ArticlePDF Available

Abstract and Figures

In common with human speech, song is culturally inherited in oscine passerine birds ('songbirds'). Intraspecific divergence in birdsong, such as development of local dialects, might be an important early step in the speciation process. It is therefore vital to understand how songs diverge, especially in founding populations. The northward expansion of the Light-vented Bulbul Pycnonotus sinensis (J. F. Gmelin, 1789) into north China in the last 30 years provides an excellent opportunity to study birdsong evolution. We compared ~4400 songs from newly established northern populations with ~2900 songs from southern populations to evaluate song divergence after recent expansion. The total pool of syllables and especially song types was considerably smaller in the north than in the south, indicating 'founder effects' in the new population. The ancestral pattern of mosaic song dialects changed into a pattern of wide geographical sharing of a few song types and syllables, likely the result of fewer geographical barriers to 'meme flow', and the recent spread across a large area in the north. Our results suggest that song evolution and vocal trait shifts can arise rapidly after range expansion, and that in the Light-vented Bulbul 'founder effects', geographical isolation, and recent rapid expansions played important roles in the evolution of song dialects.
Content may be subject to copyright.
Recent northward range expansion promotes song evolution
in a passerine bird, the Light-vented Bulbul
X. Y. XING*,P.ALSTR
OM * ,X.J.YANG§&F.M.LEI*
*Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
University of Chinese Academy of Sciences, Beijing, China
Swedish Species Information Centre, Swedish University of Agricultural Sciences, Uppsala, Sweden
§School of Environmental Studies, China University of Geosciences, Wuhan, China
Keywords:
cultural evolution;
founder effect;
geographical isolation;
newly established populations;
song dialect.
Abstract
In common with human speech, song is culturally inherited in oscine pas-
serine birds (‘songbirds’). Intraspecific divergence in birdsong, such as devel-
opment of local dialects, might be an important early step in the speciation
process. It is therefore vital to understand how songs diverge, especially in
founding populations. The northward expansion of the Light-vented Bulbul
Pycnonotus sinensis (J. F. Gmelin, 1789) into north China in the last 30 years
provides an excellent opportunity to study birdsong evolution. We com-
pared ~4400 songs from newly established northern populations with ~2900
songs from southern populations to evaluate song divergence after recent
expansion. The total pool of syllables and especially song types was consid-
erably smaller in the north than in the south, indicating ‘founder effects’ in
the new population. The ancestral pattern of mosaic song dialects changed
into a pattern of wide geographical sharing of a few song types and syllables,
likely the result of fewer geographical barriers to ‘meme flow’, and the
recent spread across a large area in the north. Our results suggest that song
evolution and vocal trait shifts can arise rapidly after range expansion, and
that in the Light-vented Bulbul ‘founder effects’, geographical isolation, and
recent rapid expansions played important roles in the evolution of song
dialects.
Introduction
Cultural evolution is the change in behavioural traits
transmitted through social learning (Whiten et al.,
1999; Freeberg, 2000; Krutzen et al., 2005; Bluff et al.,
2010; Cardoso & Atwell, 2011). Song in oscine passe-
rines, parrots and hummingbirds is a classic example of
a cultural trait (Baptista & Schuchmann, 1990; Pepper-
berg, 1994; Catchpole & Slater, 2008a). Selective pres-
sures and stochastic factors are considered to be key
drivers of song evolution, although the relative impor-
tance and interplay among these processes are poorly
understood. For example, songs have been suggested to
change in response to (i) environmental conditions
affecting sound transmission (Morton, 1975; Wiley,
1991; Badyaev & Leaf, 1997; Slabbekoorn & Peet, 2003;
Seddon, 2005); (ii) morphological adaptations influenc-
ing vocalizations, e.g. bill size/shape and overall body
size (Podos, 2001; Laiolo & Rolando, 2003; Seddon,
2005; Huber & Podos, 2006); (iii) interspecific interac-
tions, such as maladaptive hybridization (‘reproductive
character displacement’) (Seddon, 2005) or competition
for sound space (Grant & Grant, 2010); (iv) female
choice based on various song attributes (Searcy &
Andersson, 1986; Hasselquist et al., 1996); (v) male-
male competition, e.g. for efficient territorial defence
(Beecher et al., 2000; Cate et al., 2002; Ellers & Slab-
bekoorn, 2003); (vi) stochastic factors, e.g. ‘cultural
mutation’ caused by copying errors or improvisation,
and ‘cultural drift’ (Lemon, 1975; Baker & Jenkins,
1987; Lynch & Baker, 1993; Lynch, 1996; Martens,
1996; Payne, 1996; Baker et al., 2003; Lachlan &
Correspondence: Fumin Lei and Per Alstr
om, Institute of Zoology,
Chinese Academy of Sciences, No.1 Beichen West Road, Chaoyang
District, Beijing 100101, China.
Tel.: +86 6 480 7159; fax: +86 6 480 7159;
e-mails: leifm@ioz.ac.cn, per.alstrom@slu.se
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
867
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
doi: 10.1111/jeb.12101
Feldman, 2003; Parker et al., 2010; Cardoso & Atwell,
2011); or (vii) changes in the balance between natural
and sexual selection (Irwin, 2000). Song divergence as
a result of cultural evolution might cause reproductive
isolation and hence promote speciation (Grant & Grant,
1996; Slabbekoorn & Smith, 2002; Brambilla et al.,
2008; Kirschel et al., 2009), and it has been suggested
that song learning might accelerate the rate of specia-
tion (Lachlan & Servedio, 2004; Edwards et al., 2005).
Comparing song variation over time and geographical
space is one of the best methods to understand vocal
cultural evolution (Podos & Warren, 2007). A rare
opportunity is provided by recent range expansions.
Some studies have focused on populations introduced
by humans, such as North Island Saddlebacks Philestur-
nus rufusater in New Zealand (Parker et al., 2012),
House Finch Carpodacus mexicanus (Mundinger, 1975;
Pytte, 1997) and Eurasian Tree Sparrow Passer montanus
(Lang & Barlow, 1997) in eastern USA, and Common
Chaffinch Fringilla coelebs in New Zealand (Jenkins &
Baker, 1984), whereas others have examined natural
range expansions, such as Common Chaffinch in Chat-
ham Island (Baker & Jenkins, 1987), Dark-eyed Junco
Junco hyemalis in California (Newman et al., 2008),
Western Gerygone Gerygone fusca on an Australian
off-shore island (Baker et al., 2003), and two species of
Darwin’s finches (latter in response to colonization of a
third Darwin’s finch species) (Grant & Grant, 2010).
Several of these studies, as well as comparisons of
songs in island and mainland populations of unknown
age, have found depauperate pools of syllables or song
types in the isolated populations as a whole, and sug-
gested ‘founder effects’ after colonization as a likely
explanation for this pattern (Lack & Southern, 1949;
Mundinger, 1975; Mirsky, 1976; Baptista & Johnson,
1982; Baker & Jenkins, 1987; Baker, 1996; Baker et al.,
2006). However, conversely, a few studies have
reported high vocal diversity among newly established
populations, and linked this to a relatively high number
of founders, subsequent immigration, or high rates of
‘cultural mutation’ (Lynch & Baker, 1994; Lang & Bar-
low, 1997; Pytte, 1997; Kroodsma et al., 1999; Hamao
& Ueda, 2000; Baker et al., 2003). Different results may
arise at different levels of song structure, as has been
shown in studies of Common Chaffinches in New Zea-
land vs. the UK (Jenkins & Baker, 1984) and Iberia vs.
the Canary Islands (Lynch & Baker, 1993). In the
former study, one part of the song was more complex
whereas another part was simpler in the introduced
population compared with the source population.
Geographical variation in vocalizations has long been
classified into macro and micro, based on geographical
scale. The former is the variation found among geo-
graphically widely separated populations that are unlikely
to meet, whereas the latter refers to variation among
neighbouring groups of birds that might interact with
each other. Dialects are a type of micro-geographical
variation with sharp boundaries among populations
within species (Catchpole & Slater, 2008b). Besides
humans (Nettle, 1999), bats (Davidson & Wilkinson,
2002), primates (Mitani et al., 1992; de la Torre &
Snowdon, 2009), cetaceans (Weilgart & Whitehead,
1997) and a few sub-oscine passerine birds (Noad et al.,
2000; Saranathan et al., 2007; Fitzsimmons et al., 2008),
vocal dialects have been widely documented in the
groups of birds with learned vocalizations, i.e. oscine
passerines (Kroodsma, 2004), hummingbirds (Gaunt
et al., 1994) and parrots (Baker, 2000). Many hypothe-
ses have been proposed to explain how dialects are
formed (Lemon, 1975; Baker & Cunningham, 1985;
Podos, 2001) and maintained (Harbison et al., 1999).
As song is believed to be an important reproductive
isolating barrier in birds (Grant & Grant, 1997; Edwards
et al., 2005), it is relevant to understand how songs
evolve, especially in newly established populations,
which often represent the first step in the speciation
process (Mayr, 1942; Grant & Grant, 2008a,b; Price,
2008). Few of the previous studies on bird song dialects
uncovered how these changed after successful coloniza-
tion of new areas. In this study, we compared song dif-
ferentiation between founding and source populations
in the Light-vented Bulbul Pycnonotus sinensis, with the
aim to investigate if and how a recent range expansion
has affected song evolution in this species.
Materials and methods
The light-vented bulbul
The Light-vented Bulbul is a medium-sized (19 cm)
oscine passerine bird in the widespread Old World bulbul
family (Pycnonotidae). It is near-endemic to China,
where it was previously resident south of the Yangtze
River, in the Oriental region. However, it began expand-
ing northward in the 1930s, and now occupies the wide
Palearctic ecozone of northeast China (Cheng, 1976;
Zhang et al., 2003; Fishpool & Tobias, 2005; Wang et al.,
2005; Fig. 1). The expansion has been rapid: in the 1980s
and 1990s, numbers were small in northeast China
(Williams et al., 1992), but now it is locally common
(Zhang et al., 2003; Wang et al., 2005). It occurs in open
habitats with scrub and trees, including human-made
environments, such as orchards, campuses and parks. It
has various vocalizations, including several types of sin-
gle-syllable call, and more musical, complex multiple-
syllable songs (Fishpool & Tobias, 2005). Song dialects
have been noted in its southern distribution area (Jiang
et al., 1996; Ding & Jiang, 2005; Yang & Lei, 2008).
Song recording
The Light-vented Bulbul is commonly distributed south
of Yangtze River, China (red dotted line in Fig. 1;
(Fishpool & Tobias, 2005)), which we defined as the
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
868 X. Y. XING ET AL.
boundary between southern and northern populations,
as that was previously its northern limit. We chose 12
cities south of the Yangtze River to represent 12 south-
ern populations. Ten cities north of the Yangtze River
were chosen to represent the recently established
northern populations. Within each southern or north-
ern city, we recorded bulbuls at several sites, such as
parks, campuses etcetera. At each site, we recorded
birds that were sufficiently widely spaced to be consid-
ered different individuals, and each site was visited only
once to avoid the risk of recording the same individual
more than once. In the south, two persons recorded in
different places at the same time. To obtain a represen-
tative sample of each male’s repertoire, we recorded
each male for as long time as possible, usually until it
stopped singing or flew away. For each northern indi-
vidual, we recorded 27.2 32.8 songs (range: 1222;
for only 3 of 162 northern individuals only one song
was recorded; see Definitions of terms, below), and for
each southern individual 18.6 20.8 songs (range:
1172; for only 12 of 167 southern individuals only
one song was recorded). Songs were recorded during
the breeding season (MarchJune) from 2005 to 2011,
from 6 AM to 9 AM, using a TASCAM DA-P1 portable
tape recorder and Sennheiser MKH 416 directional
microphone. Recordings from Taiwan were downloaded
from the Macaulay Library, Cornell Lab of Ornithology
and http://www.xeno-canto.org/.
Definitions of terms
See Fig. 2. Song:A series of syllables (see below) sepa-
rated from other songs by distinct pauses (usually at
least 2 s in the Light-vented Bulbul). Syllable: Smallest
song unit used here. It may contain one or more
elements (i.e. unbroken patterns in a sonogram)
which appear together in a fixed sequence. There are
obvious ‘blank spaces’ between different syllables in a
sonogram. Song type: Contains specific syllable types
given in a specific sequence. Variant: song types have
one or more of these syllables deleted or repeated.
Accordingly, differences between variants of the same
song type are considerably smaller than differences
between different song types. Repertoire (song/variant/
syllable): Number of different types recorded in one
individual.
Song type 7 Song type 2
Song type 123 Song type 128
Altitude
Low: -263m
High: 8233m
kHz
kHz
kHz
kHz
2
8
0.5 1.0 0.5
0.50.5
1.0
1.0 1.0ss
ss
2
8
8
8
2
2
Fig. 1 Recording localities and
distribution of song types in Light-
vented Bulbul. Abbreviations of
localities explained in Table S1.
Northern and southern populations
indicated by green dots and red
triangles respectively. Years and red
dotted line indicate the distribution
boundary between northern and
southern populations and time of
colonization. Blue figures and letters
indicate the seven song types sung by
northern populations (cf. Fig. 3). Seven
of the ten northern populations
encircling Bohai Bay and TY sung song
types 1 and 2 (DL also had a unique
song type, 3); TY, ZZ and BJ sung song
type 4 (ZZ sang only this song type; just
few individuals of TY and BJ sung song
type 4); and XA had three unique song
types, 5, 6 and 7 (one individual also
sang song type 1). Spectrograms show
examples of different song types.
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Birdsong evolution after recent expansion 869
Song analysis
Although our sampling was uneven across populations
(Table 1), to some degree this reflected the population
densities at different sites. The northern populations
TY and TJ and the southern populations HN and NN
(cf. Fig. 1) were excluded from the statistical analyses
as only 1, 5, 1 and 2 individuals, respectively, were
recorded at each of these sites. However, these small-
sample populations were included in the qualitative
(song type distribution) analyses, as they were consid-
ered to provide some useful information despite the
small sample sizes. For example, although only one
individual was recorded at TY, its 81 songs were
classified into three song types, whereas the 437 songs
recorded from 11 individuals in another northern
population (ZZ) all belong to the same song type.
Using Avisoft-SAS Lab Pro 4.52 (Avisoft Bioacous-
tics, Berlin, Germany), we digitized song recordings
with a sampling rate of 22 050 Hz, and made spectro-
grams with frequency resolution of 56 Hz and tempo-
ral resolution of 2.90 ms (spectrogram settings: Flat
Top window, overlap 87.5%, FFT length 512 points).
Syllable types and song types were classified by visual
inspection of these spectrograms. Different syllable
types and song types differed clearly in spectrograms
(see examples in Figs. 1 and 2) and audibly. Although
there were minor differences among individuals in the
detailed appearance of syllables, classification was usu-
ally unambiguous after examination of a large sample
of recordings. As there were many more syllables and
song types in the south than in the north, two observ-
ers (X.Y.X. and X.J.Y.) classified the southern songs
independently, whereas all of the northern songs were
classified by one of these persons (X.Y.X.). Syllables
and song types were assigned numbers. For example,
syllable sequence 1-2-3 was denoted as song type 1-0,
which means the basic, most common, variant of ‘song
type 1’, in which the syllables are given in the order
syllable 1, syllable 2, syllable 3; and syllable sequence
1-1-1-2-3 was denoted as song type 1-11, which is
variant type number 11 of song type 1 in which sylla-
ble 1 is given three times, followed by syllable 2 and
syllable 3 (Fig. 2). Each syllable and song type was
coded to create a song library for all the 329 individu-
als from 22 populations.
We performed Bivariate Correlation Analysis and
made a cumulative curve to evaluate whether the sam-
pling of song, variant and syllable pools was sufficient
in the north and south. The cumulative curve was plot-
ted with the number of individuals recorded against the
number of different song/variant/syllable types found.
As more and more songs were recorded, fewer and
fewer new ones were found, and eventually, the curve
would become horizontal when all of the types have
been recorded would be expected to plateau when rep-
ertoires were well sampled (Catchpole & Slater, 2008c;
Baker, 2012).
To evaluate the similarity of the pools of song types
across population, and relate it to geographical
distances between these populations statistically, we
did a Mantel test (Payne et al., 2000; Slabbekoorn
0.5 1.0
(a) (b)
(C)
kHz kHz
Song type 1–11: 1–1–1–2–3
Song type 1–4: 2–3
Song type 1–0: 1–2–3
Syllable 1 Syllable 2
Syllable 2 Syllable 3
Syllable 3
10
8
6
4
2
0
s0.5 s
Syllable 1 Syllable 2 Syllable 3
0.5 1.0 1.5 s
10
10
kHz
8
8
6
6
4
4
2
2
0
0
Fig. 2 Definitions of song type and syllable. Song type 1-0 (1-2-3)
is the basic, commonest variant of song type 1 with a whole
version of syllable types, and has three different syllable types
arranged in a fixed order. Song type 1-4 is variant 4 of song type
1, which lacks syllable 1, and song type 1-11 is variant 11 of song
type 1, which gives syllable 1 three times in a sequence.
Table 1 Sample sizes and numbers of song, variant and syllable
types in the southern and northern populations; values per
individual were based only on a sub-sample of 18 extensively
recorded birds from each region.
Southern populations Northern populations
Total sampling
No. of songs 2922 4406
No. of individuals 167 162
No. of populations 12 10
No. of song types 118 7
No. of variant types 508 273
No. of syllable types 131 36
Re-sampling
No. of song types 23 4
No. of variant types 130 82
No. of syllable types 55 22
No. of song types
per individual
1.8 0.6
(range: 13)
1.7 0.8
(range: 13)
No. of variant types
per individual
7.6 6.4
(range: 228)
7.8 3.3
(range: 314)
No. of syllable types
per individual
7.7 3.0
(range: 414)
6.5 3.0
(range: 213)
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
870 X. Y. XING ET AL.
et al., 2003; Peakall & Smouse, 2006), as implemented
in GenALEx 6.5 based on 1000 permutations. Mantel
test is a nonparametric test that assesses the relation-
ship between the elements of any two matrices with
matching entries (Peakall & Smouse, 2006, 2012). It
uses multiple random permutations of the observed
data to generate the chance expectation and produces
an rvalue between 1 and +1 that can be interpreted
like a correlation coefficient of the two matrices (Mol-
les & Vehrencamp, 1999). Its null hypothesis is that
the two matrixes have no significant correlation. The
Mantel statistic was evaluated with the distribution of
values permuted randomly and the probability that two
matrices were more similar than expected by chance
(Payne et al., 2000). In this study, the first matrix of
population song similarity was calculated using Jac-
card’s similarity coefficient, and the second matrix was
produced using geographical distances (km) between
each two populations. The test was procedured in
northern and southern areas, respectively, both for
song type and syllable type. Significant negative r-value
means that the song similarity tended to decline with
distance increase nearby populations had more simi-
lar songs, whereas the positive r-value means oppo-
sitely. Jaccard’s coefficient (S
j
) was calculated as the
number of song types common to both populations
divided by the total number of song types across both
populations (Podos et al., 1992; Tracy & Baker, 1999).
Considering differences in individual sample sizes,
and as the Bivariate Correlation Analysis and cumula-
tive curve (Figure S1) indicated that southern sampling
were not sufficiently well sampled, we re-sampled a
subset of well-recorded individuals from the total data-
set, to evaluate whether the number of song, variant
and syllable types differ between northern and south-
ern populations, both at the individual level and at the
whole ancestral and colonial population level. Among
167 southern individuals, 40 songs were recorded
for 18 individuals, and among 162 northern individu-
als, 40 songs were recorded for 33 individuals. These
18 southern individual and 18 of the northern ones
(randomly chosen) were selected. For individuals with
more than 40 songs, we picked up 40 songs randomly
from song repertoire of each individual. T-test and
MannWhitney Utest were used to investigate differ-
ences at the individual level between north and south.
Chi-Square test was used to compare differences
between the whole northern and southern populations.
All data were tested for normality by One-sample Kol-
mogorov-Smirnov test before t-tests were performed.
These statistical analyses were conducted using SPSS
16.0 (SPSS Inc., Chicago, IL, USA).
Results
According to the Bivariate Correlation Analysis
(Table 2), in the north the number of song types and
syllable types were not correlated with the number of
recorded songs or individuals (all Pvalues >0.05),
whereas the number of variant song types was corre-
lated with the number of songs (r=0.953, P<0.01)
and individuals (r=0.868, P<0.01) recorded. In the
south, the number of song types and syllable types
were not correlated with the number of recorded songs
or individuals too (all Pvalues >0.05), but the number
of variant type was correlated significantly with the
number of songs recorded (r=0.748, P<0.05). The
cumulative curves of northern song and syllable types
became approximately asymptotic with increasing num-
ber of individuals sampled, whereas the northern curve
for number of variants and all three southern curves
did not approach the asymptote (Figure S1). These two
methods both suggested that northern populations were
well sampled with respect to song and syllable types,
whereas repertoire sizes for southern populations and
northern variant song types were insufficiently sam-
pled. For these reasons, a comparable subsample of
extensively recorded individuals was selected from the
total dataset for additional comparisons (see Materials
and methods).
In the total dataset, the newly established northern
populations had much smaller pools of song, variant or
syllable types than the combined southern source pop-
ulations (Tables 1 and 3 and Figure S1). In total, seven
song types, 273 variant types and 36 syllable types were
recorded in the north, whereas southern populations
Table 2 Results of bivariate correlation analysis.
Correlations
No. of songs
recorded
No. of individuals
recorded
Northern populations
No. of song type r0.295 0.183
P0.477 0.664
N88
No. of syllable type r0.635 0.527
P0.091 0.180
N88
No. of variant type r0.953* 0.868*
P<0.001 0.005
N88
Southern populations
No. of song type r0.403 0.188
P0.248 0.603
N1010
No. of syllable type r0.534 0.561
P0.112 0.092
N1010
No. of variant type r0.7480.33
P0.013 0.352
N1010
N stands for the number of populations.
*Correlation is significant at the 0.01 level (2-tailed).
Correlation is significant at the 0.05 level (2-tailed).
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Birdsong evolution after recent expansion 871
had a total of 118 song types, 508 variant types and
131 syllable types. For the re-sampled dataset compris-
ing 18 northern individuals and 18 southern individu-
als, the numbers of song/variant/syllable types were 4/
82/22 and 23/130/55 respectively. Despite more songs
having been recorded in northern populations
(Table 1), they had significantly smaller pools of song
types, variants and syllable types (all v
2
>54, all
P<0.001; Table 3). The same conclusion is reached
using only the subsample of extensively recorded indi-
viduals (all v
2
>10, all P<0.001; Table 3). The num-
bers of song type, variant or syllable types sung per
individual did not differ between northern and south-
ern populations (subsample of extensively recorded
individuals: t-tests, all |t|<1.2, all d.f. =17, all
P>0.25; Table 4).
In the north, a small number of song types and sylla-
ble types were widespread, and nearby localities
showed a high degree of similarity in song and syllable
type composition (Fig. 3). In contrast in the south, few
song types and syllable types were recorded at more
than one locality, even in geographically closely related
populations (three populations in Sichuan Basin: DJY,
CD, YA).The results of Mantel tests confirmed these dif-
ferences (Fig. 4). In northern populations, there was a
significant negative correlation between song/syllable
type similarity and geographical distance (for song type,
r=0.637, P<0.05; syllable type, r=0.653,
P<0.05), meaning that song/syllable type similarity
decreased significantly with increasing geographical dis-
tance, that is geographically closer populations had
more similar song types and syllable types. But this
pattern was not observed in southern populations:
there was no association between song/syllable type
and geographical distance was apparent (for song type:
r=0.218, P=0.110; syllable type: r=0.128,
P=0.842). Accordingly, northern populations showed
evidence of divergence by distance, whereas the low
level of common song types among southern popula-
tions suggested a mosaic pattern of song dialects across
the southern distribution.
On the basis of song type distributions (Figs. 1 and
3), we divided the 10 northern populations into three
dialect regions (Fig. 1): (i) seven populations around
Bohai Bay and another population (TY, n
individuals
=1)
sung song types 1 and 2; the most northeastern popula-
tion (DL) had a unique song type, number 3; (ii) ZZ
had only one song type, number 4, which was also
sung by a few individuals in BJ and TY; (iii) XA had
three unique song types, numbers 5, 6 and 7, and one
individual also sang the variant type 1-7.
Only three song types (2.4%) were sung both in the
north and in the south. The northern common song
types 1 and 2 were recorded in only one individual in
one southern population (GL). The third shared song
type, 3, was recorded in northern population DL (in 14
of 52 individuals) and in southern population DJY (in 6
of 12 individuals). Twenty-three syllable types were
sung both in the north and south, representing 63.9%
in the north (n=36) and 17.6% in the south (n=131)
of the total syllable types respectively.
Discussion
Very few song types were common to northern and
southern populations of bulbuls. In contrast, 63.9%
(n=36) of the northern syllable types were also found
in the south. This suggests that the syllable is a more
conservative unit than song type in the vocal evolution
Table 3 Song comparisons between the whole north and the
whole south.
Chi-Square test
v
2
d.f. P
Total sampling
No. of song types 98.568 1 0.000
No. of variant types 70.711 1 0.000
No. of syllable types 54.042 1 0.000
Re-sampling
No. of song types 13.370 1 0.000
No. of variant types 10.868 1 0.001
No. of syllable types 14.143 1 0.000
Table 4 Song comparisons of southern and northern individuals.
t-test
td.f. P
No. of song types Z=0.609 17 0.542
No. of variant types 0.13 17 0.897
No. of syllable types 1.166 17 0.252
Northern population
Number of individuals
50
150
100
200
0
DL WHBJBDH JNTYTJ ZZQD XA
Song type
7
3
4
5
6
1
2
Fig. 3 Song types in ten northern populations (arranged from
north to south on xaxis). Song types 1 and 2 are widespread in
the seven populations encircling Bohai Bay (DL, BDH, BJ, TJ, JN,
WH and QD) and TY (latter just one individual with three song
types). See Fig. 1 and Table S1 for explanation of locality codes.
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
872 X. Y. XING ET AL.
of the Light-vented Bulbul, in agreement with some
studies on other birds (Lynch et al., 1989; Burnell,
1998; Nelson et al., 2004).
Newly established northern populations only retained
a small subset of the total syllable pool of the ancestral
southern populations. In the north, we did not hear any
other song types in addition to the seven types that we
classified. Although we cannot be sure that we covered
each individual male’s full repertoire (in some cases we
almost certainly did not do that), we are confident that
our sampling is sufficient to broadly represent the north-
ern populations. Despite the cumulative curve for the
south (Figure S1) was still growing which suggested
the south not being sampled as exhaustively as the
north, the results still show higher diversity in the south.
So the interpretation of results is unaffected.
According to founder effect/cultural drift theory in
birdsong studies (Baker & Jenkins, 1987; Lachlan &
Slater, 2003; Huber & Podos, 2006), founders would
only sing a small subset of source populations’ song
types and syllables, thereby decreasing the total varia-
tion. This has previously been found in some founding
populations of birds (Bitterbaum & Baptista, 1979;
Baker & Jenkins, 1987; Baker et al., 2001; White,
2012). In addition, the low density of pioneers and the
concomitant small number of learning models would
probably further decrease the vocal diversity and
increase stereotypy (Bitterbaum & Baptista, 1979; Pytte,
1997; Matthysen et al., 2002). Our results agree with
these predictions. However, as there was hardly any
song type sung both in northern and southern bulbuls,
it is uncertain to what degree original southern song
types were retained in the newly colonized populations.
Alternatively, the song types might have diverged
quickly after the new colonization, as has been sug-
gested for some other birds (Jenkins & Baker, 1984;
Baker et al., 2003; F
orschler & Kalko, 2007; Parker
et al., 2012).
The wider geographical distribution of a few song
types in the north could have at least two, nonexclu-
sive explanations. One of these is that it might result
from the fewer geographical barriers and hence, more
‘meme flow’ than in the south. Several of the southern
populations are isolated by topographical barriers, such
as mountainous areas or water bodies (Fig. 1), whereas
the northern Bohai Bay populations inhabit a topo-
graphically rather homogeneous region. The northern
ZZ and especially, XA populations, which are the most
isolated ones of the northern populations, also have
the most distinct (divergent) songs. Moreover, the
northern DL population, which is the most remote of
the seven Bohai populations, is the only one of these
in which a unique song type was recorded. The differ-
ences between the southern CD, DJY and YA, which
are in close proximity and not separated by any appar-
ent geographical barriers, are more difficult to explain.
Similar microdialects have been observed in other spe-
cies (Leader et al., 2000; Baker, 2003; Slabbekoorn
et al., 2003; Podos & Warren, 2007). It is possible that
the southern populations are more resident than the
northern ones, which would further contribute to the
observed differences. This has been noted in the
White-crowned Sparrow, in which northern, migratory,
populations have been found to have more widely dis-
tributed dialects than southern populations (Baptista,
1977; Kroodsma et al., 1984; Austen & Handford, 1991;
Chilton et al., 2002). However, the statement that
northern populations of the Light-vented Bulbul are
migratory, unlike southern ones (Fishpool & Tobias,
2005), is not correct, as good numbers winter in the
north (personal observations; P. Holt and J. Hornskov
in litt.).
(b)(a)
Geographical distance (km)
100
80
60
40
20
Song type similarity
(Jaccard’s similarity coefficient)
Syllable type similarity
(Jaccard’s similarity coefficient)
Northern population
r = –0.637 P = 0.031
Southern population
r = –0.218 P = 0.110
Geographical distance (km)
02000
100
80
60
40
20
Northern population
r = –0.653 P = 0.028
Southern population
r = 0.128 P = 0.842
400 800 1200 1600
0 2000400 800 1200 1600
Fig. 4 Plot of the similarities among populations in the pool of (a) song types or (b) syllable types in relation to geographical distances.
Each dot represents a pairwise comparison between the Jaccard’s similarity coefficient for pool of (a) song types or (b) syllable types
against the geographical distances (km) between these populations both in north and south respectively. The results (regression lines, rand
Pvalues) indicate that both the similarities of song and syllable types correlated negatively with geographical distances in north, but not
correlated with geographical distances in south.
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Birdsong evolution after recent expansion 873
Another plausible explanation for the wider geo-
graphical distribution of song types in the north is that
the recent spread across a large area might have con-
tributed to the homogenization of the northern songs.
As a result of the rapid expansion, local song types may
not have had sufficient time to form. In agreement
with this is the observation that the XA population,
which is the southernmost and hence, possibly the
oldest one, had the most unique song of the northern
populations.
Conclusions
We found that compared with southern source popula-
tions, the northern, recently established populations (i)
had depauperate song type and syllable type pools, but
did not differ in repertoire size of individual birds; and
(ii) had altered the geographical distribution of song
types from mosaic to a few wide-spread song types. A
combination of ‘founder effect’, fewer geographical bar-
riers to ‘meme flow’ and the recent spread across a
large area in the north are likely explanations for these
differences. Our results show that founding populations
can change their pools of acoustic signals rapidly after
range expansion.
Acknowledgments
We are grateful to Atul Kathait, Paul Holt and Jesper
Hornskov for providing useful information. Many
thanks to Robert B. Payne and Trevor Price for their
valuable comments on an early draft, and to Thomas
Flatt and two anonymous reviewers for constructive
comments on a later version. Thanks to Lijiang Yu for
collecting some recordings, Qing Quan and Yang Liu
for assistance in preparing Figs. 1 and 4. This research
was supported by the National Science Fund for Distin-
guished Young Scientists (30925008) to Fumin Lei, the
Key Laboratory of the Zoological Systematics and
Evolution of the Chinese Academy of Sciences
(O529YX5105) to Xiaoying Xing, and by the Chinese
Academy of Sciences Visiting Professorship for Senior
International Scientists (2011T2S04) to Per Alstr
om.
Conflict of Interests
The authors have declared that no competing interests
exist.
References
Austen, M.J.W. & Handford, P.T. 1991. Variation in the songs
of breeding gambel’s white-crowned sparrows near Chur-
chill, Manitoba. Condor 93: 147152.
Badyaev, A.V. & Leaf, E.S. 1997. Habitat associations of song
characteristics in Phylloscopus and Hippolais warblers. Auk
114:4046.
Baker, M.C. 1996. Depauperate meme pool of vocal signals in
an island population of singing honeyeaters. Anim. Behav.
51: 853858.
Baker, M.C. 2000. Cultural diversification in the flight call of
the ringneck parrot in Western Australia. Condor 102: 905
910.
Baker, M.C. 2003. Local similarity and geographic differences
in a contact call of the galah (Cacatua roseicapilla assimilis)in
western Australia. Emu 103: 233237.
Baker, M.C. 2012. Silvereyes (Zosterops lateralis) song differenti-
ation in an island-mainland comparison: analyses of a com-
plex cultural trait. Wilson J. Ornithol. 124: 454466.
Baker, M.C. & Cunningham, M.A. 1985. The biology of bird-
song dialects. Behav. Brain Sci. 8:85100.
Baker, A.J. & Jenkins, P.F. 1987. Founder effect and cultural
evolution of songs in an isolated population of chaffinches,
Fringilla coelebs, in the Chatham Islands. Anim. Behav. 35:
17931803.
Baker, M.C., Baker, E.M. & Baker, M.S.A. 2001. Island and
island-like effects on vocal repertoire of singing honeyeaters.
Anim. Behav. 62: 767774.
Baker, M.C., Baker, M.S.A. & Baker, E.M. 2003. Rapid evolu-
tion of a novel song and an increase in repertoire size in an
island population of an Australian songbird. Ibis 145: 465
471.
Baker, M.C., Baker, M.S.A. & Tilghman, L.M. 2006. Differing
effects of isolation on evolution of bird songs: examples from
an island-mainland comparison of three species. Biol. J. Linn.
Soc. 89: 331342.
Baptista, L.F. 1977. Geographic variation in song and dialects
of puget sound white-crowned sparrow. Condor 79: 356370.
Baptista, L.F. & Johnson, R.B. 1982. Song variation in insular
and mainland California brown creepers (Certhia familiaris).
J. Ornithol. 123: 131144.
Baptista, L.F. & Schuchmann, K.-L. 1990. Song learning in the
anna hummingbird (Calypte anna). Ethology 84:1526.
Beecher, M.D., Campbell, S.E., Burt, J.M., Hill, C.E. & Nordby,
J.C. 2000. Song type matching between neighbouring song
sparrows. Anim. Behav. 59:2127.
Bitterbaum, E. & Baptista, L.F. 1979. Geographical variation in
songs of California house finches (Carpodacus mexicanus). Auk
96: 462474.
Bluff, L.A., Kacelnik, A. & Rutz, C. 2010. Vocal culture in New
Caledonian crows Corvus moneduloides.Biol. J. Linn. Soc. 101:
767776.
Brambilla, M., Janni, O., Guidali, F. & Sorace, A. 2008. Song
perception among incipient species as a mechanism for
reproductive isolation. J. Evol. Biol. 21: 651657.
Burnell, K. 1998. Cultural variation in savannah sparrow, Pass-
erculus sandwichensis, songs: an analysis using the meme con-
cept. Anim. Behav. 56: 9951003.
Cardoso, G.C. & Atwell, J.W. 2011. Directional cultural change
by modification and replacement of memes. Evolution 65:
295300.
Catchpole, C.K. & Slater, P.J.B. 2008a. How song develops. In:
Bird Song: Biological Themes and Variations (C.K. Catchpole &
P.J.B Slater, eds), pp. 4984. Cambridge University,
Cambridge.
Catchpole, C.K. & Slater, P.J.B. 2008b. Variation in time and
space. In: Bird Song: Biological Themes and Variations (C.K.
Catchpole & P.J.B Slater, eds, pp. 245249. Cambridge
University Press, Cambridge.
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
874 X. Y. XING ET AL.
Catchpole, C.K. & Slater, P.J.B. 2008c. Themes and variations.
In: Bird Song: Biological Themes and Variations (C.K. Catchpole
& P.J.B Slater, eds), pp. 205206. Cambridge University
Press, Cambridge.
Cate, C.T., Slabbekoorn, H. & Ballintijn, M.R. 2002. Birdsong
and malemale competition: causes and consequences of
vocal variability in the collared dove (Streptopelia decaocto).
Adv. Stud. Behav. 31:3175.
Cheng, T. 1976. Distribution List of Chinese Birds. Science Press,
Beijing.
Chilton, G., Wiebe, M.O. & Handford, P. 2002. Large-scale
geographic variation in songs of Gambel’s white-crowned
sparrows. Condor 104: 378386.
Davidson, S.M. & Wilkinson, G.S. 2002. Geographic and
individual variation in vocalizations by male Saccopteryx bi-
lineata (Chiroptera: Emballonuridae). J. Mammal. 83: 526
535.
Ding, P. & Jiang, S. 2005. Microgeographic song variation in
the Chinese bulbul (Pycnonotus sinenesis) in urban areas of
Hangzhou city. Zoolog. Res. 26: 453459.
Edwards, S.V., Kingan, S.B., Calkins, J.D., Balakrishnan, C.N.,
Jennings, W.B., Swanson, W.J. et al. 2005. Speciation in
birds: genes, geography, and sexual selection. Proc. Natl.
Acad. Sci. USA 102: 65506557.
Ellers, J. & Slabbekoorn, H. 2003. Song divergence and male
dispersal among bird populations: a spatially explicit model
testing the role of vocal learning. Anim. Behav. 65: 671681.
Fishpool, L. & Tobias, J. 2005. Family Pycnonotidae. In: Hand-
book of the Birds of the World. Volume 10: Cuckoo-Shrikes to
Thrushes Vol. 10 (J. del Hoyo, A. Elliot & D. Christie, eds),
pp. 178. Lynx Edicions, Barcelona.
Fitzsimmons, L.P., Barker, N.K. & Mennill, D.J. 2008. Individ-
ual variation and lek-based vocal distinctiveness in songs of
the screaming piha (Lipaugus vociferans), a suboscine song-
bird. Auk 125: 908914.
F
orschler, M.I. & Kalko, E.K.V. 2007. Geographical differentia-
tion, acoustic adaptation and species boundaries in mainland
citril finches and insular corsican finches, superspecies
Carduelis [citrinella]. J. Biogeogr. 34: 15911600.
Freeberg, T.M. 2000. Culture and courtship in vertebrates:
a review of social learning and transmission of courtship
systems and mating patterns. Behav. Process. 51: 177192.
Gaunt, S.L.L., Baptista, L.F., Sanchez, J.E. & Hernandez, D.
1994. Song learning as evidenced from song sharing in two
hummingbird species (Colibri coruscans and C. thalassinus).
Auk 111:87103.
Grant, B.R. & Grant, P.R. 1996. Cultural inheritance of song
and its role in the evolution of Darwin’s finches. Evolution
50: 24712487.
Grant, P.R. & Grant, B.R. 1997. Genetics and the origin of bird
species. Proc. Natl. Acad. Sci. USA 94: 77687775.
Grant, P.R. & Grant, B.R. 2008a. Pedigrees, assortative mating
and speciation in Darwin’s finches. Proc. Biol. Sci. 275: 661
668.
Grant, P.R. & Grant, B.R. 2008b. How and Why Species Multiply:
the Radiation of Darwin’s Finches. Princeton University Press,
Princeton, New York.
Grant, B.R. & Grant, P.R. 2010. Songs of Darwin’s finches
diverge when a new species enters the community. Proc.
Natl. Acad. Sci. USA 107: 2015620163.
Hamao, S. & Ueda, K. 2000. Simplified song in an island popu-
lation of the bush warbler Cettia diphone.J. Ethol. 18:5357.
Harbison, H., Nelson, D.A. & Hahn, T.P. 1999. Long-term per-
sistence of song dialects in the mountain white-crowned
sparrow. Condor 101: 133148.
Hasselquist, D., Bensch, S. & vonSchantz, T. 1996. Correlation
between male song repertoire, extra-pair paternity and off-
spring survival in the great reed warbler. Nature 381: 229
232.
Huber, S.K. & Podos, J. 2006. Beak morphology and song fea-
tures covary in a population of Darwin’s finches (Geospiza
fortis). Biol. J. Linn. Soc. 88: 489498.
Irwin, D.E. 2000. Song variation in an avian ring species. Evo-
lution 54: 9981010.
Jenkins, P.F. & Baker, A.J. 1984. Mechanisms of song differen-
tiation in introduced populations of chaffinches Fringilla coe-
lebs in New Zealand. Ibis 126: 510524.
Jiang, S.R., Ding, P., Shi, Q.S. & Zhuge, Y. 1996. Studies on
the song dialects in Chinese bulbuls. Acta Zoolog. Sin. 42:
361367.
Kirschel, A.N., Blumstein, D.T. & Smith, T.B. 2009. Character
displacement of song and morphology in African tinkerbirds.
Proc. Natl. Acad. Sci. USA 106: 82568261.
Kroodsma, D.E. 2004. The diversity and plasticity of birdsong.
In: Nature’s Music. The Science of Birdsong (P. Marler & H.
Slabbekoorn, eds), pp. 108131. Elsevier Academic Press,
San Diego, CA.
Kroodsma, D.E., Baker, M.C., Baptista, L.F. & Petrinovich, L.
1984. Vocal ‘dialects’ in Nuttall’s white-crowned sparrow.
Curr. Ornithol. 2: 103133.
Kroodsma, D.E., Byers, B.E., Halkin, S.L., Hill, C., Minis, D.,
Bolsinger, J.R. et al. 1999. Geographic variation in black-
capped chickadee songs and singing behavior. Auk 116:
387402.
Krutzen, M., Mann, J., Heithaus, M.R., Connor, R.C., Bejder,
L. & Sherwin, W.B. 2005. Cultural transmission of tool use
in bottlenose dolphins. Proc. Natl. Acad. Sci. USA 102: 8939
8943.
Lachlan, R.F. & Feldman, M.W. 2003. Evolution of cultural
communication systems: the coevolution of cultural signals
and genes encoding learning preferences. J. Evol. Biol. 16:
10841095.
Lachlan, R.F. & Servedio, M.R. 2004. Song learning accelerates
allopatric speciation. Evolution 58: 20492063.
Lachlan, R.F. & Slater, P.J.B. 2003. Song learning by chaf-
finches: how accurate, and from where? Anim. Behav. 65:
957969.
Lack, D. & Southern, H.N. 1949. Birds on Tenerife. Ibis 91:
607626.
Laiolo, P. & Rolando, A. 2003. The evolution of vocalisations
in the genus Corvus: effects of phylogeny, morphology and
habitat. Evol. Ecol. 17: 111123.
Lang, A.L. & Barlow, J.C. 1997. Cultural evolution in the Eur-
asian tree sparrow-divergence between introduced and
ancestral populations. Condor 99: 413423.
Leader, N., Wright, J. & Yom-Tov, Y. 2000. Microgeographic
song dialects in the orange-tufted sunbird (Nectarinia osea).
Behaviour 137: 16131627.
Lemon, R.E. 1975. How birds develop song dialects. Condor 77:
385406.
Lynch, A. 1996. The population memetics of birdsong. In: Ecol-
ogy and Evolution of Acoustic Communication in Birds (D.E. Kro-
odsma & E.H. Miller, eds), pp. 181197. Cornell University,
Ithaca, NY.
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Birdsong evolution after recent expansion 875
Lynch, A. & Baker, A.J. 1993. A population memetics
approach to cultural evolution in chaffinch song: meme
diversity within populations. Am. Nat. 141: 597620.
Lynch, A. & Baker, A.J. 1994. A population memetics
approach to cultural evolution in chaffinch song: differentia-
tion among populations. Evolution 48: 351359.
Lynch, A., Plunkett, G.M., Baker, A.J. & Jenkins, P.F. 1989. A
model of cultural evolution of chaffinch song derived with
the meme concept. Am. Nat. 133: 634653.
Martens, J. 1996. Vocalizations and speciation of Palearctic
birds. In: Ecology and Evolution of Acoustic Communication in
Birds (D.E. Kroodsma & E.H. Miller, eds), pp. 221240. Cor-
nell University, Ithaca, New York.
Matthysen, E., Devos, Y. & Hepp, E. 2002. Loss of song varia-
tion through cultural drift in nuthatches Sitta europaea: test-
ing an hypothesis. Avian Sci. 2:19.
Mayr, E. 1942. Systematics and the Origin of Species. Columbia
University Press, New York.
Mirsky, E.N. 1976. Song divergence in hummingbird and
junco populations on Guadalupe Island. Condor 78: 230235.
Mitani, J.C., Hasegawa, T., Groslouis, J., Marler, P. & Byrne,
R. 1992. Dialects in wild chimpanzees? Am. J. Primatol. 27:
233243.
Molles, L.E. & Vehrencamp, S.L. 1999. Repertoire size, reper-
toire overlap, and singing modes in the banded wren (Thry-
othorus pleurostictus). Auk 116: 677689.
Morton, E.S. 1975. Ecological sources of selection on avian
sounds. Am. Nat. 109:1734.
Mundinger, P. 1975. Song dialects and colonization in the
house finch, Carpodacus mexicanus, on the east coast. Condor
77: 407422.
Nelson, D.A., Hallberg, K.I. & Soha, J.A. 2004. Cultural evolu-
tion of puget sound white-crowned sparrow song dialects.
Ethology 110: 879908.
Nettle, D. 1999. Linguistic diversity of the Americas can be rec-
onciled with a recent colonization. Proc. Natl. Acad. Sci. USA
96: 33253329.
Newman, M.M., Yeh, P.J. & Price, T.D. 2008. Song variation
in a recently founded population of the dark-eyed junco
(Junco hyemalis). Ethology 114: 164173.
Noad, M.J., Cato, D.H., Bryden, M.M., Jenner, M.N. & Jenner,
K.C.S. 2000. Cultural revolution in whale songs. Nature 408:
537.
Parker, K.A., Hauber, M.E. & Brunton, D.H. 2010. Contempo-
rary cultural evolution of a conspecific recognition signal fol-
lowing serial translocations. Evolution 64: 24312441.
Parker, K.A., Anderson, M.J., Jenkins, P.F., Brunton, D.H. &
Westneat, D. 2012. The effects of translocation-induced iso-
lation and fragmentation on the cultural evolution of bird
song. Ecol. Lett. 15: 778785.
Payne, R.B. 1996. Song traditions in indigo buntings: origin
improvisation, dispersal, and extinction in cultural evolu-
tion. In: Ecology and Evolution of Acoustic Communication in
Birds (D.E. Kroodsma & E.H. Miller, eds), pp. 198220. Cor-
nell University, Ithaca, NY.
Payne, R.B., Woods, J.L., Siddall, M.E. & Parr, C.S. 2000. Ran-
domization analyses: mimicry, geographic variation and cul-
tural evolution of song in brood-parasitic straw-tailed
whydahs, Vidua fischeri.Ethology 106: 261282.
Peakall, R. & Smouse, P.E. 2006. GenAlEx 6: genetic analysis
in Excel. Population genetic software for teaching and
research. Mol. Ecol. Notes 6: 288295.
Peakall, R. & Smouse, P.E. 2012. GenAlEx 6.5: genetic analysis
in Excel. Population genetic software for teaching and
researchan update. Bioinformatics 28: 25372539.
Pepperberg, I.M. 1994. Vocal learning in gray parrots (Psittacus
erithacus): effects of social interaction, reference, and context.
Auk 111: 300313.
Podos, J. 2001. Correlated evolution of morphology and vocal sig-
nal structure in Darwin’s finches. Nature 409:185188.
Podos, J. & Warren, P.S. 2007. The evolution of geographic
variation in birdsong. Adv. Study Behav. 37: 403458.
Podos, J., Peters, S., Rudnicky, T., Marler, P. & Nowicki, S.
1992. The organization of song repertoires in song sparows:
themes and variations. Ethology 90:89106.
Price, T. 2008. Speciation in Birds. Roberts and Company,
Greenwood Village, Colorado.
Pytte, C.L. 1997. Song organization of house finches at the
edge of an expanding range. Condor 99: 942954.
Saranathan, V., Hamilton, D., Powell, G.V.N., Kroodsma, D.E.
& Prum, R.O. 2007. Genetic evidence supports song learning
in the three-wattled bellbird Procnias tricarunculata (Cotingi-
dae). Mol. Ecol. 16: 36893702.
Searcy, W.A. & Andersson, M. 1986. Sexual selection and the
evolution of song. Annu. Rev. Ecol. Syst. 17: 507533.
Seddon, N. 2005. Ecological adaptation and species recognition
drives vocal evolution in neotropical suboscine birds. Evolu-
tion 59: 200215.
Slabbekoorn, H. & Peet, M. 2003. Birds sing at a higher pitch
in urban noise. Nature 424: 267.
Slabbekoorn, H. & Smith, T.B. 2002. Bird song, ecology and
speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 357:493503.
Slabbekoorn, H., Jesse, A. & Bell, D.A. 2003. Microgeographic
song variation in island populations of the white-crowned
sparrow (Zonotrichia leucophrys nutalli): innovation through
recombination. Behaviour 140: 947963.
de la Torre, S. & Snowdon, C.T. 2009. Dialects in pygmy mar-
mosets? Population variation in call structure Am. J. Primatol.
71: 333342.
Tracy, T.T. & Baker, M.C. 1999. Geographic variation in sylla-
bles of house finch songs. Auk 116: 666676.
Wang, X.P., Du, M., Sun, L.X. & Li, J.L. 2005. New distribu-
tion of Chinese bulbuls (Pycnonotus sinensis)inL
ushun of
Dalian, China. Zoolog. Res. 1: 95.
Weilgart, L. & Whitehead, H. 1997. Group-specific dialects and
geographical variation in coda repertoire in south Pacific
sperm whales. Behav. Ecol. Sociobiol. 40: 277285.
White, P.J.C. 2012. Song characteristics vary clinally across an
active colonization zone in Eurasian nuthatches Sitta euro-
paea.Bird Study 59: 296302.
Whiten, A., Goodall, J., McGrew, W.C., Nishida, T., Reynolds,
V., Sugiyama, Y. et al. 1999. Cultures in chimpanzees. Nature
399: 682685.
Wiley, R.H. 1991. Associations of song properties with habitats
for territorial oscine birds of eastern north America. Am. Nat.
138: 973993.
Williams, M.D., Carey, G.J., Duff, D.G. & Xu, W.S. 1992. Autumn
bird migration at Beidaihe, China, 19861990. Forktail 7:355.
Yang, X.J. & Lei, F.M. 2008. Song structure and its microgeo-
graphic variation in the Chinese bulbul Pycnonotus sinensis.
Acta Zoolog. Sin. 54: 630639.
Zhang, Z.W., Bi, Z.L., Wang, N. & Song, J. 2003. Two new
records of birds found in Beijing. J. Beijing Normal Univ. (Nat.
Sci.) 39: 541543.
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
876 X. Y. XING ET AL.
Supporting information
Additional Supporting Information may be found in the
online version of this article:
Figure S1 Cumulative curves of song/variant/syllable
types for northern and southern populations. The trend
of curve showing how the number of new types found
rises as the number of individuals recorded increased,
indicating finite pools of northern song and syllable
types, but the other four seemed like not.
Table S1 Song sampling information for Light-vented
Bulbuls.
Data deposited at Dryad: doi: 10.5061/dryad.dm821
Received 20 September 2012; revised 30 November 2012; accepted 7
December 2012
ª2013 THE AUTHORS. J. EVOL. BIOL. 26 (2013) 867–877
JOURNAL OF EVOLUTIONARY BIOLOGY ª2013 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY
Birdsong evolution after recent expansion 877
... The distributions of many Chinese birds show a current northward expansion, probably due to climate change [46][47][48]. The mechanisms of the expansion and the genetic and behavioral characteristics of the established populations have attracted much attention [49][50][51][52][53]. In this study, we documented the distribution of the expanding populations of Brownish-flanked Bush Warbler, which have moved ...
... The distributions of many Chinese birds show a current northward expansion, probably due to climate change [46][47][48]. The mechanisms of the expansion and the genetic and behavioral characteristics of the established populations have attracted much attention [49][50][51][52][53]. In this study, we documented the distribution of the expanding populations of Brownish-flanked Bush Warbler, which have moved northward from 35 • N to 40 • N over the past decade. ...
Article
Full-text available
Simple Summary The distributions of many birds show a northward expansion in response to climate change. Brownish-flanked Bush Warbler (Horornis fortipes) is such a species, whose distribution expanded from 35° N to 40° N during the past decade. In this study, we documented the distribution of the newly established populations of this species and found evidence that it has bred at at least six sites north of its traditional range. Based on acoustic evidence, we inferred the source and expansion route of the individuals in Beijing and surrounding areas. This study is a case study of the dynamics of a bird species in the early stages of its northward expansion. Abstract Northward expansions of bird distributions have been commonly observed in the Northern Hemisphere, likely as a result of climate change. The causes and ecological impacts of such range shifts have received extensive attention, but studies on the process of range shifts are still relatively scarce. The Brownish-flanked Bush Warbler (Horornis fortipes) has expanded northward from 35° N to 40° N during the past decade. In this study, we collated 77 records of the species beyond its traditional distribution during the past ten years from citizen science data. Most of the new records were from northeast of its traditional distribution, including the North China Plain, Taihang Mountains, and Taishan Mountain, and a few records from the northern margin of the Qinling Mountains and Qinghai–Tibet Plateau. We concluded that the Brownish-flanked Bush Warbler has bred in this new area in at least six sites. The newly established populations are assumed to belong to the subspecies H. f. davidianus, which can be divided into eastern and western dialect groups based on differences in songs. Song recordings from 10 males from Beijing and its adjacent areas were collected. Bayesian analysis based on the acoustic traits indicated that these males were most likely from the western dialect area, with a posterior probability of 99.975%. Combining topographical data with the habitat preference of the species, we inferred that these individuals spread northeastward from the Qinling Mountains to Taihang Mountains, and further along the Yanshan Mountains. This study is a case study of the distribution expansion of a bird species, which reflects the dynamics of a species in the early stage of its northward expansion.
... Although there are 66 Pycnonotidae birds which reside in southern China [29], there are few records of expansion in other bulbuls [30]. Only the Light-vented Bulbul Pycnonotus sinensis (hereafter, bulbuls) has expanded its distribution naturally from the 1930s in China and has established stable breeding populations in the north over the last 40 years [31,32]. To date, it has become a dominant local bird species in some northern areas and is observed as frequently as is the Tree Sparrow Passer montanus [33]. ...
... Diet generalism is an important and well-known predictor of successful invasions [37,38] which indicates both the bulbul and finchbill have potential for expansion ability when feeding habits are considered. There was previous research that has demonstrated that bulbuls have vocal learning ability and showed innovation in breeding song after expansion to the north [31], but whether bulbuls explore more rapidly and more easily accept novel foods than finchbills when given the choice has not been tested. Furthermore, bulbuls and finchbills exhibit different group size in the nonbreeding season when in the wild, i.e., bulbuls forage and fly in groups of dozens of individuals, whereas finchbills are often observed singly or in groups of a few individuals. ...
Article
Full-text available
Animals can expand distributions in response to climatic and environmental changes, but the potential expansive ability of a source population is rarely evaluated using designed experiments. Group foraging can increase survival in new environments, but it also increases intraspecific competition. The trade-off between benefit and conflict needs to be determined. The expanding Light-vented Bulbul Pycnonotus sinensis was used as a model to test mechanisms promoting successful expansion. Social foraging and its advantages were evaluated using lab-designed feeding trials. Consuming novel foods was compared between bulbuls and a sympatric, nonexpansive relative species, the finchbill Spizixos semitorques, from native areas at both solitary and social levels. Bulbuls increased their eating times when transferred from solitary to group, whereas social context did not affect finchbills. Bulbuls were significantly more likely to eat with their companions than finchbills when in a group. Thus, exploring food resources in a bulbul source population was facilitated by social context, indicating that social foraging is an important means by which birds successfully expand and respond to environmental changes. This research increases understanding of successful expansion mechanisms and will consequently help predict invasive potentials of alien species.
... Moreover, pitch and duration of bird songs can show different or even opposite correlations with temperature, precipitation, and seasonality (Lawson and Weir 2014), thus we should expect that passerine songs do not vary along the temperature cline of a North-South gradient but also along gradients of other climate variables, or aspects related to the environment such as altitude, habitat structure, or human made environmental changes. Furthermore, vocal trait-shifts can arise from recent range expansions (Xing et al. 2013), which may apply to the three Thai-Malay bulbul species, indicated by late Pleistocene splits followed by Holocene range expansion (Dejtaradol et al. 2016). ...
... Research has shown that the diversity of rodents exhibited notable alterations with ancient climate change (Li et al., 2022). The apparent alteration of Pleistocene climates may have contributed to the expansion and divergence of the species (Song et al., 2013;Tagliacozzo et al., 2016;Xing et al., 2013). According to our analysis, the origin of Figure 5b4). ...
Article
Full-text available
The climbing mouse is a rare, small mammal listed as an endangered species on the China species red list. Molecular phylogenetic analyses and the evolutionary history of the genus remain unexplored because of the extreme difficulty in capturing individuals and their narrow distribution. Here, we collected 44 specimens, sequenced one mitochondrial and eight nuclear genes, and integrated morphological approaches to estimate phylogenetic relationships, delimit species boundaries, and explore evolutionary history. Molecular analyses and morphological results supported the validity of these four species. Here, we describe two new species, Vernaya meiguites sp. nov. and Vernaya nushanensis sp. nov., and recognize Vernaya foramena , previously considered a subspecies of Vernaya fulva , as a valid species. The estimated divergence time suggests that the climbing mouse began to diversify during the Pliocene (3.36 Ma).
... However, it has rapidly expanded its distribution range northward during the past few decades. By the 1980s, it crossed the Yangtze River and colonized the wide Palearctic ecozones to become residents in northeastern China by the 2000s (Figure 1) (Williams 1992;Zhang 2003 A c c e p t e d M a n u s c r i p t found significant divergence in vocalization rather than in genetics between northward expanding populations and original populations of light-vented bulbul (Song et al. 2013;Xing et al. 2013). However, it is not known whether light-vented bulbul exhibits metabolic and microbial changes in rapidly expanding populations acclimated to colder environments. ...
Article
Full-text available
Endotherms recently expanding to cold environments generally exhibit strong physiological acclimation to sustain high body temperature. During this process, gut microbes likely play a considerable role in host physiological functions, including digestion and thermogenesis. The Light-vented bulbul Pycnonotus sinensis represents one of such a species. It used to be restricted to the Oriental realm, but expanded its distribution range north to the Palearctic areas during the past few decades. Here, we explored the seasonal dynamics of the resting metabolic rate (RMR) and microbiota for local and newly colonized populations of the species. Our results showed that the mass-adjusted RMR and body mass were positively correlated with latitude variations in both seasons. Consistently, the gut microbiota showed corresponding variation to the northern cold environments. In the two northern populations, the alpha diversity decreased compared with those of two southern populations. Significant differences were detected in dominant phyla, such as Firmicutes, Bacteroidetes, Proteobacteria and Desulfobacterota in both seasons. The core microbiota showed geographic differences in the winter, including the elevated relative abundance of 5 species in northern populations. Finally, to explore the link between microbial communities and host metabolic thermogenesis, we conducted a correlation analysis between microbiota and mass-adjusted RMR. We found that more genera were significantly correlated with mass-adjusted RMR in the wintering season compared to the breeding season (71 versus 23). These results suggest that microbiota of the lighted-vented bulbul linked with thermogenesis in diversity and abundance under northward expansion.
... As the rare successful northward expanded colonizer, the light-vented bulbul provides a great model for understanding the underlying adaptive mechanisms of northward expansion in birds [17,18]. Our previous studies have found signi cant divergence in vocalization rather than in genetics between northward expanding populations and original populations of light-vented bulbul [19,20]. However, it is not known whether light-vented bulbul exhibits metabolic and microbial changes in rapidly expanding populations acclimated to colder environments. ...
Preprint
Full-text available
Background Endotherms recently expanding to cold environments generally exhibit strong physiological acclimation to sustain high body temperature. During this process, gut microbes likely play a considerable role in host physiological functions, including digestion and thermogenesis. Light-vented bulbul (Pycnonotus sinensis) represents one of such a species. It used to be restricted to the Oriental realm, and expanded its range to the Palearctic during the past few decades. Results We explored the seasonal dynamics of the resting metabolic rate (RMR) and gut microbiota for local and newly colonized populations of light-vented bulbul. Our results showed that light-vented bulbul exhibited physiological changes during northern expansion. Specifically, the RMR was positively correlated with latitude in the winter (p = 0.0011, r = 0.33). Body mass showed a significant positive correlation with latitude in the breeding (p = 0.045, r = 0.27) and wintering seasons (p = 0.012, r = 0.25), corresponding to Bergmann’s rule. Consistently, the gut microbiota showed corresponding variation to the northern cold environments. In the two northern populations, the alpha diversity decreased compared with those of two southern populations. Significant differences were detected in dominant phyla, such as Firmicutes, Bacteroidetes, Proteobacteria and Desulfobacterota in the breeding and wintering seasons (p < 0.05). The core microbiota showed geographic differences in the winter, including the elevated relative abundance of 5 species (Alistipes shahii, Bacteroides stercoris, Bacteroides vulgatus, Parabacteroides merdae and Bacteroides spp.) in northern populations. Finally, to explore the link between microbial communities and host metabolic thermogenesis, we conducted a correlation analysis between microbiota and RMR. We found that more genera were significantly correlated with RMR in the wintering season than that in the breeding season (71 versus 23). Conclusions This study suggested that key microbiota linked with thermogenesis to push lighted-vented bulbul on a path toward the north.
... Therefore, along with morphological and genetic evidence, birdsong divergences are commonly used as an essential basis of taxonomy [14,15]. Because birdsong evolves under both natural and sexual selection, it is commonly considered to have species- [16,17], subspecies- [18], and population-specific [19,20] signals resulting from morphological divergence [21,22], adaptation to local acoustic environments [23,24], or stochastic processes, such as cultural drift [25,26]. Many cryptic new bird species, subspecies, and taxa have been proposed and tested according to their song variations, combined with genetic and morphological traits [27][28][29], and acoustic divergences are considered essential factors in investigations of taxonomic status or for resolving phylogenetic issues in ornithology [30,31]. ...
Article
Full-text available
The critically endangered Yellow-breasted Bunting has undergone population collapse globally because of illegal hunting and habitat deterioration. It was listed as critically endangered (CR) by the International Union for Conservation of Nature (IUCN) in 2017 and designated a Class I (highest level) national conservation bird species in China in 2021. Birdsong in the breeding season is the main communicative signal under sexual selection, and song variations have long been considered critical evidence of divergence among subspecies or populations. We compared the songs of 89 males from 18 populations to test subspecies taxonomy. We found that songs of the Yellow-breasted Bunting Emberiza aureola are subspecies specific and that three subspecies can be clearly discriminated by song divergences. Moreover, an analysis of multiple vocal traits supports the claim that insularis is distinct from aureola and ornata. Finally, at the geographic population level, populations can be clearly classified in accordance with the three subspecies, although the aureola population in Xinjiang, China is differentiated from other populations of the same subspecies. The results of this study demonstrate that all populations and subspecies are unique and should be protected to maintain intraspecies song diversity. In addition, several specific populations, such as insularis populations in Japan and the Xinjiang, China population of aureola, need to be paid special attention to prevent the extinction of unique or local taxa.
... Instead of copying the range of sounds to which they might be exposed, juvenile oscines preferentially learn the vocalizations characteristic of their species [11] or subspecies [12], and variations that arise during song evolution may be constrained or redirected by genetically based mechanisms such as physiological song production abilities [7]. Variation may also be limited within small colonizing or isolated populations that arise from genetically depauperate founder populations such as those on islands or in recently deglaciated areas populated from glacial refugia [13][14][15][16]. Populations that become geographically isolated undergo random cultural drift [17], and the songs of isolates may ultimately evolve to the extent that conspecifics in other populations alter their responses. ...
Article
Full-text available
Louisiana Waterthrush (Parkesia motacilla) is a familiar singer in the Western Hemisphere family Parulidae, yet apparent geographic variations in its song and potentially related causal mechanisms have not received detailed examination in previously published studies. Here, we analyzed song pattern variations of 651 Louisiana Waterthrush singers in audio spectrogram recordings obtained from our field work and publicly accessible bioacoustics archives. Visual and auditory assessment of the introductory note sequence of each song identified three distinct song types (A, B, and C) and most of the songs were assigned to one of these types. Linear Discriminant Analysis and Random Forest methods were used to verify the assignments and showed strong agreement for Type A with slightly less agreement on Types B and C. User error rates (proportion of the Linear Discriminant Analysis classifications that were incorrect) were low for Types A and B, and somewhat higher for Type C, while producer error rates (proportion of the song type for which the Linear Discriminant Analysis was incorrect) were somewhat higher for Types A and C than the minimal levels achieved for Type B. Our findings confirmed that most between-individual variation was in the number of notes and note sequence duration while most within-individual variation resulted from the percent of downstrokes. The location of each singer was plotted on a map of the breeding range and results suggested the song types have large-scale discrete geographic distributions that co-occur in some regions but not range-wide. Evaluation of the distributions provided tentative support for a hypothesis that two of the song types may independently exhibit congruence with the geographic extent of Pleistocene glacial boundaries and the third song type may be distinguished by a lack of congruence, but further investigation is needed to elucidate whether the song variations represent subpopulations with three separate evolutionary histories.
Article
Full-text available
Mountains are the world's most important centers of biodiversity. The Sino-Himalayan Mountains are global biodiversity hotspot due to their extremely high species richness and endemicity. Ample research investigated the impact of the Qinghai–Tibet Plateau uplift and Quaternary glaciations in driving species diversification in plants and animals across the Sino-Himalayan Mountains. However, little is known about the role of landscape heterogeneity and other environmental features in driving diversification in this region. We utilized whole genomes and phenotypic data in combination with landscape genetic approaches to investigate population structure, demography, and genetic diversity in a forest songbird species native to the Sino-Himalayan Mountains, the red-billed leiothrix (Leiothrix lutea). We identified 5 phylogeographic clades, including 1 in the East of China, 1 in Yunnan, and 3 in Tibet, roughly consistent with differences in song and plumage coloration but incongruent with traditional subspecies boundaries. Isolation-by-resistance model best explained population differentiation within L. lutea, with extensive secondary contact after allopatric isolation leading to admixture among clades. Ecological niche modeling indicated relative stability in the extent of suitable distribution areas of the species across Quaternary glacial cycles. Our results underscore the importance of mountains in the diversification of this species, given that most of the distinct genetic clades are concentrated in a relatively small area in the Sino-Himalayan Mountain region, while a single shallow clade populates vast lower-lying areas to the east. This study highlights the crucial role of landscape heterogeneity in promoting differentiation and provides a deep genomic perspective on the mechanisms through which diversity hotspots form.
Article
We investigated cultural evolution in the song of the introduced North Amer-ican population of the Eurasian Tree Sparrow (Passer montanus), derived from 12 pairs brought from Germany in 1870. These birds were liberated at St. Louis, Missouri, and spread into Illinois. Cultural evolution is described here in terms of the processes of population differentiation where the song meme was the unit of transmission. The distribution of song syllable memes in each meme pool fit a null hypothesis of a neutral model with an equilib-rium between mutation, migration, and drift, indicating that the memes are functionally equivalent. The introduced and ancestral (German) populations showed marked divergence in the level of meme sharing. The small size of the founding North American population, the loss of genetic diversity there, and the relative susceptibility of meme pools to founder effects suggest that much of the reduction in sharing of syllable types occurred during the founding event. Because memes also are susceptible to extinction due to drift, memes were probably lost in both populations as a result of random memetic drift. Meme diversity in Illinois was comparable with that in Germany, suggesting a large mutational input into the former population following its founding. Estimates of mutational divergence based on the frequencies of song memes in meme pools showed more population structure in Illinois than in Germany. There also was less meme flow among meme pools in Illinois than in Germany. These results suggest that there were a series of founding events during the colonization of North America.
Article
An earlier study failed to find dialects in the songs of male Gambel's White-crowned Sparrows (Zonotrichia leucophrys gambelii) in Alaska. We recorded songs of males at five localities over a much greater portion of the subspecies' range, spanning 2250 km east to west and 1650 km north to south. On this scale, distinct geographical variants are evident, based on the song's terminal phrase and the fine details of other phrases. In White-crowned Sparrows, the extent of dialects is apparently positively correlated with the distance migrated by the subspecies; a demographic variable such as survivorship or natal philopatry likely results in this link. Variación Geográfica a Gran Escala en el Canto de Zonotrichia leucophrys gambelii Resumen. Un estudio anterior no encontró dialectos en los cantos de machos de Zonotrichia leucophrys gambelii en Alaska. Nosotros grabamos cantos en cinco localidades a través de un área de 2250 km este-oeste por 1650 km norte-sur, que abarca una gran parte del área de distribución de la subespecie. A esta escala, es evidente una clara variación geográfica, basada en la parte terminal de los cantos, y en detalles de las otras frases. En esta especie, la extension geográfica de los dialectos aparentemente está correlacionada de manera positiva con la distancia de migración de las subespecies. Esta correlación tal vez sea producto de factores demográficos como la supervivencia o de filopatría.
Article
I investigated geographic variation in a parrot vocalization to obtain an understanding of cultural population differentiation and exchange between hybridizing taxa. The flight calls of Ringneck Parrots (Barnardius zonarius) were tape recorded in Western Australia within and outside the zone of overlap and hybridization between the Port Lincoln (B. z. zonarius) and Twenty-eight (B. z. semitorquatus) subspecies. Measured variables distinguished the Twenty-eight call from those in the overlap populations. Although birds in typical Twenty-eight plumage were present in the overlap zone, no Twenty-eight flight calls were found, suggesting convergence by immigrants. Populations within the hybrid zone also were acoustically differentiated as dialects associated with roosting areas. Observations on the social behavior of the birds indicated that this call functions in coordination of movements of the mated pair. Roost-specific dialects might aid pairs in finding each other in the event of separation during the day's foraging activity.
Article
We investigated cultural evolution in populations of common chaffinches (Fringilla coelebs) in the Atlantic islands (Azores, Madeira, and Canaries) and neighboring continental regions (Morocco and Iberia) by employing a population-memetic approach. To quantify differentiation, we used the concept of a song meme, defined as a single syllable or a series of linked syllables capable of being transmitted. The levels of cultural differentiation are higher among the Canaries populations than among the Azorean ones, even though the islands are on average closer to each other geographically. This is likely the result of reduced levels of migration, lower population sizes, and bottlenecks (possibly during the colonization of these populations) in the Canaries; all these factors produce a smaller effective population size and therefore accentuate the effects of differentiation by random drift. Significant levels of among-population differentiation in the Azores, in spite of substantial levels of migration, attest to the differentiating effects of high mutation rates of memes, which allow the accumulation of new mutants in different populations before migration can disperse them throughout the entire region.
Article
Songs of Darwin's finches were studied on the Galápagos Island of Daphne Major from 1976 to 1995. A single, structurally simple, and unvarying song is sung throughout life by each male of the two common species, Geospiza fortis (medium ground finch) and G. scandens (cactus finch). Songs of the two species differ strongly in quantitative features, and individual variation among males is much broader in G. fortis than in G. scandens. Although there are exceptions, songs of sons strongly resemble the songs of their fathers. They also resemble the songs of their paternal grandfathers, but not their maternal grandfathers, indicating that they are culturally inherited and not genetically inherited. Female G. fortis display a tendency to avoid mating with males that sing the same type of song as their father. They also avoid mating with males that sing heterospecific song, with very rare exceptions. Thus song, an evolving, culturally inherited trait, is an important factor in species recognition and mate choice. It constrains the mating of females to conspecifics, even when there is no genetic penalty to interbreeding, and thus may play a crucial role in species formation by promoting genetic isolation on secondary contact. The barrier is leaky in that occasional errors in song transmission result in misimprinting, which leads to a low incidence of hybridization and introgression. Introgression slows the rate of postzygotic isolation, but can produce individuals in novel genetic and morphological space that can provide the starting point of a new evolutionary trajectory.