Evolution, 55(10), 2001, pp. 2097–2104

ALBINISM AND PHENOTYPE OF BARN SWALLOWS (HIRUNDO RUSTICA)
FROM CHERNOBYL
A. P. MøLLER1,2 AND T. A. MOUSSEAU3
1 Laboratoire d’Ecologie Evolutive Parasitaire, Centre National de la Recherche Scientifique, Formation en Recherche de la

Evolution 2365, Université Pierre et Marie Curie, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
2 E-mail: amoller@hall.snv.jussieu.fr
3 Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208
Abstract. The effects of mutation on phenotypic expression are supposed to be mainly deleterious because mutations
disrupt the expression of genes that function relatively well under current environmental conditions. Thus, mutations
are assumed to give rise to deviant phenotypes that are generally selected against. Radioactive contamination in the
Chernobyl region of Ukraine is associated with a significant increase by a factor two to 10 in mutation rate in
microsatellite markers of the barn swallow, Hirundo rustica. Barn swallows from Chernobyl had a temporally constant,elevated frequency of partial albinism compared to the situation before radioactive contamination and compared tobirds from a control area. Albinism disproportionately affected the carotenoid-based plumage of the head, suggestingthat carotenoid metabolism is particularly susceptible to the effects of radiation. Individuals with partially albinistic
plumage had, on average, lower mean phenotypic values than other birds, and this was particularly the case for males.
Furthermore, differences in phenotypic variation, as determined using Levene’s test, were significantly larger in partial
albinos compared to nonalbinos in males, but not in females, even though the null expectation would be the opposite
due to the lower mean phenotypic values of partial albinos. Although small phenotypes were commonly associatedwith germline mutations, there was no general decrease in overall body size during the period 1991–2000, implyingthat small individuals were selected against. Because partial albinism is disfavored by natural selection, the effects
of mutations are deleterious, giving rise to a balance between mutation and selection.
Key words.
selection.

Albinism, carotenoids, mutation, phenotypic coefficient of variation, phenotypic correlation, radiation,

Received November 22, 2000.

Mutation is a major factor contributing to the maintenanceof genetic variation (Lynch et al. 1999). Most mutations are
believed to be mildly deleterious with weakly negative effects
on fitness (reviewed in Lynch et al. 1999) because any change
in a DNA sequence will usually result in a reduction in thequality of the phenotype compared to what was produced by
the original sequence. Any change in a coadapted gene sequence will generally produce a different protein that will
result in the production of an inferior phenotype. Experimental studies in laboratory lines of Drosophila and Caenorhabditis have generally confirmed these effects (Lynch etal. 1999; Vassilieva et al. 2000). The decline in fitness per
generation in such experiments is typically in the order of
0.1–1% per generation (Lynch et al. 1999; Vassilieva et al.
2000). However, it may be difficult to extrapolate these results from the laboratory to the field because of the generally
more benign and stable environment in the laboratory.
There are very few studies of the effects of mutations on
phenotypic expression and selection under field conditions.
Of particular interest are studies finding increased mutation
rates in humans and barn swallows (Hirundo rustica) fromthe radioactive contaminated area around Chernobyl in
Ukraine (Dubrova et al. 1996; Ellegren et al. 1997). In studies
of humans mutation rates of minisatellite DNA increased bya factor two (Dubrova et al. 1996), whereas Ellegren et al.
(1997) reported an increase in mutation rates in barn swallow
microsatellite DNA by a factor two to 10. Furthermore, thegenome of somatic cells of mice exposed to radiation has
been shown to remain fragile across generations, extendingat least to the first generation (Dubrova et al. 2000). Indirect
estimates of mutation rates based on the frequency of cellswith aberrant micronuclei and chromosomes have shown thatsimilarly increased levels of cellular disruption exist in otherorganisms in contaminated areas around Chernobyl (Zakharov and Krysanov 1996).
Previous studies of the barn swallow in Chernobyl haveshown that the level of fluctuating asymmetry in the outermost
tail feathers of males increased by a factor seven in the Chernobyl area following 1986 compared to a less contaminatedcontrol area in Ukraine (Møller 1993) and museum samples
from the same areas before that date (Møller 1993). A totalof 15 different organisms have shown increased fluctuating
asymmetry around Chernobyl when compared to samples fromless contaminated areas (Møller 2001). Also, deformation of
the tips of the outermost tail feathers has been recorded in low
frequency from Chernobyl, but not from elsewhere in the rangeof the species (Møller 1993), and both malformation and asymmetry are associated with a delay in breeding date of malebarn swallows (Møller 1993). This indicates that sexual selection is acting against males with malformed and asymmetrictails. Partial albinism is an uncommon plumage aberration ofgenetic origin in birds that rarely amounts to more than 1%of all individuals (Sage 1962; Dyck 1985). Barn swallows from
Chernobyl have a highly elevated frequency of partial albinism, reaching 13–15% (Ellegren et al. 1997), and this albinism is of germline origin as determined from a significant
parent-offspring resemblance (Ellegren et al. 1997). Field studies of house sparrows (Passer domesticus) in other areas havefound that partial albinism is more common in cities (1–2%)
and smaller towns than in the countryside, where the frequencyof albinism is close to 0% (Il’enko 1960). This suggests thatthe factors associated with albinism are more prevalent inpolluted, urban areas.
A disproportionate fraction of partial albinism in the barn

2097
q 2001 The Society for the Study of Evolution. All rights reserved.

Accepted July 17, 2001.

2098

ALBINISM AND PHENOTYPE

FIG. 1. A partially albinistic barn swallow from the Chernobyl region with a typical small number of white feathers in the red facialplumage and an individual with a normal phenotype (right). Photograph by T. A. Mousseau.

swallow occurs in the carotenoid-based facial plumage, but
hardly any in the dark blue plumage of the neck, back, wings,
and tail (Camplani et al. 1999). The coloration of carotenoidbased red plumage was significantly reduced in Chernobyl
barn swallows, especially in males (Camplani et al. 1999).
Whereas males with longer, and thus more attractive, outermost tail feathers generally have a brighter red coloration,
long-tailed males from Chernobyl were no more bright redcolored than short-tailed males (Camplani et al. 1999).
The aims of the present study were to test three predictions
related to the phenotypic effects of mutations, using barnswallows from Chernobyl as a test case. First, we tested
whether mean phenotypic values of morphological traits werereduced in mutants compared to control individuals, using
partial albinism as a phenotypic marker of mutations. Second,
we tested whether the coefficient of variation for morphological traits differed between partial albinos and other individuals. Third, because the phenotypic characters of barnswallows have significant heritabilities (Møller 1994; Sainoet al. 1997; A. P. Møller, F. de Lope, and N. Saino, unpubl.
data) and the germline mutations giving rise to partial albinism are also associated with small phenotypes, we should
expect an increase in the frequency of partial albinism anda decrease in overall size during the three sampling eventsin 1991, 1996, and 2000, unless albinistic and small individuals were selected against. Because annual survival rate
is about 30% (Møller 1994), less than 1% of individuals inany given year would be present after four years, and differences in mean phenotype among the three sampling eventsshould be due to a response to selection.
MATERIALS AND METHODS
Study Area

FIG. 2. Temporal pattern of the frequency of partial albinism inbarn swallows from Chernobyl and Kanev, Ukraine. Numbers are
sample sizes.

We studied barn swallows in parts of the southern and western sector just outside the exclusion zone of the Chernobyl
area (Shestopalov 1996) during 10–29 June 1991 (APM), 16–
24 June 1996 (APM), and 6–12 June 2000 (APM, TAM). We
visited villages and stopped to check collective farms for thepresence of barn swallows. If found, we attempted to capture
as many adults as possible at windows and doors of farmbuildings using mist nets. Based on our experience, this method usually results in the capture of more than three-quartersof all barn swallows during a single day. The villages visitedand used for the study included Guda-Katyuzhanka, Kathyuskanka, Obukovichy, Phenevichy, Ivankov, Vakhovka, Glybovka, Pribirsk, Dytiatku, Pysky, Varonychi, Martynovichi,
Bober, Vesniane, and Dymir. As a control area, we used Kanev(;220 km southwest of Kiev), which has a relatively low levelof contamination. The low level of contamination was confirmed by our own measurements of radioactivity during thefield season in 2000. The control villages visited and used forthe study included Kanev, Stepatsy, and Stepanetske.

2099

A. P. MØLLER AND T. A. MOUSSEAUTABLE 1. Mean squares from three-way analyses of variance with sex, partial albinism, and year as factors for morphological traits of barnswallows from Chernobyl. The residual degrees of freedom are 254.
VariableSex (S)

Albinism (A)S3A

Year (Y)

S3Y

A3Y

S3A3Y

Beak length (mm)Beak height (mm)Beak width (mm)Tarsus (mm)Keel (mm)Wing (mm)Wingspan (mm)Tail (mm)Central tail (mm)Body mass (g)
df

11.61
1.91
21.74
4.12
339.03*5.36
85.31
7175.43***3.38
234.22***
1

126.97*2.05
51.37
305.03***65.19
44.28*
208.78*178.64
7.65
29.82
1

3.91
12.52
15.74
0.65
352.34*
32.48
27.55
74.17
6.00
9.02
1

589.37***462.43***629.39***5402.03***468.42**
1.39
2.75
190.29*60.84***
53.21*
2

10.41
0.74
69.28
51.95
20.16
14.57
41.22
17.92
1.67
53.77*
2

234.06***
6.33
53.97
9.52
55.20
4.51
41.44
116.92
0.81
27.86
2

1.68
3.21
11.62
35.59
59.06
30.85*
50.79
27.78
3.25
21.06
2

* P , 0.05, ** P , 0.01, *** P , 0.001.

Partial Albinism

Statistical Analyses

When an adult barn swallow was captured, we carefully
inspected its plumage for any signs of white feathers in theotherwise red and blue colored parts of the body. Any deviant
plumage coloration was recorded, and individuals with one
or more white feathers present in otherwise red or blue feather
tracts were classified as partial albinos. Usually only a few
feathers were white, but some individuals had a large numberof white feathers (Fig. 1).
Upon capture, a large number of morphological traits were
measured by APM in the same, standardized way. We measured the length of the beak to the feathering, the height ofthe beak at the distal end of the nares, and the width of thebeak at the commisure to the nearest 0.01 mm with a digital
caliper. Tarsus length and the length of the keel were measured likewise. The length of the right and the left flattenedwing, the right and the left outermost tail feather, and theleft and the right central tail feather were measured with aruler to the nearest 1 mm. Tail and wing length were subsequently defined as the mean of the left and the right measurement. We measured wingspan by stretching the wings to
the maximum possible and then recording the distance between the wing tips. Body mass was recorded with a Pesolabalance to the nearest 0.1 g. All measurements were highly
repeatable as demonstrated by repeat measurements of thesame individuals (Møller 1994).

We tested for differences in the frequency of partial albinism among periods and study regions using G-tests (Sokal
and Rohlf 1995). Three-way analysis of variance (ANOVA)
was used to test for phenotypic differences among albinos
and sexes and any interaction effects, while taking differencesamong years into account. Mean values for partially albinistic
and nonalbinistic individuals of each sex were compared using a paired t-test on log10-transformed values. Furthermore,
the difference in mean phenotype between albinistic and nonalbinistic individuals of each sex was compared with the null
expectation of no difference using a one-sample t-test, anddifferences for males were compared with differences forfemales using a paired t-test.
We used a principal component analysis with the varimax
procedure to extract the first five principal components fromthe 10 phenotypic variables. The scores were subsequently
used for two-way ANOVAs to test whether they differed withrespect to albinism, sex, and their interaction.
Comparison of phenotypic variation for partially albinistic
and nonalbinistic individuals of each sex was made using
Levene’s test for unequal variances, after logarithmic transformation of the variables. Tests were made separately foreach of the three periods for each sex. The null expectationin this case is that 5% of all tests are statistically significant
and that equally many tests will have a greater variance foralbinistic and nonalbinistic individuals.

TABLE 2. Mean (SE) phenotypic characters for partially albinistic and nonalbinistic male and female barn swallows from Chernobyl. Meanvalues with different superscripts are significantly different (P , 0.05) according to Fisher’s PLSD tests.
Variable

Male nonalbinos

Male albinos

Beak length (mm)Beak height (mm)Beak width (mm)Tarsus (mm)Keel (mm)Wing (mm)Wingspan (mm)Tail (mm)Central tail (mm)Body mass (g)N

7.84 (0.05)
2.60 (0.03)
11.73 (0.07)
11.57 (0.09)a
21.05 (0.08)
125.21 (0.29)a331.41 (0.68)
109.31 (0.89)a44.50 (0.16)
18.87 (1.16)
121

7.73 (0.15)
2.54 (0.09)
11.70 (0.16)
11.38 (0.24)b
20.73 (0.22)
123.52 (0.80)b
329.10 (1.01)
104.37 (1.94)b
44.29 (0.63)
18.60 (1.86)
21

a

b

Female nonalbinos

Female albinos

7.93 (0.05)
2.57 (0.03)
11.72 (0.07)
11.63 (0.10)a20.40 (0.10)
123.80 (0.28)
328.87 (0.65)
91.98 (0.62)
45.34 (0.20)
19.61 (1.45)
102

7.61 (0.13)b
2.62 (0.07)
11.51 (0.12)
11.35 (0.21)b
20.58 (0.15)
123.50 (0.68)
327.14 (1.36)
91.28 (1.51)
44.50 (0.60)
19.50 (3.37)
22

a

2100

ALBINISM AND PHENOTYPE

TABLE 3. Analysis of variance for the effect of year, area, and sex on phenotypic characters of male and female barn swallows from Chernobyl
and Kanev. Mean values (SE) for different years with different superscripts are significantly different (P , 0.05) according to Fisher’s PLSD
tests.

Variable

Beak length (mm)Beak height (mm)Beak width (mm)Tarsus (mm)Keel (mm)Wing (mm)Wingspan (mm)Tail (mm)Central tail (mm)Body mass (g)PC1df

Year (Y)Area (A)Sex (S)

Y3A

Y3S

A3S

Y3A3S

Residual

588.05***2029.96***708.71***8048.50***
1428.42***4.08
185.74*269.70*101.45***473.38***97.37***
2

111.79*77.34***
363.39**1761.20***35.08
71.98**
33.79
147.060.81
319.10***
1.04
1

11.13
0.17
11.97
154.904691.40***244.37***1265.37***
32,864.96***
38.89***
680.58***0.60
1224.38***34.44**
592.14***
2463.34***
153.28*21.46
243.44**19.75
28.73***
750.72***
1.68
2

9.31
2.21
7.80
152.24*
25.42
1.46
14.22
0.29
2.62
92.86**
0.27
2

8.64
3.08
12.71
89.94
41.58
15.05
148.86250.04
0.52
4.71
0.68
1

3.78
6.07
8.40
60.48
79.37
1.86
13.24
28.24
2.24
30.22
0.35
2

24.26
4.93
36.85
49.20
66.35
9.10
44.40
60.56
3.51
17.11
0.79
478

* P , 0.05, ** P , 0.01, *** P , 0.001.

We tested for temporal trends in phenotype by investigating whether mean phenotypes differed among 1991, 1996,
and 2000 using a three-way ANOVA with area, sex, andperiod as factors. The absence of partial albinos in some ofthe samples from the control area prevented us from includingthat factor into the ANOVA models.
RESULTS
Patterns of Partial Albinism
The percentage of individuals that were partial albinos washigh in the Chernobyl area after the radioactive contaminationin 1986, but not in museum samples predating that period(Fig. 2). For the control area, there was no such temporal
trend, and the percentage of partial albinos was consistently
low (Fig. 1). The difference between pre- and post-1986 samples for Chernobyl was statistically significant (G 5 12.79,
df 5 3, P , 0.02). Similarly, the difference between Chernobyl and Kanev post-1986 was statistically significant (G5 36.25, df 5 3, P , 0.001). There was no significant difference among years in the frequency of albinism in Chernobyl after 1986 (G 5 0.53, df 5 2, ns). Among the 43
partially albinistic individuals, 42 had white feathers in the
red facial plumage and one in the blue dorsal plumage. Given
that the red plumage accounts for less than 10% of the bodysurface, this distribution was significantly different from arandom expectation (G 5 184.13, df 5 1, P , 0.001).
Mean Phenotype of Partial Albinos and Controls
ANOVAs revealed significant effects of partial albinism
for four of the 10 morphological characters (Table 1), withmean values for partially albinistic individuals being smaller
than for nonalbinistic ones (Fisher’s PLSD test, P , 0.05).
The sex by albinism interaction, the albinism 3 year interaction, and the sex 3 albinism 3 year interaction were eachsignificant for a single character (Table 1). Mean values forthe 10 morphological characters were significantly smaller
for partial albinos than for nonalbinos in males (Table 2;paired t-test based on log10-transformed data: t 5 4.05, df 5
9, P 5 0.003), but not significantly so in females (Table 2,paired t-test: t 5 1.73, df 5 9, P 5 0.12). The difference inmean value between partial albinos and nonalbinos for males
did not differ significantly from that of females (paired t-test
based on log10-transformed data: t 5 0.86, df 5 9, P 5 0.41).
A factor analysis using the orthogonal varimax approach
extracted five principal component axes from the 10 variables. The first axis explained 24.3% of the variance, while
the following axes each explained 8.6–18.9% of the variance.
The first five axes explained in total 76.3% of the variance.
The first axis was positively correlated with all 10 variables,with wingspan (r 5 0.842), keel length (r 5 0.545), winglength (r 5 0.828), and tail length (r 5 0.567) having large
correlation coefficients. A two-way ANOVA on principal
component 1 scores gave a significant effect for albinism (F5 4.421, df 5 1, 225, P 5 0.037) and sex (F 5 4.384, df
5 1, 225, P 5 0.037), but not for the interaction (F 5 1.116,
df 5 1, 225, P 5 0.298). Mean score for albinistic birds was
20.335 (SE 5 0.160), whereas it was 0.072 (SE 5 1.047)
for nonalbinistic birds. None of the other principal component
axes showed significant differences with respect to albinism.
Variance in Phenotype of Partial Albinos and Controls
We compared variances for albinistic and nonalbinistic individuals for logarithmically transformed variables using
Levene’s test. For males we found significantly larger variances for partial albinos for five different characters (beakheight 1991: F 5 4.12, df 5 1, 61, P 5 0.047; central tail1991: F 5 7.85, df 5 1, 61, P 5 0.0069; keel 1996: F 5
4.43, df 5 1, 35, P 5 0.043; tail 1996: F 5 5.96, df 5 1,
35, P 5 0.020; central tail 1996: F 5 6.14, df 5 1, 35, P 5
0.018). The observed number of significant tests of five exceeds the expected number of 1.5 (30 tests times 0.05) by afactor of three. Furthermore, all tests showed larger varianceamong partial albinos, whereas the predicted number was
only half the tests. Among females, only two tests were statistically significant compared to the expected 1.5 tests (wing1996: F 5 5.18, df 5 1, 36, P 5 0.029; keel 2000: F 5 5.66,
df 5 1, 37, P 5 0.023). Whereas partial albinos had larger
variance than nonalbinos for wing length in 1996, the pattern
was the reverse for keel length in 2000.

2101

A. P. MØLLER AND T. A. MOUSSEAUTABLE 3. Extended

Chernobyl
Variable

1991

Beak length (mm)Beak height (mm)Beak width (mm)Tarsus (mm)Keel (mm)Wing (mm)Wingspan (mm)Tail (mm)Central tail (mm)Body mass (g)PC1N

7.76 (0.05)
2.91 (0.03)a11.38 (0.07)a
12.69 (0.05)a
20.99 (0.08)a
124.16 (0.28)
329.70 (0.62)
99.95 (1.32)
45.13 (0.26)a
19.24 (0.17)
20.10 (0.11)
99

Kanev

1996
a

2000

7.63 (0.05)
2.44 (0.02)b
12.18 (0.07)b
11.01 (0.06)b
20.43 (0.13)b
124.56 (0.39)
330.56 (0.81)
101.38 (1.36)
45.84 (0.13)b
19.00 (0.13)
0.07 (0.13)
75
a8.12 (0.05)
2.36 (0.02)c
11.68 (0.07)c
10.85 (0.05)c
20.74 (0.10)a124.48 (0.36)
329.59 (0.80)
101.26 (1.21)
43.62 (0.16)c
19.26 (0.14)
0.04 (0.12)
92

Temporal Change in Phenotypes
We found statistically significant year by area interactions
for eight of the 10 morphological characters (Table 3). Six
variables showed significant sex effects, and two of the sex
3 year interactions were statistically significant. In Chernobyl, only tarsus and beak height showed a consistently
decreasing pattern during the three study years. For overall
body size, estimated as the principal component 1 scores,
there was no significant difference in mean phenotype among
years (Table 3). There was also a decrease in phenotype in
the control area for tarsus length and beak height, but thesechanges differed significantly between areas, as indicated by
the highly significant area 3 year interactions (Table 3).
DISCUSSION
Partial albinism in birds arises as a consequence of somaticor germline mutations (Sage 1962; Dyck 1985). There is little
information on the frequency of this phenomenon in othertaxa and even less on the potential consequences (e.g., Laikre
1999; Bolker and Hill 2000). Previous studies of partial albinism in barn swallows from Chernobyl have shown thatthe frequency of partial albinism is elevated by a factor of
10 compared to before the radioactive contamination in 1986
and compared to a less contaminated control area (Ellegren
et al. 1997). This finding was replicated in the present study(Fig. 2), suggesting that an elevated frequency of partiallyalbinistic individuals still persists and that there is constancy
in the frequency of partial albinos over time. Comparisonsof the phenotype of parents and their offspring have revealed
a significant resemblance with respect to partial albinism(Ellegren et al. 1997), suggesting that partial albinism iscaused by germline mutations. The increase in the frequencyof partial albinos in the Chernobyl region is of a magnitude
similar to the increase in microsatellite mutation rates of barnswallows from this area (Ellegren et al. 1997). Thus, there
is consistency between the frequency of partial albinos andthe frequency of microsatellite mutations.
A disproportionate number of cases of partial albinism
occurred in the red facial plumage, which has a coloration
based partly on carotenoids, particularly lutein, whereas theblue dorsal coloration rarely had white feathers. This result

b

1991

1996

2000

7.83 (0.04)
3.11 (0.02)
11.94 (0.05)
11.42 (0.05)
21.19 (0.07)
125.69 (0.20)
326.63 (0.62)
100.14 (1.10)
44.40 (0.17)
18.77 (0.12)
20.01 (0.09)
141

8.01 (0.07)
2.49 (0.03)
11.98 (0.09)
11.05 (0.04)
20.55 (0.12)
124.77 (0.38)
330.00 (0.80)
103.06 (1.81)
45.94 (0.18)
21.17 (0.18)
0.07 (0.14)
51

8.09 (0.08)
2.39 (0.03)
11.96 (0.07)
10.75 (0.08)
20.75 (0.12)
125.00 (0.44)
330.34 (1.03)
101.24 (1.92)
44.55 (0.25)
19.26 (0.18)
0.11 (0.17)
55

suggests a physiological link between mutation and carotenoids. This suggestion is further supported by the fact thatmale barn swallows from Chernobyl have a pale red coloration compared to males from a control area, in particular inmales with long outermost tail feathers (Camplani et al.
1999). In contrast, there was no difference in coloration between females from Chernobyl and females from control areas (Camplani et al. 1999). Long-tailed males are usually
very attractive to females (Møller 1994), and they are also
usually in prime health status as indicated by high plasma
levels of carotenoids and low circulating levels of leukocytes
and immunoglobulins (Saino et al. 1999). Because carotenoids have the dual function of immuno-enhancement and freeradical scavenging, long-tailed males from Chernobyl may
face a different trade-off between use of carotenoids for signals and free-radical scavenging when compared to males
from other populations (Ames 1983; Krinsky 1989, 1998;
Edge et al. 1997; Rice-Evans et al. 1997; Bast et al. 1998;
Rao and Agarwal 1999; for an extensive review, see Møller
et al. 2000). Hill (1999) suggested that these patterns were
not clear, but he based this conclusion on a very small fractionof the available evidence, which is fully reviewed in Møller
et al. (2000). Camplani et al. (1999) hypothesized that malebarn swallows in the Chernobyl region may use large amountsof carotenoids for free-radical scavenging, leaving little left
for the production of plumage signals. Because long-tailed
male barn swallows are particularly successful in terms ofmating, elevated activity due to mating effort by such males
may produce large amounts of free radicals that must be
neutralized by carotenoids, that is, radioactive contamination
may be an additional factor contributing to the use of carotenoids in the Chernobyl population.
We used partial albinism as a phenotypic marker of mutation in the present study. This approach is justified by thegermline nature of partial albinism of barn swallows fromthe Chernobyl region (Ellegren et al. 1997). If carotenoids
play an important role in free-radical scavenging in the barnswallow, we could hypothesize that the suboptimal development of phenotypic traits would correlate with the presenceof partial albinism, assuming that the absence of red plumage
coloration is indicative of disrupted carotenoid absorption,
deposition, or utilization. We are currently investigating pat-

2102

ALBINISM AND PHENOTYPE

terns of carotenoid distribution in barn swallows from Chernobyl and uncontaminated populations.
Partially albinistic male barn swallows were characterized
by reduced mean phenotypic values compared to barn swallows without signs of partial albinism (Tables 1, 2). This was
the case both for skeletal characters that develop during early
ontogeny in the nest, such as beak length, but also for feather
characters that develop once a year in the African winterquarters (these include wing and tail length and wingspan).
A potential mechanism accounting for this effect is that theefficiency of the antioxidant function of a given amount ofcarotenoids is limited in Chernobyl due to the effects of radiation. Growth, which is a process that generates free radicals, may be inhibited by the lack of available free-radical
scavengers (i.e., carotenoids). However, although females
were almost equally likely to show partial albinism (Table2), there was no significant relationship between albinismand morphological trait values among females. While themean difference between albinos and nonalbinos accounted
for 64.6% of the variance in mean phenotypic values of males(r2 5 t2/[t2 1 df], where r is Pearson’s product-moment correlation coefficient and t is the t-statistic; Rosenthal 1994),
the comparable estimate for females was 25.0%, or less thanhalf of that in males. At present we have no easily testable
hypotheses to explain the observed sexual dimorphism inphenotypic correlations to albinism in this species. We hypothesize that male barn swallows may be more limited bycarotenoid availability than females, because only males from
Chernobyl had a reduction in the intensity of red plumage
coloration (Camplani et al. 1999), perhaps due to the greater
needs for carotenoids by males for coloration, immune function, and free-radical scavenging.
If there is natural selection against mutants, we might expect that the category of partially albinistic birds contained
a smaller frequency of juveniles. This could bias some of thecalculations due to age-dependent changes in phenotype.
Whereas skeletal characters change very little or not at all
in a cohort of birds, feather characters have been shown tochange. For example, wing and tail length increase slightly
from the first to the second and much less to the third yearof life, with a subsequent decrease due to senescence (Møller
1991; Møller and de Lope 1999). These changes are verysmall, averaging about 2 mm for male tail length between
year 1 and 2. Given that annual survival rate is about 30%(Møller 1994), birds older than one year comprise about 12%of the population. However, even in the unlikely event that
the Chernobyl population consisted of two or three times as
many old birds as other populations, this could not accountfor the mean difference of 5 mm in tail length between albinistic and nonalbinistic males (Table 2). Although we could
not determine the age of the birds from Chernobyl, it seems
unlikely that age-dependent mortality could account for thephenotypic differences between albinistic and nonalbinistic
individuals.
Given that partially albinistic barn swallows generally had
lower mean phenotypic values we should expect a priori that
their variance in phenotype also should be smaller than thatof nonalbinistic individuals. This prediction is based on thecommon observation that means and variances are positively
correlated. Surprisingly, we found that partially albinistic

male barn swallows had significantly higher phenotypic variation than nonalbinistic individuals for five different tests,
whereas the expected number of tests showing such a pattern
was only 0.75. This pattern was not true for females: Onlya single test showed a larger variance in albinos compared
to nonalbinos, whereas the opposite pattern was observed foranother character. The expected number of tests for females
showing these results was 0.75, which is close to the observed
number. Thus, partially albinistic male barn swallows seemed
to have a wider range of phenotypes compared to nonalbinistic individuals, which was not the case in females. Again,
it is not obvious why the effects of mutation should be greaterin males than in females.
The fitness costs of mutations have been debated to a considerable extent during the past few decades (review in Lynch
et al. 1999). The aberrant white plumage color of barn swallows from Chernobyl was associated with a generally small
body size, and this may be costly for the following reasons.
Because germline mutations arise every generation, we
should expect a steady decrease in mean phenotypic values
with time and an increase in partial albinism in barn swallows
from the Chernobyl region, because an increasing fraction of
the population would be comprised of mutants, unless small,albinistic mutant phenotypes were selected against. Six ofthe 10 morphological characters showed significant variation
among samples from 1991, 1996, and 2000 (Table 3). Only
two of these characters demonstrated a steady decrease inphenotype, whereas the others showed no consistent temporal
pattern. Tarsus length decreased by 3.7 standard deviations
during 1991–2000 in Chernobyl, and beak height decreasedby 2.8 standard deviations during the same period. The same
person measured all birds in a standardized way, thus thedifferences cannot be attributed to changes in measurement
methods or definitions of characters. These changes are verylarge compared to responses to selection recorded in otherbirds, such as 0.50–0.75 standard deviations in Darwin’s
finches (Grant and Grant 1995) and a similar magnitude oreven larger in cliff swallows (Petrochelidon pyrrhonota;
Brown and Brown 1998; Price et al. 2000). The initial responses to selection in the studies by Grant and Grant (1995)
and Brown and Brown (1998) were subsequently followedby evolutionary responses in the opposite direction.
Given that different morphological characters showed different temporal patterns of change, it might be more appropriate to investigate the overall measure of body size reflectedby the first principal component. This overall measure ofbody size in barn swallows did not show significant variation
among periods (Table 3). Similarly, there was no increase in
the frequency of albinistic individuals during the study period(Fig. 2), which would be expected if germline mutations were
continuously accumulating. Therefore, we can conclude that
there was no overall decrease in mean body size, althoughsome characters showed dramatic changes in size during thestudy period. The lack of change in overall body size is as
expected if mutant genes did not increase in frequency in the
population. This suggests that there is considerable natural
selection against small and albinistic phenotypes. Ellegren etal. (1997) showed that partially albinistic barn swallows froma Danish population had a reduced probability of survival
compared to other conspecifics. It seems unlikely that vi-

A. P. MØLLER AND T. A. MOUSSEAU

sually searching predators would be able to cue in on preywith such small amounts of white feathers. In humans, partial
albinism has been associated with immune deficiency due todefective melanosomes, platelet granules, and lysosomes (Introne et al. 1999; Baumeister et al. 2000; Spritz 2000). We
hypothesize that carotenoid-limitation of efficient immune
function and/or free-radical scavenging is the mechanism
generating reduced survival of partial albinos. The generally
low frequency of partial albinos in free-living populations,despite the germline basis of this plumage aberration, suggests that there is selection against such coloration. This interpretation is also consistent with the frequency of partiallyalbinistic birds in cities, smaller towns, and rural areas(Il’enko 1960). The higher frequency of such cases of albinism in cities may be associated with the presence of higher
concentrations of mutagens in this environment, but an alternative (although not necessarily mutually exclusive) explanation is that cities generally have a low abundance of
predators compared to rural areas. Thus, natural selection
against partial albinism may be less severe in cities comparedto rural areas.
Finally, a previous study of barn swallows in Chernobyl
has also demonstrated an increased frequency of outermost
tail feathers with aberrant morphology, and individuals withsuch disrupted phenotypes reproduced later than others(Møller 1993). This observation suggests that radioactive
contamination may disrupt normal phenotypic development,
but that sexual selection due to female choice or male-malecompetition may select against such deviant morphology.
ACKNOWLEDGMENTS
We are most grateful to G. Milinevski, A. M. Peklo, E.
Pysanets, N. Szczerbak, and A. A. Tokar for logistic help
provided during our visits to Ukraine over the years. N. Saino
kindly provided constructive comments on the manuscript.
TAM received funding from the CNRS (France), and the
University of South Carolina School of the Environment to
conduct this research. TAM gratefully acknowledges theSamuel P. Freeman Charitable Foundation for financial support.
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Corresponding Editor: S. Edwards