Behavioral Ecology Vol. 13 No. 5: 591-597
© 2002 International Society for Behavioral Ecology
Paternal care as a conditional strategy: distinct reproductive tactics associated with elaboration of plumage ornamentation in the house finch
a Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA b Department of Biological Sciences, Auburn University, Auburn, AL 36849, USA
Address correspondence to A. Badyaev, who is now at the Department of Ecology & Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA. E-mail: abadyaev{at}selway.umt.edu.
Received 17 March 2001; revised 13 November 2001; accepted 22 November 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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When individuals in a population differ in physiological condition and residual reproductive value, selection should favor phenotypic plasticity in reproductive investment such that individuals are able to adopt the reproductive tactic that results in the highest fitness under given conditions. Here we examined reproductive tactics in relation to the elaboration of condition-dependent sexual ornamentation (carotenoid breast coloration) in a Montana population of the house finches (Carpodacus mexicanus). Males used distinct reproductive tactics depending on elaboration of their sexual ornamentation. Males with red pigmentation (maximum ornament elaboration) paired with females that nested earlier, but these males did little provisioning of incubating females and nestlings. In contrast, males with yellow coloration paired with females that nested later, but these males fed female and nestlings more. Consequently, for red males offspring recruitment was primarily affected by earlier nest initiation, whereas in yellow males it was affected most by male provisioning. In males with intermediate plumage coloration, all measured components, nest initiation, provisioning of incubating female, and nestling feeding, strongly contributed to offspring recruitment. The fitness consequences of alternative reproductive tactics of males were influenced by breeding experience and fidelity of their mates. Among first-time breeders, red males achieved the highest fecundity because of the advantage gained through early nesting and pairing with more experienced females and because of compensation by their mates for low male provisioning of nestlings. Among experienced breeders, males with intermediate plumage coloration achieved the highest fecundity because of the combined benefits of relatively early pairing and high parental care. High variation in sexual ornamentation in a Montana population of house finches may favor distinct associations of sexual displays with a particular set of reproductive behaviors.
Key words: Carpodacus mexicanus, conditional strategies, house finches, parental care, reproductive investment, secondary sexual traits.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Expression of secondary sexual traits is often closely linked to the overall physical condition and health of an individual and is under strong selection by female preference (e.g., Andersson, 1986
;
Price et al., 1993). Female
preference for males in high overall condition, as advertised by development
of condition-dependent sexual traits, evolves because of direct and indirect
effects of male condition on female fitness
(Andersson, 1994). Theory
suggests that phenotypic effects of male condition that directly affect female
survival and fecundity, such as help with raising offspring, generate much
stronger selection on female preference than do indirect effects
(Kirkpatrick, 1985;
Kirkpartick and Barton, 1997). Consequently, males should invest in
advertising such direct benefits, and females should be particularly
responsive to male displays that accurately predict the resource investment of
males (Westneat and Sargent,
1996).
Despite the apparent importance to females of direct phenotypic benefits
associated with ornament display and the many empirical studies documenting
that resource benefits are often associated with condition-dependent ornaments
(reviewed in Andersson, 1994),
the processes behind the evolution of female preference for
condition-dependent sexual traits that indicate paternal care are not well
understood. The central challenge is to understand the trade-offs between
overall physiological condition, expression of condition-dependent sexual
trait, and investment in parental care (e.g.,
Badyaev and Qvarnström,
2002; Höglund and
Sheldon, 1998; Kokko,
1998; Price et al.,
1993; Sheldon,
2000; Trivers,
1972; Williams,
1966). Such trade-offs can operate both within and across
reproductive attempts. Within a current reproductive attempt, trade-offs may
occur between investment in a condition-dependent sexual trait and investment
in condition-dependent paternal activity (e.g.,
Hoelzer, 1989;
Johnstone, 1995;
Kokko, 1998;
Qvarnström, 1997). For
example, although condition-dependent ornaments must be costly to be honest,
selection should not favor costs of ornament production or maintenance that
would compromise parental care (e.g.,
Fitzpatrick et al., 1995;
Martin and Badyaev, 1996;
Owens and Bennett, 1994).
Across reproductive attempts, relative investment in condition-dependent
traits and parental care should vary among individuals of different age and
reproductive history (i.e., individuals of different residual reproductive
value; e.g., Burley, 1986;
Kokko, 1997;
Smith, 1995;
Williams, 1966). Younger
individuals with greater future breeding prospects or individuals paired with
lower quality mates may invest less parental care in the current reproductive
attempt than is indicated by their condition-dependent trait. For example, if
males with greater development of sexual traits attract better quality
females, then, under certain conditions, such males may be expected to reduce
parental care because of greater investment by their mates
(Burley, 1986;
Gowaty, 1996;
Sheldon, 2000;
Weatherhead and Robertson,
1979). Such confounding effects of female quality and effort on
male investment strategies are especially strong in monogamous species where
parental investment of sexes are similar and mutual mate choice is strong
(e.g., Johnstone et al.,
1996). Furthermore, individual condition may change since the
formation of condition-dependent sexual trait (such as in distinct timing of
molting in the fall and breeding in the spring in some birds). For example, in
individuals experiencing environmentally induced decline in overall condition
in the period between trait formation and trait use, the expression of a trait
may no longer indicate parental care that the individual can afford to provide
(e.g., Kokko, 1998;
Qvarnström, 1999).
Finally, on the individual level, fitness benefits of investment in
condition-dependent sexual trait in relation to overall condition depend on
population variation in expression of the sexual trait
(Candolin, 2000;
Gross, 1996;
Kokko, 1998).
Ultimately, such individual variation in allocation in sexual traits and
parental care should favor multiple solutions favoring a combination of
particular suites of reproductive behaviors
(Badyaev and Qvarnström,
2002; Gross,
1996). By adopting varying reproductive tactics, males and females
can maximize current fitness in relation to variation in individual condition
in a particular environment (e.g., Eadie
and Fryxell, 1992;
Kodric-Brown, 1986;
Radwan, 1993). On the
population level, variation in reproductive tactics should result in
condition-mediated association between expression of the sexual trait (which
indicates an individual's average condition) and benefits that the individual
can provide (which is influenced by allocation into current reproductive
effort in relation to condition), thus enabling evolution of female preference
for a trait.
Adoption of a conditional reproductive strategy requires an individual's
ability to choose a reproductive tactic based on the relative position of this
individual in relation to others in a population
(Gross, 1996;
Kokko, 1998). The elaboration
of an environmentally based sexual trait that is directly linked to individual
condition is especially suitable for the evaluation of such position. In male
house finches (Carpodacus mexicanus), elaboration of carotenoid
ornamentation of breast plumage (Figure
1) is directly influenced by individual physiological condition,
health status, and parasite exposure at the time of molt
(Brawner et al., 2000;
Hill, 2000). At the same time,
acquisition of carotenoid pigments is determined by environmental variation
leading to a wide fluctuation in the range of elaboration of carotenoid-based
ornamentation and its association with overall condition among populations and
across years (Badyaev et al.,
2001a). Thus, fitness consequences of variation in carotenoid
ornamentation strongly differ among house finch populations (cf.
Badyaev and Martin, 2000;
Hill, 2002).
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We studied a large population of house finches in north-western Montana to investigate whether males with different elaboration of a condition-dependent sexual trait used different reproductive tactics. First, we established that measured components of male reproductive investment had strong consequences for offspring recruitment. Second, we examined whether males with different elaboration of condition-dependent sexual traits used distinct reproductive tactics, and whether these tactics varied in fitness consequences. Third, we examined complementary interaction between male and female reproductive behaviors to address the role of female experience in the formation of female preferences for a male sexual trait.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We studied a resident population of the house finches inhabiting an isolated area of suitable habitat near Missoula, in northwestern Montana, USA (for details of the study site and field protocol, see Badyaev and Martin, 2000
). The
study site was a cluster of buildings and 46 identical ornamental shrubs
planted in a single line set in an open grassland. Finches used these 2-m-high
ornamental shrubs for nesting and several large coniferous trees at the edge
of the complex for roosting. Each year, from 1995 to 2000, all finches were
captured during January—March, measured, and marked with a unique
combination of one aluminum and three colored plastic rings. All pairing and
nesting affiliations of breeding adults were determined
(Badyaev and Martin, 2000), and
social paternity was confirmed by DNA fingerprinting analyses
(Badyaev et al., 2001a).
Upon capture, we photographed carotenoid-based breast plumage patch of each
male using a 35-mm camera mounted in a standard position. Individuals were
kept in a standardized position, on the dorsal side with the anterior point of
beak held in place by a wire loop (Badyaev
et al., 2001a). Resulting images were transferred to digital image
files. To assess the effect of bird position in the photostand on
repeatability of measured traits (repositioning error), we repositioned each
male (i.e., taken from a photo setup, put back again, and rephotographed)
three times. Each resulting image of the breast patch was further remeasured
two times (measurement error) under 6x magnification in SigmaScan
software (Jandel Scientific). Pigment hue was the average of the hue
assessment in three different areas (ca. 3 x 2 feathers) within a breast
patch. Following the protocol for visual assessment of hue outlined in Hill
(1992), we recorded pigment
hue on a scale of 1-10: 1-3 yellow, 4-7 intermediate (orange), and 8-10 red.
Details of measurement error (df = 2490, mean squares [MS] = 0.03) and
repeatabilities (r = .99 ± .001, p < .001) for all
498 males in our study population (including all males under this study) are
given in Badyaev et al.
(2001a).
In 1996-2000, age and breeding experience (i.e., "first
breeder," individuals breeding for the first time, and "older
breeders," individuals breeding for second or more times) was known for
most birds, as most the first-year breeders in the study site were marked as
hatching-year birds in the preceding fall. In addition, strong fidelity of
adult house finches to the location of previous breeding and the isolation of
our study site allowed us to evaluate breeding experience and mate fidelity
for all resident males and females (Badyaev
and Martin, 2000). To avoid pseudoreplication, we used data for
only one year of breeding per bird.
After leaving the nest at age 16 days, young finches remain within the
study site until they are 100-120 days old (see
Badyaev et al., 2001b, for
details). As a part of an ongoing study of ontogeny of sexual dimorphism,
young birds were recaptured once per 5-6 days until 100 days of age. Thus, for
each breeding pair, we were able to obtain the number of offspring that
survived to the age of 40 days (hereafter "offspring
recruitment").
In house finches only the female incubates, but males regularly bring food
to incubating females. We recorded the number of trips by males to provision
incubating females during 90-min nest watches on days 7-8 of incubation. We
monitored nests with binoculars or spotting scopes, from a parked car at the
distance of 4-8 m. Food transfers both on and near the nest were recorded. In
1995-1999, each nest was watched during three 90-min periods (morning, midday,
and afternoon), and the average number of trips was used for the analyses. In
2000, one 90-min period (between 0800 and 1100 h) was used. The number of
nestling provisioning trips by male was recorded during similar 90-min nest
watches on day 7 after hatching. In the house finches, the number of nest
visits by a male is a reliable indicator of the amount of transferred food
(i.e., an approximately equal amount of food is brought during each visit;
Nolan et al., 2001).
We used path analysis to quantify the strength of direct and indirect effects of male ornamentation and parental care on offspring recruitment while accounting for correlations among components of parental care. We used multiple regressions to examine the direction of relationships between components of paternal care and offspring recruitment and to estimate standardized regression coefficients (bST, in standard deviations) and corresponding statistics associated with these effects.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Among first-breeders, red males had the highest offspring recruitment, followed by intermediate and yellow males (within-group difference: F2,60 = 4.61, p = .03; only red vs. yellow were significantly different in post-hoc comparisons; Figure 2A). Among older breeders, red males had the lowest, intermediate males had the highest, and yellow males had the intermediate level of offspring recruitment (within-group difference: F2,107 = 10.6, p < .001; all categories were different; Figure 2B).
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Males with more elaborate ornamentation fed nestlings (young: bST = -0.46, old: -0.45) and incubating females (bST = -0.31 and -0.21) less than males with less elaborated ornamentation (Figure 3). Males with more elaborate ornamentation paired with females that initiated nests earlier (bST = 0.65 and 0.41; Figure 3). Greater offspring recruitment was strongly positively associated with greater nestling provisioning (bST = 0.39 and 0.38), and, equally strongly, with early nest initiation (0.41 and 0.56).
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In older breeders, number of breeding attempts with the same female ("retention of female"; Figure 3B) positively correlated with offspring recruitment (bST = 0.33) and strongly influenced nest initiation date (bST = 0.48); pairs that stayed together longer nested earlier. In turn, retention of female correlated with intensity of incubation feeding (bST = 0.87). Consequently, incubation feeding had significant indirect effects on offspring recruitment (i.e., through greater female retention: 0.87 x 0.33 = 0.29 and through earlier nest initiation: 0.87 x 0.48 x 0.56 = 0.23).
To evaluate contribution of different components of paternal care to
offspring recruitment in relation to elaboration of sexual traits, we fitted
path analysis models separately for yellow, intermediate, and red males. We
summed all effects (direct and indirect) of each component for first breeders
and older males separately (Figure
4). In first breeders, offspring recruitment of yellow males was
mostly a result of greater nestling feeding (50% of total effects;
Figure 4A). In intermediate
males, both nestling feeding (36%) and early nest initiation (22%) contributed
strongly to offspring recruitment (Figure
4A). In red males, offspring recruitment was mostly influenced by
earlier nest initiation (45%) and, to a much lesser degree, by nestling
provisioning (16%; Figure 4A).
Males with different trait elaboration used distinct combinations of parental
care components (
2 = 44.7, df = 6, p = .01).
Contribution of unknown (Figure
4; i.e., unmeasured) effects on offspring recruitment did not
differ among three male categories (35%, 39%, and 39%). Overall, yellow and
red males had the opposite tactics in relation to nestling feeding and nest
initiation (Figure 4A). In
older males, offspring recruitment of yellow males was mostly due to effects
of nestling feeding (44%) and incubation feeding (16%;
Figure 4B). In intermediate
males, effects of nestling feeding (21%), female retention (27%), and nest
initiation date (29%) were equally strong, while in red males, offspring
recruitment was mostly affected by early nest initiation (52%;
Figure 4B). Similarly to young
males, contributions of different components of parental care differed
strongly among males of different ornamental groups (2 =
110.3; df = 8; p = .001). In addition, the contribution of factors
not measured in this study was greater in red males compared to other males
(39% vs. 16% in both yellow and intermediate males). The sum of the effects
was the highest for intermediate males due to strong effects of most
components of parental care (Figure
4B).
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During their first breeding season, most males were paired with
first-breeder females (Figure
5A). Young red males were more likely to pair with older female
than intermediate or yellow males (2 = 9.96; df = 2;
p = .007; Figure 5A).
Among older breeders, most yellow and red males were paired with first-breeder
females, whereas intermediate males were paired mostly with older females
(2 = 36.8; df = 2; p = .001;
Figure 5B).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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When individuals differ in physiological condition and residual reproductive value, selection should favor phenotypic plasticity in reproductive investment such that individuals adopt the reproductive tactic that allows them to achieve the highest fitness under given conditions (reviewed in Badyaev and Qvarnström, 2002
; Gross, 1996;
Kokko, 1998). The decision to
adopt a particular suite of behaviors may depend on individual status relative
to population variation in condition and can be phenotypically indicated by
elaboration of a condition-dependent trait
(Andersson, 1994).
Here we documented that male house finches adopt a conditional reproductive
strategy indicated in part by elaboration of their sexual ornamentation. Males
with less elaborate sexual traits (yellow color) and males with more elaborate
sexual traits (red color) used distinct reproductive tactics: Red males paired
early, but provisioned their nestlings less, whereas yellow males paired
later, but provisioned their nestlings more. Investment in early nestling or
offspring/mate provisioning resulted in approximately equal fecundity return,
as measured by offspring recruitment
(Figure 3), so in the absence
of compensation by their mates, yellow and red males should have had similar
fecundity. However, among first-year males, red males had higher fecundity
than yellow males (Figure 2).
This was due to higher paternal investment by females paired to red males. In
a companion study, we removed for 24 h females paired to red and yellow males
and examined male provisioning of nestlings during female absence. While
provisioned only by a male, nestlings of red males grew less than 10% of
normal rate, whereas nestlings of yellow males grew 60% of normal rate
(Badyaev, in preparation). Thus, high investment in sexual ornamentation
appears to enhance the reproductive success of young males by enabling them to
attract females that nest early (e.g.,
Hill et al., 1994), that are
more fecund, or that provision nestlings more because of the male's
attractiveness (e.g., Burley,
1988; de Lope and
Møller, 1993; Sandvik
et al., 2000; Weatherhead and
Robertson, 1979).
Reproductive tactics remained the same among older males: Red males paired early but provisioned young little, whereas yellow males paired late and provisioned young more. Among older males, however, the payoffs relative to male ornamentation were different. Older males with intermediate development of ornamental plumage were able to achieve the highest fecundity; the combined contribution of relatively early nesting and relatively high provisioning led to higher offspring recruitment for intermediate males than did the single-tactic strategies of either yellow or red males. In addition, the large contribution of unmeasured effects to fecundity of red males (Figure 4B) may indicate increased investment of the mates of red males to offspring recruitment (Badyaev, in preparation).
The observation in this study that the most highly ornamented males did not
necessarily have the greatest fecundity
(Figure 1B) suggests that it is
an oversimplification to assume that elaboration of condition-dependent sexual
traits should always be positively associated with greater reproductive
success (e.g., Andersson,
1994). Instead, this association is best understood by examining
relative allocation of resources between condition-dependent sexual traits and
condition-dependent parental care. For example, if males overinvest (in
relation to male average condition) in the development of a
condition-dependent ornament, then ornament development may come at the
expense of parental care and result in lower than average annual fecundity for
the most ornamented males (e.g., Candolin,
2000; Pärt et al.,
1992). Alternatively, males with more elaborate traits can invest
less in parental care by manipulating investment of their mates and may
compensate for reduced offspring output in a given season by increasing their
probability of survival and hence their lifetime reproductive success
(Burley, 1988;
de Lope and Møller,
1993; Gowaty,
1996; Sheldon,
2000; Trivers,
1972). Indeed, in this study population, red males lived longer
and were more likely to survive winters than males with intermediate or yellow
coloration (Badyaev and Martin,
2000), whereas first-breeder females mated to red males were less
likely to survive subsequent winters than females mated to yellow and
intermediate males (Badyaev, in preparation).
Our observations from a Montana population of house finches differ
substantially from observations of house finch populations in the eastern U.S.
In two eastern populations, male plumage redness is positively associated with
both early nesting date (Hill et al.,
1999) and male provisioning of mates and nestlings
(Hill, 2002). So, unlike in
the Montana population, there appears to be only a single strategy for
ornament display and parental care in these eastern populations. How do we
reconcile these differences?
The key characteristic of a conditional strategy is that the decision of an
individual to adopt a particular tactic depends on some aspect of individual
status or condition relative to other individuals in a population
(Gross, 1996). Such
condition-dependent switchpoints (i.e., points of appropriate allocation to
the alternative tactics for fitness maximization) should be sensitive to
ecological and demographic events influencing fitness consequences of
individual tactics (Dunn and Robertson,
1992; Eadie and Fryxell,
1992; Kokko, 1997,
1998;
Radwan, 1993). We suggest that
the evolution of such switchpoints may be influenced by the distribution of
the expression of condition-dependent sexual traits within a population and by
patterns of female learning and experience (see below), and that therein lies
the key difference between the eastern and Montana populations of house
finches. The mean plumage redness of male house finches is much higher and the
range of color displays is much narrower in eastern populations than in
Montana (Badyaev et al., 2001a;
Hill, 2002). Less variation
among males in plumage coloration may favor the adoption of a single
reproductive strategy (i.e., when gain in male individual condition is evenly
partitioned between a condition-dependent sexual trait and parental care it
advertises; Kokko, 1998).
Variation among populations and species of birds in the adoption of
alternative reproductive strategies may account for frequently documented
differences in association between male sexual ornamentation and male parental
care (e.g., positive association: Hill,
1991; Linville et al.,
1998; Wiehn, 1997;
negative association: Burley,
1988; de Lope and
Møller, 1993;
Qvarnström, 1997;
Studd and Robertson, 1985; no
association: Lozano and Lemon,
1996; Sundberg and Larson, 1994;
Wright and Cuthill, 1992;
Yasukawa et al., 1987).
More generally, the direction of association between a condition-dependent
sexual trait and paternal care depends on the relative importance of direct
and indirect benefits in female mate choice (e.g.,
Fitzpatrick et al., 1995;
Kokko, 1998;
Price et al., 1993;
Wolf et al., 1997). In turn,
the relative importance of direct and indirect benefits to a female can change
with female physiological condition and experience (e.g.,
Gowaty, 1996;
Pärt et al., 1992) and
with the frequency of alternative reproductive tactics in a population
(Eadie and Fryxell, 1992;
Radwan, 1993). For example, if
a condition-dependent trait consistently indicates low parental care but high
individual condition and if condition is heritable, then females in good
condition may prefer more ornamented males because the indirect benefits they
would obtain would exceed the costs of reduced parental care, for which they
would be able to compensate (Kokko,
1998).
The importance of adaptive female choice in mediating the relationships
between male trait elaboration and male fitness
(Figure 2) is evident in the
mating patterns of experienced and inexperienced females relative to male
ornamentation (Figure 5; see
Alonzo and Warner, 2000;
Forsgren, 1997;
Reyer et al., 1999). If males
with the greatest trait elaboration provide the least parental care, and if
male parental care is important to reproductive success, then experienced
females should avoid pairing with redder males. Indeed, we observed that
younger females paired with red males at a higher frequency than did older
females (Figure 5). Initial
preference for redder males in young females may be related to strong
preference for redder ornamentation in several other populations of the house
finches (Hill et al., 1999).
Moreover, because of colonial nesting of house finches in our study population
and their strong fidelity to breeding sites, females can directly observe
parental care of males and thus select males on the basis of previous
familiarity (Wagner, 1992).
Direct selection of paternal care by females may lessen the association
between sexual trait and fitness in older males
(Figure 2B).
Our findings raise several questions. First, it is unclear what proximate
mechanisms influence changes in conditional switchpoints and corresponding
patterns of allocation to alternative strategies. In a companion study of this
population, we found that high paternal care was closely associated with
elevated levels of prolactin, a pituitary hormone that controls male parental
behavior. We found that prolactin production is condition dependent and that
higher physiological condition of red males during breeding was due to less
investment in parental care as evidenced by their lower prolactin production
(unpublished data). In addition, an increased level of testosterone, which is
physiologically costly to maintain
(Duckworth et al., 2001),
decreased male parental care in the house finch
(Stoehr and Hill, 2000). Thus,
common condition dependence of prolactin and testosterone production and
maintenance may provide a proximate link behind evolution of alternative
mating tactics. The question of proximate control is especially interesting
given strong population differences in allocation to alternative tactics.
Second, the relative importance of direct and indirect genetic benefits of
condition-dependent traits, especially those advertizing parental care, is not
known. Such knowledge is crucial to an understanding of the evolution of
reproductive tactics. Finally, individual variation in female mate choice as a
result of learning and experience needs further study. Overall, an
appreciation of individual variation in reproductive behaviors is an important
step in establishing the selective pressures and mechanisms underlying the
operation of sexual selection.
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ACKNOWLEDGEMENTS |
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We are grateful to Renée Duckworth, Derek Roff, Judy Stamps, Ron Ydenberg, and an anonymous referee for many helpful suggestions. We thank Wendy Deshamps, Casey Glen, Toni Rapone, Wendy Parciak, and Byron Weckworth for help in the field. The personnel of the Vigilante MiniStorage in Missoula, Montana, kindly allowed us to work on their property. This research was supported by Bertha Morton Research Fellowships at the University of Montana and by the National Science Foundation grants DEB-0075388 and IBN-9722171. Banding for this study was conducted under the U.S. Fish and Wildlife Service permit 23182 to A.V.B.
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