Behavioral Ecology Vol. 10 No. 6: 619-625
© 1999 International Society for Behavioral Ecology
A test of the good-genes-as-heterozygosity hypothesis using red-winged blackbirds
a Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, ON K1S 5B6, Canada b Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada
Address correspondence to P. J. Weatherhead. E-mail: pweather{at}biology.queensu.ca .
Received 7 August 1998; revised 22 February 1999; accepted 7 March 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Brown recently proposed that the "good genes" that females pursue when choosing mates may be individual heterozygosity because more heterozygous mates sire offspring with higher fitness. Further, because heterozygosity might enhance developmental stability, males with more heterozygosity are recognized by the reduced fluctuating asymmetry (FA) of their bilaterally paired traits. We used a point sample of 67 male red-winged blackbirds (Agelaius phoeniceus) to test two predictions of this hypothesis: (1) males with more heterozygosity have higher fitness, and (2) males with more heterozygosity have lower FA. We identified 7 polymorphic loci from an initial screening of 16 enzymes; 32 individuals were completely homozygous, and 35 individuals were heterozygous at at least 1 locus. Larger and older males realized higher mating success in this population, but neither size nor age was related to heterozygosity. Heterozygous males were not in better condition than homozygous males, nor were they less infected by hematozoa, lice, or mites. Among 1-year old males, epaulet length did not differ between homozygotes and heterozygotes, but among older males, heterozygotes did have longer epaulets. Homozygotes and heterozygotes did not differ in their mean FA scores for nine individual characters. Although the two groups of males did differ in composite FA, heterozygous males were less symmetrical. Interestingly, this difference was attributable to a single allele at the PGM-3 locus. Combined with previous results showing that FA was generally unrelated to male health, viability, parental care, social dominance, or mating success, the present results indicate that Brown's hypothesis does not explain mate choice or male quality in this population of red-winged blackbirds.
Key words: fitness, fluctuating asymmetry, good genes, heterozygosity, isozymes, red-winged blackbirds.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The idea that female animals might choose males to enhance the genetic quality of their offspring has a long history in evolutionary theory, although for much of that history the idea has not been generally accepted (Andersson, 1994
). However, the
combination of both theoretical (e.g.,
Pomiankowski and Møller,
1995) and empirical (e.g.,
Petrie, 1994) support have
helped move "good genes" ideas into the mainstream of evolutionary
theory. Recently, Brown (1997)
suggested that it was time for empiricists to shift their focus from asking
whether females select males for their genetic quality, to determining the
nature of that genetic quality. Furthermore, Brown
(1997) gave direction to that
focus by proposing that genetic quality might equate with genetic diversity,
such that the traits preferred in males are predictive of heterozygosity. Here
we test several predictions of this heterozygosity hypothesis using data
collected from male red-winged blackbirds (Agelaius phoeniceus).
In principle, Brown's (1997)
heterozygosity hypothesis is a clear departure from the general notion that
male genetic quality is some absolute value, whereby each male in a population
can be ranked according to that quality
(Pomiankowski, 1990). If
genetic diversification of offspring is the function of mate choice, then male
quality ceases to be absolute. Rather, what constitutes the best mate for a
given female will depend on her own genetic makeup, and thus will differ among
females. In practice, however, Brown
(1997) points out that for many
animals, females may be unable to choose mates according to specific genetic
markers. In this situation females should prefer more heterozygous males over
less heterozygous males because the progeny they sire will be genetically more
diverse. Thus, males can be ranked along a heterozygosity continuum that is
functionally equivalent to a continuum of absolute genetic quality, even
though the quality that is valued is genetic diversity rather than specific
genetic traits.
Brown (1997) linked his
good-genes-as-heterozygosity hypothesis to another idea of burgeoning interest
in behavioral ecology by suggesting that a preference for more heterozygous
males could explain why females of a number of species appear to prefer more
symmetrical males as mates (e.g., Harvey
and Walsh, 1993; McLachlan and
Cant, 1995; Møller,
1994, 1996;
Simmons, 1995;
Thornhill, 1992). Increased
heterozygosity appears to be associated with increased developmental
homeostasis, which in turn results in more symmetrical development of
bilaterally paired traits (Palmer and
Strobeck, 1986; Mitton,
1993). Furthermore, increased heterozygosity has been linked to
higher viability (Allendorf and Leary,
1986; Lynch and Walsh,
1998). Therefore, by preferentially mating with more symmetrical
males, females are likely to be mating with more heterozygous males, thereby
producing more heterozygous, and thus more fit, offspring.
We used an existing sample of male red-winged blackbirds
(Dufour and Weatherhead, 1996)
to test several of the assumptions and predictions of Brown's
(1997) hypothesis. First, we
determined whether larger males are more heterozygous, based on the evidence
that larger male red-winged blackbirds attract more mates in this socially
polygynous species, resulting in higher reproductive success
(Weatherhead and Boag, 1995),
and larger males survive better between breeding seasons
(Weatherhead and Clark, 1994).
Second, we determined whether heterozygosity differs between the two
identifiable age classes in our sample, second year (SY) and after second year
(ASY) males. ASY males include individuals that have survived at least 2 and
potentially up to 9 years in our study population
(Weatherhead and Boag, 1997),
whereas SY males have survived for only 1 year. If heterozygosity is
associated with enhanced viability, ASY males should be more heterozygous on
average. Furthermore, age contributes positively to male extrapair mating
success (Weatherhead and Boag,
1995), providing an additional reason to predict greater
heterozygosity among older males according to Brown's
(1997) hypothesis. Third, we
assessed the relation between heterozygosity and two indices of male health:
condition (mass corrected for body size) and infection by parasites (hematozoa
and two types of ectoparasites). Finally, we determined whether the extent of
fluctuating asymmetry (FA; random deviations from symmetry in paired
characters) is negatively related to heterozygosity, using allozymes to
quantify heterozygosity. We consider FA in both nonornamental traits and in an
ornamental (secondary sexual) trait, as well as using a composite index of
asymmetry that combines information across multiple characters.
We should make clear at the outset that results of an intensive
investigation of correlates of FA in this population of redwinged blackbirds
might argue against this species, or at least this population, being an
appropriate subject for current purposes. We found no evidence that more
symmetrical males were either healthier or more likely to survive the
nonbreeding season (Dufour and Weatherhead,
1998a), that they were more successful in competing for
territories, social mates, or extrapair mates
(Dufour and Weatherhead,
1998c), or that they were more successful in competing for
resources outside the breeding context
(Dufour and Weatherhead,
1998b). Thus, in this population of red-winged blackbirds, FA does
not appear to reveal anything about male quality or to be involved in mate
choice. Nonetheless, there are also strong arguments for using red-winged
blackbirds to test the heterozygosity hypothesis. First, Brown
(1997) proposed the hypothesis
as a general model of mate choice, thereby making all species in which mate
choice seems likely to occur appropriate subjects to investigate. Second, our
breadth of knowledge regarding FA and factors affecting fitness in this
population will inform our interpretation of any patterns we discover.
Finally, any of the various possible outcomes we might obtain (e.g.,
heterozygosity related to FA but not to fitness-related traits; heterozygosity
related to fitness-related traits but not to FA; heterozygosity, FA, and
fitness all unrelated) would provide important insights into the generality of
Brown's (1997) hypothesis.
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METHODS |
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The sample of birds we used in this study is the same sample Dufour and Weatherhead (1996
) used to
demonstrate that there was significant concordance in FA measured on different
bilateral traits within individuals, and that they subsequently used as part
of their analysis to assess the relation between FA and various measures of
health and viability (Dufour and
Weatherhead, 1998a). Given that detailed methods are described in
those papers, we repeat only the relevant aspects of our methods in
abbreviated form here.
Sampling birds
We collected the sample of 67 male red-winged blackbirds by capturing the
birds in mist nets as they entered a prebreeding spring roost on three
evenings in the week beginning 23 April 1993. The roost was approximately 10
km west of the Queen's University Biological Station in eastern Ontario
(44°34' N, 76°20' W). Captured birds were transported
immediately to the biological station, where we determined their age (SY or
ASY), weighed them (±0.5 g), took a blood smear for quantifying
hematozoa, and then placed the bird for 5 min in a polyethylene bag containing
a cotton bag soaked with chloroform. The chloroform killed the birds, whose
carcasses were required for skeletal analysis, and also caused ectoparasitic
mites and lice to detach, allowing us to identify and count them
(Martin, 1977). The birds were
then frozen at -20°C. We sent the blood smears to the International
Reference Centre for Avian Haematozoa, Memorial University, Newfoundland, for
analysis.
We thawed the frozen birds and measured four external paired characters:
tarsus length, wing chord, tail length. and epaulet length. We removed and
refroze a sample of approximately 500 mg of heart, liver, and skeletal muscle
tissue from each bird for subsequent allozyme analysis (see below). Carcasses
were then sent to the Royal Ontario Museum to have the soft tissue removed
from the skeletons by dermestid beetles. Lengths of the coracoids, femurs,
tibiotaris, humeri, and ulnas were then measured for each skeleton (see
Dufour and Weatherhead, 1996,
for complete descriptions of all characters). K.W.D. made all the
measurements. For both the external and internal characters, the complete set
of characters was measured once, and then a second complete set of
measurements was made. We used the mean value of the two replicate measures of
each character in all analyses to reduce the effects of measurement error
(Yezerinac et al., 1992).
Damaged skeletal elements and worn feathers were not measured, so sample sizes
vary slightly among analyses.
Quantifying FA, size, and condition
As detailed previously (Dufour and
Weatherhead, 1996), all characters showed measurable departures
from perfect symmetry (i.e., significant among-individual variability), with
character-specific levels of measurement error in signed asymmetry scores
(left minus right) ranging from very low to moderate (0.9-20.8%). Although
distributions of these measurements of asymmetry generally conformed to
patterns expected for FA (i.e., normally distributed with a mean of zero),
there was evidence of subtle directionality of asymmetry for some characters
(Dufour and Weatherhead, 1996).
Thus, we adjusted distributions of left minus right values for each character
to a mean of zero before converting these asymmetry measures to absolute
values. We then transformed absolute asymmetry scores to square roots because
the distributions of the absolute values are strongly positively skewed.
Within characters, absolute FA was unrelated to character size
(Dufour and Weatherhead,
1996).
For analyses examining the relations between FA and other variables, we
used both FA for individual characters and a composite measure of FA. Although
there is significant concordance in FA among characters, it is quite weak,
indicating that a composite measure of FA is necessary to characterize an
individual's overall FA (Dufour and
Weatherhead, 1996). Furthermore, in a previous analysis, the
composite index had revealed relations between FA and ectoparasite
infestations that were not apparent from the single character analyses
(Dufour and Weatherhead,
1998a). For each individual we computed the composite asymmetry
score as the sum of the ranks of its FA scores for all individual
characters.
We used principal components analysis (PCA) to derive a measure of body
size from the individual characters. The first principal component (PC1)
described positive covariation among skeletal characters, while PC2 described
positive covariation between feather traits (details provided in
Dufour and Weatherhead, 1998a).
We used PC1 scores as our index of body size. Three individuals were excluded
from the PCA because they were missing measurements for a particular character
(e.g., a broken feather precluded measuring tail length). We estimated their
PC1 scores from a multiple linear regression model relating PC1 to five
individual characters for which all individuals had measurements
(R2 = 0.98; Dufour and
Weatherhead, 1998a). We used residuals from simple linear
regression of mass on body size (PC1) as our measure of condition (i.e., mass
corrected for size).
Quantifying heterozygosity
We assayed allozyme variation using horizontal starch-gel electrophoresis
following Bogart (1982), with
modifications outlined by Lougheed and Handford
(1992). Tissue samples were
homogenized in an equal volume of grinding buffer (10 mM Tris, 1 mM EDTA
(disodium.2H2O), 50 mM NADP, pH 6.8). Before electrophoresis
samples were spun at 6000 rpm for 5 min. Supernatant was absorbed on Whatman
3MM chromatography paper wicks, which were inserted into 450 ml 12% (w/v)
starch gels measuring 19 x 14 cm. Samples were run under standard
voltage and current at 4°C until indicator dye (Club HouseTM green
food coloring) had migrated about 9 cm. Enzymes were stained following either
Murphy et al. (1990) or
Richardson et al. (1986).
We initially screened 16 enzymes, from which we chose 9 (representing 14 isozymes) that could be clearly resolved for all individuals (Table 1). For each individual and locus assayed, we recorded the electrophoretic genotype, designating the most common allozyme as "B," the more anodally migrating allozyme as `A,' and more cathodally migrating allozymes as "C" or "D."
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Data analysis
Our general analytical approach was to use general linear modeling
procedures (McCullagh and Nelder,
1989) to assess relations between two variables of interest (e.g.,
FA and heterozygosity), controlling for additional variables as necessary.
Where interactions between variables were not significant, reduced models
without interactions were used and reported below. All analyses were performed
using the statistical routines in JMP (version 3.1;
SAS Institute, 1994).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Of the nine clearly resolved enzymes, polymorphism was detected at one locus for five (GDH, GPI, LDH, MPI, 6PGD) and at two loci for one (PGM). Across these 7 loci, 32 individuals were homozygous, 28 individuals were heterozygous at 1 locus, 3 individuals were heterozygous at 2 loci, and 4 individuals were heterozygous at 3 loci. Because few birds were heterozygous at more than one locus, for most analyses we compare two classes of males: those that were homozygous at all loci and those that were heterozygous at one or more loci.
Age
Contrary to prediction, older males were not significantly more
heterozygous than younger males. Nineteen of 33 ASY males were heterozygous,
compared to 16 of 34 SY males (2 x 2 contingency table, G =
0.74, df = 1, p =.39).
Secondary sexual traits
The reduced two-way ANOVA with body size as the response variable and male
age and heterozygosity as predictor variables was significant (F =
3.26, df = 2, 64, p =.04) and indicated that SY males were smaller
than ASY males (F = 0.51, df = 1, 64 p =.01) but that there
was no difference in size between homozygous and heterozygous males
(F = 0.02, df = 1, 64, p =.90,
Table 2).
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In the initial analysis of epaulet length, two-way ANOVA revealed a significant interaction between age and heterozygosity (F = 7.13, df = 1, 62, p =.01). Analyses conducted separately by age indicated that, among SY males, homozygotes had longer epaulets than heterozygotes (t = 2.0, df = 32, p =.05; Figure 1), whereas among ASY males, heterozygotes tended to have longer epaulets than homozygotes (t = 1.9, df = 30, p =.07; Figure 1). The pattern for ASY males is consistent with what we predicted, but the result for SY males is opposite to what we predicted. Further exploration of these data indicated that this difference between age classes in the relation between heterozygosity and epaulet length was largely a consequence of one locus. When we reclassified males as heterozygous or homozygous excluding PGM-3, then for SY males, mean epaulet length did not differ between homozygotes (39.05 ± 0.56) and heterozygotes (39.52 ± 1.11; t = 0.4, df = 32, p =.71), and heterozygous ASY males still had longer epaulets (45.31 ± 0.53) than homozygous ASY males (43.78 ± 0.38; t = 2.4, df = 30, p =.03).
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Health
A two-way ANOVA with condition as the response variable and male age and
heterozygosity as predictor variables indicated that SY males were in poorer
condition (-1.35 ± 0.46) than ASY males (1.39 ± 0.47; F
= 16.57, df = 1, 64, p =.0001), but did not detect a difference in
condition between homozygotes (-0.37 ± 0.53) and heterozygotes (0.34
± 0.51; F = 0.43, df = 1, 64, p =.51).
For analyses of parasite infection, we treated lice, mites and hematozoa
separately. Details of the species included in each of these groups can be
found in Dufour and Weatherhead
(1998a). Because most
individuals had some lice and mites, we analyzed variation in intensity of
infestation by these two types of parasites. For hematozoa the more
appropriate approach was to analyze presence or absence of infection because a
substantial number of males had no detectable hematozoa. A two-way ANOVA
evaluating the effects of male age and heterozygosity on lice infestation
indicated a highly significant effect of male age (F = 7.66, df = 1,
64, p =.007), with younger males more heavily infested than older
males, but no significant effect of heterozygosity (F = 0.30, df = 1,
64, p =.59; Table 3).
Results were similar for mites, although the age difference was no longer
significant (F = 2.8, df = 1, 64, p = 0.10), while the
effect of heterozygosity remained nonsignificant (F = 0.6, df = 1,
64, p =.43; Table 3).
Because the proportion of SY and ASY males infected with hematozoa was not
different (44% and 36%, respectively; G = 0.42, df = 1, p
=.52), we pooled age classes for further analysis. The proportion of males
parasitized by hematozoa did not differ between heterozygotes (43%) and
homozygotes (38%; G = 0.20, df = 1, p =.66).
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Asymmetry
Our analysis of fluctuating asymmetry involved several steps, including
determining that the asymmetry observed was primarily true asymmetry rather
than measurement error, and confirming that distributions of symmetry values
are approximately normal with a mean of zero. All of these issues are dealt
with in detail in Dufour and Weatherhead
(1996). Analyses presented in
that paper also indicated there was no difference in asymmetry between SY and
ASY males. Thus, because we detected no difference in heterozygosity between
age classes, we pooled all males to assess whether heterozygotes were more
symmetrical than homozygotes. For each of the nine characters we measured,
there was no difference in asymmetry between heterozygotes and homozygotes
(Table 4). However, in our
analysis of composite asymmetry, there was a trend for heterozygotes to be
more asymmetrical (301.06 ± 11.12) than homozygotes (273.63 ±
11.66; t = 1.70, df = 61, p =.09). Closer inspection of the
data again revealed that variation at PGM-3 was responsible for this trend.
When PGM-3 was excluded, there was no difference in composite asymmetry
between heterozygotes (280.71 ± 15.82) and homozygotes (290.70 ±
9.61; t = 0.54, df = 61, p =.59). However, for PGM-3 alone,
heterozygotes were more asymmetrical (317.40 ± 13.50) than homozygotes
(273.30 ± 9.54; t = 2.67, df = 61, p =.01). At the
PGM-3 locus there were 36 males with the BB genotype, 20 with the BC genotype,
6 with the CC genotype, and a single individual with the CD genotype.
Excluding the individual with the unique genotype and comparing the composite
symmetry of males with the three more common genotypes revealed that the
symmetry difference was a consequence of a single allele. Individuals bearing
the C allele (BC and CC) were less symmetrical than individuals without the C
allele (one-way ANOVA: F = 4.9, df = 2, 59, p =.01;
Figure 2). Multiple comparisons
(Tukey-Kramer HSD tests; Sokal and Rohlf,
1981) indicated that mean composite asymmetry scores differed
between genotypes BB and BC (p <.05). Although the mean score for
CC individuals was virtually identical to that for BC individuals, it was not
significantly different from that for BB birds because the sample size was
small.
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1 loci (heterozygotes) and those homozygous for all loci surveyed
(homozygotes)
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Brown (1997
) proposed that
when animals select mates on the basis of genetic quality, the quality they
prefer is heterozygosity. Mates that are more heterozygous will sire offspring
that are more heterozygous on average, which may increase the viability of
those offspring (Allendorf and Leary,
1986). Finally, because heterozygosity may also be associated with
increased developmental stability (Mitton,
1993), Brown (1997)
proposed that greater heterozygosity is recognized in potential mates through
the higher symmetry of their bilateral traits. Thus, the key assumptions of
this hypothesis are that viability, heterozygosity, and bilateral symmetry are
all positively related.
We tested these assumptions using a sample of male redwinged blackbirds
collected from a spring roost. From previous analyses of asymmetry in this
population, we already knew that asymmetry was not related to mating success
or viability (Dufour and Weatherhead,
1998a, c).
However, the relations between heterozygosity and viability and between
heterozygosity and asymmetry were unknown. Overall, our results did not
support either of these assumptions of the heterozygosity hypothesis. Older
males were not more heterozygous than younger males, and heterozygosity was
generally unrelated to body condition or to infection by mites, lice, or
hematozoa. Heterozygosity was also generally unrelated to asymmetry in nine
bilateral characters. Finally, because heterozygosity was unrelated to both
the age and size of males, which are the two traits known to correlate
positively with mating success in this population
(Weatherhead and Boag, 1995),
it seems unlikely that heterozygosity was related to female choice in this
population of red-winged blackbirds.
Before concluding that our study does not support Brown's
(1997) hypothesis, two issues
must be addressed. First, although the weight of evidence did not support any
relation between heterozygosity and morphology, age, or parasite infection,
two significant but contrasting patterns were detected. As predicted, ASY
heterozygotes had longer epaulets than ASY homozygotes. Moreover, epaulet size
appears to be positively related to nest-defense behavior and dominance rank
in this population of red-winged blackbirds
(Eckert and Weatherhead,
1987a, b).
Although it is tempting to provide an optimistic interpretation of this result
in terms of Brown's (1997)
hypothesis, data from additional samples are required to confirm that this
lone correlation is more than just the expected type I error in a study
involving many statistical tests.
The other significant pattern in our data involves an unexpected positive
relation between heterozygosity and composite FA, due almost entirely to a
pronounced difference in FA between PGM-3 genotypes. Individuals possessing
allele C had FA scores 18.4% greater than those of BB homozygotes. There are
two possible interpretations of this result. The first is that the pattern is
simply an artifact of sampling or type I error (see above). The alternative,
genetic interpretation is that allele C is associated with decreased
developmental stability. Alternate genotypes of major glycolytic isozymes have
been shown to have clear fitness consequences for a few taxa: Colias
butterflies (PGI and PGM; Watt et al.,
1996), fire ants (PGM; Ross
and Keller, 1995), killifish (LDH;
Schulte et al., 1997), and
humans (PGM; Bottini et al.,
1994). However, there is little general evidence for phenotypic
differences among individuals bearing alternative electrophoretic alleles at
such major housekeeping genes (Lynch and
Walsh, 1998). Thus, it is more likely that the association between
allele C at PGM-3 and asymmetry would be caused by disequilibrium between it
and alleles at other loci that directly influence development.
An apparent association between allele C at PGM-3 and FA might occur if the
roost we sampled included birds from different populations that covaried in
allele frequencies at PGM-3 and average levels of FA. This possibility seems
unlikely for several reasons. When we collected the sample of birds from the
roost in late April, male red-winged blackbirds in this area had already been
back from migration for about a month
(Greenwood and Weatherhead,
1982), and females had already begun to settle on territories
(Muma and Weatherhead, 1989).
Thus, it seems most likely that the occupants of the roost at the time we
sampled were local residents, and patterns of natal dispersal in this
population indicate that the population is highly outbred
(Weatherhead and Montgomerie,
1995). Furthermore, because differences in FA should be more
readily detected between individuals from different populations than between
individuals from the same population, the contribution of more than one
breeding population to the roost we sampled should have increased the
likelihood of detecting positive correlations between heterozygosity and other
fitness components (Lynch and Walsh,
1998; Palmer and Strobeck,
1986). We found no such correlations.
The second caveat in interpreting our results in terms of Brown's
(1997) hypothesis is that our
measure of heterozygosity was based on a relatively small number of enzymes.
In historically large, randomly mating populations, it is unlikely that a
sample of 14 loci will accurately reflect genome-wide heterozygosity
(Chakraborty, 1981;
Palmer and Strobeck, 1986).
Error in measuring overall heterozygosity will weaken observed correlations
with FA or fitness componenents. Small samples of enzyme loci are expected to
index overall heterozygosity more accurately if linkage disequilibrium among
loci is generally high or if the population is somewhat inbred
(Lynch and Walsh, 1998;
Palmer and Strobeck, 1986).
This might be likely if the roosting population of blackbirds we sampled was
genetically subdivided to some extent, or if there was nonrandom mating within
breeding colonies. For the reasons given above, it seems most reasonable to
assume that our sample of birds was drawn from a large, panmictic population
at equilibrium, so heterozygosity at the small number of loci we sampled may
not be representative of overall heterozygosity.
Although our ability to interpret some of the more intriguing results from
this study is limited by the uncertainties discussed above, our data, taken
together, do not provide any compelling support for the assumptions or
predictions of Brown's (1997)
hypothesis as applied to red-winged blackbirds. Instead, the results of this
study add to the emerging picture of widely inconsistent and unpredictable
relations between heterozygosity, fitness, and fluctuating asymmetry
(Clarke, 1993;
Lynch and Walsh, 1998;
Palmer and Strobeck, 1986;
Roff, 1997).
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Kit Muma, Kevin Teather, and Stephen Yezerinac for help in the field, Kit Muma for helping with specimen preparation, Gordon Bennett and associates for hematozoa identification, Bert Nesbitt for identifying ectoparasites, the Royal Ontario Museum for use of their dermestid colonies, Queen's University for use of the Biological Station, and the Natural Sciences and Engineering Research Council of Canada for financial support.
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