Behavioral Ecology Vol. 11 No. 5: 472-485
© 2000 International Society for Behavioral Ecology
The evolution of paternity and paternal care in birds
a Laboratoire d'Ecologie, CNRS URA 258, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 5, France b Estación Experimental de Zonas Aridas, Consejo Superior de Investigaciones Científicas, Calle General Segura, E-04001 Almeria, Spain
Address correspondence to A. P. Møller. E-mail: amoller{at}hall.snv.jussieu.fr .
Received 25 July 1999; revised 30 September 1999; accepted 18 December 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Paternity has been hypothesized to be related to the evolution of paternal care because (1) there should be selection for males not to invest in broods with an uncertain parentage, or (2) male extrapair activity is traded against paternal care. We used interspecific comparisons to discriminate between these alternatives. Male participation in three kinds of parental care (nest building, incubation, provisioning of offspring) increased with high paternity in their own nests. Male parental activities at some stages of the breeding cycle were significantly correlated. A multivariate analysis taking this intercorrelation between different components of care and potentially confounding variables such as precociality, polyandry, and sexual dichromatism into account revealed that paternity was significantly positively related to offspring provisioning, while male participation in the other components of parental care did not explain a significant amount of interspecific variation in paternity. Analyses of evolutionary transitions between different dichotomized states of paternity and paternal care provided no clear conclusions concerning evolutionary scenarios. However, theoretical arguments and the results of the contrast analyses suggest that male provisioning of offspring evolved in response to paternity.
Key words: extrapair paternity, incubation, parental effort, provisioning, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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General patterns of male parental care have played an important role in shaping scientific ideas about the evolution of parental care (Clutton-Brock, 1991
).
Comparative studies of patterns of paternal care in fishes and other taxa have
demonstrated that male parental care appears to be prevalent when there is
little or no sperm competition (Ridley,
1978; Perrone and Zaret,
1979). For example, several fish species with extreme male
parental care such as pipefishes have virtually no sperm competition and thus
have small testes for their body size
(Stockley et al., 1997).
Recently, several paradoxical examples of male parental care in birds, even in
the presence of high levels of extrapair paternity
(Dixon et al., 1994;
Mulder et al., 1994), have
suggested that patterns of male parental care may not be as closely associated
with paternity as previously thought (reviews in
Gowaty, 1996;
Wright, 1998).
An inverse relationship between paternity and male parental care has been
suggested by some theoretical models
(Houston and Davies, 1985;
Houston, 1995;
Kokko, 1999;
Ridley, 1978;
Trivers, 1972;
Westneat and Sherman, 1993;
Whittingham et al., 1992;
Winkler, 1987;
Xia, 1992), but other models
with different assumptions have not predicted such a cost of lost male
parental care for females when sperm competition is prevalent
(Grafen, 1980;
Houston, 1995;
Houston and Davies, 1985;
Maynard Smith, 1977;
Werren et al., 1980;
Whittingham et al., 1992;
Wittenberger, 1979). If
certainty of paternity is the same in all breeding attempts of a male, then
paternity should have no effect on optimal paternal behavior
(Grafen, 1980; Maynard Smith,
1978). However, certainty of paternity may affect the optimal male parental
effort when the probability of future reproduction for a male is high and when
fitness gains from other activities than parental effort are high
(Houston, 1995). The
relationship between paternity and male parental effort may under other
circumstances be virtually flat or have a shallow slope, and the probability
of finding a negative relationship between paternity and male parental effort
in empirical studies with their traditionally small sample sizes is then
negligible (Houston,
1995).
The interspecific relationship between paternity and paternal care has been
investigated for birds by Møller and Birkhead
(1993) using two different
comparative methods, revealing that males provide less food for young if the
frequency of extrapair paternity is high. This relationship does not hold for
other kinds of paternal care such as nest building and incubation. These
results were subsequently questioned by Dale
(1995) and Schwagmeyer et al.
(1999), while Møller
and Birkhead (1995) and
Møller (1999) provided further evidence for their conclusions.
Males often provide parental care at different stages of the reproductive
cycle, and Ketterson and Nolan
(1994) suggested that male
care other than feeding effort may provide more substantial restrictions on
the extrapair copulation behavior of males. In particular, the male share of
incubation among birds may be incompatible with extrapair copulation behavior
because of the physiological changes involved at the proximate level, or male
incubation may result in restriction of the opportunities for males to seek
extrapair copulations at the ultimate level. Møller and Birkhead
(1993) investigated the role
of male incubation as a predictor of extrapair copulations, but found no
significant evidence of such a relationship. However, this result should be
treated cautiously because of the low power of the statistical test.
Schwagmeyer et al. (1999)
suggested that patterns of paternal care in birds supported the incubation
hypothesis, although several potentially confounding variables were not
controlled in their study. In particular, because different kinds of paternal
care tend to coevolve (Lack,
1968; Silver et al.,
1985), it is difficult to consider the importance of different
kinds of care without controlling statistically for the other kinds of care in
the analyses.
The order of evolutionary events in the transition from low to high levels
of extrapair paternity and from low to high levels of paternal care could
potentially go either way (Wright,
1998): male parental care limits the opportunity for male
extrapair activity (Ketterson and Nolan,
1994; Westneat et al.,
1990), or male parental care affects the evolution of extrapair
paternity because the high fitness costs of intense paternal care result in
the loss of such care in the presence of high levels of extrapair paternity
(Kokko, 1999;
Møller and Birkhead,
1993). Until recently such evolutionary alternatives could not be
tested empirically, but developments in comparative methods have allowed
exactly such tests (Pagel,
1994,
1997). Thus, the probability
for particular orders of evolutionary transitions in extrapair paternity and
paternal care can be tested and used to discriminate between alternative
evolutionary scenarios.
In this study we analyzed (1) paternity and paternal care at four different stages of the reproductive cycle (nest building, courtship feeding, incubation, and offspring provisioning); (2) the relative importance of incubation versus food provisioning of offspring in predicting extrapair paternity; (3) the relationship between each of these kinds of paternal care and the independent relationship between the four different kinds of paternal care and paternity in a multivariate comparative analysis, when taking potentially confounding variables into account; and (4) whether extrapair paternity preceded or followed the evolution of male parental care as determined by the probability of transition to different states of the two variables.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Categories of paternal care
We analyzed paternal care at four different stages of the reproductive cycle of birds: nest building, courtship feeding, incubation, and provisioning of offspring. Although nest building and courtship feeding may be considered to represent both male mating effort and parental effort, both activities may indirectly affect the likelihood of survival of the offspring, and males involved in nest building and courtship feeding are likely to trade these against extrapair mating effort.
Data sets
Extrapair paternity was estimated as the fraction of offspring not sired by
the attending male, or in the case of polyandrous or communally breeding
species, the fraction of offspring not sired by the dominant male, with the
sources reported in the Appendix. We obtained estimates of the frequency of
extrapair paternity using studies based on molecular methods and enzyme
polymorphism (the latter only when the estimates of extrapair paternity had
been corrected for the probability of exclusion of sires). All individuals
involved in manipulation experiments were excluded from the analyses. We
checked all major ornithological journals (Journal of Avian Biology, Ibis,
Auk, Condor, Journal of Ornithology), behavioral journals (Behavioral
Ecology, Behavioral Ecology and Sociobiology, Animal Behaviour, Behaviour,
Ethology), and evolutionary journals (Evolution, Journal of
Evolutionary Biology) for papers. Additional information for many other
species was obtained from other sources including congress proceedings, PhD
theses, and so on. We finished collection of data at the end of 1998 (with a
few unpublished studies being changed to published studies as these became
available in the literature). Our estimates of extrapair paternity provide a
repeatable, species-specific estimate as demonstrated by significantly greater
variation among than within species
(Møller and Birkhead,
1994; Owens and Hartley,
1998; Petrie et al.,
1998). We have redone the repeatability analysis
(Falconer and Mackay, 1996)
for a larger number of species with multiple estimates, in total 18 species
with a total of 50 estimates, and the repeatability of extrapair paternity was
0.68 and was statistically highly significant (F = 7.02, df = 17, 32,
p <.0001). This repeatability implies that mean estimates provide
repeatable, species-specific estimates despite considerable intraspecific
variation. If more than a single estimate was available, we used the mean
value calculated across all studies, since this was expected to be closer to
the true species-specific value than any single value.
Estimates of paternal care were based on the proportion of care provided by
the male relative to the total amount of parental care. If males do not
provide a particular kind of parental care, the estimate is 0.00; male
parental care without female care gives an estimate of 1.00. In the case of
courtship feeding, we used an estimate of 1.00 when males provided all food
for the female during the period of courtship feeding. We have whenever
possible used estimates for the populations for which extrapair paternity data
were available. However, a repeatability analysis
(Falconer and Mackay, 1996) of
estimates of paternal care in species for which multiple estimates were
available in the literature revealed that such estimates were highly
consistent among studies (nest building: F = 88.46, df = 26,27,
p <.0001, R =.98; courtship feeding: F = 74.31,
df = 22,23, p <.0001, R = 0.97; incubation: F =
145.99, df = 31,32, p <.0001, R =.98; feeding of
offspring: F = 26.44, df = 35,36, p <.0001, R
=.92). Thus, estimates were highly consistent independent of their origin. We
have consistently used active male behavior such as male provisioning of
offspring rather than male presence as a measure of male care. Comparative
analyses of studies of the effects of male removal on female reproductive
success have shown that the reduction in female success in the absence of a
male is strongly positively correlated with male provisioning, whereas male
presence is a poor predictor of the fitness consequences of male absence for
female reproductive success (Møller, 1999). The paternal care data and
the sources of information are reported in the Appendix. If estimates were
available for the populations used for the paternity studies, these were
preferred over estimates from other populations.
Species were classified as precocial or altricial to control for the fact that precociality is often associated with an absence of parental provisioning of offspring. Information on whether species were precocial or altricial was based on information in the sources in the Appendix.
Because a reduction in parental effort by a male can be compensated by the
parental activity of other males in a breeding group (e.g.,
Burke et al., 1989), it is
essential to control for such opportunities in the comparative analyses.
Furthermore, polyandry and communal breeding can directly affect the estimate
of extrapair paternity as defined in this study. Hence, we controlled for this
confounding effect by determining whether the species considered had a
polyandrous or a communal breeding mating system with more than a single male
attending each nest. This classification was based on information in the
original sources in the Appendix.
Sexual dichromatism is positively associated with the frequency of
extrapair paternity (Møller,
1997; Møller and
Birkhead, 1994; Owens and
Hartley, 1998), and we controlled for confounding effects of this
variable. As a measure of sexual dichromatism, we used the difference between
mean male and female color score in the human visual spectrum made by three
independent scorers (Møller and
Birkhead, 1994). Such scores are highly repeatable among scorers
and are positively correlated with the frequency of extrapair paternity,
implying that the scores estimate important features of color signals related
to sexual selection. Sexual dichromatism was only measured in the part of the
spectrum that is visible to humans, but birds also perceive colors in the
ultraviolet part of the spectrum (e.g,
Bennett et al., 1994;
Maier, 1994). Several studies
of birds have demonstrated a higher frequency of extrapair paternity in
species that are sexually dichromatic in the visible spectrum than in
monochromatic species (Møller,
1997; Møller and
Birkhead, 1994; Owens and
Hartley, 1998), implying that these simple but highly repeatable
scores of coloration contain biologically important information. We are
currently extending the present study using colorimetry to test whether the
results also apply to the ultraviolet spectrum.
The entire data set is reproduced in the Appendix.
Phylogenetic information
Information on phylogenetic relationships among taxa was obtained from
Sibley and Ahlquist (1990).
Although this study has been criticized
(Krajewski, 1991;
O'Hara, 1991;
Raikow, 1991), several parts
of the phylogeny have been confirmed using independent data sets and stringent
phylogenetic analysis (review in Sibley,
1995). We used additional phylogenetic information from Cibois and
Pasquet (1999), Gill et al.
(1989), Leisler et al.
(1997), Livezey
(1986), Patten and Fugate
(1998), Sheldon et al.
(1992), Short
(1982), Wink et al.
(1998), Winkler and Sheldon
(1993), and references in
Yezerinac and Weatherhead
(1995). For the Emberizinae,
we used Voous (1977) for the
position of Emberiza calandra, and the sister species E.
schoeniclus and E. yessoensis were grouped based on information
in Loskot (1986). The results
were independent of this phylogeny because qualitatively similar results were
obtained using the taxonomy of Howard and Moore
(1991). The phylogeny is shown
in Figure 1.
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Comparative analyses
We investigated the relationship between extrapair paternity and paternal
care using standardized contrasts (or differences) between taxa. We used the
statistical software CAIC (Purvis and
Rambaut, 1995) to calculate standardized differences between taxa
for the two variables of interest and for the potentially confounding
variables. Here we present the results based on a model of gradual evolution
assuming that branch lengths are related to the number of species in a clade,
but the results based on a model of punctuated evolution (with all branch
lengths being equal) gave qualitatively similar results. We used the procedure
Crunch of CAIC software to calculate contrasts, and the variables were
therefore treated as continuous variables. We treated the precociality and the
polyandry variables as dummy variables (coded as 0 or 1) in the regression
analyses, as is commonly done in regression analyses (e.g.,
Neter and Wasserman, 1974;
Sokal and Rohlf, 1995;
Zar, 1996). This procedure
also makes intuitive sense because intermediate states of these variables are
biologically meaningful. The proportion of extrapair paternity and the
proportion of male parental care were square-root-arcsine transformed to
achieve normally distributed variables; precociality, polyandry and sexual
dichromatism were untransformed.
We analyzed the contrasts by forcing a regression of the dependent variable
(extrapair paternity) on the independent variable (paternal care) through the
origin (Purvis and Rambaut,
1995). The effects of potentially confounding variables were
controlled using the same procedure with multiple linear regression analysis.
We tested specifically a number of assumptions underlying calculations of
standardized contrasts (Purvis and
Rambaut, 1995), but found no statistically significant
deviations.
The second comparative method used was the general method of comparative
analysis for discrete variables proposed by Pagel
(1994,
1997). This method controls
for similarity due to common descent and allows investigation of ecological or
evolutionary factors that have evolved as correlated traits of male parental
care. Pagel's method uses a continuoustime Markov model to characterize
evolutionary changes along each branch of a phylogenetic tree without relying
on reconstructions of the ancestral character state
(Pagel, 1994). Two models are
fitted to the data, one allowing only for independent evolution, the other
allowing for correlated evolution of the two characters. The method tests the
hypothesis of correlated evolution using a likelihood ratio test statistic,
where the likelihood ratio = -2 loge[H0/H1].
This likelihood ratio test (omnibus test) compares the fit of the independent
model as H0 (four-parameters model) to the fit of the dependent or
correlated evolution model as H1 (eight-parameters model). The
significance of this likelihood ratio test is assessed using Monte Carlo
simulations.
The model allowing for correlated evolution also enables one to test
whether changes in one variable are more or less likely given the state of the
other (contingent changes tests) and also the temporal ordering and direction
of changes (temporal order tests). These hypotheses are tested by determining
whether character transitions (qij) are significantly
different from each other. This is done by forcing certain parameters in the
matrix of transition probabilities to take the same value and fitting that
model to the data by maximum likelihood. This model (seven-parameters model)
is then compared to the model of correlated evolution (eight-parameters model)
by means of likelihood ratio tests. These tests will be asymptotically
distributed as 
2 with 1 df (see Pagel,
1994,
1997). In the same way, it is
also possible to force each parameter in the matrix of transition
probabilities to equal zero and compare the model obtained in each case
(seven-parameters model) to the full model of dependent evolution
(eight-parameters model), again by means of likelihood ratio tests distributed
as 2 with 1 df. This allows us to test whether specified
character transitions are significantly different from zero (alternative
models) and then reconstruct the flow diagram of evolutionary changes.
We used a dichotomous phylogeny (each node with only two descendant nodes). Both variables only have two states. Thus, extrapair paternity was dichotomized into species with extrapair paternity below (0) and above the median value (1; median = 10.0%). Similarly, male food provisioning of offspring was dichotomized into species with male food provisioning below (0) and above the median value (1; median = 50.0%). We have assumed a model of gradual evolution, with branch lengths related to the number of species in a clade.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Extrapair paternity and paternal care
Some of the four kinds of male parental care demonstrated significant correlations among each other (Table 1). Species in which males have a large share in nest building also had a large male share in incubation, and species with a large male share in incubation had less intense courtship feeding (Table 1). All other combinations of male parental care were statistically nonsignificant. An analysis of the restricted data set that excluded all polyandrous species, precocial species without feeding of offspring, and species without pair bonds (Acrocephalus paludicola and Tetrao tetrix) gave similar results, with the exception of incubations and courtship feeding, which was no longer statistically significant (r = -.212, N = 64, p =.090).
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Relative feeding rate of offspring by males was negatively related to extrapair paternity across species (Figure 2). A contrast analysis taking similarity due to common descent into account confirmed that this relationship was unaffected by similarity due to shared evolution [Figure 2b; slope (SE) = - 0.446 (0.084), F = 28.43, df = 1,85, r2 =.25, p <.0001]. Paternity was less strongly negatively related to male nest building and incubation (Table 2), and the relationship for courtship feeding was not statistically significant. Similar findings were obtained when excluding all polyandrous species and species without pair bonds.
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The independent relationship between extrapair paternity and different components of male parental care was investigated in a multiple regression analysis with paternity as the dependent variable and the four kinds of male parental care, polyandry, and sexual dichromatism as independent variables. This regression was highly significant and accounted for 48% of the variance in contrasts in extrapair paternity (Table 3). Male provisioning of offspring entered the regression model with a statistically highly significant partial regression coefficient, and nest building also explained a significant portion of the dependent variable. The coefficients for the other kinds of paternal care were nonsignificant (Table 3). The partial regression coefficient for male food provisioning was not significantly different from the univariate regression coefficient (Tables 2 and 3). Extrapair paternity was not significantly related to polyandry or to sexual dichromatism.
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We repeated the previous analyses using a more restricted data set, which eliminated all polyandrous species (because the absence of male care by the alpha male potentially could be compensated by other males), and all species lacking a pair bond between males and females (because males might not be near the offspring when they potentially could be provisioned with food). Note that the effects of polyandry and precociality were controlled statistically in the first series of analyses. The conclusions of the second series of analyses changed slightly because the partial regression coefficient for incubation reached statistical significance (Table 4). Male provisioning of offspring and nest building still were negatively related to extrapair paternity, and the effect of courtship feeding remained nonsignificant (Table 4). In general, partial regression coefficients for all variables were similar to those based on the full data set. Sexual dichromatism was not significantly correlated with extrapair paternity in this data set (Table 4).
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Finally, we repeated these analyses based on published information only. The results remained unchanged, with the exception of the weakly significant correlation for incubation changing into a nonsignificant correlation (Tables 3 and 4). The main conclusion for male feeding being of general importance was thus upheld.
Transitions between male parental care and extrapair paternity
We analyzed transitions between male feeding of offspring and extrapair
paternity with the program Discrete. The overall omnibus test for the
relationship between the dichotomized male parental care and the dichotomized
extrapair paternity was not statistically significant [likelihood ratio =
2.11, p =.37 (200 simulations)]. Because the overall model was not
significant, the possibility of any further tests was precluded.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Incubation versus food provisioning of offspring as determinants of paternity
The results of comparative analyses depend critically on the quality of the data used. We explicitly tested for such effects by making repeatability analyses of estimates of extrapair paternity and paternal care obtained from different studies. We found statistically significant repeatabilities for all variables, with a low value of 0.68 for extrapair paternity and high values of 0.92-0.98 for estimates of male parental care obtained from different sources. Hence, we can conclude that the data showed consistency. We used few estimates of paternal care based on unpublished data. These were derived from extensive population studies, but might still provide less reliable information than published information. Comparative analyses excluding these unpublished data did not give rise to different conclusions than analyses based on the entire data set (Tables 3 and 4). Hence, the conclusions were robust with respect to these potential problems.
There are at least two competing hypotheses for the role of paternity in
the evolution of male parental care. Males have been hypothesized to reduce
their contribution to expensive parental activities as a means of reducing the
costs of caring for unrelated offspring. Alternatively, because male parental
care may affect the opportunities for males to seek extrapair copulations,
male incubation and provisioning of offspring have been suggested to constrain
the opportunities for extrapair copulations
(Ketterson and Nolan, 1994;
Westneat et al., 1990). We
tested these alternatives by investigating the relationship between paternity
and paternal care in a large sample of birds, for which reliable estimates of
extrapair paternity and male parental care were available.
We found clear evidence of components of male parental care being
negatively related to the frequency of extrapair paternity. The relative
contribution of males to feeding offspring was negatively correlated with
extrapair paternity (Figure 2
and Table 3). Analyses of
single components of male care provided some evidence of a negative
relationship between paternity and male parental care
(Table 2). However, different
components of male parental care are not independent
(Lack, 1968;
Silver et al., 1985), as
demonstrated by several statistically significant relationships
(Table 1). A multiple linear
regression analysis revealed a significant relationship between extrapair
paternity and male feeding of offspring, but revealed nonsignificant
coefficients for the other kinds of male care
(Table 3 and
Figure 2b). These findings
provide little evidence that the male share in incubation is incompatible with
extrapair copulation behavior due to male incubation restricting the
opportunities for males to seek extrapair copulations
(Ketterson and Nolan, 1994).
However, the comparative results are consistent with the suggestion that males
in bird species with high extrapair paternity provide less feeding effort for
offspring than in species with low extrapair paternity. This relationship
could arise, as originally suggested, because there is selection for males not
to invest in broods with an uncertain parcentage or because male extrapair
activity is traded against paternal care.
Effects of paternity on the evolution of paternal care
The question of the order of events in the evolution of extrapair paternity
and male parental care was addressed using maximum likelihood methods to
investigate the probability of transitions. We found no evidence for the
hypothesis that a change in extrapair paternity was associated with a
subsequent evolutionary change in male parental care, or for the opposite
evolutionary scenario. Although these findings should be interpreted with
care, they do not suggest any clear relationships between the evolutionary
transitions between extrapair paternity and the extent of male parental
care.
The hypothesis that extrapair paternity constrains the evolution of male
parental care can also be investigated in light of the amount of time that
males spend on extrapair activity. A radio-telemetry study of hooded warblers
Wilsonia citrina (a territorial species with 26.7% extrapair
paternity, living in secluded habitats) estimated than males spent only 0-8%
of their time off their territory in pursuit of extrapair copulations
(Stutchbury, 1998). Similar
low amounts of time spent on extrapair activity have been reported for the
semicolonial barn swallow Hirundo rustica, which has 30.5% extrapair
paternity (Møller,
1985). The amount of time engaged in extrapair activity is
probably considerably lower for species with low frequencies of extrapair
paternity. Females of a number of species make excursions into the territories
of neighboring males to obtain extrapair copulations (e.g.,
Kempenaers et al., 1992;
Neudorf et al., 1999;
Otter et al., 1998;
Smith, 1988), further
reducing the time expenditure of males on extrapair copulations. If males only
spend small proportions of their total time budget on extrapair copulation
activities, it seems unlikely that this puts severe constraints on the
evolution of male parental care.
Why should paternal feeding of offspring be related to extrapair paternity,
while nest building, courtship feeding, and incubation are unrelated to
extrapair paternity? A potential answer to this question is that this
component of male reproductive effort is particularly costly in terms of
fitness (Møller and Birkhead,
1993). Empirical studies have demonstrated that male feeding
effort is a much more energy-consuming parental activity than nest building or
incubation (review in Clutton-Brock,
1991). Although this explanation is consistent with the patterns
of paternity and male nest building and incubation, it does not explain the
lack of relationship for male courtship feeding. Male investment in courtship
feeding and feeding of offspring are weakly positively associated
(Table 1). Species with a large
male investment in courtship feeding thus also tend to invest in feeding
offspring. Male feeding effort during the nestling period may be more costly
than courtship feeding because of the very high levels of activity. Perhaps
only peak activity levels will suppress male condition and hence reduce
survival prospects. This argument is supported by studies demonstrating severe
immunosuppression due to extensive exercise, but no reduced immunocompetence
in the case of moderate exercise (reviews in
Deerenberg et al., 1997;
Fitzgerald, 1988;
Hoffman-Goetz and Pedersen,
1994).
In conclusion, comparative analyses of the association between extrapair paternity and paternal care in birds revealed a strong negative relationship for male feeding of offspring but nonsignificant relationships for other components of male parental care. These results suggest that male provisioning of offspring has evolved in response to paternity, while there is little evidence of the opposite pattern.
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ACKNOWLEDGEMENTS |
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P. Gowaty and D. Westneat kindly provided constructive criticism. M. Pagel kindly provided a copy of the Discrete program. We are grateful for access to unpublished data provided by J. Briskie, J. Ekman, B. Hatchwell, H. Hoi, F. Hunter, B. Kempenaers, R. Montgomerie, H. Nagata, K. N. Rabenold, N. S. Sodhi, T. Szép, D. Vanshinsbergh, J. Wiehn, and S. Yamagishi. A.P.M. was supported by an ATIPE BLANCHE from CNRS and J.J.C. by a postdoctoral grant from the European Union (Human Capital and Mobility Program) and by the Spanish DGICYT (PB95-0110).
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