doi:10.1111/j.1420-9101.2008.01588.x
Establishing a perimeter position: speciation around
the Indian Ocean Basin
G. VOELKER & R. K. OUTLAW
Department of Biology, University of Memphis, Memphis, TN, USA
Keywords:
Abstract
dispersal;
historical ecology;
Indian Ocean;
thrushes;
vicariance.
Historical biological interactions among peripheral landmasses on the periphery of the Indian Ocean Basin (IOB) are generally poorly understood. While
interactions based on early Gondwanan vicariance have been used to explain
present day lineage distributions, several recent studies have instead inferred
dispersal across the IOB. This inference is often advanced because lineages
under study have species inhabiting IOB islands. Here we examine the roles of
continental vicariance vs. trans-IOB dispersal in the distribution of an avian
genus found around the perimeter of the IOB. A molecular phylogeny does
reveal evidence of a relationship that would require the inference of trans-IOB
dispersal between eastern Africa and Sri Lanka. However, molecular clock
data, ancestral area analyses and paleoclimatic reconstructions suggest that
vicariance related to tropical forest expansion and retraction is more likely to
have facilitated African–Asian interchange, with an initial colonization of
Africa from Asia quickly followed by a recolonization of Asia. Subsequent
dispersal from Asia to Sri Lanka and islands east of the Sunda Shelf are
inferred; these latter islands were colonized in a stepping-stone fashion that
culminated in colonization of the Sunda Shelf, and a recolonization of
mainland Asia. We propose that circum-IOB distributions, which post-date
early Gondwanan breakup, are most likely the result of continent-based
vicariant events, particularly those events related to large-scale habitat
alterations, and not trans-IOB dispersals.
Introduction
The geological and ecological history of landmasses
around the Indian Ocean Basin (IOB) provides evidence with which to test the roles that vicariance and
dispersal may have played in the establishment of
circum-IOB lineages. Historically, vicariant mechanisms
related to the geologically well-documented breakup of
Gondwanaland have been invoked to explain the
establishment of IOB distributions (McLoughlin,
2001). More recently, biogeographic patterns in diverse
lineages, including birds (Voelker, 1999, 2002; Outlaw
et al., 2007), lizards (Amer & Kumazawa, 2005),
Correspondence: Gary Voelker, Department of Biology, University of
Memphis, 3700 Walker Avenue, Memphis, TN 38152, USA.
Tel.: +1 901 678 1386; fax: +1 901 678 4746;
e-mail: [email protected]
mammals (Vrba, 1985, 1993) and plants (Trénel et al.,
2007), suggest shifting climatic cycles that post-date
Gondwanan breakup drive major ecological changes,
and have played a considerable role in driving speciation in vertebrate groups distributed in both Africa
and Eurasia.
However, strict vicariance has proven insufficient to
explain many present-day IOB distributions. Biogeographic analyses of diverse lineages, from vertebrates to
plants, have shown patterns of over-water dispersal
within the IOB system (e.g. Vences et al., 2001; Raxworthy et al., 2002; Morley, 2003; Warren et al., 2003, 2005;
Yuan et al., 2005; Rocha et al., 2006; Trénel et al., 2007).
Increasingly, over-water dispersal has been inferred as a
mechanism of colonization and speciation, because
molecular clock dates suggest that many lineages
diverged too recently to have experienced early Gondwanan rifting, or are not inferred to have dispersed
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during periods ecologically suitable for range expansion.
Thus, robust historical biogeographic analyses need to
explore the possibility of both scenarios as viable explanations for the observed, often allopatric distributions of
lineages around the IOB.
Avian distributions in and around the IOB suggest that
dispersal may indeed have played an important role in
establishing those distributions; birds fly, making longdistance over-water crossings more plausible than inferring similar sweepstake dispersals for other vertebrate
lineages. This is particularly true with respect to highly
mobile avian lineages such as seabirds. While songbirds
are typically considered less likely to cross large water
barriers than are seabirds, numerous songbird lineages
have circum-IOB distributions (or nearly so). Although
long-distance sweepstake dispersals (Simpson, 1953)
across the IOB possibly explain these patterns, an
alternative would involve stepping-stone colonizations
of land-masses in the IOB. Fuchs et al. (2006) and
Jønnson & Fjeldså (2006) have relied on an explicit
trans-IOB scenario directly linking avian lineages on the
eastern margin of the IOB (southeast Asia and Australia),
with avian lineages in Africa. This scenario relies on
stepping-stone dispersal across Eocene–Oligocene land
bridges, and currently submerged plateaus and seamounts (see also Steenis, 1962), but the scenario is not
unique to birds. A similar trans-IOB dispersal pattern
connecting southeast Asia and Australia with Madagascar
and Africa has been proposed to explain distributions in
bees (Fuller et al., 2005), lizards (Rocha et al., 2006) and
other lineages (Morley, 2003; Sanmartı́n & Ronquist,
2004; Trénel et al., 2007).
Elsewhere in the IOB, the Lemurian stepping-stones,
which connect India and Sri Lanka to Madagascar via the
Seychelles, are considered a likely IOB dispersal channel
for animals and plants (Yuan et al., 2005), and there is
clear phylogenetic evidence that a variety of lineages
have utilized them to some extent (e.g. Raxworthy et al.,
2002; Warren et al., 2003, 2005; Rocha et al., 2006).
However, the large number of avian (and other)
lineages distributed around the IOB suggests that vicariant events post-dating Gondwanan breakup might better
explain many of those distributions. The few phylogenybased studies that have dealt with this possibility in
songbirds (e.g. Voelker, 1999, 2002; Outlaw et al., 2007)
have implicated climate change and commensurate
habitat alterations as primary vicariant events driving
lineage divergence between continents surrounding the
IOB. In each case, biogeographic reconstructions and
molecular clock data supported continent-based movement in response to major paleoecological shifts. Phylogenetic support for the alternative biogeographic scenario
of dispersal could have been invoked if species with
geographically disjunct IOB distributions (e.g. southern
Africa and Southeast Asia) were shown to be sisters.
Dispersal could also have been invoked if clock dates
indicated that land-based movements occurred when
intervening habitats between distributional areas were
ecologically unsuitable for the group (i.e. requiring an
inference of dispersal over those habitats). Evidence of
either dispersal scenario was lacking in those previous
studies.
In this paper, we use a molecular phylogeny of a
songbird genus in conjunction with ancestral area reconstruction methods and molecular clock and paleoecological data to empirically test vicariance vs. dispersal
hypotheses with respect to circum-IOB distributions.
Our focal genus is currently recognized as a constituent
of Zoothera thrushes and has a distributional presence
around the margins of the IOB (Fig. 1). Zoothera is a
member of the avian family Turdidae, which has a
cosmopolitan distribution (Collar, 2005), thereby indicating a tendency for inter-continental movements that is
reflected in both inter- and intra-generic biogeographic
patterns. Many species within several Turdidae genera
(particularly Myadestes and Turdus) have proven very
successful in achieving over-water dispersal to islands and
across the Atlantic (Collar, 2005; G. Voelker, S. Rohwer,
D.C. Outlaw & R.C.K. Bowie, unpublished data), and
Zoothera has clearly dispersed to Southeast Asian islands
(see below). Therefore, while many songbird lineages are
geographically restricted to single continents and as such
are unlikely to cross ocean barriers, members of Turdidae
appear far more likely to disperse across such barriers.
Furthermore, Zoothera thrushes and their close relatives are too young to have experienced initial Gondwanaland rifting (Klicka et al., 2005; and below),
phylogenetic relationships directly linking species in
Africa with those in India, Sri Lanka or the islands of
Southeast Asia would strongly support trans-IOB dispersal events (e.g. Raxworthy et al., 2002; Fuchs et al.,
2006). This is true even if the modern-day absence of
Zoothera on major IOB islands is interpreted as an
indication that IOB islands were never colonized by this
lineage. However, the absence of distributions could be a
function of extinction. While we are unaware of fossil
evidence of Zoothera species from IOB islands, it is clear
that larger songbirds can quickly go extinct after human
colonization (Steadman, 2006). Regardless, if Zoothera
historically utilized or dispersed over IOB islands such
that they established distributions on multiple continents, evidence of this should still be reflected in the
phylogeny and dispersal could again be supported.
Specifically, this historical utilization would directly link
species in Africa with those in India or the islands of
Southeast Asia.
Narrow ranges of species divergences, as reflected by
very short internode distances, can also be indicative of
dispersal events. In such instances, barring repeated longterm migration of genes, colonists (dispersers) to new
areas will rapidly differentiate from source populations
given their reduced genetic variability (Clegg et al.,
2002). Such a pattern would not generally be expected
in response to vicariant events, which typically affect
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Fig. 1 Generalized distribution of focal species around the Indian Ocean Basin. Stippled areas show broad multi-species distributions.
Black arrows indicate vicariant movements; grey areas indicate dispersal events. The head of each grey arrow, and of all black arrows in
the Southeast Asian Islands, indicates an island that is occupied by at least one focal species. The Lemurian Stepping-stone and African–
Australian interchange over-water dispersal routes have been used to explain trans-Indian Ocean Basin distribution patterns in a variety of
lineages (see text).
population divergences over longer evolutionary periods,
thus resulting in longer internode distances.
Alternatively, the absence of Zoothera species on IOB
islands could suggest that continental vicariant events are
equally plausible alternatives that might better explain
circum-IOB distributions. In this instance, we would
expect that phylogenetic relationships would show a
pattern of movement between adjacent areas of Africa
and Asia indicative of range expansion (biotic dispersion)
rather than dispersal between distant areas (e.g. Voelker,
1999, 2002; Outlaw et al., 2007). Using molecular clock
data and ancestral area reconstruction methods, we
examined the roles that vicariance and dispersal have
played in the development of Zoothera distributions
around the IOB.
Materials and methods
Taxon sampling and molecular methods
We sampled 40 taxa comprising 29 species of Eurasian
and African Zoothera, based on previously published
taxonomy (Sibley & Monroe, 1990). These taxa formed
two distinct clades (see below), with 18 taxa forming a
clade (the sibirica clade) that is distributed around the
IOB (Table S1; Collar, 2005). We focus on this clade here.
In general, we did not use multiple samples from species,
as detecting genetic breaks within species was not the
focus of the study. The major exception is citrina, which
has a broad distribution, several major allopatric populations and significant morphological diversity across
those populations (Collar, 2005). We therefore sampled
from major citrina distributions to test for monophyly
(Table S1). We extracted whole genomic DNA from each
sample using DNeasy (Qiagen, Valencia, CA, USA) based
on the manufacturer’s protocols for tissue and blood.
The NADH subunit 2 (ND2) and cytochrome b (cyt b)
mitochondrial genes were isolated and amplified using
standard PCR protocols. Gene amplification and sequencing were performed using primers designed for other
thrushes (Voelker & Spellman, 2004; Outlaw et al., 2007)
and the following thermocycling parameters were used:
an initial 2-min denaturation at 94 C followed by 35–40
cycles of: 94 C for 45 s (denature), 50–54 C for 45 s
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(anneal) and 72 C for 2 min (extension). A final
extension of 72 C for 10 min and a 4 C soak were
used to insure reaction termination. Products were
purified using the Qiaquick PCR purification kit (Qiagen)
based on the manufacturer’s protocols.
We performed 20-lL cycle-sequencing reactions on
purified PCR products using BigDye dye-labelled terminators (ABI, Foster City, California, USA) according to
standard protocols. Reactions were purified and target
DNA precipitated with Isopropanol. Cycle-sequencing
reactions were conducted on an ABI377-automated
sequencer using acrylamide gels. Each sample was
sequenced for light and heavy strands.
All sequence data (1041 bp ND2 and 998 bp cyt b)
were aligned using Sequencher v. 4.5 (Gene Codes, Ann
Arbor, MI, USA) and by eye. For toepad samples, no
fewer than two separate DNA extractions and sequencing
reactions were performed, at intervals of up to several
months apart. Repeated toepad extractions yielded identical sequences. Relevant sequences (Table S1) are
deposited in GenBank under the following accession
numbers: EU874398-EU874429.
Phylogenetic analysis
Several initial analyses were conducted on the combined
ND2 and cyt b dataset. Zoothera has previously been
suggested to be a polyphyletic genus based on limited
sampling (Klicka et al., 2005). Therefore, our first analysis
determined to which clade each species belonged. We did
this by including previously published sequence data
(Klicka et al., 2005; Voelker et al., 2007) from most other
Turdidae genera in a maximum likelihood (ML) search.
M O D E L T E S T 3.04 (Posada & Crandall, 1998) was used to
select the most appropriate model of sequence evolution.
Hierarchical likelihood ratio tests (LRTs) and the Akaike
Information Criterion identified GTR + I + G as the best
fit model for our data. P A U P * (Swofford, 2000) was used
for all ML searches.
An initial ML search was started from a HKY-85
neighbour-joining topology using M O D E L T E S T parameters. After 5000 rearrangements without a change in
likelihood score, parameters were re-estimated on the
resulting topology, and a subsequent search was initiated
using this topology and the re-estimated parameters. This
process was repeated a second time, running 10 000
rearrangements without a change in likelihood score or
parameters.
Bayesian inference was implemented using M R B A Y E S
3.0 (Huelsenbeck & Ronquist, 2001) to assess nodal
support. We used the GTR + I + G model of sequence
evolution, and each gene was allowed to vary in parameter
estimates. Three Bayesian analyses were initiated from
random starting trees, with four MCMC chains running for
two million generations and sampled every 100 generations, yielding 20 000 trees. The first 5000 trees from each
analysis were discarded to ensure chain stationarity.
Remaining trees were combined yielding a total of
45 000 topologies from which a 50% majority rule
consensus tree was reconstructed. Nodes having posterior
probability values of 95% or greater were deemed significantly supported. We further assessed node support using
ML bootstrap analysis in T R E E F I N D E R (Jobb, 2005), using
the GTR + I + G model with 500 pseudoreplicates.
Subsequent analyses focused on the ‘sibirica’ clade (see
below); sibirica was identified in the above analyses as the
basal (albeit distantly related) member of the focal clade,
and it was used as an outgroup. This clade is distributed
around the perimeter of the IOB (Fig. 1). In assessing
relationships within this clade, we again used the
GTR + I + G for ML searches, based on new M O D E L T E S T
(Posada & Crandall, 1998) results. All ML and support
analyses for this clade followed the protocols described
above.
Molecular clock
In applying a molecular clock, many avian studies utilize a
2% sequence divergence per million year value, around
which most calibrations for cyt b cluster (Garcı́a-Moreno,
2004; Ho et al., 2005). Despite this, studies (Arbogast &
Slowinski, 1998; Garcı́a-Moreno, 2004) have questioned
the validity of this rate even when applied to lineages
related to those initially calibrated (songbirds). An additional problem is that most songbird lineages, including
Zoothera, do not have a deep fossil record to aid in applying
temporal calibration points to phylogenies. In the absence
of fossils, Barker et al. (2004) applied a calibration date
from a geological event to the basal passeriform divergence, with the assumption that one divergent lineage
was present on New Zealand during its rift from Antarctica. This method eliminates some of the issues surrounding the application of a DNA-based molecular clock.
We employed this concept, relying on the historical
ecology of the equatorial tropical forest of Africa, which
reached its maximum eastward extent (to the Kenyan
coast) about 3 Mya (Hamilton & Taylor, 1991; Feakins
et al., 2005; Sepulchre et al., 2006). Subsequent forest
retraction to the west from 3 Mya was rapid, as indicated
by the loss of east African equatorial high forest mammalian fauna from the fossil record 2.95–2.52 Mya
(Wesselman, 1995). This would suggest that the establishment of east African montane refugia to the south
was also rapid. We therefore used 3 My to date the
divergence between gurneyi and its sister clade (see
below), all of which occupy montane areas around the
East African Rift system (Collar, 2005). This assumes
niche conservatism of species through time. Calibrating
this same node using a standard rate applied to songbirds
(2% divergence per My; Garcı́a-Moreno, 2004; Ho et al.,
2005) provides a congruent date of 3.2 My.
Divergence times were estimated by incorporating the
calibration date into a nonparametric rate-smoothing
analysis (Sanderson, 2002) using likelihood branch
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lengths estimated from our cyt b dataset. The Langley–
Fitch method was applied under a truncated Newton
algorithm for this analysis.
Ancestral area reconstruction
For biogeographic analysis, we used both dispersal–
vicariance analysis (DIVA; Ronquist, 1997) and weighted
ancestral area analysis (WAAA; Hausdorf, 1998). Our
focus was to determine the most likely ancestral area(s)
for the sibirica clade and to infer movement patterns
between major areas. Movements at finer scales are more
readily interpreted from distributions mapped on the
phylogeny. In both analyses, we coded each species as
present or absent in each of four major areas: Asia,
India + Sri Lanka (India), Africa and Southeast Asian
Islands (Islands). To minimize the number of areas
recovered as potentially ancestral, we set the maximum
areas allowed at any node to two (the lowest possible
setting) in DIVA, and the minimum Probability Index
threshold in WAAA to 0.2.
Results
Phylogenetic analyses and taxonomic considerations
Klicka et al. (2005) have suggested that Zoothera comprises up to three distinct lineages. Our results, which
incorporated additional species sampling, confirm
Zoothera polyphyly, with all species sampled falling into
two distantly related (nonsister) clades (not shown). ML
analyses identified 18 species as belonging unambiguously to a derived clade of Afro-Asian ‘Zoothera’, and we
focus on this clade here.
Initial ML analyses identified sibirica as the basal extant
taxon in the focal clade, with wardii being the next to
diverge (not shown). Subsequent analysis with sibirica as
an outgroup confirms the position of wardii (Fig. 2).
Bayesian analysis indicates posterior probabilities of 1.0
for the position of these taxa relative to the remaining
species, and ML bootstrap support is similarly high
(Fig. 2).
Results of ML analyses indicate that the next divergence
resulted in two distinct clades to which all remaining focal
‘Zoothera’ belong (Fig. 2). The first of these clades (cameronensis–gurneyi) comprises the African spot-winged
thrushes, all of which have distributions that include the
East African Rift system. Our results confirm a prediction
from morphology (Klicka et al., 2005) that crossleyi and
oberlaenderi are members of this clade (Fig. 2). The phylogenetic placement of oberlaenderi suggests that it is best
recognized as a distinct species; it has previously been
recognized as a race of both piaggiae and gurneyi. The ML
topology further indicates that crossleyi is not a race of
gurneyi, where it has been placed in the past despite
substantial plumage differences (Collar, 2005).
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The second major clade (guttata–cinerea) is comprised of
a plumage-diverse assemblage of species that are distributed around the IOB (Figs 1 and 2). Although nodal
support for the placement of guttata and spiloptera is
lacking (Fig. 2), all ML analyses placed them at the base
of this clade. These species are clearly not part of the
African spot-winged thrush clade or of the clade to which
they are basal (the citrina clade); both of these clades are
well-supported (Fig. 2).
‘Zoothera’ citrina diverged early from a common ancestor with other Southeast Asian species (Fig. 2). The
cinerea clade is sister to citrina and comprises at least six
species, all of which occur primarily on Southeast Asian
Islands (Figs 1 and 2). Although support is lacking for
three nodes in this clade, molecular clock dates (and
distributions; see below) suggest rapid, and thus difficult
to support, divergences.
Our analyses concur with the previous suggestion
(Klicka et al., 2005) that Zoothera is polyphyletic, and the
type (Zoothera monticola) falls in an assemblage of
Austral-Asian species that is not sister to our focal clade
(see Klicka et al., 2005; Voelker & Klicka, 2008).
Following taxonomic priority for Zoothera (see Mayr &
Paynter, 1964), the next available genus name is
Geokichla. The type, by original designation, is Turdus
citrinus, which is included in our focal clade (Geokichla
citrina; Müller, 1835, in Mayr & Paynter, 1964). We
therefore recognize Geokichla as the valid taxonomic
designation for all members of the sibirica clade, and
apply it below.
Biogeography
Both methods of ancestral area reconstruction identify
Asia as the most likely area for the origin of Geokichla
(Fig. 2, Table S2). Geokichla sibirica and wardii are distributed in Asia and both are inferred to have arisen in the
late Miocene (Fig. 2). The sister clade to Geokichla
comprises the genera Psophocichla (monotypic) and
Turdus (65 species) (Voelker et al., 2007). While the
former is distributed in Africa, the ancestral area for
Turdus is clearly Asia, and several purely Eurasian species
are the basal members of this genus (Voelker et al., 2007).
Therefore Asia would remain the most likely ancestral
area for Geokichla in a broader multi-genus analysis.
Despite arising approximately 8.5 Mya, just two
speciation events appear to have occurred in Asia over
the next 4.5 My (Fig. 2). From 4–3.4 Mya, lineage
diversification increased, following the colonization of
Africa (Figs 1 and 2). Most African species form a single
clade, the spot-winged thrushes, and their diversity is
centred around the East African Rift system (Collar,
2005). As all have distributions including the Rift system,
this is the most likely ancestral area for this clade.
Additional sampling of races and isolated populations
in the Rift system is necessary to resolve taxonomic
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cameronenensis
2.49
Africa
crossleyi
3.58 2.49
2.57
3.0
Africa
princei
Africa
piaggiae
2.12
Africa
Africa
tanganjicae
gurneyi
Africa
Philippines
cinerea
interpres
1.74
2.46 1.78
4.14
1.98
3.37
3.87
2.74
AFRICA
ISLANDS
Sulawesi
citrina Borneo
Borneo
citrina China
1.07
ISLANDS
Lesser Sundas(E)
Tanimbar
schistacea
4.07
8.42
Lesser Sundas(W)
erythronota
1.60
5.45
Sundas, Borneo,Asia
dohertyi
peronii
2.09
AFRICA
Africa
oberlaenderi
Asia
citrina Ghats
citrina Nepal
ASIA
Asia
Sri Lanka
spiloptera
guttata
wardii
INDIA
INDIA
India
AFRICA
ASIA
Africa
Asia, India
Asia
sibirica
0.05
Fig. 2 Left: maximum likelihood phylogeny of Geokichla species. Where no major genetic or biogeographical differences exist, species
represented by multiple samples were collapsed to single exemplars. Circles at nodes indicate support values, with Bayesian posterior
probabilities in the top hemisphere (‡ 95% in black, 85–94% in grey), and maximum likelihood bootstrap support in the lower hemisphere
(‡ 90% in black, 75–89% in grey, otherwise white). Numbers at nodes are lineage divergences estimates, in millions of years. Centre:
distributional area for each species. Right: ancestral area reconstructions based on dispersal–vicariance analysis and weighted ancestral area
analysis.
affinities and biogeographic reconstructions of the spotwinged thrushes.
Although guttata is distributed in Africa, it is clearly
sister to an Asian clade, and not to the African spotwinged thrushes (Fig. 2). Thus, we infer from ancestral
area analysis a recolonization of Asia, via India (Figs 1
and 2; Table S2), which accounts for the presence of
spiloptera on Sri Lanka, and citrina throughout much of
Southeast Asia. Two movements to Southeast Asian
Islands follow. One of these movements can explain the
distribution of citrina aurata on Borneo, while a second
movement would explain the distribution of the cinerea
clade throughout Southeast Asian Islands (Fig. 2).
Within the cinerea clade, most species distributions
reflect a high degree of island endemism (or nearly so if
small satellite islands are considered; Figs 1 and 2). Only
interpres has a broad distribution, which includes overlap
on Borneo with citrina, and a recolonization of mainland
Asia (Figs 1 and 2). Distribution across, and speciation in,
the Southeast Asian Islands occurred rapidly. Molecular
clock dates suggest that initial diversification in this
lineage occurred in the late Pliocene, with a pulse of
speciation occurring from 2.09–1.74 Mya (Fig. 2) near
the Plio–Pleistocene boundary. Distributions in this clade
suggest a stepping-stone pattern of colonizations through
Southeast Asian Islands (Figs 1 and 2). Five islands must
have been colonized via dispersal, as they fall east of the
Sunda Shelf (Fig. 1) and therefore have no historical
interconnection between them or the mainland. Rapid
dispersal across islands, with subsequent loss of gene
flow, would account for rapid divergences evident in the
phylogeny (Clegg et al., 2002).
Discussion
Which process, dispersal or vicariance, explains more of
the variance in Geokichla distribution? Recalling the ability
of Turdidae (and other) lineages to disperse over water
barriers, and more specifically the distribution of some
Geokichla species on oceanic islands (Fig. 2), it is impracticable to a priori hypothesize an inability to disperse
across the IOB. Indeed, we note that barring any correlation between divergence dates, paleoecology and habitat adaptation, the structure of the phylogeny (Fig. 2, left)
would clearly support a dispersal event between southeastern Africa (guttata) and Sri Lanka (spiloptera).
Despite phylogenetic structure, the most parsimonious
explanation for African–Asian interchange in Geokichla is
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vicariance. The colonization of Africa is dated at 4.1 Mya,
and recolonization of Asia occurred almost simultaneously (Fig. 2). From 5–3 Mya, African tropical forests
extended to coastal Kenya and through Ethiopia (Hamilton & Taylor, 1991; Cane & Molnar, 2001; Feakins et al.,
2005; Sepulchre et al., 2006). Divergence dates suggest
that ancestral movements between Asia and Africa
occurred during this period, when forest connectivity
was high. Virtually all Geokichla are (now) forest adapted,
making intercontinental movements during periods of
forest expansion a likely event. Similar ‘suitable paleoecology’ arguments have, when temporally associated
with lineage divergences, been used to explain African–
Asian interchange in lizards (Amer & Kumazawa, 2005),
and nonforest-adapted birds (Voelker, 1999, 2002) and
mammals (Vrba, 1985, 1993).
Following intercontinental movements by Geokichla,
African tropical forests began to rapidly retract westward
between 3–2.5 Mya (Hamilton & Taylor, 1991; Feakins
et al., 2005; Sepulchre et al., 2006). This retraction served
as a driving vicariant event that eliminated Asian–African
forest connectivity, and montane forest connectivity in
Eastern Africa. The resulting retraction greatly impacted
small mammal distributions (Wesselman, 1995), and
vicariance-driven speciation in forest refugia would
explain the major radiation of African thrushes, in which
most speciation events occurred after 3.0 Mya. This
pattern of lineage diversification via forest fragmentation
has been proposed for other thrushes, which, like most
African Geokichla, are isolated in montane forest refugia
around the African Rift system (Bowie et al., 2005).
Although a vicariant explanation is plausible to explain
divergence between Asian and African lineages, the
ranges of guttata (southeast coast of Africa), spiloptera (Sri
Lanka) and the cinerea clade (southeast Asian islands)
require exploring the possibility of dispersal across the
IOB. Avian lineages have clearly used the Lemurian
stepping-stones to colonize IOB islands from both India
and Africa (Warren et al., 2003, 2005), and lineages far
less mobile than birds, such as chameleons, have
dispersed from Madagascar to India (Raxworthy et al.,
2002). The trans-IOB distributions of bees (Fuller et al.,
2005), Cryptoblepharus lizards (Rocha et al., 2006) and
plants (Morley, 2003; Sanmartı́n & Ronquist, 2004;
Trénel et al., 2007) have been explained by dispersal,
often times with molecular clock support for that
conclusion, rather than by land-based vicariant explanations.
Although there is clear evidence that diverse lineages
have dispersed across the IOB, there is no evidence to
support trans-IOB dispersal by Geokichla from Africa to
either southern Asia or Southeast Asian Islands. No
Geokichla species are distributed on Madagascar or other
potential Africa-to-Asia stepping-stone islands; phylogenetic evidence suggests no relationships that might
have required utilization of these islands. Further, evidence is lacking that submerged plateaus and seamount
1785
formations formed aerial land-masses (Fuchs et al., 2006;
Jønnson & Fjeldså, 2006) at temporal intervals consistent
with Geokichla evolution. Finally, the lineage divergence
dates inferred in connection with these potential plateaufacilitated dispersals are far older (ca. 45 Mya) than those
we consider here (Fuchs et al., 2006; Jønnson & Fjeldså,
2006). We therefore conclude that trans-IOB dispersal
by Geokichla is unlikely to have taken place, and that
vicariant mechanisms better explain IOB perimeter
distributions in Africa and continental Asia.
Dispersal can, however, explain Geokichla distributions
on islands located on the IOB perimeter. Geokichla
spiloptera, endemic to Sri Lanka, diverged from its sister
clade of derived Asian Geokichla in the early Pliocene.
During this period, it appears that northern Sri Lanka had
subsided below sea level, isolating southern Sri Lanka
from India (Jacob, 1949). Dispersal may therefore
account for the distribution of spiloptera.
Dispersal is inferred to explain the distributions of
Geokichla species on the northern Philippines, Sulawesi,
Tanimbar and the Lesser Sunda Islands. These islands are
not part of the Sunda Shelf system, which precludes the
possibility of historical movements across the exposed
shelf during periods of low sea level. Most Southeast
Asian Islands have been in their current geographical
position for 10 My (Hall, 1998), which, when considered
with molecular clock dates, eliminates the possibility of
Geokichla distributions resulting from tectonic rifting. The
distribution of interpres on Sunda Shelf islands and
mainland Asia (Figs 1 and 2), and a race of citrina on
Borneo, is likely due to vicariant isolation following
movement onto the islands during periods of low sea
level. Short-range dispersal is necessary to account for
the interpres–dohertyi sister relationship; dohertyi is distributed east of the Sunda Shelf. A similar pattern of
dispersal across nonshelf islands, followed by recolonization of the mainland or Sunda Shelf islands, has also
been documented in the avian genus Ficedula (Outlaw &
Voelker, 2008). The question of why Geokichla skipped
over the Sunda Shelf islands early in its biogeographic
history remains. Given that Geokichla subsequently and
rapidly established distributions on Sunda Shelf islands,
extinction of ancestral Sunda Shelf lineages seems
unlikely.
The narrow range of divergence dates (ca. 0.75 My)
across the cinerea clade suggests rapid island colonizations. The initial divergence of this clade from its sister
(citrina) is coincident with the closing of the Indonesian
seaway 3–4 Mya (Cane & Molnar, 2001); associated
regional climate and habitat changes might explain rapid
colonization of islands. These alterations positively
impacted the ability of vertebrates to expand from Asia
onto Sunda Shelf islands and beyond (Tedford, 1985;
Voelker, 1999; Gorog et al., 2004). Divergence dates
between members of the cinerea clade also imply rapid
speciation, which is expected unless continued dispersal
from source areas maintains gene flow (Clegg et al.,
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JOURNAL COMPILATION ª 2008 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
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G. VOELKER AND R. K. OUTLAW
2002). Species relationships within the clade suggest that
distributions were achieved by a series of stepping-stone
movements, beginning with colonization of the Philippines, and ending with colonization of islands on the
eastern perimeter of the IOB (Figs 1 and 2). Relationships
and distributions within the citrina clade indicate a
complex pattern of mainland–Sunda Shelf–nonshelf
island dispersals similarly reflected in other lineages
(Evans et al., 2003; Filardi & Moyle, 2005).
It is evident that vicariance and dispersal have both
operated in generating Geokichla distributions around the
perimeter of the IOB, and that they have done so at
different temporal and geographical scales. Vicariance via
ecological discontinuity is evident early in Geokichla
evolution, and involved African–Asian interchange and
subsequent divergence. This interchange is similar to
historical geographic patterns found in similarly distributed songbird lineages (Voelker, 1999, 2002), yet temporally dissimilar from those lineages due to differing
ecological associations. Similar temporal ecological associations, driven by repeated climatic shifts (Hamilton &
Taylor, 1991; Feakins et al., 2005; Sepulchre et al., 2006),
have also proven important to the establishment of interand intra-continental distributions in other vertebrate
lineages (Vrba, 1985, 1993; Wesselman, 1995; Amer &
Kumazawa, 2005).
Such ecological associations allow a general temporal
prediction for African–Asian interchange of lineages:
forest-adapted species (e.g. sunbirds; R.C.K. Bowie,
unpublished data) and thrushes (this study) should
colonize during periods of forest expansion (5–3 My),
whereas nonforest-adapted species (e.g. pipits, Voelker,
1999; wagtails, Voelker, 2002; rock-thrushes, Outlaw
et al., 2007) should colonize during periods of forest
retraction. Further, forest-adapted lineages should experience increased cladogenesis during periods of forest
retraction, and arid species should do the same during
periods of forest expansion. Thus far, these predictions
seem to hold for songbird lineages and fossil mammal
lineages; analyses of other lineages are clearly necessary
to test whether this prediction applies more broadly
across other vertebrate lineages. Another potential vicariant signature is evident late in Geokichla evolution as
well, but is limited to a few movements presumably
linked to low sea levels across the Sunda Shelf.
By comparison, dispersal has played a predominant
role in establishing distributions at the northern and
eastern margin of the IOB, and through the islands of
Wallacea. The possibility of derived Asian lineages having
stemmed from a single trans-IOB dispersal, or via
stepping-stone movements across the IOB for Geokichla,
seems unlikely. Yet, it is clear from studies of a variety
of lineages (Raxworthy et al., 2002; Morley, 2003;
Warren et al., 2003, 2005; Sanmartı́n & Ronquist, 2004;
Fuller et al., 2005; Yuan et al., 2005; Rocha et al., 2006;
Trénel et al., 2007) that such dispersal events cannot be
discounted out of hand. Despite evidence of IOB dispersal
patterns, we suggest that, barring extant or fossil taxa on
IOB islands or future evidence of seamount exposure that
is temporally relevant, vicariant speciation related to
continental paleoecological shifts should be considered
the null hypothesis for any nonseagoing lineage distributed around the perimeter of the IOB.
Acknowledgments
We thank the Curators and staff of those museums that
provided us with samples. We thank E. Dickinson and
S. Gregory for clarifying the taxonomic vagaries surrounding Geokichla vs. Geocichla. Two anonymous referees
made constructive comments. This work was supported in
part by NSF DEB-0613668 to GV and R. C. K. Bowie.
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Table S1 Specimens used, sample sources and locality
information for species in the sibirica clade.
Table S2 Results of weighted ancestral-area analysis.
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