (Aves: Zosteropidae: Zosterops), a lineage containing both widespread ‘supertramp’ species and a high proportion of island endemics, have provided invaluable models. Molecular tools have increased speciation research, but delimiting species remains problematic. We investigated the evolutionary history of Zosterops species in south-east Sulawesi using mitochondrial DNA, morphometric, song and plumage analyses, to draw species limits and assess which techniques offer best resolution. Our investigation revealed a novel Zosterops species, >3000 km from its closest relative. Additionally, we demonstrated unanticipated diversity in the alleged ‘supertramp’ Zosterops chloris and propose the Wakatobi Islands subspecies (Z. c. flavissimus) to be given full species status. Furthermore, we provide the first molecular and phenotypic assessment of the Sulawesi endemic Zosterops consobrinorum. While local populations of this species vary in either genetics or morphometrics, none show consistency across measures. Therefore, we propose no change to Zosterops consobrinorum taxonomy. This study gives insight into one of the great Indo-Pacific radiations and demonstrates the value of using multiple lines of evidence for taxonomic review.
... White-eyes (Zosteropidae) stand out as a lineage in which diversification rates have been exceptionally high, and with nearly half of the world's forms being single-island endemics, they appear to respond rapidly to the geographical drivers of speciation [26][27][28]. A number of islands are occupied by more than one recognized species, but the presence of multiple species on a single island has been attributed to multiple colonizations in all cases [6,[29][30][31][32]. Uniquely among whiteeyes, and even among birds in general, the Reunion grey white-eye displays geographical variation in morphological and plumage colour traits within the small and remote volcanic oceanic island of Reunion (2512 km 2 ) [33]. ...
... In fact, across all islands currently occupied by more than one Zosterops species, separate colonizations can be easily invoked (see e.g. [29][30][31][32]). This suggests that in most species, low dispersal ability mainly corresponds to low 'over-water' dispersal. ...
Article
The presence of congeneric taxa on the same island suggests the possibility of in situ divergence, but can also result from multiple colonizations of previously diverged lineages. Here, using genome-wide data from a large population sample, we test the hypothesis that intra-island divergence explains the occurrence of four geographical forms meeting at hybrid zones in the Reunion grey white-eye (Zosterops borbonicus), a species complex endemic to the small volcanic island of Reunion. Using population genomic and phylogenetic analyses, we reconstructed the population history of the different forms. We confirmed the monophyly of the complex and found that one of the lowland forms is paraphyletic and basal relative to others, a pattern highly consistent with in situ divergence. Our results suggest initial colonization of the island through the lowlands, followed by expansion into the highlands, which led to the evolution of a distinct geographical form, genetically and ecologically different from the lowland ones. Lowland forms seem to have experienced periods of geographical isolation, but they diverged from one another by sexual selection rather than niche change. Overall, low dispersal capabilities in this island bird combined with both geographical and ecological opportunities seem to explain how divergence occurred at such a small spatial scale.
... mya) (this study) and Zosterops ceylonensis 1.79 (95% HPD 1.31-2.32 mya) (Wickramasinghe et al., 2017). Aridification-driven speciation in Peninsular India during the Late Miocene and Pliocene has been reported for dryzone adapted lizards too, such as Sitana (Deepak & Karanth, 2018) and Ophisops (Agarwal & Ramakrishnan, 2017). ...
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We examined the phylogenetic relationships of South Asian bulbuls with focus on endemic species to understand the historical biogeography of the region. Molecular phylogenetic analysis, divergence date estimation and ancestral area reconstruction were performed to understand the role of paleoclimate on extant bulbul diversity and their distribution. We tested for vicariance, dispersal and in situ speciation events that defined the bulbul assemblage in the region. Using morphometric data and phylogeny, we resolved taxonomic uncertainties. There was a single event of in situ speciation of a dry-zone species, and isolation of species to the wet zone, causing endemism. Diversification rates remained relatively constant during late Miocene and Pliocene. Sundaland-Philippines served as the seat of diversification of bulbul lineages, and Indochina was part of the dispersal route. Bulbul diversity in the region has been shaped due to dispersal events at different time periods ranging from late Miocene to early Pleistocene. Post-Miocene aridification was an important driver of diversification in the region, by creating barriers for wet-zone species, and opening up new habitats for dry-zone species.
... A species of particular importance is the Indian White-eye (earlier Oriental White-eye) that has been observed and is known to breed in some of the islands of Lakshadweep (Hume 1876;Betts 1938;eBird 2021). Biogeographical and phylogenetic studies have addressed the colonization by this species of various Indo-Pacific islands (O'Connell et al. 2019;Moyle et al. 2009;Wickramasinghe et al. 2017;Martins et al. 2020). The species occurring in Lakshadweep is Z. p. egregius (Mees 1957), but Mees had noted the very long tails, like that of Z. p. nilgiriensis, in the four specimens he studied. ...
... A species of particular importance is the Indian White-eye (earlier Oriental White-eye) that has been observed and is known to breed in some of the islands of Lakshadweep (Hume 1876;Betts 1938;eBird 2021). Biogeographical and phylogenetic studies have addressed the colonization by this species of various Indo-Pacific islands (O'Connell et al. 2019;Moyle et al. 2009;Wickramasinghe et al. 2017;Martins et al. 2020). The species occurring in Lakshadweep is Z. p. egregius (Mees 1957), but Mees had noted the very long tails, like that of Z. p. nilgiriensis, in the four specimens he studied. ...
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A checklist of the birds of Lakshadweep Islands, comprising 145 possible species was pared down to 115 definite species based on various evidence such as specimens, photographs, and field descriptions. These islands are important in terms of valuable habitats, though small, that serve as a halting site for migratory species, and breeding sites for pelagic birds. They often host stragglers or nomadic birds, and exhausted migrants. A definitive checklist will aid in forming management and conservation plans for vulnerable ecosystems in these small atolls, and their dependent species.
... If we had sampled dry forest habitats in southernmost India and Sri Lanka, their species compositions would have been more similar than the species compositions of rainforest habitats (Kotagama and Ratnavira 2010). Our study, along with previous studies, suggests that the high dissimilarity in rainforest communities between Western Ghats and Sri Lanka should be taken into account during the global analysis of biodiversity hotspots (Bossuyt et al. 2004;Ramachandran et al. 2017;Wickramasinghe et al. 2017). ...
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In the last 50 years, intensive agriculture has replaced large tracts of rainforests. Such changes in land use are driving niche-based ecological processes that determine local community assembly. However, little is known about the relative importance of these anthropogenic niche-based processes, in comparison to climatic niche-based processes and spatial processes such as dispersal limitation. In this study, we use a variation partitioning approach to determine the relative importance of land-use change (ranked value of forest loss), climatic variation (temperature and precipitation), and distance between transects, on bird beta diversity at two different spatial scales within the Western Ghats-Sri Lanka biodiversity hotspot. Our results show that the drivers of local community assembly are scale dependent. At the larger spatial scale, distance was more important than climate and land use for bird species composition, suggesting that dispersal limitation over the Palk Strait, which separates the Western Ghats and Sri Lanka, is the main driver of local community assembly. At the smaller scale, climate was more important than land use, suggesting the importance of climatic niches. Therefore, to conserve all species in a biodiversity hotspot, it is important to consider geographic barriers and climatic variation along with land-use change.
... Although several examples exist where multiple white-eye Zosterops species or subspecies coexist and are thought to have come into secondary contact within the last 2 million years (e.g., Warren et al. 2006;Clegg and Phillimore 2010;Melo et al. 2011;Wickramasinghe et al. 2017), we know of only two previous studies in which gene flow has been examined and hybridization detected between two parapatric subspecies of white-eyes using multiple genomic markers. One is between subspecies of Zosterops barbonicus on Reunion Island (0.434 my diverged; Milá et al. 2010), and the other is in Zosterops virens subspecies in Cape Region of South Africa (0.77 my diverged; Oatley et al. 2012Oatley et al. , 2017. ...
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Examining what happens when two closely‐related species come into secondary contact provides insight into the later stages of the speciation process. The Zosteropidae family of birds is one of the most rapidly speciating vertebrate lineages. Members of this family are highly vagile and geographically widespread, raising the question of how divergence can occur if populations can easily come into secondary contact. On the small island of Kolombangara, two closely‐related non‐sister species of White‐eyes, Zosterops kulambangrae and Z. murphyi, are distributed along an elevational gradient and come into secondary contact at mid‐elevations. We captured 134 individuals of both species along two elevational transects. Using genotyping‐by‐sequencing data and a mitochondrial marker, we found no evidence of past hybridization events and strong persistence of species boundaries, even though the species have only been diverging for approximately two million years. We explore potential reproductive barriers that allow the two species to coexist in sympatry, including premating isolation based on divergence in plumage and song. We also conducted a literature review to determine the time it takes to evolve complete reproductive isolation in congeneric avian species/subspecies in secondary contact (restricted to cases where congeneric taxa are parapatric or have a hybrid zone), finding our study is one of the youngest examples of complete reproductive isolation studied in a genomic context reported in birds. This article is protected by copyright. All rights reserved
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Despite advances in biodiversity exploration, the origins of Sri Lanka's fauna and flora have never yet been treated in a synthetic work. This book draws together the threads that make up that fascinating 100-million year story. Encompassing the island's entire biota while emphasising the ecology, biogeography and phylogeography of freshwater fishes, it provides a comprehensive context for understanding how the island's plants and animals came to be as they are. The 258-page text contains more than 200 figures, photographs and maps. It provides a clear account of how, when and from where the ancestors of the plants and animals that now inhabit Sri Lanka came. For the first time, the island's unique biodiversity can be understood and appreciated in its historical and evolutionary context in this invaluable sourcebook, designed for scientists, students and biodiversity enthusiasts alike.
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Among birds, white-eyes (genus Zosterops) have diversified so extensively that Jared Diamond and Ernst Mayr referred to them as the “great speciator.” The Zosterops lineage exhibits some of the fastest rates of species diversification among vertebrates, and its members are the most prolific passerine island colonizers. We present a high-quality genome assembly for the silvereye (Zosterops lateralis), a white-eye species consisting of several subspecies distributed across multiple islands. We investigate the genetic basis of rapid diversification in white-eyes by conducting genomic analyses at varying taxonomic levels. First, we compare the silvereye genome with those of birds from different families and searched for genomic features that may be unique to Zosterops. Second, we compare the genomes of different species of white-eyes from Lifou island (South Pacific), using whole genome resequencing and restriction site associated DNA. Third, we contrast the genomes of two subspecies of silvereye that differ in plumage color. In accordance with theory, we show that white-eyes have high rates of substitutions, gene duplication, and positive selection relative to other birds. Below genus level, we find that genomic differentiation accumulates rapidly and reveals contrasting demographic histories between sympatric species on Lifou, indicative of past interspecific interactions. Finally, we highlight genes possibly involved in color polymorphism between the subspecies of silvereye. By providing the first whole-genome sequence resources for white-eyes and by conducting analyses at different taxonomic levels, we provide genomic evidence underpinning this extraordinary bird radiation.
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Three species of closely related woodpeckers (sapsuckers; Sphyrapicus) hybridize where they come into contact, presenting a rare 'λ-shape' meeting of hybrid zones. Two of the three arms of this hybrid zone are located on either side of the Interior Plateau of British Columbia, Canada bordering the foothills of the Coast Mountains and the Rocky Mountains. The third arm is located in the eastern foothills of the Rocky Mountains. The zones of hybridization present high variability of phenotypes and alleles in relatively small areas and provide an opportunity to examine levels of reproductive isolation between the taxa involved. We examined phenotypes (morphometric traits and plumage) and genotypes of 175 live birds across the two hybrid zones. We used the Genotyping By Sequencing (GBS) method to identify 180 partially diagnostic single nucleotide polymorphisms (SNPs) to generate a genetic hybrid index (GHI) for each bird. Phenotypically diverged S. ruber and S. nuchalis are genetically closely related, while S. nuchalis and S. varius have similar plumage but are well separated at the genetic markers studied. The width of both hybrid zones is narrower than expected under neutrality, and analyses of both genotypes and phenotypes indicate that hybrids are rare in the hybrid zone. Rarity of hybrids indicates assortative mating and/or some form of fitness reduction in hybrids, which might maintain the species complex despite close genetic distance and introgression. These findings further support the treatment of the three taxa as distinct species. Journal of Avian Biology
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Among birds, white-eyes (genus Zosterops) have diversified so extensively that Jared Diamond and Ernst Mayr referred to them as the "great speciator". The Zosterops lineage exhibits some of the fastest rates of species diversification among vertebrates, and its members are the most prolific passerine island colonisers. We present a high-quality genome assembly for the silvereye (Z. lateralis), a white-eye species consisting of several subspecies distributed across multiple islands. We investigate the genetic basis of rapid diversification in white-eyes by conducting genomic analyses at varying taxonomic levels. Firstly, we compare the silvereye genome to those of birds from different families and searched for genomic features that may be unique to Zosterops. Secondly, we compare the genomes of different species of white-eyes from Lifou island (South Pacific), using whole genome re-sequencing and restriction-site associated DNA. Thirdly, we contrast the genomes of two subspecies of silvereye that differ in plumage colour. In accordance with theory, we show that white-eyes have high rates of substitutions, gene duplication and positive selection relative to other birds. Below genus level, we find that genomic differentiation accumulates rapidly and reveal contrasting demographic histories between sympatric species on Lifou, indicative of past interspecific interactions. Finally, we highlight genes possibly involved in colour polymorphism between the subspecies of silvereye. By providing the first whole-genome sequence resources for white-eyes and by conducting analyses at different taxonomic levels, we provide genomic evidence underpinning this extraordinary bird radiation. © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
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The Eastern Afromontane biodiversity hotspot composed of highly fragmented forested highlands (sky islands) harbours exceptional diversity and endemicity, particularly within birds. To explain their elevated diversity within this region, models founded on niche conservatism have been offered, although detailed phylogeographic studies are limited to a few avian lineages. Here we focus on the recent songbird genus Zosterops, represented by montane and lowland members, to test the roles of niche conservatism versus niche divergence in the diversification and colonization of East Africa's sky islands. The species-rich white-eyes are a typically homogeneous family with an exceptional colonizing ability, but in contrast to their diversity on oceanic islands, continental diversity is considered depauperate and has been largely neglected. Molecular phylogenetic analysis of ~140 taxa reveals extensive polyphyly among different montane populations of Z. poliogastrus. These larger endemic birds are shown to be more closely related to taxa with divergent habitat types, altitudinal distributions and dispersal abilities than they are to populations of restricted endemics that occur in neighbouring montane forest fragments. This repeated transition between lowland and highland habitats over time demonstrate that diversification of the focal group is explained by niche divergence. Our results also highlight an underestimation of diversity compared to morphological studies that has implications for their taxonomy and conservation. Molecular dating suggests that the spatially extensive African radiation arose exceptionally rapidly (1-2.5 Ma) during the fluctuating Plio-Pleistocene climate, which may have provided the primary driver for lineage diversification. This article is protected by copyright. All rights reserved.
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The native land-snail fauna of the Hawaiian islands was investigated from a combined perspective of ecological and historical, vicariant, and dispersalist biogeography. There were more than 750 described, valid species; almost all were endemic to the archipelago, many to single islands. Path analysis showed that island area, per se, had the strongest influence on numbers of species. Island altitude and number of plant communities, both strongly related to area and both dimensions of habitat diversity, also had major influences. The influence of island age was complex. A direct effect, older islands having more species, was more than counterbalanced by the strong indirect effects of age on area and altitude: older islands are smaller and lower, and smaller, lower islands had fewer species. Distance of an island from a source of colonization was of minor importance. Species richness thus appears to be related almost exclusively to evolutionary radiation in situ and not to an equilibrium between immigration and extinction. Islands need not be extremely isolated for evolutionary radiation to be more important than immigration/extinction dynamics in determining species richness, but isolation is a relative term dependent on the dispersal abilities of the organisms in question. Numbers of recorded species were also strongly correlated with collecting effort on each island, a result that stands as a warning to others involved in such studies. Numbers of species in different families were not evenly distributed across islands. Notably, Kauai had more amastrids and helicinids and fewer achatinellids than predicted; Oahu had more amastrids but fewer pupillids and succineids than predicted; Hawaii exhibited the opposite pattern from Oahu. These patterns may partly reflect the vagaries of collecting/describing effort, but some may be due to the combined effects of historical factors and competitive exclusion. The distribution of shell height/diameter was bimodal with a distinct absence of more or less equidimensional species, a general pattern seen in other faunas. Among the pulmonates, tall species predominated, suggesting a relative lack of opportunity for globular/flat species. Notably, amastrids occurred in both modes, evidence that, at least in part, ecological not taxonomic factors underlie the bimodality. The proportions of tall and globular/flat species did not vary among islands. Prosobranchs were mostly low-spired but generally less flat than the pulmonates in the low-spired mode. The islands were probably colonized originally by small taxa. Large, tall shells are found only on Kauai and Niihau, the oldest of the main islands, suggesting that opportunities for such species are probably available on other islands.
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Diamond, J. M. (Physiology Department, University of California Medical Center, Los Angeles, California 90024) 1977. Continental and insular speciation in Pacific land birds. Syst. Zool. 26:263-268. —Three modes of allopatric speciation can be distinguished, depending on whether the isolating geographic barrier is within a single land mass (“continental speciation”), between islands of the same archipelago, or between different archipelagoes (“insular speciation”). The contributions of these three modes to speciation in Pacific land birds are analyzed. Continental speciation in birds has occurred in no Pacific land mass smaller than Australia, New Guinea, and possibly New Zealand; intraarchipelagal speciation has occurred only on six of the most remote archipelagoes; and inter-archipelagal speciation has produced most of the sympatric bird species pairs from the Bismarcks to Samoa. The frequency of each mode depends on area and isolation of the island, and on mobility and perhaps population density of the taxa involved. What is an “island” to some taxa may be a “continent” to others. For example, New Caledonia behaves as a continent to higher plants, insects, and lizards, but not to birds or ferns. [Speciation; Pacific land birds.]