The Mediterranean Alectoris (including A. rufa, A. graeca, A. chukar, and A. barbara) comprise a group of closely related and morphologically uniform partridges with largely allopatric distributions and instances of natural hybridization in parapatric contact zones. Their taxonomic status and evolution are controversial. We have used multilocus protein electrophoresis to estimate the extent of genetic divergence among nominal Alectoris species and within A. chukar, A. graeca and A. rufa. The average Nei's (1978) genetic distance among conspecific populations (D[bar] = 0.008; range 0.003-0.021) was 26 times smaller than among species (D[bar] = 0.208; range 0.071-0.312). The most genetically similar species were A. rufa and A. graeca (D[bar] = 0.081); A. barbara and A. chukar were the most divergent (D[bar] = 0.303). The Fst, values among species (Fst, = 0.75) were more than eight times larger than among conspecific populations (Fst = 0.09). The gap in D and Fst, values for intraspecific and interspecific comparisons indicates a prolonged interruption of gene flow among species and independent evolution of their gene pools. Dendrograms summarizing genetic distance matrices and cladistic analyses of discrete character states suggested that A. rufa and A. graeca are sister species of recent origin, followed by the most distantly related and ancient A. chukar and A. barbara. Because protein electrophoresis results are concordant with biogeographical and paleontological information, we construct a hypothesis for the evolution of the Mediterranean Alectoris. Received 2 May 1991, accepted 13 January 1992.
lIstituto Nazionale de Biologia della Selvaggina via, Cd Fornacetta, 9,
40064 Ozzano dell'Emilia (Bo), Italy;
2Dipartimento di Biologia Animale, Universitd di Pavia, Piazza Botta, 9, 27100 Pavia, Italy; and
3Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev,
Sede Boqer Campus 84990, Israel
THE ALCTORIS partridges (Galliformes, Pha-
sianidae) are distributed widely in the Palaearc-
tic (Fig. 1). They present intriguing and chal-
lenging questions with regard to taxonomic and
evolutionary relationships. Peters (1934) in-
cluded graeca, chukar, and magna as subspecies
of A. graeca, a taxonomy that was followed by
Dementiev and Gladkov (1952). Voous (1960)
largely accepted this classification, but ques-
tioned the separate species rank assigned to A.
rufa. From ethological evidence, Menzdorf
(1984) agreed that graeca, chukar, and rufa had
not yet attained true species status. Vaurie (1959),
on the contrary, argued that these forms com-
prised separate species owing to diagnostic dif-
ferences in facial plumage and vocalizations.
This view was supported by Watson (1962a, b),
who offered additional evidence of species-spe-
cific plumage characters, and of behavioral and
ecological separation among parapatric popu-
lations. The Vaurie (1959) and Watson (1962a,
b) view of seven closely related Alectoris species
is now widely accepted (Cramp and Simmons
1980, Johnsgard 1988).
Most Alectoris species are very similar mor-
phologically, differing only with respect to sub-
tle but diagnostic face and throat plumage pat-
terns (Johnsgard 1988). Their natural ranges (Fig.
1) are largely allopatric, except for sympatry
between melanocephala and philbyi in southern
Arabia. Parapatric contact zones exist between
chukar and graeca at the border of Greece and
Bulgaria, between rufa and graeca in the French
Alps, and probably between magna and chukar
in central China (Watson 1962a, Bernard-Lau-
rent 1984). Only two zones of overlap and hy-
bridization (sensu Short 1969) have been re-
ported: a well-documented rufa and graeca
hybrid zone in the southern French Alps (Ber-
nard-Laurent 1984); and an unconfirmed graeca
and chukar hybrid zone in Thrace south of the
Rhodope Mountains (Dragoev 1974). Extant
Alectoris populations of Mediterranean and
North Atlantic islands probably resulted from
human introductions (Watson 1962b, Blondel
1988). The present pattern of only one species
per island may represent the outcome of com-
petitive exclusion among two or more species
following repeated introductions (Blondel 1988).
Therefore, several lines of evidence, including
allopatric distributions, natural hybridization,
ecological exclusion, and morphological simi-
larity have been used in support of hypotheses
of a recent radiation, and perhaps incomplete
speciation, of the Mediterranean Alectoris par-
tridges (Voous 1960, Watson 1962a, b, Blondel
1988).
Two conflicting models have been recently
proposed to explain evolution and speciation
in Alectoris (Fig. 1). Watson (1962a) argued that
Alectoris comprises: (1) the "superspecies" grae-
ca (encompassing graeca, and magna); (2) the
"superspecies" chukar (encompassing chukar,
philbyi, barbara, and tufa); and (3) melanocepha-
la, a separate and more distantly related species.
From morphological and biogeographical evi-
dence, Watson argued that graeca was the an-
cestor of the chukar lineage, and that rufa evolved
recently in southwestern Europe after barbara
crossed the Straits of Gibraltar. Span0 (1975)
criticized Watson's model and suggested close
relationships of chukar with graeca and rufa, but
not with barbara and philbyi. Bernard-Laurent
(1984) and Blondel (1988) cited extant zones of
overlap and hybridization for including graeca,
rufa, and chukar in a single superspecies of which
graeca was the ancestral form. According to these
authors, barbara never crossed Gibraltar to Eu-
rope and is only distantly related to graeca.
We used multilocus protein electrophoresis
to estimate the extent of genetic divergence
among the four Mediterranean species of Alec-
toris: Red-legged Partridge (A. rufa), Rock Par-
tridge (A. graeca), Chukar (A. chukar), and Bar-
bary Partridge (A. barbara). In particular, we
examined the following hypotheses posed by
previous authors: (1) the Mediterranean Alec-
toris speciated very recently (Watson 1962a) and,
perhaps, incompletely (Voous 1960, Blondel
1988); (2) graeca was the ancestral form of a su-
perspecies from which chukar and rufa origi-
nated at the eastern and western range bound-
aries, respectively (Bernard-Laurent 1984,
Blondel 1988); or, alternatively, (3) chukar, bar-
bara, and rufa constitute a superspecies, with
rufa originating from barbara after crossing Gi-
braltar (Watson 1962a). Genetic distances were
used to estimate levels of divergence among
conspecific populations and among species, and
to obtain dendrograms showing phenetic and
phylogenetic relationships among species. A
tentative calibration of the average rate of pro-
tein evolution was used to estimate divergence
times, which have been related to current evo-
lutionary and biogeographical hypotheses.
MATERIAL AND METHODS
We analyzed 117 specimens belonging to the fol-
lowing populations: A. tufa population 1 (n = 12, wild,
SW Spain); A. tufa 2 (n = 20, captive-reared, Italy); A.
graeca 1 (n = 10, wild, E Alps, Italy); A. graeca 2 (n =
20, captive-reared, Italy); A. chukar 1 (n = 20, wild,
China); A. chukar 2 (n = 5, captive-reared, Bulgaria);
and A. chukar 3 (n = 20, wild, central Israel); A. barbara
(n = 20, wild, Sardinia, Italy). Captive specimens were
obtained from pure-bred, [arm-reared stocks. Given
the recent [oundation of the captive stocks, and their
derivation from more than 20 breeding pairs, there
was little likelihood that the source populations were
subject to substantial inbreeding. Wild birds were col-
lected [rom localities at which there have been no
restocking with reared birds. We also analyzed tissues
of Gray Partridge (Perdix perdix, n = 2) and Ring-
necked Pheasant (Phasianus colchicus, n = 2) as out-
groups for rooting phylogenetic trees.
Liver and heart samples were dissected from fresh-
ly-killed birds, stored at -20øC for several hours after
death, and then stored at -80øC until processing. We
separately homogenated about 0.5 g of each tissue in
1 ml of 0.01 M Tris/HC1 pH 7.5, 0.001 M Na2.EDTA,
and 0.001 M B-mercaptoethanol buffer and centri-
fuged for 15 rain at 13,000 rpm. Supernatants were
diluted in one volume o[ a 40% glycerol solution,
aliquoted in Microtiter plates, and frozen at -80øC
until used. Vertical polyacrylamide gel electropho-
resis (concentration of 7.5% monomers in the contin-
uous systems) was used to resolve 33 loci. Staining
recipes were adapted from Harris and Hopkinson
(1976). Electromorphs were presumed to have a sim-
ple genetic basis, and were considered as alleles. A1-
leles were coded by their mobility from the starting
line, with the most anodal allele coded as "a."
The BIOSYS-1 program (Swofford and Selander
1989) was used to compute percent polymorphic loci
(P) and heterozygosity (H) values. Agreement with
Hardy-Weinberg expectations was tested using chi-
square analysis (Sokal and Rohlf 1981). Other statis-
tical procedures included: contingency tests of allelic
heterogeneity among populations (Workman and
Niswander 1970); Nei's (1978) and Rogers' (1972) ge-
netic distance matrices, UPGMA phenograms (Sneath
and Sokal 1973); and Wagner networks (Swofford
1981). We have computed F-statistics (Wright 1978)
within and among nominal species. These provided
two lines of evidence (i.e. genetic distances and F,)
on the extent of genetic divergence at different tax-
onomical levels (Corbin 1987). Cladistic trees were
constructed using the program PAUP (Swofford 1985)
after coding alleles as present or absent according to
the independent-allele model (Buth 1984). The SPSS
Fig. 1. Distribution of partridges of genus Alectoris (adapted from Watson 1962a and Blondel 1988). Con-
tinuous lines indicate the evolutionary relationships among species as suggested by Watson (1962a, b). Broken
lines indicate evolutionary relationships as hypothesized by Blondel (1988).
(Nie et al. 1975) package was used to compute a Mann-
Whitney U-test of difference of heterozygosity among
populations.
RESULTS
We were able to resolve 33 presumed genetic
loci among eight populations of Mediterranean
Alectoris, and the Perdix perdix and Phasianus col-
chicus outgroups (Table 1). Observed hetero-
zygosity ranged from 0.018 (rufa 1) to 0.085 (chu-
kar 3), and percent polymorphic loci ranged from
6.1 (barbara) to 39.4 (chukar 2, Table 2). Similar
levels of genetic variability have been observed
in many other bird species (Corbin 1987, Evans
1987). Heterozygosity did not differ between
wild and captive populations of the same spe-
cies (Mann-Whitney U-test, P < 0.05). All poly-
morphic loci were at Hardy-Weinberg equilib-
rium, excepting sME in rufa 2 and PEP-2 in
chukar 3 (P < 0.01; x2-test with Levene's [1949]
correction for small sample size, and exact prob-
ability test). A positive fixation index F (Wright
1965) indicated a significant deficiency of het-
erozygotes in both cases.
Allele frequencies over all polymorphic loci
differed significantly among all species (P <
0.01; contingency x2-test), and among the three
populations of chukar (P < 0.01) and two pop-
ulation of graeca (P < 0.05). The average F
among species was 0.75, more than eight times
higher than the average F, among conspecific
populations (0.09).
There were no fixed allelic differences be-
tween rufa and graeca. We found that chukar had
fixed allelic differences at 12% of loci from rufa
and graeca, while there were 24% fixed allelic
differences between barbara and the rufa-graeca
pair. There were 27% fixed differences between
chukar and barbara. Allele frequencies of rufa and
graeca differed significantly (single-locus con-
tingency x2-test) at six (18%) of their polymor-
phic loci. Major differences in allele frequencies
between these two species occurred at EST-2,
sGOT, and sME. The mean F, between them
was 0.572, as compared to only 0.063 and 0.076
among the two rufa and the two graeca popu-
lations, respectively. Intraspecific heterogene-
ity was greater among chukar populations (ist =
0.159).
Nei's (1978) standard unbiased genetic dis-
tances averaged 26 times larger among nominal
Alectoris species (b = 0.208; range 0.071-0.312)
than among conspecific populations (/ = 0.008;
range 0.003-0.021; Table 3). Interspecific ge-
netic distances were lowest between A. rufa and
A. graeca, but even these values (9 = 0.081; range
0.071-0.091) were 18 times larger than the av-
erage interpopulation genetic distance within
the two species (b -- 0.0045; range 0.003-0.006).
The largest genetic distance of the study was
between barbara and chukar (/ = 0.303), which
is one of the highest D-values obtained between
what are considered to be congeneric bird spe-
cies (Zink 1988, Gill and Gerwin 1989).
A phenogram was generated with the un-
weighted pair-group method using arithmetic
averages (UPGMA) of Nei's distances (Fig. 2A).
A Wagner network (Fig. 2B) was derived using
Rogers' (1972) distances. Nei's D, a nonmetric
distance measure, has been widely applied in
ornithological research and, therefore, enabled
us to compare our results with previous work.
Moreover, Nei's D is intended to estimate the
proportion of mutational divergence among
pairs of lineages, and is related to the time of
divergence from the last common ancestor in
case of regular rates of molecular evolution (Nei
1978). The two dendrograms were topologically
identical. They indicated that rufa and graeca
are most similar, linked at 0.081, followed by
chukar at 0.168, and barbara at 0.282. To construct
the Wagner tree, we used Perdix perdix and Phasi-
anus colchicus as outgroups to root the multiple-
addition-criteria network. We optimized branch
lengths to maximize goodness-of-fit statistics.
Similar lengths among sister branches suggest-
ed a regular rate of protein divergence among
the lineages. A relative rate test (Beverley and
Wilson 1984) was performed using Perdix perdix
and Phasianus colchicus as outgroups. The aver-
age ratio of branch lengths among lineages was
1.0133 + 0.0039, confirming the idea of a reg-
ular rate of protein evolution. Parsimony trees
(not shown) were derived by cladistic analysis
(PAUP) of allele distribution among species.
These agreed in topography with the dendro-
grams shown in Figure 2.
DISCUSSION
Applications of multilocus protein electro-
phoresis in the study of avian evolution have
consistently indicated a comparatively slow rate
of genetic divergence among avian taxa. Avise
and Aquadro (1982) derived an average Nei's
(1972) D of 0.08 among 173 congeneric species
of birds, an order of magnitude lower than the
average of other vertebrates. Variation of pair-
wise interspecific genetic distances is large,
ranging from 0.00 to 0.39 (Gill and Gerwin 1989,
Zink and Avise 1990). Many conspecific bird
populations are little differentiated, and it is
difficult to find local populations or subspecies
with F,-values greater than 0.05 and D greater
than 0.02 (Barrowclough 1983). Exceptions have
been found recently in some Neotropical birds,
which had comparatively large genetic dis-
tances: (a) among conspecific populations oc-
cupying separate Amazon banks (e.g. b = 0.040
between trans-Amazonian populations of Pipra
coronata; Capparella 1988); (b) among subspe-
cies (e.g. / = 0.066 among subspecies of Chi-
roxiphia pareola; Capparella 1988); and (c) among
species (Hackett and Rosenberg 1990). These
phenomena have been attributed to mecha-
nisms of geographic variation and speciation
that may be peculiar to South American birds
(Capparella 1988). Hackett and Rosenberg (1990)
have suggested the findings may indicate that
a reconsideration of the taxonomy of Neotrop-
ical birds is warranted.
While theory provides no absolute thresholds
of genetic distance for ranking bird taxa (John-
son and Zink 1983), the large body of empirical
evidence provides useful guidance. Corbin
(1987) described the occurrence of different
slopes of the regression line of D on Ft between
conspecific populations or between species.
Large, abrupt differences in D and Ft between
intraspecific and interspecific levels suggest
historical interruption of gene flow among taxa
and reorganization of the genomes (e.g. found-
er effect, random drift, natural selection), and
indicate speciation.
The average genetic distance among Alectoris
(b = 0.208) was substantially higher than values
obtained for most other congeneric bird species
(Gill and Gerwin 1989). However, the low av-
erage difference among conspecific populations
of our study (t3 = 0.008) is typical of birds in
general, and of galliforms in particular. Inter-
specific genetic distance between Lagopus lago-
pus and L. mutus in Scandinavia was 0.046, as
compared to an average of only 0.0035 and 0.0009
among their conspecific populations, respec-
tively (Gyllensten et al. 1985). The average ge-
netic distance among seven populations of Cal-
lipepla californica was 0.005 (Zink et al. 1987),
and their estimated level of gene flow of 5.5
birds per generation was nearly identical to the
rate estimated among three populations of Coli-
nus virginianus (Ellsworth et al. 1989).
Intraspecific genetic distances among the
Alectoris populations of this study ranged from
0.003 to 0.021, and were only about 5% of the
average interspecific genetic distance of 0.208.
The Fs,-values among Alectoris species were more
362 RAr E'r At. [Auk, Vol. 109
vv vv
TABLœ 2. Genetic variability at 33 loci in Mediter-
ranean Alectoris partridges.
Percent
poly- Heterozygosity
morphic
Population loci Observed Expected
A. rufa I 12.1 0.018 0.017
A. rufa 2 18.2 0.029 0.039
A. graeca I 21.2 0.052 0.051
A. graeca 2 21.2 0.042 0.053
A. chukar I 15.2 0.050 0.047
A. chukar 2 12.1 0.048 0.042
A. chukar 3 39.4 0.085 0.100
A. barbara 6.1 0.030 0.028
than eight times higher than among conspecific
populations. We found rufa and graeca to be the
least divergent species, with an average genetic
distance of 0.081, 18 times larger than their av-
erage interpopulation distance of 0.0045. Ge-
netic distances and F, within and between spe-
cies of Alectoris are comparable to the values
found in Palaearctic and North American birds
(Corbin 1987, Evans 1987). The relatively large
gap between the population and the species lev-
els suggests an extended interruption of gene
flow and an independent evolution among the
various Alectoris gene pools. The genetic dis-
tances (/ = 0.303) between barbara and chukar
populations are very high for congeneric birds.
The extent of genetic heterogeneity among chu-
kar populations (F, = 0.159) is three to five times
larger than the values usually observed among
conspecific bird populations, and indicates the
existence of significant geographic divergence
within the chukar range.
The pattern of phylogenetic relationships de-
picted by our dendrograms and cladistic trees
(Fig. 2) suggests that Alectoris species did not
result from contemporaneous episodes of spe-
ciation (i.e. as consequence of the fragmenta-
tion of an ancestral population). Rather, they
arose from at least three waves of speciation.
Therefore, the two reported hybrid zones in-
volve sister taxa (rufa and graeca) and nonsister
taxa (chukar and graeca). The ability to hybridize
is most probably attributable to the conserva-
tive morpho-anatomical evolution and conse-
quent retention of ancestral characters, rather
than to incomplete speciation (McKitrick and
Zink 1988, Cracraft 1983, 1989). The rare in-
stances of natural hybridization (which do not
compromise the evolutionary independence of
the rufa, graeca, and chukar genomes), the large
TABLE 3. Nei's (1978) genetic distances (lower left) and Rogers' (1972) genetic distances (upper right) among
Mediterranean Alectoris partridges and the outgroups Perdix perdix and Phasianus colchicus.
A B C D E F G H I L
A A. rufa 1 -- 0.019 0.114 0.108 0.181 0.159 0.183 0.249 0.605 0.572
B A. rufa 2 0.003 -- 0.107 0.100 0.177 0.155 0.176 0.245 0.601 0.566
C A. graeca 1 0.091 0.074 -- 0.035 0.210 0.194 0.188 0.252 0.592 0.563
D A. graeca 2 0.087 0.071 0.006 -- 0.197 0.177 0.179 0.253 0.605 0.563
E A. chukar 1 0.181 0.171 0.211 0.193 -- 0.042 0.059 0.284 0.628 0.567
F A. chukar 2 0.154 0.144 0.184 0.162 0.008 -- 0.065 0.270 0.626 0.566
G A. chukar 3 0.161 0.151 0.161 0.147 0.021 0.017 -- 0.287 0.628 0.571
H A. barbara 0.272 0.263 0.266 0.267 0.312 0.297 0.300 -- 0.599 0.568
I Perdix perdix 0.926 0.920 0.898 0.924 0.994 0.990 0.993 0.917 -- 0.394
L Phasianus colchicus 0.849 0.838 0.831 0.830 0.839 0.836 0.839 0.843 0.501 --
gap between interpopulation and interspecies
genetic distances, and the existence of diag-
nostic phenotypic characters indicate that the
Mediterranean Alectoris are composed of what
can be considered good evolutionary species.
A
chukar 1
chukar 2
chukar 3
graeca 1
graeca 2
rua 1
Perdix
Phasianu$
1.00 0.83 0,67 0.50 0,33 0.17 0.Nei'sD
chukar 1
chukar 2
chukar 3
graeca 1
graeca 2
rufa 1
rufa 2
barbara
Perdx
Phaslanu$
0'.00'0107 0113' 0.20 0,27' 0133' 0.40
Distance from the Root Rogers' D
Fig. 2. (A) UPGMA dendrogram of Nei's standard
unbiased genetic distances (Table 3) among Mediter-
ranean Alectoris and outgroups Perdix perdix and Phasi-
anus colchicus. Cophenetic correlation is 0.994. Time
scale computed using calibration 1 D = 22.9 myr. (B)
Wagner tree obtained from Rogers' genetic distances
(Table 3). Cophenetic correlation is 0.999.
Comparisons of sister-branch lengths in
UPGMA and Wagner dendrograms (Fig. 2), as
well as the relative rate test, indicate a rela-
tively constant rate of protein evolution in Alec-
toris. Therefore, we can attempt a calibration of
the molecular clock in order to date the diver-
gence times of Alectoris species. Based on a gal-
liform fossil (the odontophorin North Ameri-
can quail Cyrtonyx cooki), Gutierrez et al. (1983)
proposed Nei's values of 1 D = 23.6 million
years (myr). Marten and Johnson (1986) pro-
vided a similar estimate of 1 D = 19.7 myr. These
rates have proved useful in estimating times of
evolutionary branchings in several bird taxa
(Johnson and Zink 1983, Zink and Johnson 1984,
Randi et al. 1991b), and also approximate the
rate of mtDNA evolution in Ammodramus (Zink
and Avise 1990). From multiple comparisons of
nDNA (Helm-Bychowski and Wilson 1986) and
enzyme phylogenetic trees, as well as several
informative fossils, Randi et al. (1991a) derived
the calibration 1 D = 22.9 myr for phasianid
birds. Assuming this rate, we derived the fol-
lowing divergence times (Fig. 2A); (1) an initial
splitting of the ancestral Alectoris into the pres-
ent barbara and chukar lineage about 6.4 million
years ago (mya); (2) a second splitting of the
chukar and graeca-rufa lineages about 3.8 mya;
(3) a final splitting of graeca and rufa only 1.8
mya.
Our results indicate that genetic divergence
among the Mediterranean Alectoris is great and
that they can be considered good evolutionary
species, as proposed by Vaurie (1959) and Wat-
son (1962a, b). Phylogenetic relationships among
the species as indicated by our studies do not
support the evolutionary scenarios proposed by
Watson (1962a) and Blondel (1988): chukar is not
strictly related to barbara and rufa; graeca is not
the ancestral form of a superspecies encom-
passing rufa and chukar; and barbara is not the
stem species of rufa. Evolution and speciation
of Alectoris are not recent Pleistocene events as
supposed by Watson (1962a); based on our es-
timated divergence times, speciation events
could span from the Miocene-Pliocene bound-
ary to early Pleistocene. The conservative mor-
phology and the small plumage difference are
consistent with a slow rate of morphologic evo-
lution and not with recent origins of these spe-
cies.
We propose the following model of Alectoris
evolution, substantially concordant with Span0
(1975), and characterized by at least three waves
of speciation. About 6 mya, at the Miocene-Plio-
cene boundary, and ancestral species split into
barbara and in the chukar lineage. This division
occurred during a period of climatic warming
and aridity that resulted in the closure of the
Mediterranean Sea at Gibraltar and its subse-
quent dessication (Voous 1974). Concurrently,
uplift of the Carpathian Mountains created an
east-west divide of the central European plains,
and separated the Sarmatic Sea from the Med-
iterranean (Voous 1974). The climate probably
favored the spread of birds adapted to arid and
steppe habitats, such as barbara and chukar. We
suppose that geologic events resulted in an east-
west splitting of the ancestral populations in
which the chukar lineage spread eastward around
the Sarmatic Sea, while barbara spread westward
along the Mediterranean littoral of the Middle
East and Africa. Following speciation, barbara
eventually crossed the Straits of Gibraltar, and
then spread eastward along the European Med-
iterranean coasts, thereby explaining the pres-
ence of fossil barbara in France up to the middle
Pleistocene (Mourer-Chauvir 1975). Then,
about 4 mya (early Pliocene), the ancestral chu-
kar populations, spreading westward, gave rise
to the graeca-rufa lineage. Finally, at the start of
the Pleistocene glaciations, about 1.8 mya, chu-
kar populations in western Europe survived in
fragmented populations, which probably un-
derwent repeated contraction and expansion
according to climatic changes. The fossil record
indicates that barbara disappeared from Europe
during the middle Pleistocene, while both rufa
and graeca occurred in France (Mourer-Chau-
vir 1975). The origin of graeca and rufa was
probably fostered by climate-driven contrac-
tions of steppe habitat during the early Pleis-
tocene (Blondel 1988). Postglacial warming and
extensive deforestation during the Holocene
throughout the Mediterranean basin favored
expansion of the European and Middle-Eastern
populations of rufa, graeca, and chukar. They be-
came parapatric, and originated the actual zones
of overlapping and hybridization.
The model is consistent with available fossil,
biogeographic and genetic information on the
Mediterranean Alectoris. It also leads to the fol-
lowing hypothetical predictions for other Alec-
toris species: (1) First, melanocephala and philbyi,
the only two sympatric Alectoris (Watson 1962a),
arose during the first wave of speciation from
anciently separated lineages. They came into
extensive contact in the Arabian Peninsula, and
evolved character displacement and ecological
compatibility (Watson 1962a), allowing their
sympatry. From plumage characters (Watson
1962a), we hypothesize that melanocephala is re-
lated to the barbara lineage, and that philbyi is
related to the chukar lineage. (2) Second, magna
arose from ancient fragmentation of chukar pop-
ulations in China. Plumage similarities be-
tween magna and graeca resulted from conver-
gence rather than from common ancestry. This
is in contrast to Watson's (1962a) argument
that magna is a relic population of a widespread
ancestral graeca lineage. Our model indicates
that graeca never reached central Asia. These
hypotheses are amenable to testing by expand-
ing biochemical genetic research to all seven
extant species of Alectoris.
ACKNOWLEDGMENTS
We thank Ariane Bernard-Laurent and T. Crowe
for the comments and suggestions that greatly im-
proved an early version of the manuscript. We are
indebted to J. Blondel and S. J. Hackett for the ex-
cellent reviews of the paper.
LITERATURE CITED
AVISE, J. C., AND C. F. AQUADRO. 1982. A comparative
summary of genetic distances in the vertebrates.
Evol. Biol. 15:151-158.
BARROWCLOUGH, G. F. 1983. Biochemical studies of
microevolutionary processes. Pages 223-261 in
Perspectives in ornithology (A. H. Brush and G.
A. Clark, Jr., Eds.). Cambridge Univ. Press, Cam-
bridge.
BERNARD-LAURENT, A. 1984. Hybridation naturelie
entre Perdrix bartavelle (Alectoris graeca saxatilis)
et Perdrix rouge (Alectoris rufa rufa) dans les Alpes-
Maritimes. Gibier Faune Sauvage 2:79-96.
BEVERLEY, S. M., AND A. C. WILSON. 1984. Molecular
evolution in Drosophila and the higher Diptera.
II. A time scale for fly evolution. J. Mol. Evol. 21:
1-13.
BLONDEL, J. 1988. Biogographie volutive/ diff-
rentes chelles: L'histoire des avifaunes mditer-
ranennes. Pages 155-187 in Acta XIX Congr. Int.
Ornithol. (H. Ouellet, Ed.). Natl. Mus. Nat. Sci.,
Ottawa, Ontario.
BUTH, D.J. 1984. The application of electrophoretic
data in systematic studies. Annu. Rev. Ecol. Syst.
15:501-522.
CAPPARELLA, A. P. 1988. Genetic variation in Neo-
tropical birds: Implications for the speciation
process. Pages 1658-1664 in Acta XIX Congr. Int.
Ornithol. (H. Ouellett, Ed.). Natl. Mus. Nat. Sci.,
Ottawa, Ontario.
CLAYTON, J. W., AND D. N. TRETIAK. 1972. Amino-
citrate buffers for pH control in starch gel elec-
trophoresis. J. Fish. Res. Board Can. 29:1169-1172.
CORBIN, K.W. 1987. Geographic variation and spe-
ciation. Pages 321-353 in Avian genetics. A pop-
ulation and ecological approach (F. Cooke and P.
A. Buckley, Eds.). Academic Press, London.
CRCRFr, J. 1983. Species concepts and speciation
analysis. Curr. Ornithol. 1:159-187.
CRCRFr, J. 1989. Speciation and its ontology: The
empirical consequences of alternative species
concepts for understanding patterns and pro-
cesses of differentiation. Pages 60-81 in Specia-
tion and its consequences (D. Otte and J. A. End-
let, Eds.). Sinauer Associates, Sunderland, Mas-
sachusetts.
CRMP, S., AND K. E. L. SImmONS (EDs.). 1980. Hand-
book of the birds of Europe, the Middle East and
North Africa. Vol. 2, The birds of the western
Palearctic. Oxford Univ. Press, Oxford.
DAviS, B.J. 1964. Disc electrophoresis. II. Method
and application to human serum proteins. Ann.
N.Y. Acad. Sci. 121:404-427.
DEMENTIEV, G. P., AND N. A. GLADKOV (EDs.). 1952.
Birds of the Soviet Union. Translated in 1967 by
the Israel Programme for Scientific Translations,
Jerusalem.
DRAGOEV, V. 1974. On the population of the Rock
Partridge (Alectoris graeca Meisner) in Bulgaria
and methods of census. Acta Ornithol. 14:251-
255.
ELLSWORTH, D. L., J. L. ROSEBERRY, AND W. D. KLIMSTRA.
1989. Genetic structure and gene flow in the
Northern Bobwhite. Auk 106:492-495.
EVANS, P. J.H. 1987. Electrophoretic variability of
gene products. Pages 105-162 in Avian genetics.
A population and ecological approach (F. Cooke
and P. A. Buckley, Eds.). Academic Press, Lon-
don.
GILL, F. B., AND J. A. GERWIN. 1989. Protein relation-
ships among Hermit Hummingbirds. Proc. Acad.
Nat. Sci. Phila. 141:409-421.
GUTIeRReZ, R. J., R. M. ZINK, AND S. Y. YANG. 1983.
Genetic variation, systematic, and biogeographic
relationships of some galliform birds. Auk 100:
33-47.
GYLLENSTEN, U., N. RYMAN, AND T. SAETHER. 1985.
Genetic divergence between Willow Grouse (La-
gopus lagopus L.) and Rock Ptarmigan (Lagopus mu-
tus L.) and the genetic structure of Scandinavian
grouse populations. Hereditas 102:47-55.
HACKETT, S. J., AND K. V. ROSENBERG. 1990. Com-
parison of phenotypic and genetic differentiation
in South American antwrens (Formicariidae). Auk
107:473-489.
HARRIS, H., AND D. A. HOPKINSON. 1976. Handbook
of enzyme electrophoresis in human genetics.
North Holland Publishing Co., Amsterdam.
HELM-BYCHOWSKI, K. M., AND A. C. WILSON. 1986.
Rates of nuclear DNA evolution in pheasant-like
birds: Evidence from restriction maps. Proc. Natl.
Acad. Sci. USA 83:688-693.
JOHNSGARD, P.A. 1988. The quails, partridges, and
francolins of the world. Oxford Univ. Press, Ox-
ford.
JOHNSON, N. K., AND R. M. ZINK. 1983. Speciation
in sapsuckers (Sphyrapicus): I. Genetic differen-
tiation. Auk 100:871-884.
JOLLE"V, W. B., AND H. W. ALLEN. 1965. Formation of
complexes between basic proteins of leucocytes
and plasma globulins. Nature 208:390-391.
LEVENE, H. 1949. On a matching problem arising in
genetics. Ann. Math. Stat. 20:91-94.
MACLELLAN, T., AND J. A.M. RAMSHAW. 1981. Serial
electrophoretic transfers: A technique for the
identification of numerous enzymes from single
polyacrylamide gels. Biochem. Genet. 19:647-653.
MARTEN, J. A., AND N. K. JOHNSON. 1986. Genetic
relationships of North American cardueline
finches. Condor 88:409-420.
McKITRICK, M., AND R. M. ZINK. 1988. Species con-
cepts in ornithology. Condor 90:1-14.
MENZDORF, A. 1984. Zur Kenntnis des Sozialver-
haltens und der Lautiu0erungen einiger Feld-
huhnarten (Phasianidae, Perdicinae: Alectoris
spp.). Vogelwelt 105:9-21.
MOURER-CHAUVIR, C. 1975. Les oiseaux du Pleis-
tocene moyen et suprieur de France. Thse d'Etat,
Univ. Claude-Bernard, Lyon.
NE,M. 1972. Genetic distance between populations.
Am. Nat. 106:283-292.
NEI, M. 1978. Estimation of average heterozygosity
and genetic distance from a small number of in-
dividuals. Genetics 89:583-590.
NIE, N. H., C. H. HULL, J. G. JENKINS, K. STEINBRENNER,
AND D. H. BENT. 1975. Statistical package for the
social sciences. McGraw-Hill, New York.
PETERS, J.L. 1934. Check-list of birds of the world,
vol. 2. Harvard Univ. Press, Cambridge.
RANDI, E., G. FUSCO, R. LORENZINI, AND T. M. CROW.
1991a. Phylogenetic relationships and rates of
allozyme evolution within the Phasianidae. Bio-
chem. Syst. Ecol. 19:213-221.
RANDI, E., G. FUSCO, R. LORENZINI, AND F. SPINA. 1991b.
Allozyme divergence and phylogenetic relation-
ships within the Strigiformes. Condor 93:295-
301.
ROGERS, J. S. 1972. Measures of genetic similarity
and genetic distance. Studies in Genetics, Univ.
Texas Publ. 7213:145-153.
SHORT, L.H. 1969. Taxonomic aspects of avian hy-
bridization. Auk 86:84-105.
StmA?H, P. H., AD R. R. SOV, AL. 1973. Numerical
taxonomy. W. H. Freeman and Co., San Francisco.
SOV, AL, R. R., AD F. J. ROHF. 1981. Biometry, 2nd
ed. W. H. Freeman and Co., San Francisco.
SPAC, S. 1975. Considerazioni biogeografiche sul
genere Alectoris Kaup, 1829 (Galliformes, Phasi-
anidae). Ann. Mus. Civ. Stor. Nat., Genova 80:
286-293.
SWOFFORV, D.L. 1981. On the utility of the distance
Wagner procedure. Pages 25-43 in Advances in
cladistics: Proceedings of the first meeting of the
Willi Hennig Society (V. A. Funk and D. R.
Brooks, Eds.). New York Botanical Garden, Bronx.
SWOFFORV, D.L. 1985. PAUP, Phylogenetic analysis
using parsimony, version 2.4. Illinois Nat. Hist.
Surv., Champaign.
SWOFFORV, D. L., AV R. K. SEDER. 1989. BIOSYS-
1. A computer program for the analysis of allelic
variation in population genetics and biochemical
systematics, release 1.7. Illinois Nat. Hist. Surv.,
Champaign.
VAURIE, C. 1959. The birds of the Palearctic fauna.
Non-Passeriformes. H. F. and G. Witherby, Lon-
don.
Voovs, K.H. 1960. Atlas of European birds. Nelson,
London.
Voovs, K.H. 1974. The birds of the tropical 'Middle
Seas,' past and present. Pages 697-704 in Proc.
XVI Congr. Int. Ornithol. (H. J. F. Frith and J. H.
Calaby, Eds.). Canberra, Australia.
WATSON, G.E. 1962a. SympatryinPalearcticAlectoris
partridges. Evolution 16:11-19.
WATSON, G. E. 1962b. Three sibling species of Alec-
toris partridges. Ibis 104:353-367.
WIrrs, D. E., AV R. A. REISFV. 1964. Disc elec-
trophoresis in polyacrylamide gels: Extension to
new conditions of pH and buffers. Ann. N.Y.
Acad. Sci. 121:373-381.
WORKMAN, P. L., An J. D. NISWANDER. 1970. Pop-
ulation studies on southwestern Indian tribes. II:
Local genetic differentiation in the Papayo. Am.
J. Hum. Genet. 22:24-29.
WRYtilT, S. 1965. The interpretation of population
structure by F-statistics with special regard to sys-
tems of mating. Evolution 19:395-420.
WRIGHT, $. 1978. Evolution and the genetics of pop-
ulations. Vol. 4, Variability within and among
natural populations. Univ. Chicago Press, Chi-
cago.
ZINc, R.M. 1988. Evolution of Brown Towhees: A1-
lozymes, morphometrics and species limits. Con-
dor 90:72-92.
Zc, R. M., A J. C. AvsE. 1990. Patterns of mi-
tochondrial DNA and allozyme evolution in the
avian genus Ammodramus. Syst. Zool. 39:148-161.
Zc, R. M., AV N. K. JOHnSOn. 1984. Evolutionary
genetics of flycatchers. I. Sibling species in the
genera Empidonax and Contopus. Syst. Zool. 33:
205-216.
ZIc, R. N., D. F. Lor, AD D. W. AVRSO. 1987.
Genetic variation, population structure, and evo-
lution of California quail. Condor 89:395-405.