Behavioral Ecology Vol. 12 No. 1: 103-110
© 2001 International Society for Behavioral Ecology
Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba)
a Department of Zoology, University of Bern, CH-3032 Hinterkappelen, Switzerland b F-51340 Trois Fontaines l'Abbaye, France c Department of Zoology, University of Groningen, NL-9750 Haren, The Netherlands d The Swiss Cancer Research Institute (ISREC), chemin des Boveresses 155, CH-1066 Epalinges, Switzerland
Address correspondence to A. Roulin, who is now at Department of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, England. E-mail: ra241{at}hermes.cam.ac.uk .
Received 11 November 1999; revised 9 January 2000; accepted 7 July 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The hypothesis that extravagant ornaments signal parasite resistance has received support in several species for ornamented males but more rarely for ornamented females. However, recent theories have proposed that females should often be under sexual selection, and therefore females may signal the heritable capacity to resist parasites. We investigated this hypothesis in the socially monogamous barn owl, Tyto alba, in which females exhibit on average more and larger black spots on the plumage than males, and in which males were suggested to choose a mate with respect to female plumage spottiness. We hypothesized that the proportion of the plumage surface covered by black spots signals parasite resistance. In line with this hypothesis, we found that the ectoparasitic fly, Carnus hemapterus, was less abundant on young raised by more heavily spotted females and those flies were less fecund. In an experiment, where entire clutches were cross-fostered between nests, we found that the fecundity of the flies collected on nestlings was negatively correlated with the genetic mother's plumage spottiness. These results suggest that the ability to resist parasites covaries with the extent of female plumage spottiness. Among females collected dead along roads, those with a lot of black spots had a small bursa of Fabricius. Given that parasites trigger the development of this immune organ, this observation further suggests that more spotted females are usually less parasitized. The same analyses performed on male plumage spottiness all provided non-significant results. To our knowledge, this study is the first one showing that a heritable secondary sexual characteristics displayed by females reflects parasite resistance.
Key words: bursa of Fabricius, Carnus hemapterus, fecundity, female plumage ornamentation, good gene, parasite resistance, Tyto alba.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Hamilton and Zuk (1982
)
proposed that individuals that are more resistant against pathogen attacks
develop more extravagant ornaments. They assumed that the ability to resist
the invasion of parasites is heritable and the expression of ornaments is
condition-dependent, so that individuals that possess genes conferring lower
susceptibility to parasites can invest more energy in the production of
ornamental traits (Hamilton and Zuk,
1982; Zahavi,
1975). Thus, the cost to produce ornaments would allow individuals
to honestly signal to potential mates current health state and/or intrinsic
properties to resist parasites (Clayton,
1991; Kodrik-Brown and Brown,
1984; Zahavi,
1975). Later, Folstad and Karter
(1992) proposed, with the
"immunocompetence handicap hypothesis," that the cost to producing
an ornament is mediated by circulating sex-hormones. For instance,
testosterone can induce the production of large male ornament and
simultaneously depress the full immunological capacity to eliminate pathogens
or to control the level of pathogen infection
(Hillgarth and Wingfield,
1997; Salvador et al.,
1996; but see Braude et al.,
1999). Under this hypothesis the sex with a higher concentration
of circulating sex-hormones should be more susceptible to parasites, and only
high quality individuals may cope with the immunosuppressive effects of
producing large ornaments (Saino et al.,
1995).
Because males are usually under stronger sexual selection than females, and
almost always more ornamented (Andersson,
1994), researchers focused mainly on males when studying the
relationship between morphological traits, parasite resistance and mate choice
(e.g., Møller, 1990;
Møller et al., 1998;
Zuk, 1991). The best evidence
so far for parasite-mediated sexual selection has been found in the barn
swallow, Hirundo rustica. In this species, long-tailed males are
preferred by females both to form a pair bond and to engage in extrapair
copulations (Møller,
1994). Møller
(1990) also proposed that
long-tailed males are preferred over short-tailed ones because they pass on to
offspring good genes conferring resistance against parasites. At the
interspecific level, Zuk
(1991) found that species
displaying a brighter plumage were more often infected by blood parasites
suggesting that those bird species are at a higher selection pressure to
develop bright plumage that signals parasite resistance.
Because males often transmit genes coding for an ornament into daughters,
females may also exhibit the male trait but in a reduced state
(Lande, 1980). Where a
sex-trait can signal immunocompetence and improve mating success of males, it
may not necessarily have a signal function when expressed in females
(Cuervo et al., 1996;
Hill, 1993;
Muma and Weatherhead, 1989;
Tella et al., 1997; but see
Amundsen et al., 1997; Jones
and Hunter, 1993,
1999;
Møller, 1993;
Potti and Merino, 1996). Even
if females displaying a male trait have higher viability or achieve higher
annual reproductive success than unadorned females
(Møller, 1993), this
does not necessarily imply that males exert sexual selection on them to
express this trait (Cuervo et al.,
1996). Indeed, the covariation between life-history traits and
expression of a male ornament within females can be the mere consequence of a
genetic correlation between the sexes for both properties
(Halliday and Arnold, 1987;
Lande, 1980), that is both
sons and daughters may be simultaneously immunocompetent and ornamentated but
only sons will be chosen as a mate for those characteristics. Indeed, if the
cost of mate choice is high for males, males may not have the possibility to
exert strong sexual selection on females
(Johnstone et al., 1996).
Thus, the study of female signals of immunocompetence may be facilitated in
species in which females display a morphological trait to a larger extent than
males, because the larger expression of the trait may result from sexual
selection exerted on females rather than on males.
In this context, the barn owl is a relevant model organism, because plumage
varies from immaculate to heavily marked with black spots, and females usually
display more and larger spots than males
(Roulin, 1999a). This trait is
heritable and its expression was not found to be mediated environmentally or
to be condition-dependent (Roulin et al.,
1998). Thus, plumage spottiness may potentially reflect the
possession of good genes that improve the control of parasite infestation.
And, because males that changed mates between two breeding attempts acquired a
similarly spotted female as the previous one they were mated with, and the
mates of sons and father resembled each other
(Roulin, 1999b), the
assessment of plumage spottiness may allow males to select females possessing
good genes. In support of this proposition, the extent of female plumage
spottiness was experimentally shown to reflect the offspring ability to mount
an immune response towards an artificially administrated antigen
(Roulin et al., 2000).
The objectives of our study were to test the hypothesis that female plumage spottiness reflects parasite resistance. Using both observational and experimental approaches, we investigated in a Swiss and a French population the relationship between plumage spottiness and: (1) the offspring's burden of ectoparasitic flies Carnus hemapterus, (2) the fecundity of this ectoparasite, and (3) the size of an immune organ (bursa of Fabricius) of birds found dead along roads.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The studied organisms and the bursa of Fabricius
Nests of barn owls are located in cavities, and composed of straw, dust, and pellets. Parents do not bring any material in their nest, but females frequently clean it by removing pellets. Young defecate in the nest and as a result, the odor is often ammoniac. Clutch size ranges from two to 11 eggs, brood reduction is frequent and nestlings spend 2 months in the nest before fledging (personal observation). Sex-roles in reproduction are well defined with the mother brooding the young and distributing small mammals brought by her partner (Baudvin, 1986
).
When the young are about 3 weeks old, the mother provides to the brood
one-third of the food (Roulin,
1999b).
The ectoparasite C. hemapterus is a 2 mm long blood-sucking fly
that parasitizes nestling birds (Dawson
and Bortolotti, 1997;
Kirkpatrick and Colvin, 1989;
Roulin, 1998;
Walter and Hudde, 1987). They
emerge when the eggs of their hosts hatch and they lose their wings before
reproducing. Parasite prevalence and intensity are high in the barn owl with
94% of the nestlings being infested with on average 40 flies per nestling
(Roulin, 1998). Whereas flies
are more abundant in nest boxes used the previous year by a family of barn
owls than in boxes previously unused, their fecundity is unaffected by the
status of nest boxes (Roulin,
1998,
1999c).
The bursa of Fabricius is an organ located just beside the cloaca. It grows
during the nestling stage, and regresses prior to sexual maturity. In young
birds (in chickens up to 2-weeks-old), the main production site of B cells is
the bursa of Fabricius, and later B cells are produced not only by this organ
but by the thymus and the bone marrow. Therefore, this organ is essential for
immune defense in juveniles. The size of the bursa of Fabricius reflects its
cell population, and thus its antibody production. Interindividual differences
in the size of this organ can have both a genetic and a phenotypic component.
Parasites promote the development of the bursa of Fabricius (all information
in Glick, 1983; Møller
et al., 1996,
1998).
Plumage spottiness, ectoparasite intensity and clutch size of C.
hemapterus
General method
The study was performed in Switzerland (46°49' N,
06°56' E) in an area covering 190 km2 and located at an
altitude ranging from 430 to 520 m. Since 1987, 110 nest boxes have been
fastened to barns where breeding adults and their offspring have been
captured. Breeding females were recognized by the presence of a brood patch.
The sex of the nestlings was determined using the CHD-gene method (for details
see Roulin et al., 1999).
Plumage spottiness was assessed on all nestlings and breeding adults from
1994 to 1999. Within a 60 x 40 mm frame, AR counted the number of spots
on the breast, belly, flanks and underside of the wings. The diameter of three
to 24 spots was measured with callipers to the nearest 0.1 mm. For each body
part, the percentage of the 2400 mm2 surface covered by spots was
calculated using the formula 100 x 
x number of spots x
(mean spot diameter/2)2/2400. Values found for the left and right
flanks were averaged, and the same procedure was applied for the left and
right wings. Then, values of the four body regions were averaged. This mean
value was square-root transformed, called "plumage spottiness,"
and used in the statistical analyses. The method of assessing plumage
spottiness has already been shown to be accurate
(Roulin, 1999b;
Roulin et al., 1998).
Observational design
In 1996, AR counted the number of C. hemapterus on each nestling
when the oldest nestling of the brood was 25 days old. The whole body was
screened with the exception of places where flies were not visible such as the
openings of the ears. For each brood, the mean number of flies per nestling
was defined as "parasite intensity." The method of assessing
ectoparasite intensity is reliable
(Roulin, 1998). Nest boxes
were not cleaned during the whole study period allowing pupae to overwinter in
the nest of their host.
In 1998, 1458 gravid famale C. hemapterus were collected on 184 nestlings from 36 nests. Their white abdomen makes them easily recognizable. Each fly was put separately in a small Eppendorf tube (1.5 ml) at 37°C. After 24 h, all ectoparasites were dead, and A.R. counted the eggs laid in the tubes. Mean clutch size was not significantly correlated with altitude (Pearson correlation: r =.10, p =.55, n = 36) and thus, we did not control for this factor in the statistical analyses
Experimental design
In 1999, 34 nests were matched in pairs with approximately the same
hatching date (r =.98, p <.001, n = 17) and
clutch size (r =.77, p <.001, n = 17). After 3
weeks of incubation, the entire clutch of a nest was transferred in the nest
of its pair, and vice-versa. In this way, all nestlings were raised by foster
parents. We cross-fostered clutches instead of hatchlings to ensure that
C. hemapterus are in contact with nestlings of only one origin. For
the same reason, we performed a full cross-fostering (i.e., entire clutches
were swapped between nests) instead of a partial cross-fostering (i.e., half
of the eggs of a clutch are swapped), because it cannot be excluded that in a
nest flies move from one nestling to another. Two nests were abandoned before
the eggs hatched (6%), and because of technical problems (the car used to
visit nest boxes broke down) one nest could not be visited. Sample size is
therefore 31 experimental nests.
One week after cross-fostering incubating females were captured and randomly assigned to one of two experimental treatments. (1) Females with reduced plumage spottiness: for 15 females, the tip of the feathers was cut off with a scalpel to remove black spots. After the manipulation, plumage spottiness was significantly reduced by 4.7 times (paired t test, t14 = -9.9, p <.001); (2) Control: for 16 females, feathers were not manipulated (for six of these females feathers were mutilated with a scalpel without removing black spots). Females belonging to the two treatments did not differ in initial plumage spottiness (i.e., spottiness before treatment assignment) (Student t test, t29 = 0.19, p =.86), in laying date (t29 = 0.03, p =.97) and they laid a same-sized clutch (t29 = 0.39, p =.70).
As soon as the older nestling was 20 days of age, the nest was checked every 5 days up to fledging. At each visit and on each nestling, up to five gravid female C. hemapterus were captured. The mean number of visits with capture of flies was 4.8 per nest (range: 3-7). In total, 12 to 141 flies were collected per nest, and summed over the 31 nests 2087 flies were sampled. Each fly was put in a small Eppendorf tube, put at 37°C during 24 h, and AR counted the eggs laid in the tubes. For each nest box visit and for each nestling, the mean number of eggs laid by C. hemapterus was calculated. Then, values found for all siblings were averaged thereby providing a mean clutch size for that nest box visit. Finally, the mean clutch size found at all visits were averaged providing a mean clutch size for that nest box. This last value was used in the statistical analyses.
Measurement of the bursa of Fabricius
Between 8 December 1996 and 5 August 1998, dead barn owls were collected
daily on 350 km of the French National roads in the regions Champagne and
Lorraine. Cadavers were put in a freezer until dissection for sex
determination, analysis of stomach content and measurement of the bursa of
Fabricius (the spleen was unfortunately not measured). All measurements have
been taken on 27 March 1997 and 22 September 1998. Body mass is the mass
measured at the day of collection minus the mass of the stomach content. As an
univariate measure of body size, we considered bill length because it reflects
reliably the size of the skeleton (correlation between bill length and culmen,
r =.89, p <.001, n = 81; maxilla, r
=.49, p <.001, n = 77; femur, r =.42, p
=.002, n = 54; tarsus, r =.26, p =.018, n
= 81; data from the Natural History Museum of Basel). Fresh weight of the
bursa of Fabricius was measured to the nearest 0.1 g, and its length and width
to the nearest 0.1 mm. In the statistical analyses, we used the value
"length x width" as an index of the size of this organ
because it varied to a larger extent than the fresh mass (coefficient of
variation 1.68 versus 1.19). Note that the surface of the bursa of Fabricius
was strongly correlated with its fresh mass (r =.91, p
<.001, n = 103). The date when birds were collected was not
significantly correlated with plumage spottiness (Spearman correlation;
female, rs = -.19, p >.20, n = 47;
male, rs = -.19, p >.20, n = 58).
However, since in birds this organ regresses from fledging to the first-year
of age (Glick, 1983), we
statistically controlled for date of cadaver collection (30 June is defined as
day 0) to assess the relationship between the size of the bursa of Fabricius
and plumage spottiness. Adult birds have no bursa of Fabricius
(Glick, 1983), and to ensure
that we consider only birds in their first-year of life, we used only
individuals in which this organ was found.
Statistical procedure
Statistical analyses were performed using the Systat statistical package
(Wilkinson, 1989). Because in
some cases only the female parent was captured, sample sizes can differ
between statistical analyses including mother and father plumage spottiness,
and figures including only mother plumage spottiness. Statistical analyses
were two-tailed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Plumage spottiness and ectoparasite intensity
Nestlings were significantly more parasitized by C. hemapterus in nest boxes used than unused the previous year by a brood of barn owls and in nests where the mother was less heavily marked with black spots (ANCOVA: occupation of the nest box as a factor, F1,44 = 25.3, p <.001; mother plumage spottiness as a first covariate, F1,44 = 4.8, p =.03; father plumage spottiness as a second covariate, F1,44 = 0.02, p =.68) (Figure 1). Note that ectoparasite intensity was not significantly correlated with the date of its census (r = -.23, p =.12, n = 50), and brood size was not associated with female plumage spottiness (r = -.01, p =.94, n = 50). As can be seen in Figure 1, the relationship between parasite intensity and female plumage spottiness is evident only in nest boxes occupied by a family in 1995 (r = -.44, p =.01, n = 34; r2 =.19) and not in nest boxes unoccupied the year before (r =.24, p =.38, n = 16). Because older females were spottier (r =.43, p =.002, n = 50), we controlled for female age in a partial correlation, and found that the negative relationship remained significant (female plumage spottiness, rpartial = -0.40, t31 = -2.46, p <.02; female age, rpartial =.04, t31 = 0.2, p >.50).
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One potential hypothesis accounting for this negative relationship is that more spotted females have access to nest boxes that are initially less infested by C. hemapterus. Two observations do not support this hypothesis. First, from 1994 to 1999 nest boxes not used the year before by a family of barn owls were not more often occupied by heavily than little spotted yearling females (Student t test, t35 = 1.16, p =.25). The age of these females was known with accuracy because they were ringed as nestlings. Second, by considering nest boxes in which the female breeding in 1997 was not the same as the one breeding in 1996, we found no significant correlation between ectoparasite intensities determined in nest boxes occupied in 1996 and plumage spottiness of the new 1997 female (r =.11, p =.67, n = 17).
Susceptibility to C. hemapterus did not appear to differ between the sexes, since female and male nest mates beared similar loads of flies (Wilcoxon matched-pairs signed-rank, z = 0.09, p =.93, n = 36) and brood sex-ratio was not correlated with ectoparasite intensity (r =.07, p =.64, n = 50). Although plumage spottiness of mothers reflected parasite intensity of their offspring, plumage spottiness of female off-spring did not predict the intensity of parasitism. Indeed, more spotted female nestlings were not less parasitized than their less spotted female nest mates (comparison of mean ectoparasite loads of female nestlings above and below their median plumage spottiness, z = 0.58, p =.56, n = 28).
Plumage spottiness and clutch size of ectoparasites
Observations
In 1998, C. hemapterus laid clutches of smaller size when
collected in the nest of more heavily spotted females (partial correlation
between the mean number of eggs and mother plumage spottiness,
rpartial = -.37, t30 = -2.18,
p <.05 versus father plumage spottiness:
rpartial =.21, t30 = 0.84, p
>.40) (Figure 2). Because
the production of eggs by C. hemapterus tended to increase with
advancing date (r =.32, p =.06, n = 36), we
calculated residuals from the regression of the mean number of eggs on date.
The correlation between these residuals and mother plumage spottiness was
significantly negative (r = -.34, p =.04, n = 36).
Note that in this sample female plumage spottiness was not correlated with
female age (r =.01, p =.95, n = 36).
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Fecundity of C. hemapterus was apparently not affected by the sex of their host, since C. hemapterus did not lay more eggs when collected on female nestlings than on their male nest mates (paired t test, t22 = -0.52, p =.61) and brood sex-ratio was not correlated with the fecundity of ectoparasites (r =.02, p =.93, n = 36). Although ectoparasitic fecundity was correlated with plumage spottiness of mothers, it was not with plumage spottiness of female nestlings. Flies collected on more spotted female nestlings were not less fecund than those collected on less spotted female nest mates (comparison between the mean number of eggs laid by flies collected on female nest mates above and below their median plumage spottiness, z = 0.06, p =.95, n = 23).
Experiment
Because in 1999 both fecundity of C. hemapterus and mother plumage
spottiness were not correlated with the hatching date of the first barn owl's
egg (r =.16, p =.38, n = 31 versus r =.13,
p =.48, n = 31), we did not control for date in the
statistical analyses. Note that plumage spottiness of foster and genetic
fathers were not significantly correlated with the fecundity of parasites
(r =.25, p =.19, n = 30 versus r = -.19,
p =.33, n = 28), and that the mean clutch size of C.
hemapterus captured at different days in the same nest was repeatable,
but not to a large extent (repeatability, 24% ± 9%,
F30,113 = 2.57, p <.001) as already found in
1998 (Roulin, 1999c). Thus, a
larger number of nest box visits with collection of C. hemapterus may
provide a more accurate approximation of ectoparasite fecundity. Because the
number of visits was not significantly correlated with plumage spottiness of
foster (r = -.03, p =.88, n = 31) and genetic
mothers (r = -.26, p =.16, n = 31), and did not
differ between the treatment "female with reduced plumage
spottiness" and "control" (Mann-Whitney U test:
U = 110, p =.67, n = 15, 16), variation in the
number of nest box visits with capture of ectoparasites is unlikely to have
biased the results.
In an ANCOVA model, ectoparasite fecundity was the dependent variable, the treatments "females with reduced plumage spottiness" and "control" as a factor, and plumage spottiness of foster and genetic mothers covariates. Treatment had no significant effect on ectoparasitic fecundity (F1,27 = 0.36, p =.55), initial plumage spottiness of foster mothers was not significantly related to the mean fecundity of C. hemapterus (F1,27 = 1.07, p =.31), and we found a significant effect of initial plumage spottiness of genetic mothers on the mean number of eggs the collected flies laid (F1,27 = 4.41, p =.04) (Figure 3).
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Plumage spottiness and the size of the bursa of Fabricius
Male and female juveniles did not differ significantly in the size of their
bursa of Fabricius (ANCOVA: sex factor, F1,101 = 0.08,
p =.78), and this organ regressed from the first summer onwards (date
as a covariate, F1,101 = 56.7, p <.001) in a
similar magnitude in the two sexes (sex by date interaction,
F1,101 = 2.37, p =.13)
(Figure 4). For each sex, we
calculated residuals from the regression of the size of this organ on the date
when birds were collected. We found that more heavily spotted females had a
smaller bursa of Fabricius (r = -.47, p =.0008, n =
47, r2 =.22) (Figure
5). Same relationship did not hold in males (r =.09,
p =.51, n = 58). We did not control for body size, because
within each sex both residual size of the bursa of Fabricius and plumage
spottiness were not significantly correlated with body mass (Pearson
correlation, p-values >.32) and bill length (p-values
>.29).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Prior to our study, researchers have found that more ornamented male birds are less infested by ecto- (Møller, 1991
) and endoparasites
(Höglund et
al., 1992; Wiehn et al.,
1997), produce offspring that are less infested by ectoparasites
(Møller, 1990), and
have a smaller bursa of Fabricius
(Møller et al., 1996)
and spleen, another organ responsible for the production of lymphocytes
(Møller et al., 1998).
Thus, males that are more resistant against invasion of parasites are commonly
more brightly feathered. An exception to this male-bias in signaling parasite
resistance is the study of Potti and Merino
(1996). They observed that
female pied flycatchers, Ficedula hypoleuca, not infected by
trypanosomes displayed a male secondary sexual character (forehead white
patch) to a larger extent than infected females. Because in the barn owl
females usually exhibit more and larger black spots than males, and males pair
non-randomly with respect to female plumage spottiness
(Roulin, 1999b), we
investigated the hypothesis that female plumage spottiness reflects parasite
resistance. Both observational and experimental results supported this
hypothesis. In Switzerland, we found that ectoparasite intensity and fecundity
of ectoparasites were lower when the mother was more heavily spotted. A
cross-fostering experiment demonstrated that offspring of more heavily spotted
females have the pre-determined ability to impair the fecundity of
ectoparasites. Finally, in France more heavily spotted females had a smaller
bursa of Fabricius.
Ectoparasite intensity and female plumage spottiness
At least four potential mechanisms can explain the fact that offspring of
more spotted mothers supported a lower burden of ectoparasites. First, females
may be not randomly distributed among environments with more spotted females
occupying nest boxes containing a naturally lower number of ectoparasites. The
observation showing that nest boxes containing a small number of parasites the
year before were not preferentially used by more heavily spotted females
suggests that this explanation does not hold.
Second, at night females often clean the nest by removing detritus within
which C. hemapterus are often located (Roulin A, personal
observation). Therefore, results may be explained by a more intense nest
sanitation by more spotted females. Because the time invested in nest
sanitation may be traded against other activities
(Christe et al., 1996) such as
feeding rate, this second hypothesis would predict that offspring of more
spotted females are fed at a lower rate. However, another study indicated that
offspring of more spotted females were fed at higher rates
(Roulin, 1999b). Thus, the
nest sanitation hypothesis may not be a likely one unless more spotted females
are better individuals at all breeding related activities.
Third, because nestlings raised by little spotted females were in worse
condition than those raised by heavily spotted females
(Roulin, 1999b), we may have
detected a negative relationship between ectoparasite intensity and female
plumage spottiness if parasites build up a larger population when their hosts
are in poorer condition. However, given that brood size manipulations
significantly affected nestling body condition
(Roulin et al., 1999) without
altering ectoparasite intensity (Roulin,
1998), this third explanation can be rejected.
Finally, a previous study showed that plumage spottiness is heritable
(Roulin et al., 1998), and
following sexual selection theory secondary sexual characteristics may have
evolved to signal the heritable ability to resist parasites
(Hamilton and Zuk, 1982).
Thus, ectoparasites were less numerous in broods of heavily spotted females
perhaps because offspring have the pre-determined ability to resist invasion
of ectoparasites so that C. hemapterus may have more difficulties to
build up a large population. Since the quantity of winged flies remains
constant throughout the rearing period and since the total number of flies met
in a brood is larger in experimentally enlarged than reduced broods
(Roulin, 1998), several
generations of flies may be produced during a single barn owl breeding
attempt. In this context, we predicted that the fecundity of ectoparasites to
be lower when feeding on the off-spring of heavily spotted mothers.
Fecundity of C. hemapterus and female plumage
spottiness
To our knowledge the present study is the first one to measure the
fecundity of parasites in relation to secondary sexual characteristics. The
idea behind this approach is that reproductive success of parasites is likely
to depend more strongly on host characteristics than parasite intensity.
Indeed, while fecundity may be related to the intake rate of high quality food
extracted by parasites from their host
(Brossard and Girardin, 1979;
Brossard et al., 1991),
population size of ectoparasites depends also on other factors including
immigration and previous occupation status of nest boxes
(Roulin, 1998). In agreement
with the good gene theory of sexual selection
(Hamilton and Zuk, 1982), we
found that C. hemapterus collected on cross-fostered nestlings were
less fecund when the genetic mother was more heavily spotted. At least three
mechanisms may cause such a reduction of the fecundity.
The first mechanism relies on the fact that if males invest more effort in
reproduction when mated to more heavily spotted females (Roulin, 1999), such
pairs would produce off-spring in higher condition that can also invest more
energy to combat parasites. This hypothesis would suggest that the
relationship between the fecundity of ectoparasites and female plumage
spottiness has a phenotypic rather than a genotypic basis. This is unlikely
because nestling phenotypic condition did not affect the fecundity of C.
hemapterus, as suggested by the absence of significant correlations
between ectoparasitic egg output and several indexes of nestling condition
(Roulin, 1999c). Furthermore,
since plumage spottiness of foster mothers was not correlated with the
fecundity of ectoparasites, more spotted females probably did not occupy
territories where parasites are characterized by a low fecundity, and those
mothers did not provide high quality parental care that could have reduced the
fecundity of C. hemapterus. Finally, the experimental manipulation of
female plumage spottiness did not affect parasites.
The second mechanism is based on the knowledge that biting insects,
including mosquitos and ticks are limited by the skin thickness/composition of
their host to extract large amounts of blood
(Lehane, 1991). C.
hemapterus feed on the blood of their host
(Kirkpatrick and Colvin,
1989), and hence one may speculate that young of more spotted
females possess, for instance, a thicker skin preventing flies from
efficiently taking blood meals. This hypothesis has not yet been
investigated.
The third mechanism proposes that more spotted females have a more
efficient immunological system. It has been shown that ectoparasites elicit an
immune response of their host (Allen and
Nelson, 1982). For instance, ticks fed on the blood of
immunologically resistant rabbits obtained smaller bloodmeals and produced
fewer eggs (Brossard and Girardin,
1979). Moreover, in the barn swallow more ornamented males mounted
higher immunological response towards injection of sheep red blood cells
(Saino and Møller,
1996) suggesting that plumage ornamentation may signal the ability
to mount higher immunological defences to resist parasites. In this context,
we measured the size of the bursa of Fabricius to get an index of the immune
status of barn owls in relation to plumage spottiness. We predicted that more
spotted females should develop a smaller bursa of Fabricius by analogy to the
study of Møller et al.
(1996) showing that more
ornamented male house sparrows, Passer domesticus, were less infested
by a mallophagan and had a smaller bursa of Fabricius. Our hypothesis was
supported. Aware that other interpretations of this result are potentially
plausible, we performed a more stringent test of this hypothesis
(Roulin et al., 2000). The
idea of this test was that although offspring of more spotted females are less
parasitized, and hence less challenged immunologically, once challenged they
would be more efficient at clearing pathogens. Using artificial injection of
sheep red blood cells, cross-fostered offspring of more heavily spotted
mothers were more capable to mount an humoral immune response
(Roulin et al., 2000).
Implication for the good gene theory of sexual selection
The present study and a previous one
(Roulin et al., 2000) suggest
that female plumage spottiness signals the heritable capacity to resist
parasites and pathogens. Resistance may be inherited via genes (i.e., heavily
spotted mothers transmit genes into offspring and when active they confer
resistance) or via substances included in the eggs that improve offspring
resistance (maternal effect). These two possibilities are not mutually
exclusive, and results in the barn owl may suggest that the resistance
conferred to offspring is a maternal effect that depends on whether mothers
have good genes or not. This speculation arises from two observations. First,
since: (1) C. hemapterus does not feed on adults, (2) C.
hemapterus emerge when barn owl nestlings hatch
(Kirkpatrick and Colvin, 1989;
Roulin, 1998), and (3) more
heavily spotted females do not occupy nests where the initial number of flies
is higher, more spotted females are probably not better vaccinated against
C. hemapterus. Therefore, if more heavily spotted mothers include in
their eggs more molecules (e.g., antibodies) specifically directed against
C. hemapterus, this may not be because such females had been
vaccinated against C. hemapterus, but probably because they have good
genes. Given that more spotted mothers also conferred to offspring immune
protection against an artificially administrated antigen
(Roulin et al., 2000), these
good genes may improve the overall pathogen/parasite resistance of offspring.
Second, if the pathogen/parasite resistance resulted from the expression of
good genes in offspring, we should have expected that (1) compared to male
nestlings, females nestlings are parasitized by a lower number of C.
hemapterus that have also a lower fecundity, and they mount a more
intense immune response against an antigen, and (2) more spotted female
nestlings are parasitized by a lower number of less fecund flies than their
less spotted female siblings, and they mount a more intense immune response
against an antigen. These two predictions were not supported
(Roulin et al., 2000; present
study) suggesting that females may transfer in their eggs good gene products
that confer better overall immune protection to their offspring. This
speculation should motivate detailed research on the mechanisms of the good
gene theory of sexual selection.
|
ACKNOWLEDGEMENTS |
|---|
This paper is dedicated in homage to Martin Epars, with whom A.R. studied barn owls for ten years. We are grateful to M. Epars and H. Etter for their help while collecting data in Switzerland, to H. Baudvin for organizing the collection of dead barn owls along French roads by the SAPRR (Société des Autoroutes Paris-Rhin-Rhône), and to Guido Meeuwissen for his help in the determination of the sex of the Swiss nestlings. Heinz Richner provided logistic facilities at the University of Bern. P. Christe, I. Cuthill, P. Heeb, J. L. Tella, F. Tripet and two anonymous referees provided helpful suggestions to improve an earlier draft of this paper. R. Winkler, the curator of the Natural History Museum of Basel, kindly provided measurements of skeleton and allowed us to measure the bill length of skins. We thank the "Service vétérinaire du canton de Vaud" to have delivered us the authorization to cross-foster eggs in 1999 and to take blood samples. The work performed in 1999 was granted by the "Stiftung zur Förderung der wissenschaftlichen Forschung and der Universität Bern" and by "le Cercle Ornithologique de Fribourg."
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