Behavioral Ecology Vol. 13 No. 1: 87-93
© 2002 International Society for Behavioral Ecology
Reduction of maternal care: a new benefit of multiple mating?
Department of Biological Sciences, State University of New York, Albany, NY 12222, USA
Address correspondence to J.L. Brown. E-mail: jlb81{at}albany.edu . S.-H. Li is now at the Department of Biology, National Taiwan Normal University, Taipei, Taiwan.
Received 28 February 2000; revised 12 March 2001; accepted 21 March 2001.
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ABSTRACT |
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Cost/benefit analyses have been used to understand the evolution of mating by females with multiple males, as in extrapair copulations (EPCs), which are now known to occur commonly in socially monogamous and polygynous birds. Indirect (genetic) benefits have been invoked to explain such mating patterns in some cases, but direct benefits have received less attention. We report a study of direct benefits in the communally rearing Mexican jay (Aphelocoma ultramarina). The social mate of the mother (putative father) is the most reliable feeder of the young in his nest, regardless of cuckoldry. Feedings provided by social fathers are not reduced in relation to their paternity loss. In contrast, mothers having nestlings sired by a second male tend to have lower feeding rates than those without such young. Secondary fathers provided a significantly higher level of feeding to the brood of their female than did (1) random nonbreeders of all ages and both sexes, (2) random male nonbreeders of all ages, and (3) older (2+ years), male nonbreeders. Surprisingly, however, broods with two fathers did not receive a higher level of total feeding, despite our observation that two-father broods had two more helpers, on average, compared to broods without extra fathers. Regardless of age or breeding status, males were more frequent feeders than females. This study provides the first evidence that one of the major costs of reproduction, maternal care of nestlings, is reduced for females that have young sired by secondary males.
Key words: Aphelocoma ultramarina, communal rearing, extrapair copulation, extrapair fertilization, feeding rates, helping, male bias, mating system, Mexican jays, multiple mating, parental care.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The widespread occurrence of extrapair fertilizations (EPFs), which have been reported in many avian species once thought to be monogamous, has raised important questions about why females mate with more than one male (reviewed in Birkhead and Parker, 1997
).
Evolutionary cost—benefit analyses have identified two types of benefits
of EPFs to females. Most popular are indirect benefits, as postulated by the
good genes, sexy sons, and genetic diversity hypotheses. Such benefits have
been proposed in several studies (Brown,
1997; Kempenaers et al.,
1992; Weatherhead and Boag,
1995; Wetton et al.,
1995; Zeh and Zeh,
1996,
1997).
In colonies or territories that contain more than one male of breeding age,
females could receive some direct benefits from additional male partners.
Dunnocks (Prunella modularis) illustrate the direct benefit that
females can receive by copulating with multiple males in a polyandrous species
(Davies, 1992; Davies et al.,
1992,
1996). In cases of polyandry
or polygynandry, male dunnocks provided paternal care proportional to the
mating they shared, with increased success of the nestlings. The levels of
paternal care and chick success were maximized when two male dunnocks shared
copulations with one female (Hartley and
Davies, 1994). For polygynous species, such as the red-winged
blackbird (Agelaius phoeniceus), the female might be allowed to
forage in the territory of her extrapair copulation (EPC) partner, and males
might have a higher level of surveillance of their EPC broods
(Gray, 1997).
Mexican jays live in groups of 5-25, in which 2-4 pairs usually build nests
and breed (Brown, 1994).
Unlike the socially monogamous or biandrous dunnock, in which females build
their nests without aid from males, a female jay is aided in nest building
usually by only a single male. Indeed, that male often initiates the nest,
giving a strong impression of behavioral monogamy. For this reason we define a
pair as the primary or nest-building male and female. Males do not cooperate
with each other in building a nest; they are rivals. The nest-building male
guards his female intensively during her fertile period, but dominant pairs
may harass the nest building of the other pairs in the group. Nest building by
pairs of Mexican jays has been recognized by several authors (in Arizona:
Gross, 1949; in Texas:
Brandt, 1940;
Ligon and Husar, 1974;
Van Tyne and Sutton, 1937) and
has been described in detail for color-banded birds in Arizona
(Brown, 1963).
Multiple paternity has been established in Mexican jays using allozyme
polymorphisms (Bowen et al.,
1995) and DNA microsatellite typing analysis
(Li, 1997;
Li and Brown, 2000). Our
examination of 51 complete broods of Mexican jay nestlings showed that more
than 60% of females had at least one nestling fathered by a second male. In
contrast to other communally rearing species, most secondary fathers live
within the same social group as the female they fertilize. This observation
raises the question, why do Mexican jays have such a high level of paternally
mixed broods?
Could female jays gain direct benefits by copulation with two or more males
within their groups? Because we found that secondary fathers were not
superior, on average, to social fathers in dominance rank, age, or
reproductive success, there was little evidence to suggest indirect benefits
by having additional fathers (Li,
1997). Therefore, we focus here on the possibility of direct
benefit for females. In this species, helpers, including unmated mature males,
contribute a large proportion of feedings to the young. Nonbreeding and
breeding helpers commonly feed the female during incubation and brooding
periods and also feed nestlings and fledglings (Brown,
1970,
1972). Helpers contribute about
50% of total feedings to the nestlings, but the putative parents are
consistently the most frequent feeders. Consequently, we investigated whether
a female jay might benefit from secondary fathers by receiving more feedings
for her young, thereby allowing her to feed less.
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MATERIALS AND METHODS |
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Study population
Mexican jays live in pine-oak woodland from central Mexico north in the western mountains to central Arizona and New Mexico and in the eastern mountains to southern Texas. The population under study is in the Chiricahua Mountains of southeastern Arizona at the Southwestern Research Station of the American Museum of Natural History. This population has been color banded and studied since 1969. During 1991-1996, 10 flocks of jays were included in this paternity study. Further details on this population are available (Brown, 1994
). The population size in 1991-1996 ranged from 92 to 133 birds and included 207 color-banded individuals (over the years) for a total of 618 bird-years (excluding birds of the year and a few unbanded individuals). Average flock size ranged from 9.2 to 13.8 jays. We treated each bird-year as independent because the size, composition, social structure, and environmental conditions of each flock changed continually due to climate, age, dispersal, birth, and death, while the social roles of individuals changed with age, year, experience, and dispersal.
Each year from March through late June, we searched thoroughly to locate nearly all nests. Nests that were discovered early in the nesting cycle were monitored intensively to identify the builders and putative parents. For nests that we found later in the nesting cycle, we tried to identify the birds that attended the nest and the males that mate guarded females. The female who built the nest and incubated and brooded the young was designated the mother. The male who built the nest and accompanied the mother was designated her social mate unless he was replaced by another during her fertile period (16% of cases), in which case the latter male was the putative father. When the mate guarding male was not identified, we designated the male that helped the female to build the nest as the father. Genetic fathers other than the putative father were designated secondary fathers. Sexually mature adults were defined as being 2 years of age or more. No 1 year olds have been observed breeding, and only a small fraction of 2 year olds have been observed breeding.
Genetic data
We took 50-100 µl of blood when we banded the nestlings and trapped the
adults. The blood was stored immediately in Queen's lysis buffer
(Seutin et al., 1990) and
quickly refrigerated. DNA was extracted from blood samples by using
conventional phenol-chloroform extraction
(Sambrook et al., 1989) or
LiCl extraction (Gemmell and Akiyama,
1996) after proteinase K digestion. The purified DNA was stored in
Tris-EDTA buffer pH 8.0 at 4° or -20°C. We used five polymorphic
(AAAG)n microsatellite loci (MJG1, MJG3, MJG6, MJG7, and MJG8) isolated from
the Mexican jay genome by a microsatellite enrichment protocol
(Table 1;
Li et al., 1997). By applying
MJG1 and MJG8 alone, the combined paternity exclusion possibility is 0.87. If
using all five loci, which we did in 84 cases, the combined paternity
exclusion possibility is 0.9997 for a randomly mixed population. Lower values
are obtained when close relatives are together. Details of the paternity data
are described in Li (1997). In
this study, we used the results of complete broods
(Li and Brown, 2000), with
additional information from incomplete broods where noted.
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Feeding data
We observed feedings of 34 broods in a total observation time of 820.9 h in
10 flocks from 1991 to 1996. We monitored the feeding of broods intensively
several days before and after the nestling age of 14 days from 1991 to 1996.
Feeding data were collected on separate days between 0815 and 1200 h and
between 1330 and 1730 h. Each observation period lasted at least 60 min. Our
samples of feeding observations were limited to broods in which the total
period of observations for a given brood was at least 9.1 h (mean = 24.14 h).
This cutoff provided at least 30 feeds by identified feeders at each nest. To
obtain an approximately normal distribution, the feeding rates for individual
feeders were transformed by eighth root. We observed 3320 feedings provided by
identified individuals.
Statistical analysis
Before examining feeding rates as a function of parental status, we tested
for a relationship with brood size so that we could control it. We found a
weak but significant relationship; larger broods were fed more than smaller
ones. The effect of brood size, b, on transformed individual feeding
rates (all feeders), fi, was controlled using residuals
from the equation relating individual feeding rates to brood size in our data,
as follows:
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The feeding rates of the combined helpers at each nest were transformed by
square root, and the brood size effect was controlled using residuals from the
equation relating feeding rates of combined helpers, fc,
to brood size as follows:
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The total feeding rate of each brood, fb, was
transformed by square root, and the effect of brood size was controlled by the
following equation:
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RESULTS |
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Feeding rates of helpers compared to parents
To avoid confusion, note that we use the term "helper" in its original sense to mean an individual actually observed feeding young not its own in company with parents at the nest of the parents (Skutch, 1935
). We do not use
"helper" to signify nonbreeding or auxiliary status. In the
Mexican jay a few individuals are seen that are not observed helping at a
particular nest; they may or may not help at another nest in the same group.
We call secondary fathers helpers because they feed young not their own
belonging to the putative father. Without genetic information, such birds
would have been called helpers also. The cuckolded father is in this sense
also a helper, but we do not use the term for putative fathers. The mean feeding rate was 4.12 feeds/brood/h (SD = 1.73; maximum 8.43 feeds; minimum 1.24 feeds; n = 34 broods). Putative fathers fed 1.0 feeds/brood/h (SD = 0.5), and putative mothers fed 0.7 feeds/brood/h (SD = 0.4). All other feeders (helpers, n = 251) on average fed 0.3 feeds/brood/h per helper (SD = 0.4). The feeding rates of putative parents and helpers were significantly different (ANOVA, F2,316 = 53.47, p <.0001). The mean feeding rate of putative fathers was significantly higher than that of putative mothers and higher than that of individual helpers; the feeding rate of putative mothers was higher than that of individual helpers (comparisons of each pair using Student's t, p <.05). Therefore, putative parents were in general the most frequent feeders. Although the putative parents had the highest individual feeding rates, helpers (including secondary fathers and all age classes) cumulatively provided about 59% of feedings (2.43 feeds per h/4.12 total feeds per h). Thus, the combined contribution of the helpers outweighed that of the combined putative parents.
Sex and age differences among helpers
The feeding rates of helpers are listed in
Table 1 according to sex and
age class. Excluding the unsexed helpers, there were 93 male helpers with 0.43
feeds/brood/h (SD = 0.46) and 62 female helpers with 0.22 feeds/brood/h (SD =
0.17) on average. The average feeding rate of male helpers was higher than
that of female helpers overall (t = 3.46, p =.0007, df =
153), but within age categories the sex difference was significant for only
the most numerous age category (age 2-4 years;
Table 1). Within each sex, the
feeding rates were not significantly different among the four age-class
categories (yearlings, 2-4 years old, 5-7 years old, or older than 7 years;
ANOVA; males: F3,89 = 1.31, p =.28; females:
F3,58 = 0.21, p =.89). Clearly, male helpers were
the most significant source of aid to breeding pairs because of their greater
number and higher feeding rates as individuals.
Feeding rates to broods with and without secondary fathers
On average, broods with two fathers (10.71 ± 0.54 helpers) had 2.31
more helpers than broods with one father (8.4 ± 0.64 helpers;
t = 2.77, df = 32, p =.009), even though no significant
difference between the flock sizes of one-father and two-father broods was
observed (13.6 ± 21.0 vs. 12.4 ± 20.8 jays; t = 1.04,
df = 32, p =.31). Although two-father broods received more total
feedings from helpers (Wilcoxon test, Z = 2.60, p =.009;
Figure 1), there was no
significant difference in total feeding rate between two-father and one-father
broods (Wilcoxon test, Z = 1.39, p =.17;
Figure 1).
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Feeding rates of parents with and without secondary fathers
The corrected feeding rates of the putative mother and father (standardized
residual after controlling the effect of brood size) were not correlated with
the number of helpers in the group (r =.09 and.18 for putative
mothers and fathers, respectively, n = 32 broods), nor were they
correlated with the feeding rates of all helpers combined and corrected for
brood size (r =.06 and.01 for putative mothers and fathers,
respectively, n = 32 broods). Although the feeding rates of cuckolded
fathers were slightly lower than those of uncuckolded ones (0.89 vs. 1.06
feeds/h), there was no significant difference in corrected feeding rate
between cuckolded and uncuckolded fathers (Wilcoxon test, Z = -1.26,
p =.21; Figure 2).
Only one cuckolded male totally deserted his brood (7.7%, 1/13), but no
desertion by uncuckolded males was observed (n = 20). In contrast,
feeding rates to nestlings by mothers with young sired by secondary males were
significantly lower than by those without such young (0.50 vs. 0.83 feeds/h;
for corrected feeding rates: Wilcoxon test, Z = -2.45, p
=.01; Figure 2).
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Secondary fathers compared to putative fathers
Secondary fathers had a lower feeding rate (0.4 feedings/h, SD = 0.34,
n = 14) than did putative fathers (Wilcoxon test, Z = -3.18,
p <.0015). The difference in feeding rate among not cuckolded,
cuckolded, and secondary fathers was highly significant
(Table 2; ANOVA,
F2,46 = 6.69, p =.003). Putative fathers not
cuckolded had the highest feeding rate, and the feeding rate of cuckolded
males was significantly higher than that of secondary fathers (multiple
comparisons of means by Student's t test, p <.05).
Although secondary fathers had a lower feeding rate on average than putative
fathers, most secondary fathers indeed fed the young in the nest that
contained their own young (85.7%, 12/14). Four of them (28.6%) were the
helpers who fed young most (n = 3) and second most (n = 1)
in the group. These secondary fathers provided on average 16.8% of the total
feedings to the broods they aided. Although this is lower than the percentage
of feedings provided by putative fathers (25.3%, n = 35 broods), it
is as important as the feedings provided by cuckolded fathers (17.5%,
n = 14 broods). Therefore, 50% of secondary fathers provided aid that
was at least as significant as that of the cuckolded fathers.
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Secondary fathers compared to other helpers
Do secondary fathers feed at a higher rate than other helpers because they
copulated with the mother? We did not approach this question experimentally,
but nonexperimental answers were obtained by comparison to three progressively
narrower categories of helpers. We used Monte Carlo simulations to test
whether the median of feeding rates of secondary fathers was different from
that of all possible helpers, including the secondary fathers. Putative
fathers were excluded from the simulations. Monte Carlo simulation is a
resampling technique that is especially appropriate to test whether the
observation is statistically different from random expectation when the
sampling distribution is unknown (Sokal
and Rohlf, 1995). Our simulation was done by randomly sampling one
individual from each group and resampling from those individuals in the sample
size that is comparable to our observation. Medians of helper feeding rates
were calculated from these resampled individuals. This process was iterated
10,000 times for each simulation. The simulation generates a distribution of
the median of feeding rates that represents the behavior of random
individuals. The possibility that the distribution of feeding rate provided by
secondary fathers is different from random can be determined by the location
of the median feeding rate of secondary fathers within the distribution
generated by simulation.
The median feeding rate provided by secondary fathers was 0.46 feedings/brood/h. The Monte Carlo simulations showed that this value is significantly greater than random compared to any nonbreeder of any age or sex (p =.001). Because females fed at lower rates than males (Table 1), we next restricted the sample to males. Secondary fathers also fed at a higher rate than any male nonbreeder of any age (p =.005). Although we found that yearling males fed at the same rate as older males, to make the comparison as strict as possible we then also eliminated the yearling males. We found that secondary fathers fed at a higher rate than male nonbreeding helpers of comparable age (age 2+ years, p =.006; Figure 3). Indeed, there was less than a 1% chance that the feeding rate of a random individual male of breeding age could be as high or higher as that of the median for secondary fathers. This result suggests that the rate of feeding by a secondary father was significantly higher than what a female might expect to receive from a random nonbreeder, especially a male of comparable age.
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DISCUSSION |
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Feedings by fathers
In our study 63% of 51 complete broods contained young with secondary fathers, but only 40% of the 139 nestlings from complete broods were sired by secondary fathers (Li and Brown, 2000
). We identified genetic fathers for 82 of 85 nestlings
without secondary paternity and 46 of 55 nestlings with secondary paternity.
No nests with more than two fathers were found, and at least 96.1% of
secondary fathers came from within the same social group. Perhaps the lesser
genetic representation of secondary fathers, combined with their lack of
investment in nest building, provides some insight into why they did not work
as hard as the primary fathers.
Direct benefits of multiple mating: maternal care reduction
Three lines of evidence suggest that broods of female Mexican jays receive
additional feedings from secondary fathers. First, broods of two or more
fathers usually had more helpers and received more aid from helpers than
broods containing young with only one father. Second, the helpers that
provided the most alloparental care were usually sexually mature males in the
group, who could have copulated with the mother. And third, secondary fathers
usually fed more frequently than any other nonbreeders. These considerations
suggest that broods with two fathers receive more feedings than broods with
one father.
The additional aid from extra fathers and other helpers could significantly
reduce the feeding load of females. Because parental effort is negatively
associated with annual survival in other avian species
(Gustafsson and
Pärt, 1990;
Gustafsson and Sutherland,
1988; McDonald et al.,
1996; Nilsson and Svensson,
1996; Pugesek and Diem,
1990), this relationship is likely in Mexican jays as well.
Therefore, multiple fathers should allow mothers to improve their future
fitness by reducing costly maternal care and thereby promoting maternal
longevity. Consequently, our results also suggest that a direct benefit to
mothers in the form of a reduction of maternal feeding effort could be one of
the factors that drives the evolution of mating and care systems in this
species.
This benefit in the Mexican jay differs from that found in another species
with two fathers at some nests, the dunnock. Aid from a second male dunnock
increases the overall feeding rate to the young, but, in contrast to the
Mexican jay, it does not lower the feeding rate of the mother in comparison to
mothers in pairs (Davies,
1992; Hatchwell and Davies,
1990). Furthermore, compared to pairs alone, trios of dunnocks had
heavier young and lower rates of starvation
(Davies, 1992). Thus, the
benefit in jays differs from that in dunnocks in the way that the female takes
advantage of the increased feedings from additional males, leading to greater
production of young in the same season for dunnocks and to reduced parental
effort and presumed longer life in the Mexican jay. This difference is
consistent with the longer life of Mexican jays, which can live up to 20 years
(Brown, 1994;
Davies, 1992).
Multiple mating: a costly behavior for female jays?
Theoretically, it is a waste for males to invest much in young that they do
not sire (Houston, 1995;
Møller and Birkhead,
1993; Owens, 1993;
Trivers, 1972;
Westneat and Sargent, 1996;
Westneat and Sherman, 1993).
In some of the species studied, putative fathers often reduced their feeding
rate when they were cuckolded (e.g., Dixon
et al., 1994; Møller,
1988; Wagner,
1992; Wagner et al.,
1996), though this is not a universal result
(Mulder et al., 1994;
Wright et al., 1999). In
Mexican jays there was no significant difference in feeding rates between
cuckolded and uncuckolded males. The relatively low paternal investment in the
Mexican jays (averaging less than 25% of total feedings) might partially
explain why the level of paternal care did not respond to high rates of
cuckoldry. Low paternal investment could be an evolutionary strategy that
corresponds to the highly mixed paternity in Mexican jays. It could also
result in part from the large contribution made by helpers to the feeding of
the brood. Because about 60% of broods were sired at least partly by secondary
males (Li and Brown, 2000),
natural selection should not favor putative fathers that invest high levels of
paternal effort in broods that might contain unrelated nestlings. On the other
hand, because cuckolded fathers most likely are the dominant and older males
in the group (Li and Brown, manuscript in preparation), they still have the
highest access to females during their fertile period. Because male birds seem
unable to discriminate their own young from others in a brood
(Kempenaers and Sheldon, 1996;
Westneat et al., 1995;
Wright et al., 1999), male
jays are unlikely to feed their own young preferentially as a strategy to
reduce their investment in unrelated nestlings. Neither should males be
favored to desert an entire brood that might be cuckolded because they would
risk losing all their reproductive success for the year and perhaps the future
if females avoid that male. As a compromise, males might be favored to lower
their level of paternal care in such situations regardless of paternity of
young. This strategy would work only when paternal care is not critical for
the survival of nestlings. Aid from helpers probably releases male jays from
being punished by lowering their paternal effort.
Because paternal care is usually crucial for the success of nestlings, aid
from social mates can in theory constrain a female from becoming polyandrous
(Birkhead and Møller,
1996; Gowaty,
1996; Westneat et al.,
1990), even though she might potentially benefit from doing so
(reviewed in Birkhead and Møller,
1992; Westneat et al.,
1990). In Mexican jays, paternal effort is not reduced by
cuckolded fathers; therefore, there is no severe penalty of paternal care
reduction for females who engage in mating with multiple males. When coupled
with the recruitment of additional helpers, copulation with secondary males is
not likely to be a costly behavior for female jays.
Causes of multiple mating
Reduction of maternal workload is one possible predisposing factor toward
multiple mating by female Mexican jays, but many factors probably combine to
cause this behavior. First, the jays must have sufficient tolerance for each
other to live in groups. Second, an extra level of tolerance is needed for the
coexistence and simultaneous breeding in the same group territory of rivals of
the same sex. Third, the risk of inbreeding depression is involved in some
cases. Fourth, the large contribution of feedings by nonbreeding helpers
reduces the mother's dependence on the nest-building father, as in fairy wrens
(Mulder et al., 1994). We
interpret our finding of a reduction in maternal workload as one of many
contributing factors to multiple mating. Conscious motivation of the female
for multiple mating does not seem to be a necessary factor. We did not see
females seeking out certain males. Instead, the numerous occasions on which a
guarding male left a receptive female to defend the territory or deal with
predators provided opportunities for access to females by secondary males.
Male-biased helping
The age, sex, and breeding status of helpers varies from breeding system to
breeding system (Brown, 1987).
In singular breeding species, in which only one pair of birds breeds in the
territory, helpers are commonly offspring from previous seasons, but they can
also be unrelated immigrants (Emlen,
1997; Stacey and Koenig,
1990). In the case of the Mexican jay, a plural breeder, the
composition of helpers is far more complicated. Helpers in Mexican jays can be
offspring of breeders, unrelated nonbreeders, breeders at failed nests, or
rarely parents from the other active nests
(Brown and Brown, 1990). In
this study, we found that males with paternity in the nests are likely to act
as particularly active helpers. Regardless of paternity, however, helping
behavior in this species is male biased. Although the sex ratio is roughly
even among breeding adults (Brown,
1994), male jays were disproportionally likely to be helpers. Male
helpers also fed more frequently than female helpers at the nest. Sex-biased
helping behavior is not well documented in communally breeding species that
have both male and female helpers. Consequently, Mexican jays provide a
special opportunity to study sex-biased helping behavior. For sexually mature
males, such bias might be partially due to the potential sexual dynamic among
those males and breeding females. Although genetic data have provided a new
insight into the evolution of male-biased helping in this species, this
insight is not applicable to male yearlings, which do not breed but also
attend nests as often as do older male helpers. The role of possible sex bias
in this species, therefore, needs more study before the helper system can be
fully understood.
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ACKNOWLEDGEMENTS |
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We thank the many field assistants who participated in the field work, C.B. Stewart who provided lab space and equipment, E.R. Brown for comments on the manuscript, and the Southwestern Research Station of the American Museum of Natural History, New York, for the opportunity to work there. Funding was supplied by grants from the U.S. National Institute of Mental Health, National Science Foundation and the State University of New York.
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