SPECIALPAPER

Determining biogeographical patterns ofdispersal and diversification in oscinepasserine birds in Australia, SoutheastAsia and Africa

Knud A. Jønsson* and Jon Fjeldsa

INTRODUCTION

Passerine birds (order Passeriformes) comprise 5739 species or

59% of the total number of birds, making it the largest avian

order (Monroe & Sibley, 1993). Within this order the oscine

passerine birds (suborder Passeri) constitute the main clade,

with 80% of all passerines, or 47% of all bird species on earth.

This group is monophyletic judging from syringeal anatomy

(Muller, 1847, 1878; Ames, 1971) and other morphological

evidence (e.g. Raikow, 1982), and from molecular data (Sibley

& Ahlquist, 1990; Barker et al., 2004; Beresford et al., 2005). It

is also highly heterogeneous, and several subdivisions have

been proposed over the years (for review see Sibley & Ahlquist,

1990). Sibley & Ahlquist (1990) based their study on

Vertebrate Department, Zoological Museum,

University of Copenhagen, Copenhagen Ø,

Denmark

*Correspondence: Knud Jønsson, Vertebrate

Department, Zoological Museum, University of

Copenhagen, Universitetsparken 15, DK-2100

Copenhagen Ø, Denmark.

E-mail: kajonsson@snm.ku.dk

ABSTRACT

Aim Several independent studies suggest that oscine passerine birds originated in

Eastern Gondwana/Australia and from there spread to Southeast Asia and then to

Africa. A recently constructed supertree including 1724 oscine taxa forms the

basis for this study, in which we present a more detailed hypothesis of this out-of-

Australia scenario.

Location Australia, Africa, Southeast Asia, western Pacific, Indian Ocean.

Methods We used the computer program DIVA to identify putative ancestral

areas for each node. We also applied a molecular clock calibrated with three

recently conducted studies of passerines to estimate the ages of basal nodes.

Although these time estimates are rough they give some indication that, together

with the putative ancestral areas, they can be compared with known events of

plate tectonic movements in the Australian, Southeast Asian and western Pacific

regions.

Results The DIVA analysis shows that Basal Corvida and Crown Corvida

originated in Australia. Ancestral nodes for Picathartes/Chaetops and Passerida

originated in Africa, and the basal nodes of Sylvioidea also originated in Africa.

For Muscicapoidea and Passeroidea we were unable to establish ancestral

patterns. The molecular clock showed that Crown Corvida radiated between 20

and 30 Ma whereas Basal Corvida and the Passerida clade radiated from c. 45 to

50 Ma.

Main conclusions Both approaches agree that: (1) Crown Corvida spread from

Australia to Southeast Asia, with several dispersal events around the time when

the terranes of Australian and Indomalayan origin came close together some

15 Ma, and (2) a single dispersal event went from Australia across the Indian

Ocean to Africa c. 45–50 Ma, leading to the very large radiation of the parvorder

Passerida. The latter hypothesis is novel, and contrary to the general view that

oscines spread exclusively via Southeast Asia.

Keywords

Africa, Asia, Australia, biogeography, dispersal events, Gondwana, molecular

clock, oscines, Passeriformes.

Journal of Biogeography (J. Biogeogr.) (2006) 33, 1155–1165

ª 2006 The Authors www.blackwellpublishing.com/jbi 1155Journal compilation ª 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2006.01507.x

DNA–DNA hybridization and proposed two main parvorders,

Corvida and Passerida, with a third parvorder Incertae sedis

comprising four species of two African genera, Picathartes and

Chaetops. Further investigations have proven Corvida to be

paraphyletic, whereas Passerida appears to be monophyletic

(Ericson et al., 2000, 2002b; Barker et al., 2004).

The basal lineages of Corvida are endemic to the Australo-

Papuan region, which suggests that oscines originated in

eastern Gondwana/Australia and spread from there to other

continents via the Indo-Malayan Archipelago (Christidis, 1991;

Barker et al., 2002; Edwards & Boles, 2002; Ericson et al.,

2002a). Only a few of the Corvida lineages escaped from the

Australian region, but Passerida very successfully diversified

and spread throughout the world. The position of the

Australian Petroicidae is controversial, as Barker et al. (2004)

and Beresford et al. (2005) place it above the Picathartes–

Chaetops branch with the Passerida. Ericson et al. (2002b)

discovered an insertion in the c-myc gene common to all

Passerida and Picathartes and Chaetops, but not to Petroicidae.

Therefore, they argued that Petroicidae is basal to Passerida

and Picathartes/Chaetops, which is now also supported by

Fuchs et al. (2006).

Based on a recently developed oscine supertree (Jønsson &

Fjeldsa, 2006) we aimed to make a renewed biogeographical

analysis. In conjunction with detailed reconstructions of the

plate tectonics of south-eastern Asia, the western Pacific and

the Indian Ocean (McCall, 1997; Hall, 1998; Holloway, 1998;

Moss & Wilson, 1998; Marks & Tikku, 2001; Briggs, 2003), we

present a more detailed picture of how oscine passerine birds

dispersed from Australia to the rest of the world.

METHODS

We applied two approaches to assess the dispersal of oscines

from Australia to the other continents. Firstly, we used the

computer program DIVA to identify putative ancestral areas for

each node; secondly, we applied a molecular clock model.

Although controversial, this may give some rough indications of

the time of dispersal from Australia that can be compared with

time estimates for continent movements. These two methods

complement each other well and help to obtain a more refined

model for the sequence of biogeographical events.

DIVA

Analysis using DIVA (dispersal–vicariance analysis) ver. 1.1

(Ronquist, 1996) was undertaken to elucidate the relative

influence of different processes in shaping the biogeographical

history of oscine passerine birds. DIVA is a simple program for

reconstructing ancestral distributions based on a phylogeny

and using dispersal–vicariance analysis, a method in which

ancestral distributions are inferred based on a three-dimen-

sional cost matrix derived from a simple biogeographical

model (Ronquist, 1996). In contrast to other methods used in

historical biogeography, DIVA does not assume anything

about the shape or existence of general biogeographical

patterns. Therefore DIVA is particularly useful in reconstruct-

ing the distributional history of a group of organisms in the

absence of a general hypothesis of area relationships. The

method remains applicable even when area relationships are

expected to be reticulate rather than hierarchical.

Our supertree was constructed manually without the aid of

matrices or computer programs. Firstly, a strict consensus

supertree was created for all 1724 taxa in accordance with the

general direct supertree construction (Sanderson et al., 1998).

Subsequently we evaluated each source tree in order to

strengthen the resolution, thereby assigning individual weight

to each tree. The source trees were evaluated according to the

number of base pairs used to construct the source phylogenies,

analytical methods favouring maximum likelihood (ML) trees

over Bayesian trees over maximum parsimony (MP) trees and

favouring branches in source trees with high bootstrap support

or posterior probabilities, unique insertions and choice of

outgroup.

We use the supertree constructed by Jønsson & Fjeldsa (2006),

based on 1724 oscine species, as a guideline for choosing the taxa

of interest for the analysis. DIVA allows only a limited amount of

taxa to be included in an analysis, so we picked 127 taxa

representing all clades. As we are particularly interested in the

nodes where Passerida split from Corvida, we selected relatively

more taxa from the basal branches of Passeroidea, Muscicapo-

idea and Sylvioidea, and only a few taxa from the distal branches.

DIVA is rather sensitive to the misplacement of taxa, therefore,

we removed troublesome taxa to enhance the distribution

pattern basally. As DIVA works only with fully bifurcate

phylogenies, we had to assess which taxa were basal to others.

We did this by investigating the source trees and then evaluating

overall which taxa could be basal to others. The polytomies that

had to be evaluated were rather distal and amounted to one for

Muscicapoidea, four for Passeroidea, five for Sylvioidea and four

for Crown Corvida. The polytomies were all resolved easily by

following the overall consensus of source trees, although support

values are weak, which is why they were unresolved in the

supertree. Although all basal taxa are distributed in Australia or

New Guinea, we sampled this part thoroughly to achieve a solid

assessment of basal nodes. The taxa chosen from the full

supertree are presented in Fig. 1.

In total, 15 geographical regions are recognized for consid-

ering the evidence of historical relationships of geological

plates and terranes (Audley-Charles, 1981; Hall, 1998; Moss &

Wilson, 1998): (a) New Zealand, NZ; (b) Australia, AUS; (c)

New Guinea and Moluccas (including the islands east of

Halmahera, Obi, Buru, Timor and Sumba), NG; (d) western

Pacific Islands including the Melanesian Arc, WPI; (e)

Sulawesi, SUL; (f) Lesser Sunda Islands (including Lombok,

Sumbawa, Flores and Wetar), LSI; (g) Philippines, PHI; (h)

Southeast Asia and Greater Sunda Islands (including Bali),

SEA; (i) India and Sri Lanka, IND; (j) Eastern Palearctic, EPA;

(k) Western Palearctic, WPA; (l) subSaharan Africa, AFR; (m)

Indian Ocean Islands, IOI; (n) North America including the

Mexican highlands, NA; (o) South America (including the

Caribbean islands), SA. Since the emphasis is on how the birds

K. Jønsson and J. Fjeldsa

1156 Journal of Biogeography 33, 1155–1165ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

Figure 1 DIVA analysis: 127 taxa were used to identify putative ancestral areas for the basal nodes. Distributions are given in parentheses.

This tree indicates only tree topology, not branch lengths.

Biogeography of oscine passerine birds

Journal of Biogeography 33, 1155–1165 1157ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

dispersed from Australia, the subdivision of areas is most finely

resolved for the Australasian region. We classify areas accord-

ing to the geological origin of landmasses (Fig. 2, based on

Audley-Charles, 1981; Moss & Wilson, 1998). Thus Sumba and

Timor, which are of Gondwanan rather than Eurasian origin,

are included with the Mollucas, although they are presently

part of the Lesser Sunda Islands. Sulawesi, which is a

composite of several terranes, was considered one area because

taxa with Gondwanan affinities are likely to have spread to the

rest of the island, which initially belonged in the Philippine

archipelago, and vice versa. Bali is included with Southeast Asia

as Wallace’s Line is considered to run between Bali and

Lombok. Maxarea values were set to 2–15, delimiting an upper

boundary as to how many ancestral areas are allowed at each

node. The setting maxareas ¼ 2 makes the assumption that no

ancestor is widespread. In contrast, maxareas ¼ 15 allows all

ancestors to be widespread. The latter setting has the effect that

the deeper nodes, especially, will have most or all areas

included as potential ancestral areas. To avoid this, the results

of the DIVA analysis reflect only maxareas ¼ 4. Only areas

that were represented in more than 50% of the output areas in

the DIVA analysis were accepted as putative ancestral areas.

The analysis was carried out several times, exploring the effect

of changing the cost settings (codivergence ¼ 0–5; duplica-

tion ¼ 0–5; sorting ¼ 0–5; switching ¼ 0–5). These changes

had no effect for the ancestral areas of basal branches, and

caused only minor changes in the distal part of Muscicapoidea

and Passeroidea (nodes 26–31). The identification of ancestral

areas therefore appears robust, overall.

Species were chosen from each clade for the DIVA analysis:

first the basal taxon represented in the supertree, then more

distal taxa with another distribution. If the whole clade is

distributed in one area, it was sufficient to choose one taxon to

represent the clade. Taxa very distal from the root of a clade

may reflect secondary expansions, which are generally ignored

in this analysis. This means that if one clade is distributed in

Asia it would suffice to pick one taxon. If, however, a clade

consists basally of taxa distributed in Asia and more distally in

Africa and North America, we would pick one taxon repre-

senting each area. In most cases this would mean any taxon

with a different distribution, although exceptions were made in

very distal parts of clades if they showed clear secondary

distributions. Overall, we consider this a sound way of choosing

taxa, as the taxa picked for the DIVA analysis directly reflect

dispersal patterns of focal clades. As we are mostly interested in

identifying the dispersal patterns for deeper nodes at the border

between Corvida and Passerida, we have chosen a high

proportion of taxa among the basal clades and picked only a

few taxa among more distal clades. We also tried choosing taxa

randomly to see if this would change the outcome of the

analysis. This was the case only for rather distal nodes within

Passerida, and it was therefore assumed that it had little

influence on the overall results of the DIVA analysis. The taxa

used for the molecular clock analysis and the DIVA analysis

differ slightly because we were constrained to use taxa for which

we could readily obtain RAG-1 sequence data in Genbank for

the molecular clock analysis, and these were not always the ideal

taxa for the DIVA analysis. However, the outcome of the DIVA

analysis was not affected by the taxa used and we therefore used

taxa of higher interest in the DIVA analysis.

Estimating divergence time

Several authors have used various methods to estimate

divergence times for oscine passerines. Barker et al. (2004)

used nonparametric rate smoothing (NPRS) and penalized

Figure 2 Geological origin of present-day Southeast Asia, Wallacea and northern Australo-Papuan region. Detailed map showing areas

of Australian/Gondwanan, Laurasian and Melananesian geological origin. Note how land masses and terranes of different origin inter-

mingle in the Lesser Sunda Islands and in Sulawesi. Thin lines mark the continental shelves. The volcanic islands of Bali, Lombok, Sumbawa,

Flores and Wetar (Inner Banda Arc) are of Asian origin, whereas the volcanic islands of Sumba and Timor (Outer Banda Arc) are of

Australian origin. (Redrawn from Smith et al., 1994; Hall, 1998 and bathymetric maps.)

K. Jønsson and J. Fjeldsa

1158 Journal of Biogeography 33, 1155–1165ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

likelihood (Sanderson, 1997, 2002) based on nuclear genes

(RAG-1 and RAG-2). Zuccon (2005) used NPRS based on

nuclear genes (RAG-1 and RAG-2) and mitochondrial genes

(GAPDH, ND2 and Myoglobin). Fuchs et al. (in press) used

NPRS, penalized likelihood and a Bayesian approach based on

mitochondrial genes (ND2 and Myoglobin). We used time

estimates from these three studies as calibration points to

assess the evolution of the nuclear gene RAG-1.

Dating nodes on molecular phylogenies has received much

criticism (e.g. Heads, 2005). In our study the three studies that

form the basis for our time estimates essentially relate to one

palaeogeographical calibration point, the divergence of

Acanthisitta from all other passerines, when New Zealand

rifted from the Antarctica at a minimum of 82 Ma. Ericson

et al. (2002a) and Barker et al. (2004) used this calibration

point to estimate other, more distal divergence times. Fuchs

et al. (in press) used calibration points outside the oscine clade.

These included time estimates from the studies conducted by

Ericson et al. (2002a) and Barker et al. (2004), together with a

time estimate for the divergence of oscines–suboscines esti-

mated by van Tuinen & Hedges (2001), which is essentially

based on one calibration point (a correlation with fossil age for

a reptile–mammal at 310 Ma). Furthermore, Fuchs et al. (in

press) based their calibrations on two calibration points

estimated by Sibley & Ahlquist (1990) based on an ostrich–

rhea vicariance calibration. This calibration, however, is now

considered to be both phylogenetically and temporally incor-

rect (van Tuinen et al., 1998). Zuccon (2005) used data

recalculated from the study conducted by Barker et al. (2004).

These time estimates are subject to considerable error margins,

but may still present some indication of divergence times.

Twenty-one calibration points were used from the above-

mentioned studies (Table 1). The relative sequence divergence

was calculated using 139 RAG-1 sequences: 123 RAG-1

sequences of 930 base pairs (see Fig. 4) in addition to the

following of 2872 base pairs (accession numbers are given

before the taxon name) – AY307187, Cinnyricinclus sharpii;

AY307207, Poeoptera lugubris; AY307182, Aplonis panayensis;

AY307212, Sarcops calvus; AY307181, Ampeliceps coronatus;

AY307193, Gracula religiosa; AY307200, Mino anais;

AY307210, Rhabdornis mysticalis; AY307197, Margarops fusc-

atus; AY307183, Buphagus erythrorhynchus; AY307199, Mela-

notis caerulescens; AY057005, Mimus patagonicus; AY307188,

Copsychus malabaricus; AY056985, Cinclus cinclus; AY056981,

Bombycilla garrulus; AY307180, Acridotheres fuscus. These were

downloaded from Genbank and used to calculate pairwise

distances as implemented in PAUP* 4.0b10 (Swofford, 2001)

(Table 1).

We applied two algorithms to assess the degree of associ-

ation between differences in RAG-1 sequences and time

estimates. One of these assumes a linear relationship; more

realistically, the other assumes saturation of sequence muta-

tions over time. The latter is in agreement with the general

assumption of sequence mutations (Swofford et al., 1996;

Table 1 Calibration data used for time

estimatesSpecies complex comparisons Myr Distance

A 11. Creatophora/Sturnus nigricollis–Sturnus sinensis/cineraceus/Acridotheres 5.9 0.46

A 6. Mino/Gracula/Ampeliceps/Sarcops–Scissirostrum/Aplonis 9.45 1.28

A 10. Sturnus unicolor/vulgaris–other Sturnus/Acridotheres 9.80 0.77

A 9. Lamprotornis corruscus–Sturnus/Acridotheres 13.85 1.46

A 8. Poeoptera/Spreo–Saroglossa/Sturnus 14.95 1.39

B 17. Corvus–Cyanocitta 15.50 0.59

A 5. Rhabdornis–Mino/Gracula/Ampeliceps/Sarcops/Scisirostrum/Aplonis 19.15 2.76

A 4. Rhabdornis/Aplonis–Lamprotornis/Sturnus 20.00 2.63

B 15. Mimus–Sturnus 21.00 3.05

A 3. Sturnini–Mimini 21.95 2.91

B 14. Vireo–Erpornis 26.50 2.26

A 2. Cinclidae/Muscicapidae–Sturnidae 24.30 3.88

B 11. Cracticus/Artamus clade–Batis/Vanga clade 27.50 2.11

A 1. Bombycilla/Regulus–all other Muscicapoidea 29.05 4.60

C Vanga/Batis–Dryoscopus/Telophorus 33.75 1.87

B 13. Sitta/Certhia–Polioptila/Troglodytes 34.00 4.91

C Aegithina/Gymnorhina–Batis clade 35.17 2.06

B 10. Vireo–other Crown Corvida 38.50 2.73

B 9. Petroicidae–Passerida 44.50 4.56

B 8. Picathartes–Passerida 46.00 4.44

B 7. Menura–other oscines 63.50 5.19

Twenty-one calibration points from three different studies were used to calibrate the molecular

clock for nuclear RAG-1 sequence data: 10 calibration points (A) from Zuccon (2005); nine (B)

from Barker et al. (2004); two (C) from Fuchs et al. (in press). RAG-1 sequences were down-

loaded from Genbank and distance analysis was performed under the pairwise distance option as

implemented in PAUP. Numbers refer to numbers given in the respective papers used as cal-

ibration references.

Biogeography of oscine passerine birds

Journal of Biogeography 33, 1155–1165 1159ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

Graur & Li, 2000). These two estimates constitute the basis for

estimating divergence times (Fig. 3).

RAG-1 sequences of 930 base pairs were downloaded from

Genbank for as many taxa in the oscine supertree as possible.

This amounted to sequences for 123 taxa (Fig. 4). The

sequences were aligned manually, which was straightforward,

and it was necessary to insert or delete one or more base pairs

only in a few cases. We applied no further correction to the

sequences used for molecular clock calibrations. Distance

analysis was performed under the pairwise distance option as

implemented in PAUP* 4.0b10 (Swofford, 2001). Two ages are

given in Fig. 4, corresponding to the two approaches for

calculating divergence times. One approach assumes a linear

relationship given by y ¼ 0.0950365x (lower 95%

CI, y ¼ 0.077812381x; upper CI, y ¼ 0.112260598x;

R2 ¼ 0.506254634). Because it is generally assumed that the

number of observed mutations decreases over time, we

estimated a line of best fit based on a nonlinear assumption.

This calculation was performed under the proc NLIN (non-

linear) function as implemented in the statistical program SAS

9.1. The relationship of the nonlinear fit is given by:

S ¼ Smax(1 ) e)at) (Smax ¼ 7.6027, SE ¼ 3.8894; a ¼ 0.0175,

SE ¼ 0.0123; S ¼ percentage sequence divergence, t ¼ time,

R2 ¼ 0.63).

We realize that the analysis is, in a sense, circular and is to be

regarded only as a simple way of obtaining a rough divergence

time estimate for the clades of interest.

RESULTS AND DISCUSSION

DIVA

The result of the DIVA analysis gives some detailed ideas of

ancestral patterns and suggests general patterns of oscine

dispersal. It supports the idea that no Basal Corvida (‘stem

Corvida’ of Barker et al., 2002) left the Australian continental

plate (Fig. 1). For nodes 9–16, however, it is obvious from the

distributions that oscines began spreading to Southeast Asia.

This could have happened via different routes: either they

followed marginal north-western Australian terranes that were

later incorporated into Indonesia; or they could have crossed via

the dynamic Melanesian island arc to the Moluccas (Hall, 1998).

The dispersal was not a one-time occurrence. All nodes 9–16

support an Australian ancestor. This means that, although the

clades contain species distributed in Asia, Africa and the

Americas, the source area was still Australia. In effect, Australia

was pumping corvoid oscines across to Asia, from where some

continued onwards to Africa and even to the Americas. The

ancestral origin of node 11 in the DIVA analysis is not entirely

certain, but biogeographically it makes most sense if the

ancestor was Australian rather than colonizing India/Asia, back

to Australia, and then colonizing Asia a second time.

Nodes 7, 8 and 17 in the DIVA analysis suggest that Passerida

spread from Australia across to Africa and then from Africa

onwards to Asia. This is a novel interpretation of oscine

dispersal, and is contrary to all previous studies (Barker et al.,

2002; Edwards & Boles, 2002; Ericson et al., 2002a). The

supertree that we used represents about 37% of all oscines, and it

is possible that an analysis of a more complete data set would

have given a different result. However, it is noteworthy that

southern Africa has other odd oscine species, such as Hyliota,

which evidently represent very deep members of Passerida along

with Promerops and Modulatrix (Fuchs et al., 2006), although

this is not substantiated sufficiently for inclusion in our analysis.

If the hypothesis of Passerida spreading via Africa is true, it

is easy to explain that nodes 18–24 all have an African or a

Southeast Asian origin, and furthermore that a number of

basal branches of the major Passerida clades, which are widely

distributed in the Northern Hemisphere, are absent from

Wallacea excluding dispersal via Wallacea, e.g. Sittidae,

Troglodytidae, Bombycillidae, Cinclidae and Paridae. After

colonizing Africa, Passerida would have expanded rapidly

through Asia, as suggested by the presence of some deep

branches of widespread and partly nomadic taxa (Bombycilla,

Panurus, Regulus) and some large Oriental radiations. Alter-

natively, some birds could have island-hopped across the

Indian Ocean to India. This phenomenon of retro-migration

has been documented in some cases (Warren et al., 2003;

Fuchs et al. in press). The possibility that an early oscine

dispersal event went via Asia to Africa and later became extinct

in the Asian region cannot be ruled out entirely, but a dispersal

event across the Indian Ocean is more likely and is possible if

we consider the distribution of presently submerged land

masses (see below).

0

1

2

3

4

5

6

7

8

0 20 40 60 80

Time (My)

% S

equ

ence

div

erg

ence

Figure 3 Relationships between sequence divergence and diver-

gence time for RAG-1. Twenty-one calibration points were used to

evaluate the relationship between percentage sequence difference

and age of divergence for oscine passerine birds. The correlation

between time and sequence divergence is shown. Linear regression

(thin black plot), y ¼ 0.0950365x (lower 95% CI,

y ¼ 0.077812381x; upper CI, y ¼ 0.112260598x, dotted lines;

R2 ¼ 0.506254634). Because it is generally assumed that the

number of observed mutations decreases over time, we also cal-

culated a line of best fit, based on this assumption, in the statistical

program sas 9.1. This relationship is given by

S ¼ 7.60(1 ) e)0.0175t) (thick black plot), 95% CI shown as thin

stippled lines. S ¼ percentage sequence divergence; t ¼ time in

Myr; R2 ¼ 0.63.

K. Jønsson and J. Fjeldsa

1160 Journal of Biogeography 33, 1155–1165ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

Figure 4 A total of 123 taxa were used to estimate divergence times based on percentage difference in RAG-1 sequence data. Two time

estimates are given: a linear relationship and, more realistically, one that assumes saturation of sequence mutations over time. Genbank

accession numbers are given in parentheses.

Biogeography of oscine passerine birds

Journal of Biogeography 33, 1155–1165 1161ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

The results for Passeroidea and Muscicapoidea (nodes

25–31) are rather uncertain. The DIVA analysis could not

confidently present putative ancestral patterns for these

groups. The ancestral patterns are obscured by massive

secondary expansions. Although we have included the results,

we have not attempted to answer any biogeographical ques-

tions from these highly uncertain data.

Molecular clock data agree with geological events

Molecular clocks are subject to great controversies and,

although the time estimates presented here are essentially

based on two calibration points, they still indicate two

important points (Fig. 4).

1. The basal lineages of Corvida diverged from each other

some 40–60 Ma. At that time Australia was isolated and it

seems that none of these lineages was able to expand out of the

Australian continent. In general, these birds do not appear to

cross water, although some Meliphagidae lineages had a certain

success in colonizing the Pacific archipelagos. Only one lineage

colonized another continent within this time frame, as

evidenced by the genera Picathartes and Chaetops, which are

specialized forms of rocky places in tropical rain forests and

montane heathlands near the Cape, respectively. Assuming

that oscines dispersed from Australia to Asia, the geographical

distribution of Picathartes/Chaetops has been interpreted as

relictual. Considering that Africa also has several other deep

Passerida lineages (Hyliota, Promerops, Modulatrix, Stenostira)

(Beresford et al., 2005; Fuchs et al., 2005), other interpreta-

tions should also be mentioned. When Picathartes/Chaetops

diverged from the other basal oscines (45–50 Ma, Table 1),

Australia was nearly the same distance from Africa as from

Asia (Briggs, 2003). There are no known examples of passerine

birds managing a flight of 5000–6000 km, the approximate

distance between Australia and Africa 50 Ma. However, the

Kerguelen and Crozet Plateaus of the southern Indian Ocean,

along with the Broken Ridge south-west of Australia, would

have formed an almost continuous chain of submarine

plateaus linking Australia and East Antarctica with Madagascar

and Africa (Fig. 5). Although we are not aware of geological

data documenting vertical movements of these plateaus during

the Tertiary, it appears that at least the Kerguelen plateau was

above sea level in the late Cretaceous (Anon, 1988). It seems

unlikely that India served as a stepping-stone between

Australia and Africa, since India was about to be integrated

into the Asian land mass at 55–65 Ma (Beck et al., 1995;

Briggs, 2003). However, as India moved northward it left

fracture zones with volcanoes and submerged sea-mounds

along the Ninety East Ridge and the Chago-Laccadive Ridge

(Briggs, 2003). It has been documented that sea-mounds along

the strike–slip fault in the Mozambique Channel were above

sea level in the mid-Tertiary (McCall, 1997), therefore we

cannot exclude other, similar changes along ridges in the

Indian Ocean, creating stepping-stones for dispersal. Even

within-archipelago radiations are possible, as demonstrated

recently for Pacific Monarchidae (Filardi & Moyle, 2005).

2. Up to some 25–30 Ma, no species appeared to be able to

cross to Southeast Asia. At this time, however, Australia had

moved sufficiently north for dispersal from this continent to

Southeast Asia to take place. This dispersal probably did not

happen directly from the Australian main plate, but occurred

when terranes of Australian origin started intermingling with

plate fragments in the Australian–Asiatic borderline (Hall,

1998). The basal nodes of Crown Corvida (nodes 8–10)

contain relatively few species that managed to get across

to Southeast Asia c. 25–30 Ma. Five million years later,

c. 20–25 Ma, the distal lineages of Crown Corvida (nodes

11–13), which are relatively species-rich, dispersed through

Wallacea. The most important Cenozoic plate boundary

organization within Southeast Asia took place 20–30 Ma.

The East Sulawesi terranes had moved from west of the

Vogelkop terrane of western New Guinea and were slowly

being pieced together with North Sulawesi, which was initially

part of the Philippine archipelago (Fig. 5). Also Timor, Sumba

and other tiny islands of Australian origin were linked with the

volcanic chain of the Lesser Sunda Islands (Fig. 2). These

movements caused the Philippine plate to start rotating

clockwise and, at about the same time, the Melanesian Arc

collided with the Javan Plateau linking the Melanesian Arc to

New Guinea terranes (Hall, 1998; Moss & Wilson, 1998). As

distances between land of the Australian plate and the

Southeast Asian Plate decreased, avian dispersal across the

Figure 5 The Indian Ocean 45 Ma. Margins of continents and

possible land bridges are marked: thin lines, contemporary

coastlines; bold lines, edges of continental shelves and edges of

submerged terranes and plateaus; stippled lines, strike–slip faults

with rows of sea-mounds and volcanic islands. Ti ¼ Timor;

Se ¼ Seram; S ¼ terranes corresponding to contemporary

Sulawesi; Ph ¼ terranes corresponding to contemporary Philip-

pines. (Redrawn from Smith et al., 1994; Hall, 1998 and bathy-

metric maps.)

K. Jønsson and J. Fjeldsa

1162 Journal of Biogeography 33, 1155–1165ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

ocean barrier became much easier. It is thought-provoking

that oscines dispersed from Australia to Asia when very few

suboscines (except a few migratory Pitta species) dispersed

from Asia to Australia. Perhaps the ecological niches were

already effectively occupied in Australia by members of the

Corvida radiation?

At this time, Australia was probably beginning to change

from a humid tropical climate to the modern arid climate. This

could have made it more difficult for forest-adapted suboscines

to establish themselves on the Australian continent (Rowley &

Russell, 1997; Ericson et al., 2003). The molecular clock

estimates are in good agreement with the time of integration

of Australian and Asian plate fragments in Sulawesi and the

Melanesian Arc/Philippines. The oscine stepping-stone disper-

sal across the Indian Ocean could have been helped further by

prevailing east–west tropical winds in the Indian Ocean at that

time. Although this is pure speculation, wind is suggested as a

vehicle for plant dispersal in the Southern Hemisphere

(Munoz et al., 2004; Renner, 2004), and could also have

helped avian dispersal.

CONCLUSIONS

The DIVA analysis supports the idea that Passerida spread

from the Australian plate across the Indian Ocean to Africa

and then rapidly onwards to other continents, with massive

radiations. The time estimates provide a temporal correlation

and indicate that this spreading event took place c. 45–

50 Ma.

At that time the distance would have been more-or-less the

same between Australia and Africa and Australia and Southeast

Asia, and it is possible that the warm global climate (Kennett,

1995) and prevailing winds would have assisted this oscine

dispersal across the Indian Ocean. This was probably a one-

time event. It is possible, but less likely, that this dispersal event

affected Southeast Asia. Furthermore, the African colonization

is supported by several basal African lineages within the three

major Passerida clades.

As Australia moved northwards, closer to Southeast Asia,

and the plates finally collided 15–20 Ma, there was a significant

dispersal taking place. This gave rise to Crown Corvida which

crossed several times and more frequently as the ocean barrier

diminished. Crown Corvida radiated markedly but were never

as successful as Passerida. It is possible that the ecological

niches were already occupied by Passerida, which had under-

gone a remarkable adaptive radiation by the time that the more

stenotrophic, insectivorous Crown Corvida entered Asia via

Wallacea.

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K. Jønsson and J. Fjeldsa

1164 Journal of Biogeography 33, 1155–1165ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd

BIOSKETCHES

Knud Jønsson is a Master’s student at the University of Copenhagen. He is interested in avian systematics, mostly based on

molecular data and the biogeographical patterns of dispersal and diversification in passerines, mainly oscines, within Australia,

Southeast Asia and Africa.

Jon Fjeldsa is a biodiversity professor and curator of birds at the Danish Natural History Museum. His research is on avian

systematics and biogeography, with special emphasis on the tropical Andes region of South America and Africa. His main interests

are mode of speciation and the interaction of historical and ecological factors in moulding regional patterns of endemism and species

richness. This is developed through traditional biogeographical methods and analysis of comprehensive distributional data bases and

conservation priority analysis.

Editor: Jose Alexandre Diniz-Filho

Biogeography of oscine passerine birds

Journal of Biogeography 33, 1155–1165 1165ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd