Behavioral Ecology Vol. 13 No. 5: 682-689
© 2002 International Society for Behavioral Ecology
Nonlocal male mountain white-crowned sparrows have lower paternity and higher parasite loads than males singing local dialect
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544-1003, USA
Address correspondence to E.A. MacDougall-Shackleton, Department of Biology, University of Western Ontario, London, Ontario N6A 5B7, Canada. E-mail: eams{at}sympatico.ca. E.P. Derryberry is now at the Department of Biology, Duke University, PO Box 90338, Durham, NC 227708, USA. T.P. Hahn is now at the Section of Neurobiology, Physiology and Behavior, University of California Davis, Davis, CA 95616-8761, USA.
Received 24 February 2001; revised 28 January 2002; accepted 12 February 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Bird song often varies geographically, and when this geographic variation has distinct boundaries, the shared song types are referred to as song dialects. We investigated the role of song dialect in male mating success in a wild breeding population of mountain white-crowned sparrows (Zonotrichia leucophrys oriantha). In 2 of 3 years, males singing unusual songs ("nonlocal" males) had lower total fertilization success (measured by microsatellite paternity analysis) than did males singing the local dialect ("local" males). Similarly, females produced disproportionately more young with local than with nonlocal males. However, dialect was not a significant predictor of male mating success when controlling for other factors that might affect paternity. Instead, the low mating success of nonlocal males was apparently due to an interaction between song dialect and parasite load. Nonlocal males were more severely infected by bloodborne Haemoproteus than were local males, although they did not differ in any other measured aspect of quality. Immigrant birds may be immunologically disadvantaged, possibly due to a lack of previous experience with the local parasite fauna, resulting in low mating success.
Key words: Haemoproteus, parasite load, parasite resistance, paternity, song dialect, white-crowned sparrows, Zonotrichia leucophrys oriantha.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Among nonhuman animals, the best studied example of a stable, culturally transmitted trait is bird song. Oscine birds (suborder Passeri) learn their songs, with young birds generally learning to produce species-typical songs by copying conspecific adults (Catchpole and Slater, 1995
). As a result of vocal learning, bird song often
varies geographically within a species. This geographic variation is thought
to be due to the combined effects of imperfect song copying and philopatry
(Baker and Cunningham, 1985).
When the geographic variation in song has well-defined boundaries, so that
variation between groups is greater than that within groups, the shared song
types are referred to as dialects (Marler and Tamura,
1962,
1964). Song dialects have been
described in many song-bird species
(Lemon, 1966;
Mundinger, 1975;
Nottebohm, 1969;
Payne et al., 1981;
Rothstein and Fleischer,
1987). Vocal dialects in general have been documented in such
diverse vertebrate taxa as yellow-naped amazon parrots (Amazona
auropalliata; Wright,
1996), sperm whales (Physeter macrocephalus;
Whitehead et al., 1998), and
humans. It has been proposed that song dialects facilitate assortative mating,
and thereby restrict gene flow among songbird populations (Marler and Tamura,
1962,
1964). Thus, song dialects may
represent a behavioral mechanism whereby a culturally transmitted trait
affects the genetic structure of populations.
Three major hypotheses have been proposed to explain the adaptive
significance (if any) of song dialects. The genetic adaptation hypothesis
(Marler and Tamura, 1962,
1964;
Nottebohm, 1969) proposes that
dialects serve as behavioral isolating mechanisms and restrict gene flow among
populations. According to this hypothesis, young birds learn to produce or
recognize song early in life, while still in their natal region, and adult
birds use song as a cue for assortative mating. The social adaptation
hypothesis (Payne, 1981) also
proposes that song dialect affects social and sexual interactions, but asserts
that males can modify their songs to match those of a new dialect area into
which they disperse as juveniles or to match those of their neighbors during
their first breeding season. By learning to produce the predominant local
dialect and thus disguising their nonlocal origins, immigrant males might
benefit through enhanced attractiveness to local females and/or greater
ability to defend a territory through song. Thus, the genetic and social
adaptation hypotheses differ with respect to the relative timing of song
learning and dispersal. The epiphenomenon hypothesis
(Andrew, 1962) suggests that
song dialects are mere byproducts of vocal learning and are not behaviorally
salient.
These three hypotheses can be distinguished primarily by the predictions they make regarding whether song dialect affects individual fitness and/or the genetic structure of a population. Specifically, the genetic adaptation hypothesis predicts that dialect causally affects both mating success and population genetic structure. The social adaptation hypothesis predicts that dialect affects the fitness of individual males, but not population genetic structure (because song does not necessarily indicate place of origin). The epiphenomenon hypothesis proposes that song dialect does not affect mating success but may be correlated with population genetic structure.
The present study addressed a long-standing problem: the relationship
between song dialect and mating success in a wild population. Bird song
generally serves a dual purpose of attracting mates and deterring competitors,
so if there is a mating advantage associated with producing the local song
dialect, it might be mediated by female preference, male aggression, or both
(Baker and Cunningham, 1985).
Thus, distinguishing among the genetic adaptation, social adaptation, and
epiphenomenon hypotheses requires first determining whether song dialect
affects paternity and then identifying the mechanism(s) driving this effect.
Although the effect of song dialect on male mating success has been the
subject of much speculation, previous research has focused on the proximate
mechanisms by which paternity might be affected (in particular the song
preferences of captive females), without first ascertaining whether singing
the local song actually confers a mating advantage in the wild. Furthermore,
little consensus has been reached even within a single species. The studies
reviewed below examine song preferences and mating behavior in white-crowned
sparrows, Zonotrichia leucophrys.
The effect of song dialect on male mating success is ideally studied in the
field, as captive studies may have only limited applicability to the behavior
of free-living individuals (Chilton and
Lein, 1996) unless combined with field studies. The evidence that
wild songbirds pair assortatively based on song dialect is mixed. The presence
or absence of assortative mating in the wild is sometimes inferred by treating
females with testosterone to induce song and comparing the females' songs to
those of their social mates. Using this technique to infer assortative mating
relies on the assumption that females treated with testosterone will sing
their natal song type, but testosterone-treated females may instead sing the
song of their first mate (Chilton and
Lein, 1996). Female Z. l. nuttalli treated with
testosterone did produce songs similar to those of their social mates,
suggesting that these females had mated assortatively
(Tomback and Baker, 1984).
However, other studies conducted on Z. l. nuttalli and Z. l.
oriantha found no consistent similarity between the songs induced from
females and those of their social mates
(Baptista and Morton, 1982;
Petrinovich and Baptista,
1984). In a mixed-dialect population of Z. l. gambelii
and Z. l. oriantha, the mates of individual females in successive
years were not more likely to be of the same dialect than predicted by chance
(Chilton et al., 1990). Thus,
there is little consensus even within this species whether song dialect is
likely to affect male mating success. In any case, looking only at social
mating success (whether a male can attract a social mate) is unlikely to prove
very informative in species where extrapair mating is frequent, as it is in
mountain white-crowned sparrows (Sherman
and Morton, 1988). The ideal way to compare the fitness of local
and nonlocal males is to measure mating success directly, using genetic
markers to assess paternity in a wild population.
In this study we addressed the relationship between song dialect and
genetic mating success in a wild population where approximately 90% of males
in any given year sing the local dialect and where previous estimates
indicated that about 40% of nestlings were extrapair young
(Sherman and Morton, 1988).
First, we compared the mating success of male mountain white-crowned sparrows
singing local and nonlocal song dialects to test the hypothesis that local
males father more young than do nonlocal males. Second, we controlled for
other potential determinants of paternity to determine whether the observed
difference in paternity was attributable to song dialect or to other
differences in quality between local and nonlocal males. In addition to song
dialect, the other potential determinants of paternity we investigated
included age, body size, mass, territory quality, and bloodborne parasite
load. Differences between local and nonlocal males in any of these factors
might suggest possible proximate mechanisms for a mating advantage to local
males.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study site and population
We investigated the role of song dialect in male mating success in a migratory population of mountain white-crowned sparrows (Z. l. oriantha) breeding at and around Tioga Pass, California, USA, from May to August 1997, 1998, and 1999. Long-term studies of this population indicate high natal and adult philopatry in general, with males being more philopatric than females (Morton, 1992
).
Mountain white-crowned sparrows are socially monogamous, although extrapair
matings are frequent (Sherman and Morton,
1988). This population, particularly the 20-30 pairs of adults
breeding on an area of about 50 ha called Tioga Pass Meadow, has been studied
from 1968-1997 by M. L. Morton and colleagues, and by us since 1995. These
birds are ideal for a study of parentage because many variables that may
influence paternity (such as age and territory quality) are known and can be
controlled for statistically.
Patterns of geographic variation in song and the maintenance of song
dialects have been well studied in Sierra Nevada Z. l. oriantha. The
song typically consists of an introductory whistle, a buzz, or whistle-buzz, a
highly variable note complex, a variable trill of simple syllables, and a
terminal vibrato (Nelson et al.,
1995; Orejuela and Morton,
1975). Song is generally similar within geographic areas, with
sudden discontinuities, indicative of song dialects
(Nottingham, 1999;
Orejuela and Morton, 1975).
These dialects appear to be temporally stable, having changed little over at
least 26 years (Harbison et al.,
1999). Although there is no strict consensus in the literature on
what constitutes a dialect versus variation in song type within a dialect, our
research team uses both note complex and trill elements, the two most variable
elements of the song, to define dialect membership (see "Song recording
and analysis," below). Of the birds breeding at Tioga Pass, about 60%
produce song type T1 of the local dialect, and 20-30% produce song type T2 of
the local dialect (see Harbison et al.,
1999, for detailed descriptions and exemplars). From 10% to 20% of
males sing nonlocal songs characteristic of other regions in the Sierra Nevada
or elsewhere (Harbison et al.,
1999; Nottingham,
1999; Orejuela and Morton,
1975).
Field techniques
In the spring of 1997, 1998, and 1999, we captured adult mountain
white-crowned sparrows arriving at Tioga Pass in a trapline of seed-baited
Potter traps. We followed Morton
(1992) in considering any
unbanded adults arriving at the study area ("adult recruits") to
be yearlings, for several reasons. First, an intensive long-term band and
recapture study of this population indicated that return rates are much higher
for adults of both sexes (> 50%) than for juveniles
(Morton, 1992;
Morton et al., 1972),
suggesting near-total adult philopatry. Second, a great effort is made each
year to capture and band any unbanded adults and juveniles in the study area,
so that adult recruits are presumably visiting the site for the first time.
Finally, adult recruits generally had one or more brown feathers among the
black feathers at the base of bill or in the crown (typical of known
yearlings) and shorter wings than birds known to be 2 years or older
(MacDougall-Shackleton et al., personal observations;
Morton et al., 1990).
From each newly arrived individual, we collected morphological measurements (body mass upon arrival at the breeding grounds and wing chord, tarsus length, and keel length). We marked each bird with a U.S. Fish and Wildlife Service leg band (banding permit no. 22712) and a unique combination of color bands to allow individual identification from a distance. To avoid an effect of trapping on paternity, we discontinued the trapline once females were judged to be depositing yolk for eggs (as determined by increased body mass). We located almost all of the nests initiated on Tioga Pass and the surrounding area, then checked each nest every few days until the nestlings fledged or the nest failed. In 1999 extra field hands were available and the study area was expanded to include areas a few kilometers to the north of Tioga Pass.
From each breeding adult, we collected a small blood sample (<50 µL) by brachial venipuncture, then blotted these samples onto individual filter papers (Whatman) saturated with 0.5 M EDTA. The samples were allowed to dry and stored desiccated at ambient temperature for several months before laboratory analysis. We collected small blood samples from all nestlings (using femoral venipuncture), usually on day 1 after hatch. We collected and froze eggs that remained unhatched several days after their nest mates had hatched. We stored eggs at -20°C for several months until the embryos could be dissected for genetic analysis (see below).
In 1999 we prepared blood smears from all adults to check for the presence
of hematozoa, bloodborne parasites transmitted by biting Diptera. Most smears
were collected within a month of the birds' arrival, shortly before nesting
began. To prepare slides, we touched a 50 µL capillary tube against a glass
slide to deliver a small drop of blood, then used a clean slide to push the
blood across the slide as a thin layer. Slides were air dried and fixed in
100% methanol for 30 s, within 24 h of sampling. The slides were kept at
ambient temperature for several months until they could be stained and
analyzed. For each slide we examined 10 fields of view, each containing
approximately 1000 erythrocytes, under oil immersion at x500 or
x1000 magnification, and noted the number of hematozoa (if any) from
genus Haemoproteus. Hematozoa were identified with reference to
Campbell (1995).
Song recording and analysis
We recorded songs from all males at the study area as early as possible
after their arrival on the breeding grounds, using a Sony TCM-5000EV recorder
and Sennheiser ME66 directional microphone. At least 10 songs were recorded
from each individual; mountain white-crowned sparrow song is highly
stereotyped, and approximately 95% of Tioga Pass individuals produce only a
single song type (Harbison et al.,
1999). We used the sound analysis program Canary 1.2.4 (Cornell
Laboratory of Ornithology) to generate sound spectrograms of digitized songs.
We categorized songs as local or nonlocal dialect based on the nature of the
note complex and the trill (Nottingham,
1999). In most cases nonlocal songs were easily assigned to other
nearby dialect areas in the Sierra Nevada
(Harbison et al., 1999;
MacDougall-Shackleton and
MacDougall-Shackleton, 2001;
Nottingham, 1999). Thus, we
are confident that a nonlocal song probably indicates that a male was reared
outside the local dialect area, rather than representing an improvisation or
an error in song imitation.
Genetic analysis
We used a guanidine-based method
(Ausubel et al., 1988) to
extract genomic DNA from blood samples and estimated DNA concentration by
agarose gel electrophoresis. Unhatched eggs were thawed and opened, and
embryos were homogenized for DNA extraction with Chelex (Biorad). Genotyping
was performed in a 96-well format. The polymerase chain reactions (PCRs; total
volume 10 µL) contained approximately 25 ng DNA, 50 mM KCl, 10 mM Tris-HCl
pH 8.3, 2.5 mM MgCl2, 0.2 mM of each dNTP, 0.5 µM of each primer
(12.5% of one primer end-labeled with 32P-ATP) and 0.5 units Taq
polymerase. Thermocycling conditions included a step of 94°C for 3 min, a
cycle of 94°C for 40 s, 50°C for 40 s, and 72°C for 40 s repeated
33 times, and a final extension step of 72°C for 5 min. We ran the PCR
products on 6% acrylamide gels (90 individuals per gel) along with
cycle-sequenced pVZ plasmid size-standards. Gels were dried, then exposed
overnight to X-ray film to visualize the PCR products.
We scored the developed films manually, with reference to the pVZ size standards. At each locus, the genotypes of individual nestlings were compared to those of their putative parents. We characterized each allele as consistent or inconsistent with their social parents' genotypes. In a few cases a single mismatch of one repeat unit (2 base pairs) was noted and attributed to mutation. If a nestling was mismatched at more than one locus, or by more than one repeat unit, the nestling was categorized as extrapair. To determine whether such nestlings resulted from extrapair mating by the female at the nest or from intraspecific brood parasitism (egg dumping), we assessed allele sharing between the nestlings and their social mothers. In all cases, extrapair nestlings were determined to result from extrapair mating.
We determined the genotype of each individual at eight microsatellite loci,
all developed for use in other Emberizid species
(Hanotte et al., 1994;
Jeffery et al., 2001;
Petren, 1998). All the loci
were polymorphic, with a mean observed heterozygosity of 0.592 (range
0.321-0.881). Analysis of genotype frequencies revealed no linkage
disequilibrium (
2 analysis, p > .05 for all locus
pairs), indicating that these loci are inherited independently. The loci used
had a combined exclusion probability (likelihood of correctly identifying a
nestling as extrapair) of greater than 0.9999, and a combined identification
probability (likelihood of misassigning an extrapair nestling to an unrelated
male) of 3.47 x 10-7.
To identify the genetic fathers of extrapair young, we compared the nestlings' genotypes with those of their mothers and identified the paternally inherited alleles. In 122 of 141 cases, only 1 of the males sampled could have been the genetic father of a certain nestling, and the nestling was ascribed to that male's extrapair mating success. An additional 14 nestlings could have been sired by either one of a father—son pair of males breeding on the study site who had similar genotypes. Each of these nestlings came from territories immediately adjacent to one or the other of these two related males and was assigned to that individual. The remaining five nestlings were not assigned to a male parent; these nestlings were found in nests near the periphery of the study area and had evidently been sired by males from whom blood samples were not obtained.
Total mating success (also referred to here as fertilization success or paternity) was measured as the number of young in the nest on day 1 that a male had sired with his social mate, plus those sired with other females on the study site. We used this metric (fertilization success) rather than number of fledglings produced, as we were primarily interested in how song dialect affects a male's ability to obtain successful copulations.
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RESULTS |
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Breeding conditions and extrapair mating
The 3 years of the study had quite disparate breeding phenologies. The first year, 1997, was characterized by approximately average snowpack and breeding density of Z. l. oriantha (Morton ML, personal communication). A heavy snowpack in 1998 was followed by a low breeding density for that year. In 1999 the snowpack was again near average, with higher than average breeding density. One male in 1997 and three males in 1999, all of whom were yearlings singing nonlocal song types, defended territories but did not attract social mates. The numbers of males singing local versus nonlocal song, and their ages, are summarized in Table 1. Extrapair paternity was common throughout all 3 years of the study. Forty-five percent to 68% of females produced at least one extrapair nestling (17/25, 16/24 and 21/47 females in 1997, 1998, and 1999, respectively). Overall, 30-56% of nestlings were fathered by a male other than their social father (45/90, 45/81, and 51/171 nestlings in 1997, 1998, and 1999, respectively).
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Song dialect and paternity
In 2 of 3 years, males singing the local song dialect (hereafter termed
"local" males) had greater fertilization success than did males
singing nonlocal dialects ("nonlocal" males;
Table 2). Total fertilization
success (within-pair + extrapair young) was greater for local than for
nonlocal males in 1997 and 1999 (Mann-Whitney U test; 1997:
Z = 2.674, p = .0075, N = 20 local, 7 nonlocal;
1999: Z = 1.996, p = .0459, N = 36 local, 9
nonlocal), but not in 1998 (Z = .266, p = .7900, N
= 18 local, 5 nonlocal). Similarly, local males had greater paternity with
their social mates than did nonlocal males in 1997 and 1999 (1997: Z
= 2.136, p = .0327, N = 19 local, 7 nonlocal; 1999:
Z = 2.125, p = .0336, N = 36 local, 9 nonlocal),
but not in 1998 (Z = 0.502, p = .6155, N = 18
local, 5 nonlocal). Nonlocal males had reduced extrapair mating success in
1997 (Z = 2.294, p = .0218, N = 26 local, 7
nonlocal), but not in 1998 or 1999 (1998: Z = 0.360, p =
.7189, N = 23 local, 5 nonlocal; 1999: Z = 1.047, p
= .2949, N = 40 local, 9 nonlocal).
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To determine whether local males fathered a disproportionate number of nestlings during all 3 years of the study, we analyzed the mating history of each female that bred at least once on the study site and whose immediate neighbors were known. For each female we compared the observed and expected number of young fathered by local males. Expected values were calculated by multiplying the total number of young produced by a female in a given year, by the proportion of males that sang local dialect in that female's immediate area (social mate plus males on adjacent territories). Expected values thus assume that females mate randomly within their immediate areas, which is probably not strictly true, but the high incidence of extrapair fertilization suggests that this assumption is not completely unreasonable. For females that returned to breed in multiple years, we summed the annual values for observed and expected young produced by local males. Females produced disproportionately more young fathered by local than by nonlocal males (Wilcoxon signed-rank, Z = 2.512, p = .012; Figure 1). Thus, the number of young produced by nonlocal males is lower than that expected if females mate randomly with respect to song type.
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Nests attended by local males produced more fledglings than those attended by nonlocals in 1999 (Z = 2.015, p = .0439, mean = 3.49 local, 1.86 nonlocal, N = 36 local, 7 nonlocal), although not in the 2 previous years (1997 Z = 0.575, p = .5654, mean = 3.25 local, 3.00 nonlocal, N = 18 local, 4 nonlocal; 1998 Z = 0, p = .999, mean = 2.67 local, 2.75 nonlocal, N = 18 local, 4 nonlocal).
Determinants of paternity
To investigate the relationship between song dialect and male mating
success while controlling for other potential determinants of paternity, we
ran a stepwise regression (Statview 5.0, SAS Institute). We used song dialect,
age, mass, body size, parasite load, and territory quality as independent
variables and measured their ability to explain total fertilization success in
1999 (the year in which the most complete data were collected). As an index of
body (skeletal) size, we summed the lengths of tarsus and keel for each male.
We used the number of Haemoproteus per 10,000 cells as an index of
parasite load. To estimate territory quality, we used the number of nests that
had been initiated in a given 100 x 100 m area over the last 30 years
(Morton ML, personal communication). We plotted the distributions of all
continuous variables to check for normality and used natural log or
square-root transformations to normalize distributions where needed. The
stepwise regression indicated that the three most useful variables in
explaining fertilization success are (in decreasing order of importance) body
size, parasite load, and age. These three factors combined explained about 60%
of the variation in fertilization success
(Table 3); specifically,
larger, less heavily parasitized, and older males had higher total
fertilization success. Song dialect, mass, and territory quality did not
contribute significantly to the predictive value of the model when these other
factors were controlled. A reverse stepwise regression confirmed that song did
not contribute to the model's predictive value (data not shown). Thus, song
dialect was probably not excluded inappropriately via intercorrelation of the
independent variables (Crawley,
1993).
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We ran similar stepwise regressions on the 1997 and 1998 data sets, for which only data on song dialect, body size, mass, and age were available. In 1997, song type was the only significant predictor of fertilization success (r2 = .209, p = .0372, N = 17), whereas in 1998, the only predictive factor was body mass (r2 = 0.134, p = .0572, N = 21). Reverse stepwise regressions (data not shown) confirmed that the other factors were not inappropriately excluded.
Because nonlocal singers had low mating success relative to local singers (Table 2), but song dialect itself appears not to drive this difference in success, it is likely that local and nonlocal singers might differ in some other determinant of mating success. To test this possibility, we ran a series of unpaired t tests comparing local and nonlocal males' age, mass, body size, parasite load, and territory quality. Local and nonlocal males did not differ in mean age, mass, body size, or territory quality, but nonlocal males had significantly higher parasite loads than local males (Table 4). The likelihood of being parasitized at all was not significantly different between local and nonlocal males (10/42 locals vs. 4/8 nonlocals, Fisher's Exact p = .1966).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Determinants of paternity
Extrapair mating represented an important part of the breeding strategy for mountain white-crowned sparrows at Tioga Pass, with 30-56% of nestlings each year resulting from extrapair fertilizations. This proportion is consistent with a previous estimate that 38-40% of nestlings in this population are extrapair (Sherman and Morton, 1988
). Extrapair paternity was less common in 1999, when breeding
density was highest, in contrast to patterns reported for other songbirds
(e.g., Bullock's oriole, Icterus galbula bullockii;
Richardson and Burke, 2001).
It is not yet clear what factors might drive this among-year variation in
Z. l. oriantha.
A major finding of this study is that males singing local song enjoyed
higher total fertilization success in 2 of the 3 years examined. Similarly,
females produced disproportionately more young fathered by local than by
nonlocal males. In contrast, previous studies of wild mountain white-crowned
sparrows found no assortative mating based on song similarity between mated
pairs and no apparent advantage to local males in attracting social mates
(Baptista and Morton, 1982).
Given that extrapair mating is widespread among songbirds in general
(Birkhead and Møller,
1992) and among mountain white-crowned sparrows in particular
(Sherman and Morton, 1988;
this study), it is important to measure actual paternity to detect the reduced
mating success of males singing nonlocal song dialects.
Although nonlocal males suffered reduced mating success, song dialect in itself did not explain a significant amount of variation in paternity. Instead, body size, parasite load, and age predicted most of the variation in male fertilization success. The low mating success of nonlocal males appears to be due to an interaction between song dialect and parasite load. That is, nonlocal males were more heavily parasitized by Haemoproteus and, possibly as a result, fathered fewer offspring than did local males. This finding should, however, be viewed with some caution until it can be confirmed by experimental studies addressing the relationships between song, immune function, and parentage.
We found considerable interyear variation in terms of which variables best
predicted male mating success. In 1997, the apparent importance of song
dialect in predicting paternity may have been due to a link between song and
parasie load (which was not measured that year), rather than to a behavioral
advantage to the local dialect as such. Conversely, in 1998 (the coldest of
the three summers), parasitic infection by Haemoproteus may have been
a relatively weak selective force, as biting flies (vectors for hematozoa)
likely emerged later and/or in lower numbers. Furthermore, in 1997 and 1999
most of the nonlocal singers were yearlings, whereas in 1998 all nonlocal
singers were 2 years or older and had bred (or attempted to breed) at Tioga
the previous year (Table 1).
Presumably, then, in 1998 all nonlocal males had prior experience with the
local parasite fauna and may have been less immunologically challenged. The
possible importance of prior exposure to the local parasites is discussed
below. This population routinely experiences strikingly different breeding
environments from year to year. For example, the onset of nesting can vary by
a month or more depending on the residual snowpack
(Morton, 1978). Such
variability in breeding conditions may well result in differences in the
strength of sexual selection and in the traits favored among years.
Song dialects and parasite load
Why should nonlocal males have heavier parasite loads than males singing
the local dialect? There are several potential explanations for this finding.
First, if bloodborne parasites or their vectors are more abundant in other
dialect regions than in our study area, then males singing nonlocal dialect
might show higher parasite loads due to previous infection in their natal
regions. Similarly, birds may have been infected on the wintering grounds or
during migration. Haemoproteus may be detected in the blood as early
as 6 days after infection (Shutler et al.,
1995), which is well within our 1-month time frame during which
most blood smears were collected. However, this latency period can be as long
as 21 days for some songbird hosts
(Kirkpatrick and Suthers,
1988). Although studies of other northern temperate birds have
shown that Haemoproteus and other hematozoa are transmitted primarily
during the breeding season (Atkinson and
Van Riper, 1991), making broad generalizations about transmission
across species and habitats is problematic. Thus, we cannot exclude the
possibility that some of the infections we sampled may have been acquired
before arrival at the breeding grounds. We are currently collecting data on
the age at which juvenile Z. l. oriantha first display evidence of
parasitic infections, which should cast some light on the timing of infection
relative to detection in this population.
A second possible explanation is that males that disperse out of their natal dialect regions might be lower in quality than more philopatric males. If so, dispersing males might have less effective immune systems and hence inferior ability to deal with parasitic infection. However, the fact that local and nonlocal singers differed only in parasite load but not in body size, age, or any other measured aspect of quality strongly suggests that nonlocal males are disadvantaged specifically in terms of their immune response to local parasites.
A third potential explanation for their increased parasite load is that
nonlocal birds are poorly adapted genetically to the selective pressures posed
by local parasite fauna. That is, populations characterized by different
dialects might be evolutionarily adapted to different local conditions
(Nottebohm, 1969). Such local
conditions were originally thought to involve habitat structure, but a similar
argument could be made for parasites or other pathogens as selective forces.
In humans, for example, populations of different ethnicities differ in rates
of infection by the malaria-causing hematozoan Plasmodium falciparum;
this difference appears to be genetically based
(Modiano et al., 1996).
However, despite the low mating success of nonlocal males shown here, mountain
white-crowned sparrows exhibit considerable gene flow across dialect borders
(although dialects are associated with some reduction in gene exchange;
MacDougall-Shackleton and
MacDougall-Shackleton, 2001). Gene flow among dialects might be
sufficient to prevent local populations from evolving resistance to the local
suite of parasites.
A fourth possibility is that the immunological disadvantage to nonlocal
males is based on experience rather than on genetics. That is, nonlocal males
may be more susceptible to hematozoan parasites because they have not been
previously exposed to the local parasite strains. Among humans, unfamiliar
strains of P. falciparum do appear to be more destructive than
previously encountered strains (Gupta et
al., 1994). In mountain white-crowned sparrows, previous infection
with Haemoproteus might similarly induce some degree of
strain-specific immunity. Consistent with this possibility is the fact that
nonlocal males returning for a third or fourth breeding season were less
heavily parasitized than were first- and second-year nonlocals (although this
comparison reduces sample sizes to the point where inferential statistics are
inappropriate). Morton (1992)
noted that previous familiarity with the study area may enhance male
reproductive success, as yearling males that had been banded as juveniles on
the study area were more likely to breed than adult recruits. One mechanism
for this effect of previous familiarity could be experience with local strains
of parasites.
Dialects, parasites, and mate choice
Parasitic infection is thought to affect fitness in many songbird species.
For example, secondary sexual characteristics of affected individuals may be
compromised (e.g., Buchanan et al.,
1999; Hamilton and Zuk,
1982; Møller,
1990; Thompson et al.,
1997), presumably resulting in decreased attractiveness to
potential mates. In mountain white-crowned sparrows, song dialect appears to
be a fairly reliable index of male parasite load and may thus represent a
useful cue with which females can select mates. That is, by mating
preferentially with local singers, females may avoid mating with parasitized
or parasite-susceptible males. Our findings neither support nor conclusively
contradict this possibility. Dialect did not predict male mating success when
parasite load and other variables were controlled for. However, given the
correlation between song and parasite load and the relatively low power of
this analysis to detect an effect of song (song varies discretely rather than
continuously, and there were relatively few nonlocal males in the analysis),
we cannot yet dismiss the possibility that dialect affects paternity.
If females do use song dialect as a cue to avoid mating with parasitized or
parasite-susceptible males, they would presumably benefit by enhanced
offspring survival. In this population, nests at which both parents are free
of hematozoan infection are more likely to fledge young successfully than are
nests at which one or both parents are parasitized
(Derryberry, 2000;
Richardson, 1997).
Furthermore, if the difference in parasite load between local and nonlocal
males reflects genetic differences in parasite resistance, offspring sired by
local males may be better adapted to the local parasite fauna. In bluethroats
(Luscinia svecica), extrapair nestlings are more immunocompetent than
their half-sibs, suggesting that at least in this species, females use
extrapair mating to enhance offspring immunocompetence
(Johnsen et al., 2000).
Conversely, song dialect may not be directly involved in mating success except as a correlate of parasite load. As a consequence of being heavily parasitized, nonlocal males may be less able than locals to attract mates or defend territories. We found no difference between locals and nonlocals in age, body size, mass, or territory quality, but parasite load might affect more immediate behavioral measures such as song rate or ability to patrol a territory, which could in turn influence male mating success. Severe parasitic infection might also compromise sperm viability (by inducing fever, for example) and thereby reduce paternity.
Conclusions
Our findings suggest that the relationship between song dialect and fitness
is more complex than previously supposed. As predicted by both the genetic and
social adaptation hypotheses, males singing the local dialect enjoyed enhanced
fertilization success relative to nonlocal singers. However, this effect
appears to be due to an interaction between song dialect and parasite load
rather than to the effects of dialect per se. Furthermore, it remains unclear
whether the low parasite loads of local singers result from genetic
adaptations to the local parasite fauna or from previous exposure to these
parasites (in which case males of any genotype might eventually be able to
develop resistance). Thus, the adaptations apparently favoring local males
might be experiential rather than genetic. Conversely, nonlocal (dispersing)
males might have inherently poor immune systems relative to local
(nondispersing) males, rather than a specific inability to deal with local
parasites. Conclusively addressing this possibility will require experimental
manipulations with familiar and novel pathogens. In any case, parasitic
resistance and susceptibility may provide a mechanism to explain the
relationship between song dialects and population genetic structure found in
these birds (MacDougall-Shackleton and
MacDougall-Shackleton, 2001). This study has taken a novel
approach in using molecular techniques to identify parentage and measuring
multiple variables that may contribute to fertilization success. This new
approach provides direction for future research that may further clarify
whether the genetic adaptation, social adaptation, epiphenomenon, or some
other hypothesis best explains the evolution and maintenance of song dialects
in these, and perhaps in other, songbirds.
|
ACKNOWLEDGEMENTS |
|---|
We thank Marty Morton and Ken Petren for invaluable advice in the field and lab. Johannes Foufopoulos kindly advised parasite identification and scoring, and Merilee Temple shared unpublished microsatellite primer sequences with us. We thank Shallin Busch, Amy MacDougall, Regan Marsh, and Jody Sanders for help in the field and Scott MacDougall-Shackleton, Ron Ydenberg, and two anonymous referees for comments that improved the manuscript. This research was supported by the National Science Foundation (NSF 9801580 to T.P.H. and E.A.M.S.; E.P.D. was supported by an REU supplement to NSF 9806765); the American Museum of Natural History, the Animal Behaviour Society, and the Association of Princeton Graduate Alumni.
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