J. Zool., Lond. (1999) 247, 53±64 # 1999 The Zoological Society of London Printed in the United Kingdom
Dynamics of a clinal hybrid zone and a comparison with island
hybrid zones of ¯ycatchers (Ficedula hypoleuca and F. albicollis)
G.-P. Sñtre1*, M. KraÂl2, S. BuresÏ3 and R. A. Ims1
1
Department of Biology, Division of Zoology, University of Oslo, P. O. Box 1050 Blindern, N-0316 Oslo, Norway
Forestry Commission, ValsÏuv DuÊl 499, 783 86 Dlouha LoucÏka, Czech Republic
3
Laboratory of Ornithology, Palacky University, TrÏ. Svobody 26, 771 46 Olomouc, Czech Republic
2
(Accepted 22 April 1998)
Abstract
Breeding data for pied ¯ycatchers Ficedula hypoleuca and collared ¯ycatchers F. albicollis, from 47
localities in the Czech Republic and Slovakia, were analysed. We show that co-existence and hybridization
were mainly restricted to a rather narrow, latitudinal cline. The distribution of the two ¯ycatchers coincides
with topography and habitat, collared ¯ycatchers dominating in warmer habitats than pied ¯ycatchers.
Maintained co-existence within the same locality was the exception rather than the rule and most matings
occurred in allopatry. In sympatry hybridization occurred at a frequency that was much lower than
expected from random mating. Hybrids had low hatching success but some hybrids were apparently fertile.
Shortage of conspeci®c mates may explain why individual birds engage in mixed species pairs. The
proportion of pied ¯ycatchers that was involved in mixed pairs was high and increased with decreasing
relative frequencies of pied ¯ycatchers in the population. The proportion of collared ¯ycatchers involved in
mixed pairs was low, re¯ecting the higher relative frequency of this species in most mixed populations.
Comparisons suggest that fewer hybrids are breeding in the Central European, clinal hybrid zone than in
the isolated hybrid zones of the Baltic Isles. Moreover, hybrid fertility was apparently higher in the island
zones than in the clinal zone. We suggest that more extensive introgression in the isolated island
populations has resulted in an increase in hybrid ®tness by an accumulation of fertile individuals of mixed
ancestry (i.e. F2, F3 . . . Fn-hybrids) acting as bridges for gene exchange. Differences in the dynamics of the
two classes of hybrid zones, especially in pattern of gene ¯ow, may explain these differences in frequency
and fertility of hybrids.
Key words: ¯ycatchers, cline, hybrid zone, hybrid fertility, relative ®tness
INTRODUCTION
When closely related but differentiated populations
come to live within the same area, interactions between
them tend to in¯uence their ecology and evolution.
Initially, they may have overlapping ecological requirements resulting in competition for resources. There may
also be suf®cient similarity in the characteristics used
for mate recognition for interbreeding to occur. The
production of offspring of mixed ancestry with reduced
viability or fertility increases the complexity of the
dynamics of interactions between populations. Several
developments are possible, including fusion of the populations, speciation through reinforcement, geographic
separation, stable co-existence, stable maintenance of
*All correspondence to: G.-P. Sñtre, Department of Biology, Division
of Zoology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo,
Norway. E-mail: [email protected]
the hybrid zone by in¯ux of pure types from the
parental populations, and extinction of one of the
parental types (Dobzhansky, 1940, 1941; Lack, 1944;
Brown & Wilson, 1956; Sibley, 1957; Wilson, 1965;
Remington, 1968; Grant, 1972; Paterson, 1978; Barton
& Hewitt, 1985; Butlin, 1987, 1989; Hewitt, 1988, 1989;
Harrison, 1990; Liou & Price, 1994).
A hybrid zone may be de®ned as a region in which
genetically distinct populations come into contact and
produce at least some offspring of mixed ancestry
(Futuyma, 1998). Hybrid zones vary in a number of
characteristics, including width, phenotypic and genotypic differentiation of the hybridizing taxa, relative
®tness of individuals of mixed ancestry, spatial distribution of the taxa within the zone and the factors causing
it, and level of assortative mating within the zone (e.g.
Endler, 1977, 1982; Moore, 1977; Barton & Hewitt,
1981, 1985, 1989; Harrison, 1990, 1993; Noor, 1995;
Sñtre, Moum et al., 1997). Analyses of such character-
54
G.-P. Sátre et al.
istics of the hybrid zone may throw light upon past and
present ecological and evolutionary processes and developments, i.e. by inferring process from patterns.
However, based on empirical evidence generalizations
about how structures of co-existence affect hybrid zone
dynamics have been problematic because usually only
one contact zone exists between the hybridizing taxa.
Zones of overlap between pied Ficedula hypoleuca
and collared ¯ycatchers F. albicollis are good models for
studies of hybrid zone dynamics for three main reasons.
First, these birds prefer good quality nest boxes to
natural holes as breeding sites. It is therefore possible to
attract almost the whole breeding population within a
woodland to boxes (Lundberg & Alatalo, 1992). Hence,
within local populations it is relatively easy to obtain
good estimates on important parameters such as patterns of hybridization and species-assortative mating,
and consequences of hybridization on ®tness. Here, we
present such data from a large number of localities in
the Czech Republic and Slovakia. The likelihood of
fusion of two differentiated populations may be reduced
by responses to at least two selective mechanisms, i.e.
reduced hybrid ®tness, and/or by adaptation to different
environments (see Harrison 1990, 1993, for reviews).
Hence, in the present study we look for environmental
correlates of breeding densities and distribution of the
two ¯ycatcher species as well as patterns of mating and
hybrid ®tness.
The second reason these ¯ycatchers are important
models for studying hybrid zone dynamics is that they
are found in hybrid zones of fundamentally different
structures, i.e. in isolated island populations in the Baltic
Sea, and in a large cline running through Central and
Eastern Europe (Fig. 1). The structure and dynamics of
the hybrid zones of the Baltic Isles have been investigated in some detail (Alerstam et al., 1978; Alatalo,
Gustafsson & Lundberg, 1982, 1994; Alatalo, Eriksson
et al., 1990; Lundberg & Alatalo, 1992). Similar information from the large Central and Eastern European
contact zone has not previously been investigated. In the
present study we compare the patterns found in Central
Europe with those in the island populations of the Baltic
Isles. We expected to ®nd differences between these two
classes of hybrid zones. Historical information indicates
that pied and collared ¯ycatchers colonized the Baltic
Isles rather recently, i.e. some 150 years ago (Lundberg
& Alatalo, 1992). Possibly, the two species have lived
together for a much longer time on the European mainland and so evolution may have produced differences,
e.g. in adaptations to avoid hybridization. Moreover,
the isolated nature of the island populations may in¯uence ecological and evolutionary dynamics. On the
islands there is little gene ¯ow of collared ¯ycatchers
from allopatric populations because of the great distance
to the nearest population on the European mainland,
whereas pied ¯ycatchers come in from nearby, surrounding mainland populations (Alatalo, Eriksson
et al., 1990). Here we assess the dynamics of the mainland hybrid zone for comparison and look for potential
consequences of the eventual differences.
The third interesting feature of the hybrid zones of
these birds is the apparent sympatric character displacement of male secondary sexual characteristics, notably
plumage colour (Rùskaft & JaÈrvi, 1992; Sñtre, KraÂl &
BicÏõÂ k, 1993; Sñtre et al., 1997a). Experimental evidence
shows that this colour divergence facilitates species
recognition (Sñtre, Moum et al., 1997). Character divergence of male pied ¯ycatchers in the Baltic Isles is much
less pronounced (Alatalo, Gustafsson et al., 1994).
Hence, we expected the frequency of heterospeci®c
matings would be higher in the Baltic Isles compared
with Central Europe.
MATERIALS AND METHODS
The data presented here comprise a synopsis of several
long-term and short-term studies of pied and collared
¯ycatchers from 47 localities in the Czech Republic and
Slovakia, made by several ornithologists. Many of the
data have not previously been published; otherwise the
data are taken from published work (KlõÂ ma, 1959;
Ferianc, FeriancovaÂ-MasaÂrova & Brtek, 1973; SÏtÏastnyÂ,
1973, 1974; Salaj 1974, 1980; FeriancovaÂ-MasaÂrova &
Ferianc, 1977; MasÏtalka & StaÂrek, 1978; RandõÂ k, 1980;
Chytil, 1984; SÏtÏastnyÂ, RandõÂ k & Hudec, 1987;
KanÏusÏcÏaÂk, 1988; Kropil & Paulen, 1988; KrisÏtõÂ n &
Degma, 1990; PalieskovaÂ, Janiga & Kocian, 1990;
Pressen, 1990; FeriancovaÂ-MasaÂrova et al., 1991;
KrisÏtõÂ n, 1991; Pykal, 1991; SÏaÂlek & SÏmilauer, 1993;
Brandl & Brandl, 1994; KlimesÏ, 1994; Zasadil, 1994).
The following information was available from all localities: latitudinal and longitudinal co-ordinates, altitude,
relative amount of coniferous and deciduous forest
(estimated to nearest 5%), nest site facilities, i.e. nest
boxes or natural holes (data missing from 3 localities),
relative frequency of pied and collared ¯ycatchers (i.e.
the proportion of 1 species among all ¯ycatchers in a
locality, estimated from breeding densities (see below) if
actual numbers were not available), and breeding densities (average annual number of breeding pairs divided
by the size of the locality in ha) of pied and/or collared
¯ycatchers (data missing from 11 localities). The size of
each locality was estimated from maps, based on the
boundaries formed by the outermost nest sites. Population sizes/densities were estimated by counting all
breeding pairs within each area by inspection of nest
sites (25 localities). From the remaining localities such
information is based on indirect measures, i.e. mapping
of territories or parallel line transects. These latter
localities are used only in the assessment of the structure
of the hybrid zone.
From 25 localities (7 allopatric pied ¯ycatcher populations, 3 allopatric collared ¯ycatcher populations and
15 mixed populations) breeding records were available
through 1±14 years, i.e. number of breeding pairs of the
various breeding constellations (pure-bred pairs, heterospeci®c pairs and pairs involving a hybrid) each year. In
four of the areas where hybrids were found breeding we
also have information on their hatching success (no. of
Dynamics of hybrid zones
55
N
0
50
100
150
200 km
Fig. 1. Relative frequency of pied ¯ycatchers (white area) and collared ¯ycatchers (black area) in 47 localities in the Czech
Republic and Slovakia. The frequency of the rarer species was rounded up to the nearest 5% to make low, but positive
frequencies visible on the map. *, Localities where hybrids were found breeding. Inset: breeding distributions of the pied (light
shaded area) and the collared ¯ycatcher (dark shaded area) and the zone of distributional overlap of the two species (medium
shaded area) in Europe. The Baltic Isles, Czech Republic and Slovakia are marked with B, C and S respectively.
eggs in each clutch that hatched). The reduced ®tness of
È land in the Baltic
hybrids observed at Gotland and O
Sea was caused mainly by low hatching success (low
fertility) of hybrids (Alatalo, Eriksson et al., 1990).
Finally, egg-laying dates, clutch sizes, and hatching
success of the breeding pairs of various breeding constellations were available from a 13-year study in a
mixed population at Dlouha LoucÏka in the Czech
Republic (498 50' N, 178 15' E), studied by one of the
authors (M. K.). From this locality we also have
information on hatching success of some hybrid
matings collected from the 12 years preceding the
13-year study (i.e. 1973±1984). We used mating events
as sample units because we obtained only summary
statistics of the breeding data from the various localities.
Data points are therefore not completely independent
because some individuals return to their previous
breeding site the following year(s) (M. KraÂl, pers. obs.).
Lack of independence may result in underestimates of
variance although overall effects should be little affected, as this would be compensated for by the large
sample sizes used. Moreover, we do not think underestimates of variance are a great problem in this study.
For instance, at Dlouha LoucÏka, the same individuals
formed a pair in preceding years only once (a female
collared ¯ycatcher was mated to the same hybrid male
in 2 years).
Species identity was determined by morphological
and behavioural cues. Males are easy to distinguish:
plumage colour, song and alarm calls are highly speciesspeci®c. Male hybrids are also easy to identify on their
intermediate appearance. A typical male hybrid has an
incomplete collar and smaller white patches on the
wings and rump than a pure-bred collared ¯ycatcher, a
mix of black and brown feathers on the head and back
(collared ¯ycatchers are black, pied ¯ycatchers are
brown), and song and alarm calls that are intermediate
to those of the 2 pure species (KraÂl, 1991). The species
identity of females was determined by the amount of
white on the outer webs of primaries, by the colour of
the light patch on the feathers on the back of the neck
(Svensson, 1984), and by their species-speci®c alarm
calls. In female hybrids these characters are intermediate
to those of the two pure species. Species differentiation
is larger in males than in females, hence misclassi®cations could be higher in females. However, an equal
G.-P. Sátre et al.
56
(b)
(a)
100
(c)
80
60
40
20
82 83 84 85 86 88 89 90 91 92 93 94 95
95 96 97
91 92 93 94 95
(e)
(d)
100
Relative frequency
80
60
40
20
85 86 87 88 89 90 91 92 93 94 95 96 97
66 67 72 73 74 75 76 77 78 79 80 81
(g)
(f)
100
80
60
40
20
78 79 80 83 84 85 86 87 88 89 90 91 92 93
79 80 81 82 87 88 89 90 91 92 93
Year
proportion of males and females were classi®ed as
hybrids; estimated proportion of female hybrids using a
binomial model = 0.52 [95% C.I.: 0.36, 0.67] (excluding
the data from 1973±1984 from Dlouha LoucÏka where
breeding records were incomplete, see above).
RESULTS
Structure of the hybrid zone
A total of 6786 mating events from 25 populations was
documented. Hybrids were found in nine of the 25
localities examined. Eight of the localities where hybrids
were found breeding were located along a latitudinal
belt where the main distributions of the two ¯ycatchers
appear to meet (Fig. 1). The majority (129 out of 135) of
the documented non-pure matings occurred in these
eight localities. One or a few individuals of one species
were occasionally found breeding together with the
other species in other localities further away from the
main contact zone. The pied ¯ycatcher was the dominant species in the north and the collared ¯ycatcher in
the south (Fig. 1).
The geographic distribution of the two ¯ycatchers
documented above coincides with topography and
habitat. That is, pied ¯ycatchers are dominant in submontane areas with mixed deciduous and coniferous
forests and collared ¯ycatchers are dominant in deciduous lowland forests, but also in some deciduous forests
Dynamics of hybrid zones
(i)
(h)
100
57
80
60
Relative frequency
40
20
84 85 86 87 88 89 90 91 92 93
88 89 90 91 92 93 94 95 96 97
(j)
100
(l)
(k)
80
60
40
20
87 88 89 90 91 92 93 94 95
84 85 86
89 90 91 92 93 94 95
Year
Fig. 2. Temporal changes in relative frequency of pied ¯ycatchers (open bars), collared ¯ycatchers (shaded bars) and hybrids
(hatched bars) in twelve mixed populations: (a) Turnov (508 34' N, 158 09' E), (b) Mala Moravka (508 01' N, 178 19' E),
(c) SÏumperk (508 07' N, 178 07' E), (d) Dlouha LoucÏka (498 50' N, 178 15' E), (e) Trilna (498 53' N, 168 57' E), (f ) Hukvaldy
(498 41' N, 188 40' E), (g) Ostrava (498 47' N, 188 09' E), (h) SluzÏõÂ n (498 33' N, 178 03' E), (i) Litovel (498 40' N, 178 10' E),
( j) ProsteÏjov (498 32' N, 178 04' E), (k) Horna Oravcova (488 27' N, 188 23' E), and (l) BrÏeclav (488 45' N, 168 54' E).
at high altitudes in the south. The average relative
frequency of collared ¯ycatchers in the population was
negatively associated with latitude (r2 = 0.50; d.f. = 46;
P = 0.0001), altitude (r2 = 0.23; d.f. = 46; P = 0.0006),
relative amount of coniferous forest (r2 = 0.18; d.f. = 46;
P = 0.0018), and longitude (r2 = 0.093; d.f. = 46;
P = 0.037; simple regressions, data normalized by standard transformations). However, in a multiple
regression only altitude and latitude were of signi®cance
(altitude: partial F = 24.1; d.f. = 1, 46; P = 0.0001; latitude: partial F = 60.3; d.f. = 1, 46; P = 0.0001). The
relative amount of coniferous forest increased northwards (r2 = 0.18; d.f. = 46; P = 0.0029), westwards
(r2 = 0.11; d.f. = 46; P = 0.025), and with increasing altitude (r2 = 0.07; d.f. = 46; P = 0.064, simple linear
regressions) in these localities.
The majority of localities were provided with nest
boxes (29 of 44 localities, information missing for three
localities). Breeding densities of ¯ycatchers may become
much higher in areas provided with nest boxes than when
only natural holes are available (Lundberg & Alatalo,
1992). Hence, we use one-factor ANCOVA, with type of
nest as the factor to analyse potential covariates of the
absolute breeding densities of the ¯ycatchers (data were
normalized by standard transformations for parametric
tests). In populations where pied ¯ycatchers occurred,
and where we had data on breeding densities, n = 21,
their breeding density was not related to altitude, latitude, type of forest, nest box vs natural holes, or any
interaction of variables (one-factor ANCOVA: P > 0.1).
The breeding density of collared ¯ycatchers was negatively associated with the relative amount of coniferous
forest (coniferous forest: F = 9.90; d.f. = 1, 25;
P = 0.0044); nest box vs natural holes: F = 9.12; d.f. = 1,
25; P = 0.0059; one-factor ANCOVA). Neither latitude,
altitude, nor any interactions of variables were of any
signi®cance (one-factor ANCOVA: P > 0.1).
The breeding densities of collared ¯ycatchers were
generally high (areas with nest boxes: mean 1.77 pairs/
ha; range 0.02±7.50; n = 19; areas with natural holes:
mean 0.47 pairs/ha; range 0.03±1.10; n = 8). The
breeding densities of pied ¯ycatchers were much lower
(areas with nest boxes: mean 0.21 pairs/ha; range 0.001±
1.20; n = 15; areas with natural holes: mean 0.10 pairs/
ha; range 0.022±0.32; n = 6). In general, the densities of
pied ¯ycatchers found in the nest box areas were much
G.-P. Sátre et al.
58
lower than densities reported from other nest box
populations of this species in Europe (Lundberg &
Alatalo, 1992).
Temporal changes in species composition
Breeding records through 3±14 years were available
from 12 mixed populations (localities where members of
one species, hybrids, or both, were found breeding
together with members of the other species, Fig. 2).
Binomial models assuming a constant proportion of
pied ¯ycatchers (using sum of the pure-bred pairs as the
binomial denominator) over time, did not ®t the data
for three localities, thus indicating a signi®cant year-toyear variation (signi®cant goodness of ®t test for localities: Dlouha LoucÏka: error deviance = 73.1; d.f. = 12;
P < 0.0001; Hukvaldy: error deviance = 36.5; d.f. = 13;
P = 0.0006; SluzÏõÂ n: error deviance = 18.3; d.f. = 9;
P = 0.032. At Hukvaldy a monotonous decline in the
proportion of pied ¯ycatchers (Fig. 2) explained the
extraneous variation apparent in the constant model
(likelihood ratio w2 = 29.5; d.f. = 1; P < 0.0001) for year
included as a linear term in the model (error deviance = 7.0; d.f. = 12; P = 0.85). The time trend was
more complex for Dlouha LoucÏka (Fig. 2) and the best
model included year as a third order polynomial (likelihood ratio w2 = 54.9; d.f. = 3; P < 0.0001) and the
model was still overdispersed (error deviance = 18.9;
d.f. = 9; P < 0.03). No consistent time trends could be
detected for SluzÏõÂ n. In most of the other localities the
rarer species (and/or hybrids) occurred only sporadically
(Fig. 2). Hence, maintained co-existence of the two
species was the exception rather than the rule in these
mixed populations.
At the two localities where hybrids were present for
more than 2 years (Dlouha LoucÏka and Hukvaldy),
constant binomial models ®tted the proportion of
hybrids well (Dlouha LoucÏka: error deviance = 10.0;
d.f. = 12; P = 0.61 and Hukvaldy: error deviance = 16.2;
d.f. = 13; P = 0.24) indicating no time trends.
Patterns of hybridization
A total of 2529 mating events occurred in temporal and
spatial sympatry (i.e. sympatric populations excluding
those years where only one of the species was found
breeding). There was a clear overall dominance of
conspeci®c matings: 2394 (94.7%) of the mating events
were conspeci®c, 67 (2.6%) were heterospeci®c and 68
(2.7%) involved one hybrid.
We tested the null hypothesis of random mating by
regressing the empirical proportion of ¯ycatchers
involved in hybridization (with a hybrid or a heterospeci®c) against the frequency of possible hybrid or
heterospeci®c mates at a locality in a given year. We
used the logit regression model:
Log ( pmix/[1 7 pmix]) = a + b log ( pm/[1 7 pm]) (1)
Where pmix is the proportion of pied (or collared)
¯ycatchers involved in hybridization, pm is the observed
proportion of mates that could be involved in hybridization and a and b are the regression parameters to be
estimated. By this model, under the null hypothesis
(random mating), the ®tted proportion pmix are equal to
the measured pm in the entire range of pm. Expressed in
terms of the regression parameters we expected that
b = 1 and a = 0. We estimated the regression parameters
and their 95% con®dence intervals by maximum likelihood, assuming binomial residual error.
Using the proportion of pied ¯ycatchers as the
expectation in equation (1) yielded the regression
parameters with con®dence intervals scaled according to
error deviance b = 0.68 [95% C.I.: 0.38, 0.98] and
a =72.71 [73.40, 72.01] (error deviance = 91.5;
d.f. = 55; P < 0.002). Thus, the incidence of hybridization events increased with the frequency of putative
hybridization partners, but less than expected from the
null hypothesis (Fig. 3). Mating was nearly perfectly
species-assortative at high relative frequencies of pied
¯ycatchers, but a steeply increasing proportion of pied
¯ycatchers became involved in mixed pairs at high
relative frequencies of heterospeci®cs and hybrids. In
regression using the proportion of collared ¯ycatchers
involved in mixed pairs as the response variable, the
following values of the regression parameters and goodness of ®t statistics were obtained: b = 0.54 [0.34, 0.73],
a = 72.31 [72.79, 71.83] (error deviance = 79.9;
d.f. = 58; P = 0.03). Consequently, the proportion of
collared ¯ycatchers involved in mixed pairs was also
signi®cantly lower than expected from the null hypothesis and furthermore, the ®tted proportion pmix
increased with increasing values of pm (Fig. 4).
Hybrid ®tness
Both clutch size and ¯edging success in ¯ycatchers
decline as the breeding season progresses (Lundberg &
Alatalo, 1992). At Dlouha LoucÏka, pairs of collared
¯ycatchers started egg-laying signi®cantly earlier than
pairs of pied ¯ycatchers (Table 1; t =75.15; d.f. = 435;
P < 0.0001; t-test). Heterospeci®c pairs initiated egglaying at a similar time as pied ¯ycatcher pairs and
signi®cantly later than collared ¯ycatcher pairs
(t =73.54; d.f. = 409; P = 0.0004). In pairs with one
hybrid, egg-laying was initiated at an intermediate date,
not signi®cantly different from collared ¯ycatcher pairs
but earlier than pied ¯ycatcher pairs (t =72.22;
d.f. = 75; P = 0.03). Clutch size did not differ signi®cantly among any of the breeding constellations (Table
1). Hence, heterospeci®c pairs and those with one
hybrid were not at any clear selective disadvantage with
respect to these measures related to ®tness. However,
note that the difference between the species in laying
implies some temporal isolation in timing of breeding
that could reduce the frequency of hybridization.
Turning to hatching success, the differences were
pronounced. Noteworthy, infertile eggs were not bi-
Proportion of collared flycatchers in mixed pairs
Proportion of pied flycatchers in mixed pairs
Dynamics of hybrid zones
1.0
0.8
0.6
0.4
0.2
0.0
0.0
0.2
0.4
0.6
0.8
1.0
Frequency of collared flycatchers and hybrids
59
1.0
0.8
0.6
0.4
0.2
0.0
0.0
0.2
0.4
0.6
0.8
Frequency of pied flycatchers and hybrids
1.0
Fig. 3. Logit regression line with 95% con®dence interval
(broken lines) for the proportion of pied ¯ycatchers involved
in hybridization (mating with a heterospeci®c or a hybrid)
against relative frequency of heterospeci®cs and hybrids in the
population each year. Each point represents the relationship at
one locality in one year.
Fig. 4. Logit regression line with 95% con®dence interval
(broken lines) for the proportion of collared ¯ycatchers involved in hybridization (mating with a heterospeci®c or a
hybrid) against relative frequency of heterospeci®cs and
hybrids in the population each year. Each point represents the
relationship at one locality in one year.
nomially distributed among the two categories of hybrid
pairs, as indicated by a highly signi®cant goodness of ®t
test (Table 2). Hatching failure in pairs with a hybrid
was either complete or very low (Fig. 5). In contrast, the
low proportion of infertile eggs was binomially distributed in pure collared ¯ycatcher pairs and only slightly
non-binomial in pied ¯ycatcher pairs (Table 2). The
estimated proportion of infertile eggs was low among
pure-bred and heterospeci®c pairs (Table 2). However,
the frequency of hatching failures was signi®cantly
higher in pairs involving a hybrid mate. Furthermore,
the gender of the hybrid in those pairs was in¯uential:
pairs with a female had signi®cantly more infertile eggs
than pairs with a male hybrid (Table 2).
In ®ve ¯ycatchers, individual marking revealed that
the hybrid was a second or a third generation hybrid.
Hatching failure was signi®cantly lower in these
multiple-generation hybrids than in other hybrids
(Z =73.68; n = 64; P = 0.0002, Mann±Whitney U-test).
cies of 2.6% and 2.7% respectively for heterospeci®c
pairs and pairs with a hybrid in temporal and spatial
sympatry in Central Europe. The difference in frequency of heterospeci®c matings is not signi®cant
(w2 = 1.55; d.f. = 1; P = 0.21), whereas the frequency of
pairs with one hybrid was signi®cantly higher in the
Baltic Isles (w2 = 7.78; d.f. = 1; P = 0.005). The relative
frequency of pied ¯ycatchers in the populations of the
Baltic Isles appears to be approximately similar or
slightly lower than the average for the Central
European populations investigated here, but Alatalo,
Eriksson et al. (1990) do not provide data on how
many pied ¯ycatchers were mated to hybrids.
Turning to hybrid ®tness, 45.1% of pairs with one
hybrid experienced complete hatching failure in the
study from the Baltic Isles (Alatalo, Eriksson et al.,
1990), compared with 71.9% in our study from Central
Europe (Fig. 5). The difference is signi®cant (w2 = 9.4;
d.f. = 1; P = 0.002).
Comparison with the hybrid zones in the Baltic Isles
If plumage colour of male pied ¯ycatchers is important
for species recognition we might expect differences in
frequency of hybridization between the Central European hybrid zone and the hybrid zones of the Baltic
Isles. This is because Baltic male pied ¯ycatchers are
darker coloured than Central European pied ¯ycatchers and, hence, are more similar to male collared
¯ycatchers (Lundberg & Alatalo, 1992). Alatalo,
Eriksson et al. (1990) reported an average frequency of
3.3% heterospeci®c pairs and 4.3% pairs with one
hybrid for the Baltic Isles, compared with our frequen-
DISCUSSION
Structure of the hybrid zone
On a large scale, there is a rather broad latitudinal zone
through Central and Eastern Europe wherein the distributions of the two ¯ycatchers overlap. However, the
present study suggests that the main contact zone of the
two species is restricted to a rather narrow cline within
the geographical range we have investigated. Collared
¯ycatchers are rare north of the main contact zone and
pied ¯ycatchers south of the zone.
G.-P. Sátre et al.
60
Table 1. Date of ®rst egg (day 1, 1 May) and clutch size of different breeding constellations of pied and collared ¯ycatchers at
Dlouha LoucÏkaa
Date of ®rst egg
Clutch size
Breeding constellation
Mean
sd
n
Mean
sd
n
PF6PF
CF6CF
PF6CF
PF or CF6hybrid
15.1
10.6
15.1
12.1
5.7
5.5
6.7
5.7
46
391
20
31
6.44
6.25
6.17
6.37
0.73
0.73
0.62
0.83
43
365
18
41
a
Data on hybrids also from four other populations.
Table 2. Estimated proportion of infertile eggs within clutches of different breeding constellations and goodness of ®t to a
binomial model. 95% con®dence intervals for the two hybrid breeding constellations are estimated by quasi-likelihood procedure
due to highly signi®cantly overdispersed error deviance
Goodness of ®t statistics
Breeding constellation
Prop. (95% c. i.)
Error deviance
d.f.
P
CF6CF
PF6PF
CF6PF
PF or CF6male hybrid
PF or CF6female hybrid
0.04 (0.03, 0.05)
0.07 (0.05, 0.10)
0.07 (0.03, 0.13)
0.64 (0.46, 0.79)
0.92 (0.81, 0.97)
375.5
84.9
18.3
305.5
74.5
376
63
16
38
24
0.50
0.03
0.31
< 0.0001
< 0.0001
50
No. of clutches
40
30
20
10
0
1
2
3
4
5 compl.
clutch
No. of eggs that failed to hatch
Fig. 5. Distribution of hatching failure, number of eggs in the
clutch that failed to hatch, in clutches of pairs involving a male
(open bars) and a female (hatched bars) hybrid.
Ecological dynamics of the hybrid zone
The cline running through the Czech Republic corresponds with topography and habitat. Hence, in the
north, the distribution of the collared ¯ycatcher stops at
high altitudes where coniferous forest begins to dominate, re¯ecting a colder climate. We suggest that the
distribution of collared ¯ycatchers is limited at the
northern border of the country by inappropriate
habitat. The breeding density of collared ¯ycatchers was
negatively associated with the amount of coniferous
forest. In a mixed population near the northern limit of
the distribution of the collared ¯ycatcher in the Czech
Republic the birds had much higher nestling mortality
than in a population further south (deciduous forest
and low altitude; BuresÏ, 1995; BuresÏ & KraÂl, 1995).
Comparison of nestling diet suggests that collared ¯ycatchers are more dependent upon mobile prey than are
pied ¯ycatchers (BuresÏ, 1995). Hence, a plausible
hypothesis for the observed habitat separation may be
that collared ¯ycatchers have greater problems ®nding
suitable prey in cold habitats than have pied ¯ycatchers.
Indeed, in the above mentioned mixed population pied
¯ycatchers had lower nestling mortality than had
collared ¯ycatchers (BuresÏ, 1995; BuresÏ & KraÂl, 1995).
The distribution of pied ¯ycatchers may also be
related to habitat. However, they are found in a broader
range of habitats and climates than collared ¯ycatchers
(Lundberg & Alatalo, 1992; Glutz von Blotzheim &
Bauer, 1993), and their breeding density was not related
to any habitat measure in the present study. We suggest
that competition and hybridization with collared ¯ycatchers may also be important factors limiting the
distribution and abundance of pied ¯ycatchers in the
southeast. Collared ¯ycatchers are socially dominant
over pied ¯ycatchers in the competition for limited
available nest sites (LoÈhrl, 1955; Sñtre, KraÂl & BicÏÂãk,
1993; Alatalo et al., 1994). The rarer species also suffers
more from hybridization than the more common one.
In the present study, a much higher proportion of
individual pied ¯ycatchers were involved in hybridization than collared ¯ycatchers. Because hybridization
Dynamics of hybrid zones
yields low ®tness return compared with speciesassortative breeding, the average annual production of
pied ¯ycatchers would be low in a mixed population.
This may help to explain why the mixed populations
investigated here were rarely inhabited by both species
for long periods of time. Finally, the resulting habitat
separation of these two species within the zone of
overlap is an important factor reducing the frequency of
hybridization. Indeed, the majority of matings occurred
in allopatry.
Patterns of hybridization
In sympatry there was a clear tendency for speciesassortative mating. However, in this analysis we have
included only birds that did mate. We observed several
males of the rarer species that remained unmated
throughout the season. It is also possible that females
that failed to ®nd conspeci®cs within an area chose not
to breed there and moved away. Hence, the deviation
from random mating may actually have been larger
than our data imply.
In Central and Eastern Europe, males of the two
species are highly differentiated in plumage colour and
song. We may therefore ask, why does hybridization
occur at all? In mate choice trials where females of the
two species could choose between one male of each
species, they always chose the conspeci®c male (Sñtre,
KraÂl & BuresÏ, 1997). Mating with a member of the
other species would often result in zero contribution to
the gene pool because of high rates of infertility in the
hybrid offspring. In addition, the birds would pay the
cost of reproduction. We do not know how costly
reproduction is in ¯ycatchers relative to forgoing
breeding. In tits breeding individuals have much higher
annual mortality rates than non-breeding individuals
(Ekman & Askenmo, 1986). In pied ¯ycatchers adult
mortality peaks during the breeding season (Slagsvold
& Dale, 1996), suggesting that the cost of reproduction
may also be substantial in ¯ycatchers (see also
Gustafsson & PaÈrt, 1990; PaÈrt, Gustafsson & Moreno,
1992). It is therefore possible that hybridization is
maladaptive even when the only alternative option is
forgoing breeding. Alternatively, the average ®tness
return from hybridization may outweigh costs of reproduction. If so, hybridization could be a best of a bad
situation strategy applied when no conspeci®c mates
have been found. Note also that the cost to females of
becoming socially mated to a heterospeci®c or a hybrid
male may be reduced by extra-pair copulations (EPC)
with conspeci®c males. EPC is known to occur in other
¯ycatcher populations (e.g. Lundberg & Alatalo, 1992).
Unfortunately, we do not have any data on EPC in the
populations investigated here.
The proportion of pied ¯ycatchers that were involved
in non-pure matings was low in a wide range of relative
frequencies of pied ¯ycatchers vs heterospeci®cs and
hybrids, but increased steeply when the relative frequency of heterospeci®cs and hybrids became very high.
61
A similar pattern, although less conspicuous, was found
also for collared ¯ycatchers. This pattern suggests that
¯ycatchers mate species-assortatively when conspeci®cs
are found available but tend to hybridize when only
heterospeci®cs or hybrids are present. In an allopatric
population female pied ¯ycatchers have been shown to
visit only a few males during a relatively short time span
before settling and to search over a geographically
restricted area (e.g. Dale, Rinden & Slagsvold,1992).
We found that collared ¯ycatchers on average initiated egg-laying earlier than pied ¯ycatchers although
there was considerable overlap. Nevertheless, the observed differentiation in timing of breeding may be a
factor reducing the frequency of hybridization between
the two species.
Hybrid ®tness
Whereas breeding success of heterospeci®c pairs was
similar to that of pure pairs, pairs with one hybrid had
low breeding success. This was because hatching success
(fertility) was low in pairs with a hybrid. There was a
signi®cant difference in hatching success depending on
whether the male or the female was a hybrid. This is
probably because hybrid females are more often infertile
than hybrid males, as has been shown in the ¯ycatcher
hybrid zone of the Baltic Isles (Gelter, 1989; Alatalo,
Eriksson et al., 1990; TegelstroÈm & Gelter, 1990). This
is in accordance with Haldane's rule stating that the
heterogametic sex is more often sterile than the homogametic sex (Haldane, 1922). However, the sexual
difference in hatching success of hybrids was less
pronounced in the present populations than in those on
the Baltic Isles (Alatalo, Eriksson et al., 1990). Male
extra-pair paternity (EPP) and female egg dumping may
confound hatching success of hybrids. Cases of EPP are
known from other ¯ycatcher populations whereas eggdumping appears to be extremely rare (e.g. Lundberg &
Alatalo, 1992). Hence, hybrid ®tness may be lower than
our data imply.
Infertile eggs were not binomially distributed among
pairs with a hybrid. In particular in pairs with a male
hybrid hatching success was either zero or very high. We
do not know the mechanism producing this pattern, but
apparently the biochemical/genetical incompatibility of
reproduction between genetically differentiated parents
is either absent or total in these birds. It is also possible
that high success was attributable to EPC. We do not
think, however, that EPC can explain all cases of
apparent fertility in male hybrids. Using DNA-®ngerprinting, Gelter (1989) showed that a high proportion of
the apparently fertile male hybrids on Gotland really
were the true fathers of the offspring they raised.
Comparisons with the hybrid zones in the Baltic Isles
The species difference in male plumage colour is larger
in the Central and Eastern European hybrid zone than
62
G.-P. Sátre et al.
in the hybrid zones in the Baltic Isles. The colour
divergence of the males in sympatry in Central and
Eastern Europe has been explained by natural selection
against the production of un®t hybrids (i.e. reinforcement of pre-mating isolation), in that colour divergence
reduces the probability of heterospeci®c mating (Sñtre
et al., 1997a). The less pronounced colour divergence of
male pied ¯ycatchers in the isolated island hybrid zones
indicates that reinforcement may not operate to a
similar extent in these populations. This could be
explained by the presumably shorter time available for
evolution to produce a colour divergence in the latter
zones because the Baltic Isles probably were colonized
by ¯ycatchers rather recently (Lundberg & Alatalo,
1992). Alternatively, pattern of gene ¯ow may affect the
potential for reinforcement to evolve. Computer simulations indicate that reinforcement is more likely to evolve
when gene ¯ow to and from the hybrid zone is symmetric than when it is asymmetric, with respect to the
species involved (Servedio & Kirkpatrick, 1997), i.e. an
introduced preference allele that characterizes one of the
populations is much more likely to spread in the former
case. Pattern of gene ¯ow is typically asymmetric in the
island populations of the Baltic Isles, as the collared
¯ycatcher is quite isolated from mainland populations
whereas there is an in¯ux of pied ¯ycatchers from the
surrounding mainland (Alatalo, Eriksson et al., 1990;
Lundberg & Alatalo, 1992). Gene ¯ow is probably more
symmetric in the Central and Eastern European hybrid
zone because the two species have continuous breeding
distributions on each side of the main contact zone
(Fig. 1).
Given the difference in plumage colour divergence
between the two classes of hybrid zones we expected to
®nd corresponding differences in the frequency of
hybridization. However, frequency of heterospeci®c
mating was not signi®cantly higher in the Baltic Isles
(see Alatalo, Eriksson et al., 1990, for a comparison).
Why is this? It is possible that a dark male pied
¯ycatcher is suf®ciently dissimilar from a male collared
¯ycatcher to allow perfect species recognition in most
instances. On the other hand, there is some evidence
suggesting that heterospeci®c matings may sometimes
occur because of imperfect species recognition in the
hybrid zone of the Baltic Isles. Alatalo, Eriksson et al.
(1990) found that male pied ¯ycatchers singing a mixed
kind of song were more often involved in heterospeci®c
pairs than males singing the species-typical song. In
addition, Alatalo, Gustafsson et al. (1994) found some
evidence suggesting that darker male pied ¯ycatchers
may be more subject to heterospeci®c matings than
more brownish male pied ¯ycatchers. Finally, it has
been shown experimentally that differences in plumage
colour affect the probability of heterospeci®c mating
(Sñtre, Moum et al., 1997). The present study indicated
that hybridization mainly occurred when few conspeci®c
mates were present. Several factors may affect the
frequency of hybridization, such as relative frequency of
the two species at a given time and place. It is possible
that such differences on a local scale could mask an
actual difference in species recognition.
Our comparison suggests that hybrid ®tness is lower
in Central Europe than in the Baltic Isles. With species
asymmetric in¯ux of pure-bred individuals, the isolated
island populations of collared ¯ycatchers would constantly receive introgressors from allopatry and as a
result hybrids would accumulate. In most of the Central
European populations investigated here the two species
occurred together in the same locality only sporadically.
Hence, there may be less opportunity for accumulation
of hybrids and introgression. Indeed the frequency of
hybrids was found to be higher in the Baltic Isles than in
the Central European populations investigated here. A
high proportion of the ¯ycatchers of the Baltic Isles may
therefore actually be multiple-generation (F2, F3, Fn)
hybrids. Such individuals may act as bridges for gene
exchange between the species. In the present study we
found that multiple-generation hybrids (second and
third generation) were more fertile than F1 hybrids.
Hence, asymmetric gene ¯ow to the island populations
may further reduce the probability of reinforcement and
speciation because the resulting higher level of introgression would reduce the cost of hybridization by
increasing hybrid fertility and hence, reduce the selective
force favouring reinforcement.
Although our data are consistent with the suggestions
above these should only be considered as weakly tested
hypotheses at present. For instance, different observers
have classi®ed birds into hybrids or pure species in the
different populations. Individual differences in classi®cation criteria could potentially affect both the
estimated frequencies of hybrids and their fertility. We
suggest that genetic markers should be applied to gain
further insight into the differences between the zones in
dynamics of hybridization and introgression.
Acknowledgements
We wish to thank BorÏivoj HolõÂ nek, Karel BroulõÂ k, Petr
Ï ervenka, Ivan Chumchal, Jitka ChumchalovaÂ,
C
Jaroslav Fisera, Jan GruÂz, Jan KosÏtÏaÂl, FrantisÏek
Krause, Pavel KuÊrka, Jan Pavelka, Karel Pithart, Bronislav PrazÏaÂk, Otakar PrazÏaÂk, JirÏõÂ RuÊzÏicÏka, Jan SÏevcÏõÂ k
and Jan StrÏõÂ tesky for lending us their unpublished
breeding records of ¯ycatchers, and Tore Slagsvold for
comments. The Norwegian Research Council provided
®nancial support.
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