Current Biology 19, 2097–2101, December 29, 2009 ª2009 Elsevier Ltd All rights reservedDOI 10.1016/j.cub.2009.10.061
Contemporary Evolution of Reproductive
Isolation and Phenotypic Divergence
in Sympatry along a Migratory Divide
Gregor Rolshausen,1Gernot Segelbacher,2
Keith A. Hobson,3and H. Martin Schaefer1,*
1Department of Evolutionary Biology and Animal Ecology,
Faculty of Biology, University of Freiburg, Hauptstrasse 1,
D-79104 Freiburg, Germany
2Department of Wildlife Ecology and Management, University
of Freiburg, Tennenbacher Strasse 4, D-79106 Freiburg,
3Environment Canada, 11 Innovation Boulevard, Saskatoon,
SK S7N 3H5, Canada
Understanding the influence of human-induced changes on
the evolutionary trajectories of populations is a fundamental
problem [1, 2]. The evolution of reproductive isolation in
sympatry is rare, relying on strong selection along steep
ecological gradients [3–7]. Improved wintering conditions
owing to human activities promoted the recent establish-
ment of a migratory divide in Central European blackcaps
(Sylvia atricapilla) [8, 9]. Here, we show that differential
migratory orientation facilitated reproductive isolation of
sympatric populations within <30 generations. The genetic
divergence in sympatry exceeds that of allopatric blackcaps
separated by 800 km and is associated with diverse pheno-
typic divergence. Blackcaps migrating along the shorter
northwestern route have rounder wings and narrower beaks
and differ in beak and plumage color from sympatric south-
west-migrating birds. We suggest that distinct wing and
resulting from divergent, multifarious selection regimes
during migration. We hypothesize that restricted gene flow
accelerates the evolution of adaptive phenotypic divergence
toward the contrasting selection regimes. Similar adaptive
processes can occur in more than 50 bird species that
recently changed their migratory behavior [10, 11] or in
species with low migratory connectivity. Our study thus
illustrates how ecological changes can rapidly drive the
contemporary evolution of ecotypes.
Results and Discussion
There is growing recognition that ecological and evolutionary
dynamics can occur on the same timescales and thereby influ-
ence each other [12–14]. A good example is the contemporary
evolution of a migratory divide in Central European blackcaps
(Sylvia atricapilla) that was favored by warmer climate and
increasing food supply provided by humans in the United
Kingdom [8, 9]. Part of the blackcap population breeding in
southern Germany and Austria established a new migratory
direction toward the northwest (NW) in the 1960s. The new
wintering areas are 1200–1800 km north of the traditional
western Mediterranean overwintering sites of sympatrically
breeding southwest (SW)-migrating blackcaps [8, 9]. Within
less than 30 generations, the proportion of NW-migrating
blackcaps breeding in southern Germany has increased to
approximately 10% . Crossbreeding experiments estab-
lished that hybrids between birds with the two migratory
directions migrate in an intermediate direction and that the
inheritance pattern is consistent with migratory orientation
being controlled by one or only a few major genes . Further
experiments showed that migratory behavior in blackcaps can
evolve within a few generations owing to substantial additive
genetic variation for migratory traits . Blackcaps form
seasonal pair bonds upon arrival at the breeding grounds.
Differences in migratory orientation lead to temporal segrega-
tion upon spring arrival and, consequently, assortative mating
between birds with the same migratory orientation [8, 17]. As
such, divergence in migratory orientation could potentially
lead to premating isolation mediating the evolution of
ecotypes and, possibly, even incipient ecological speciation
in the blackcap.
Evidence for migratory behavior promoting speciation in
birds is limited. Previous studies on avian populations with
distinct migratory orientation reported little genetic diver-
gence in neutral markers [18, 19], and, although there are
some possible exceptions [20, 21], divergence in sympatry is
thought to be rare in birds [22, 23]. Given that migratory birds
are the prime example of highly mobile organisms, the lack of
genetic diversification might be caused by interbreeding
among different populations. Also, it may reflect the limited
genetic response of populations that experience differential
selection along a single ecological dimension . Here, we
investigated potential adaptive divergence in the contempo-
rary evolution of migratory behavior of the blackcap. We
used stable isotope analysis to assign sympatric populations
to their wintering quarters and measured various phenotypic
traits as well as neutral genetic differentiation to determine
whether divergent selection occurs along one or multiple
tory birds, previous analyses of mitochondrial DNA (mtDNA)
haplotypes revealed no genetic structure among Western
European blackcaps indicating that any differences in migra-
tory behavior are of very recent origin .
The recent establishment of a NW migratory route in Central
European blackcaps resulted in genetic divergence of neutral
markers from sympatrically breeding SW migrants within <30
affiliation for individual genotypes  assigned more than
85%of theindividuals correctly totheirrespectivepopulations
(Figure 1). The presence of two distinct genetic clusters was
supported with the software STRUCTURE  (see Figure S1
available online), but STRUCTURE did not assign individuals
to their source population. This result was expected because
STRUCTURE is not a powerful tool when genetic differentia-
tion is slight. Importantly, the low but significant genetic diver-
gence in sympatry (FST= 0.008; p < 0.005) exceeds the genetic
divergence of these populations and an allopatric population
of SW migrants from northern Germany separated by 800 km
(FST= 0.0001–0.004; all p > 0.5; Table 1). The genetic diver-
gence in sympatry was consistently found in different years
and different sampling sites (Table S1). Interestingly, genetic
differences are larger within years than when years arepooled,
a result that corroborates our conclusions on the genetic
divergence in sympatry.
We thus conclude that, owing to assortative mating, the
evolution of a migratory divide has initiated reproductive isola-
tion among the sympatric blackcap populations. Drift seems
unlikely to be a powerful mechanism creating genetic diver-
gence within <30 generations or even <60 generations if the
NW migratory orientation evolved 100 years ago but remained
undetected because few individuals were initially involved.
More likely, the genetic divergence might be attributable to
founder effects because NW migrants had a higher proportion
of homozygotic individuals than SW migrants (G.R., unpub-
A drift-immigration equilibrium between NW and SW
migrants is unlikely owing to the recent origin of reproductive
cate the current level of gene flow. The migratory divide might
thus either cause further divergence between sympatric pop-
ulations or collapse owing to hybridization between birds of
different migratory direction.
Analysis of molecular variance (AMOVA) of five blackcap
populations from Europe with distinct migratory strategies
(Figure 2) indicated low but significant levels of genetic struc-
turing (overall FST= 0.016; 95% confidence interval = 0.005–
0.028; p = 0.00228, AMOVA). Pairwise FST comparisons
revealed the strongest genetic differentiation between SE
migrants from Rybachy, Russia and the other populations
(FST= 0.037–0.050; all p < 0.00001). This differentiation reflects
the secondary contact zone of populations from different
Pleistocene refugia where a migratory divide separates SW
and SE migrants at 12?E–13?E in Central Europe . Similarly,
sedentary blackcaps from southern Spain differed from the
three migratory Central European populations (FST= 0.012–
0.020; all p % 0.005). Our results suggest that genetic diver-
gence in blackcap populations is determined mainly by migra-
tory behavior (Mantel test of genetic and geographic distance:
r = 0.504, p = 0.255).
Apart from the well-known examples of introduced species
and populations, this is among the few studies to provide
evidence that ecological changes associated with human
activities are strong enough to initiate evolution of reproduc-
tive isolation among sympatric populations. The alternative
hypothesis of an allopatric origin of the NW-migrating pop-
ulation is not supported by our data and previous genetic
data from other European blackcap populations . Further-
more, this hypothesis is unlikely because NW-migrating black-
caps were not recorded in Europe or elsewhere prior to the
We found divergence in various phenotypic traits among
sympatric SW and NW migrants. Blackcaps migrating along
the shorter NW route (w1090 km) had rounder wings than
birds traveling the longer SW route (w1640 km). The observed
difference in wing shape among sympatric populations is
consistent with the Europe-wide pattern that a shorter migra-
tory route is associated with a decrease in wing pointedness
(Holynski index) of blackcaps (Figure 3). We consider founder
effects as unlikely to have caused the difference in wing shape
because NW migrants would have then originated from a more
southern population with an originally shorter migratory route
(resulting in a longer current NW route), a pattern that is not
confirmed by ringing records. Birds from both populations
molt their wing feathers in a common garden situation on the
Table 1. Pairwise FSTComparisons between Five Different Blackcap Populations from Europe
Southern Germany Southern GermanySpain Northern GermanyRussia
n142 5549 2720
Pairwise FSTcomparisons are shown below the diagonal, standardized FSTcomparisons above it. We genotyped 293 individuals that included a random
sample of the SW migrants (comprising 50% of these birds) and all NW migrants except for 6 birds that were excluded owing to insufficient DNA material.
Data are based upon ten microsatellites . *p < 0.005; **p < 0.001; adjusted nominal level (5%) for multiple comparisons: 0.005.
−60 −55−50−45 −40−35−30−25
Figure 1. Log-Log Plot of the Likelihood of Genetic Assignment to the
Source Population in Sympatric Blackcaps
We used multilocus assignment of individual birds without any a priori infor-
mation other than isotope signature. Black circles (d) indicate northwest
(NW) migrants; white circles (B) indicate southwest (SW) migrants. The
dashed line depicts 1:1 correspondence. Note that the two populations
are genetically similar because a large proportion of individuals cluster
close to the 1:1 correspondence line.
Current Biology Vol 19 No 24
necessarily molt at the same time, it is unlikely that different
environmental conditions during molt alone determine the
differences in wing shape. Rather, we suggest that incipient
reproductive isolation of NW and SW migrants has facilitated
Geographic distance (km)
Genetic distance: FST/(1-FST)
Figure 2. Genetic Distance among Blackcap
Populations Is Primarily a Function of Migratory
Orientation Rather Than Geographic Distance
Genetic and geographic distances are illustrated
relative to the SW-migrating blackcaps from
southern Germany (gray dot). The respective
migratory distances are denoted on the z axis.
The map of Europe shows the breeding grounds
of the sampled populations and the two pro-
nounced migratory divides in the blackcap. The
dotted line corresponds to the migratory divide
at 12?E–13?E separating SE- from SW-migrating
populations . The arrows indicate the distinct
migratory orientations in the recently established
Central European migratory divide. ‘‘W. haven’’
adaptive phenotypic divergence toward
the new migratory route.
NW and SW migrants also differ in
beak morphology, but not in tarsus
length (p > 0.4). Beak shape differed
among populations and sexes (beak
PC2: F = 12.32, p < 0.001), and there
was a sex effect in beak size (beak
PC1: F = 10.05, p < 0.01; nNW migrants=
61, nSW migrants= 264, type II analysis of variance): females of
both populations had larger beaks than males. Divergence in
beak shape in birds can reflect adaptation toward differential
exploitation of food resources , a scenario that might
also hold for the blackcap. In the Mediterranean area, fruits
make up 95% of the diet of blackcaps , whereas blackcaps
wintering in Britain are known to feed primarily on seeds and
fat at garden feeders . Given that gape width is the main
constraint determining the size of fruits that a bird can exploit
, we hypothesize that the relatively broader bills of SW
migrants are adapted to a more specialized, frugivorous diet.
In contrast, the relatively narrower and longer beaks of NW
migrants likely reflect a more generalistic feeding behavior at
Analysis of beak and plumage colors revealed significant
differences between NW and SW migrants in avian visual color
space. The beak and the feathers of the back were relatively
browner (with a tinge of olive in males) in NW migrants,
whereas they were relatively greyer in SW migrants indepen-
dent of sex or age (Table S2). The browner coloration of NW
migrants suggests a different ratio of eumelanin and pheome-
lanin. Alternatively, and unlike the differences in wing shape,
differences in feather color may be explicable by differential
the color differences because blackcap populations wintering
farther north renew fewer feathers during the prenuptial molt
than those wintering further south . Unlike feathers, beaks
constitute a fast-responding tissue sensitive to fluctuation in
abiotic stress, health, and diet . Differences in beak color
might therefore reflect various divergent ecological con-
straints that are partly associated with distinct foraging in
both wintering areas.
In total, five traits that were uncorrelated among each other
(wing morphology, beak shape, back plumage color, head
plumage color, and bill color; all p > 0.2; see Table S2) differed
between the two populations. The diverging traits correspond
to multiple ecological dimensions: wing shape is associated
151050 500 5000
Migration distance (km)
Figure 3. Wing Pointedness as Measured by the Holynski Index Changes
According to Migratory Distance
Short-distance migrants (<500 km) or sedentary blackcaps (; n = 99) from
the Mediterranean area (additional data from ) have rounder wings than
long-distance migrants (1800–5000 km, ; n = 315, meanHolynski= 0.52 6
0.009 standard error). NW-migrating blackcaps (; n = 61) have rounder
wings than sympatric blackcaps that migrate along the longer SW route
(; n = 264; F = 6.23, p < 0.05, type II analysis of variance; see Figure S2
for the distribution of the Holynski index among the two sympatric popula-
tions). Wing traits have a heritability of >0.6 in southern German blackcaps
. Note the logarithmic scale of the x axis. Means and standard errors are
Contemporary Evolution along a Migratory Divide
with migratory distance, beak shape is associated with
foraging, and plumage coloration is associated with molting
strategies or melanin synthesis.
Because selection on and the heritabilities of the five traits
probably differ, distinct evolutionary mechanisms are likely
to contribute to the phenotypic divergence among sympatric
blackcaps. First, reproductive isolation might facilitate adap-
tive phenotypic divergence in response to contrasting, multi-
farious selection regimes associated with each migratory
route. In this case, divergence is adaptive and evolved owing
to the establishment of the migratory divide. We suggest that
this scenario is particularly likely for divergence in wing and
beak shape. Second, phenotypic differences might have
been caused by drift following incipient reproductive isolation.
Third, founder effects might explain phenotypic differences
that would have been present before—and might have even
facilitated—the evolution of the migratory divide. Because an
in these traits.
Even if we assume that divergence evolved after the evolu-
tion of the migratory divide, microevolutionary rates (mea-
sured in haldanes) are high, but not exceptionally so. The rates
of phenotypic divergence in wing morphology (hp(1.43)= 0.014)
and beak shape (hp(1.43)= 0.020) in blackcaps would be at the
upper limit of the third quartile of studies on microevolutionary
rates summarized by Hendry etal. (; quartiles from haldane
database: first: 0.002; second: 0.006; third: 0.014). If the migra-
tory divide is twice as old as the first sightings of blackcaps
wintering in the United Kingdom suggest, the microevolu-
tionary rates would be lower (Table S3) but still above the
median given in .
It is unknown whether selection will lead to further diver-
gence among NW and SW migrants. We note, however, that
the evolution of differential plumage coloration in NW and
SW migrants provides a proximate mechanism for reinforce-
ment allowing for the evolution of active recognition and
further premating isolation. If the intermediate migratory
routes of hybrids lead them to unsuitable wintering grounds,
mate selection according to migratory orientation could over-
ride assortative mating as a by-product of differential migra-
We suggest that alternative migratory behavior can initiate
reproductive isolation in sympatry, leading to the evolution
of genetically distinct ecotypes. We hypothesize that the
ecotypes experience different selection regimes that are
temporarily restricted to an allopatric phase during the annual
cycle but that can entail significant carryover effects upon the
sympatric breeding phase. In this scenario, a single trait,
migratory orientation, initially restricts gene flow but concom-
itantly results in divergent multifarious selection during migra-
tion. Adaptive divergence might then secondarily lead to
a further reduction in gene flow and—owing to positive feed-
gence—a scenario of incipient ecological speciation.
Theoretical considerations predict that if multifarious selec-
tion causes divergence, the resulting widespread evolutionary
response might be more effective in driving speciation than
the more limited response caused by single-trait selection.
Because migratory orientation in the blackcap can potentially
result in subsequent multifarious selection upon other, uncor-
relatedtraits, the distinction between single-traitselectionand
multifarious selection might be less pronounced than recently
Ourstudyillustrates theprofound impactofhumanactivities
on the evolutionary trajectory of populations. Food provided
during winter in the United Kingdom contributed to the
establishment of the NW migratory route that would probably
have been maladaptive previously. Because anthropogenic
changesoccur in general concomitantly on multiple ecological
dimensions, they can result in multifarious selection upon
multiple traits and thereby drive contemporary evolution.
We propose that the evolution of migratory ecotypes is
a subtle but potentially widespread process that improves
adaptive responses toward the diverse ecological settings
that migrants experience. We predict that the evolution of
migratory ecotypes occurs in species with low migratory
connectivity where individuals disperse to different overwin-
tering quarters or habitats.
We caught birds in four regions. In spring 2006–2008, we caught blackcaps
upon arrival at their breeding grounds in southern Germany in Radolfzell
(47?450N 08?590E) and Freiburg (48?000N 07?510E). These birds comprised
SW migrants (main migratory direction southern Spain) and NW migrants
(wintering in Britain) that were caught at each site within an area of w50
hectares in the same mist nets. We also sampled sedentary blackcaps
caught in winter 2006–2008 near Sevilla, Spain (37?390N 5?350W); northern
German blackcaps caught in summer 2007 at their breeding grounds in
Wilhelmshaven (53?310N 08?070E); and blackcaps caught in spring/summer
2007 at Rybachy, Russia (55?090N 20?510E). Blackcaps from Wilhelmshaven
are SW migrants traveling to the Mediterranean and to sub-Saharan Africa,
whereas blackcaps from Rybachy migrate along the eastern route to Africa
. We calculated the number of generations separating the sympatric
populations by dividing the time since the appearance of the migratory
We recorded the following phenotypic traits of blackcaps from southern
Germany and Sevilla: lengths of tarsus and wing; lengths of all long prima-
ries and the first secondary (P1–P9, S1); length, width, and height of beak;
plumage coloration of back, breast, and head feathers; and beak coloration.
Variation in beak morphology was analyzed via a principal component
analysis (PCA) on the beak measurements. PC1 was interpreted as
beak size (50% variance explained; loadings: length: 20.31, width: 20.64,
height: 20.69) and PC2 as beak shape (33% variance explained; loadings:
length: 20.91, width: 0.39, height: 0.04). Moreover, we obtained 2–4 distal
claw sections from each individual for individual assignment via stable
isotope analysis of deuterium (see Figure S3).
We measured plumage and beak coloration with an AvaSpec 2048 spec-
trometer and AvaLight-DH-S deuterium halogen lamp (Avantes). We took
five measurements per body part per bird and averaged spectra in 5 nm
intervals from 300 to 700 nm. Using an avian eye model , we modeled
the probability of photon catches of the four avian cone types used for color
DNA was extracted from blood samples with a DNeasy Blood and Tissue Kit
(QIAGEN). Locus characteristics, amplification of loci, and polymorphic
information content were as described in  and Table S4. We conducted
calculations of pairwise FST, partitioning of molecular variance (AMOVA),
and individual genotype-population assignment. To account for variation
in heterozygosity within populations that differ in degree of isolation ,
we used a standardized measure of differentiation scaling FSTinto the
same range (0–1) for all levels of variation among loci and populations
. We report the standardized measure together with the original FST
values. Moreover, we tested for robustness of our set of ten loci because
our estimates may be biased by low sample sizes relative to the number
of alleles (Table S5).
Supplemental Data include Supplemental Experimental Procedures, five
tables, and three figures and can be found with this article online at http://
Current Biology Vol 19 No 24
We thank W. Salzburger, G. Evanno, and two referees for many helpful
comments; N. Chernetsov (Biological Station Rybachy) and D. Serrano
(Sevilla) for sampling blackcaps in their respective areas; C. Catoni and
F. Bairlein for collection of data from blackcaps from Wilhelmshaven;
R. Bloch, M. Lucas, K. Stournaras, S. Vetter, and F. Wehrle for assistance
with field work; and L.I. Wassenaar for assistance with isotope analyses.
This work was supported by Deutsche Forschungsgemeinschaft grant
Scha 1008/6-1. Data were collected under Regierungspra ¨sidium Freiburg
permission number 55-8853.17/0.
Received: July 24, 2009
Revised: October 16, 2009
Accepted: October 16, 2009
Published online: December 3, 2009
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Contemporary Evolution along a Migratory Divide