Behavioral Ecology Vol. 13 No. 4: 450-455
© 2002 International Society for Behavioral Ecology
Monandry and polyandry as alternative lifestyles in a butterfly
Department of Zoology, University of Stockholm, S-106 91 Stockholm, Sweden
Address correspondence to N. Wedell, who is now at the School of Biology, University of Leeds, Leeds LS2 9JT, UK. E-mail: n.wedell{at}leeds.ac.uk . P.A. Cook is now at the School of Health, Liverpool John Moores University, 79 Tithebarn Street, Liverpool L2 2ER, UK.
Received 5 July 2000; revised 2 June 2001; accepted 12 August 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Butterflies show considerable variability in female mating frequency, ranging from monandrous species to females mating several times in their lifetime. Degree of polyandry also varies within species, with some females only mating once and others mating multiply. Previous studies have shown that one reason for female multiple mating is to obtain nutritious male donations that both increase the longevity of females and result in higher lifetime fecundity. Despite the presence of male nutrient donations, some females of the green-veined white butterfly (Pieridae: Pieris napi) never mate more than once. In this study, we examined this apparent paradox. We assessed to what degree polyandry is under genetic control by a full-sib analysis, and we also estimated the broad sense heritability of female lifetime fecundity in singly mated females. Both polyandry and lifetime fecundity have a genetic component. However, degree of polyandry appears to be traded off against reduced longevity when denied the opportunity to mate more than once. It is possible that female P. napi display different reproductive strategies, with some females relying on male donations to realize their potential fecundity and others relying on their own resources for egg production. In nature, polyandrous females may be prevented from mating multiply due to unfavorable weather. We discuss the possibility that the trade-off between degree of polyandry and life span when singly mated may affect the maintenance of genetic variability in female mating frequency in this species. Possible reasons for these different reproductive strategies are discussed.
Key words: body size, fecundity, life history, nuptial gifts, polyandry, sexual selection, trade-offs.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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There is considerable variation in female mating frequency, both across and within species and populations of animals (Andersson, 1994
;
Birkhead and Møller,
1998). For most species, mating frequency is difficult to assess
in the wild. Butterflies are particularly well suited for studying natural
variation in female mating frequency because, unlike most other insects,
reasonably accurate estimates can be made for wild populations. This is
because in most butterfly species remnants of the spermatophore (one is
transferred per mating) remains within the female's reproductive tract
throughout her lifetime, making it possible to determine the number of times a
female has mated by dissecting and counting the number of spermatophore
remains (Drummond, 1984). This
approach has revealed considerable variation in female mating frequency among
species and populations (Drummond,
1984; Gage, 1994;
Wiklund and Forsberg,
1991).
Repeated mating can pose a cost to females in terms of time and energy
waste and increased risk of predation and disease transmission, and it can
even have a direct cost due to toxic properties of males' ejaculates
(Chapman et al., 1995).
Therefore, females must benefit in some way by being polyandrous. There are
several potential reasons that females mate multiply. One reason is to obtain
good or compatible genes resulting in offspring of higher fitness
(Kempenaers et al., 1992;
Tregenza and Wedell, 1998;
Zeh and Zeh, 1997). Another
reason for multiple mating is to acquire direct benefits such as paternal care
or male nutrient donations (Clutton-Brock,
1991; Gwynne,
1984). In some species of butterflies, females essentially forage
for male nutrient-rich spermatophores by mating several times
(Boggs and Gilbert, 1979;
Kaitala and Wiklund, 1994),
and recently Stjernholm and Karlsson
(2000) showed that multiply
mated females allocated a larger fraction of their soma to reproduction
compared to singly mated females (by means of thorax muscle histolysis),
thereby boosting their reproductive output. In a review, Arnqvist and Nilsson
(2000) showed that female
fitness increased steadily with female mating rate, and in polyandrous
green-veined butterflies (Pieris napi)—for example, female
longevity and lifetime fecundity is increased when the amount of male
donations received by females is experimentally increased (Wiklund et al.,
1993,
1998).
Despite the demonstrated direct benefits of polyandry in P. napi,
a fraction of the population never mates more than once. Why do females
exhibit this apparently maladaptive behavior? It is unlikely to be explained
by polyandrous females suffering a cost of mating
(Holland and Rice, 1999)
because experimentally increasing spermatophore material results in increased
longevity and lifetime fecundity (Wiklund et al.,
1993,
1998). Variation in female
mating frequency is not simply a consequence of variation in female age, as
old, singly mated females are frequently caught
(Wiklund and Forsberg, 1991).
It also cannot be explained by competition between females for access to male
donations, as females do not court males and are unable to discriminate
between virgin and mated males (Kaitala
and Wiklund, 1995). Males are also not a limited resource because
their reproductive rate is substantially greater than that of females,
resulting in a male-biased operational sex ratio
(Wiklund et al., 1998).
One potential reason for variation in female mating frequency is that there is some advantage to females of not relying on male nutrient donations for their own reproductive performance. That is, polyandrous females denied the opportunity to mate as many times as they want may suffer reduced reproductive output compared to singly mated females that mainly rely on their own resources for egg production. One possibility is that a trade-off exists between degree of polyandry and lifetime fecundity and/or longevity, which could affect variability in degree of polyandry. If such a trade-off is present in the green-veined white butterfly, we predict that (1) polyandry has a genetic component because any trade-off requires a genetic basis; (2) only polyandrous individuals are able to benefit from multiple mating because they efficiently convert male donations into more eggs; (3) polyandrous females denied the opportunity to mate more than once will show reduced lifetime fecundity and/or longevity because they depend on male nutrient donations to realize their potential fecundity; and (4) monandry is a strategy adopted by some females that rely mainly on their own resources for reproduction.
We explored the possibility of a trade-off between degree of polyandry and fecundity and/or longevity in the green-veined white butterfly. By providing females with the opportunity to mate as many times as they want (given that there is genetic variation in degree of polyandry), females from polyandrous families ("genetically polyandrous" females) should benefit to a greater extent from male-derived nutrients compared to females from less polyandrous families. This is because females are expected to differ in their ability to utilize male nutrient donations, and hence a positive correlation between degree of polyandry and fecundity and/or longevity is expected. Accordingly, the reverse is expected when these females are prevented from remating. In nature, it is likely that females do not always have the possibility to mate as frequently as is optimal. If females are denied the opportunity to mate multiply and forced to be monandrous, genetically polyandrous females may potentially suffer more in terms of reduced fecundity and longevity than genetically monandrous females, which are able to rely mainly on their own resources for reproduction. Provided degree of polyandry has a genetic basis, we therefore expect genetically polyandrous females denied the opportunity to remate, by forcing them to become monandrous, to suffer reduced lifetime fecundity and/or longevity compared to singly mated, genetically monandrous females. The aims of this study were therefore twofold: first, to determine the extent to which female fecundity and degree of polyandry is under genetic control, and second, to explore the possibility of a trade-off between female mating frequency on one hand and lifetime fecundity and longevity under an experimentally imposed monandrous situation on the other.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Lifetime fecundity and polyandry
Adult females were captured early in the flight season from the field to maximize the chances that females had only mated once. They were brought back to the lab and provided with garlic mustard leaves (Alliaria petiolata) for egg laying. Each female was kept in a separate egg-laying cage and provided with 25% sugar solution added to flowers. After females had laid eggs that hatched successfully, they were dissected and the number of spermatophore remnants present counted. In the green-veined white butterfly, residues of old spermatophores remain in the female throughout her life, making it possible to assess the total number of matings performed. Only offspring from females with one spermatophore remains (hence only mated once) were reared to ensure that that all resulting offspring were full-sibs. Only six wild-caught females that had more than one spermatophore remains were excluded.
We reared 30 offspring from each female in sib-groups of five in plastic cups containing garlic mustard leaves to minimize the effect of variation of larval host-plant quality. Individuals were reared at 24°C and a 22:2 h light:dark cycle to ensure direct development. Emerging individuals were weighed the morning after eclosion and given a unique color mark on their wings with a marker pen, guaranteeing that individuals could be assigned to their family of origin. In total, offspring from 39 singly mated wild-caught females were reared. Four daughters emerging from different rearing containers (to reduce the effect of common environment) of the F1 generation of each family were assigned to either determine their lifetime fecundity after one mating or determine their degree of polyandry (n = 2/trait/family).
All females were mated at 1 day of age to a 1-day-old unrelated virgin male. Females assigned to the lifetime fecundity treatment were placed in 1.5-1 plastic cups provided with leaves of A. petiolata and a cotton bud soaked in 25% sugar solution. Females were provided with new sugar solution every day and the leaves were checked daily for eggs, which were removed and counted. Females were removed from the experiment when they died and their longevity noted. These females were prevented from remating and hence experienced forced monandry.
Females in the polyandry treatment were placed in mating cages (70 x 70 x 50 cm); provided with males, egg-laying plants (A. petiolata), and sugar solution added to flowers twice a day; and allowed to mate and lay eggs freely throughout their lives. Full sisters were kept in separate cages to reduce any cage effects. We checked cages daily and removed any dead individuals. Males were removed after about 5 days and new males were added, keeping the ratio of males to females constant (about 1.5 as many males as females), with each cage containing about 20 individuals in total. This ensured that females always had access to males willing to mate. Females were removed on the day they died and dissected, and the number of matings was determined by counting the total number of spermatophore residues present in the female. We recovered and scored two females from each of 37 families for degree of polyandry and longevity.
Phenotypic correlations
Female body weight, fecundity, and longevity were normally distributed, but
degree of polyandry was not. Therefore, correlations with degree of polyandry
were done using Spearman rank correlations corrected for ties. Relative female
fecundity was calculated as the residuals of the regression of lifetime
fecundity on female body weight because this is an effective way of removing
the effect of female body weight.
Genetic estimates
Broad sense heritabilities were estimated from a one-way ANOVA
(Roff, 1997). Polyandry is not
normally distributed, and normality could not be achieved with any
transformation. However, the residuals of the ANOVAs did not differ across
families for any of the characters measured. Therefore, when calculating
heritabilities of polyandry, repeated-measures ANOVA was also used. The
standard error of the heritability was estimated following Roff
(1997) for full-sibs with
equal family size:
 | (1) |
,
1998). Hence, by mating a male
to two females, the first female that a male mates with receives a
substantially larger nutrient contribution, affecting both her reproductive
output (Wiklund et al., 1998)
and the performance of her offspring (Wedell, unpublished data). The effect of
common environment was minimized by rearing individuals at the same
temperature and on the same larval host plant. The mating status of the males
that the wild-caught females had mated with is unknown, which may pose a
problem if variation in paternal provisioning affects lifetime fecundity and
mating frequency of his offspring. However, P. napi is protandrous
(males emerge before females), resulting in early emerging females having a
high probability of mating with virgin males
(Wiklund and Forsberg, 1991).
This reduces the risk that the singly mated, wild-caught females had mated
with males of varying mating history and therefore received different amount
of male donations, although this possibility cannot be ruled out. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Genetic components
Lifetime fecundity of singly mated females had a genetic component (h2 = 0.776 ± 0.276), even after controlling for female body weight (h2 = 0.748 ± 0.279; Figure 1) because heavier females were more fecund (r =.388, p =.0147). The heritability of relative fecundity was of similar magnitude as total fecundity, indicating that this character is not simply a function of female body weight covarying with number of eggs laid, but a trait independent of body weight (Figure 1B). Degree of polyandry also had a genetic component (h2 = 0.627 ± 0.305; Figure 2). All heritability estimates differed significantly from zero at p <.007 for fecundity and relative fecundity and at p <.03 for polyandry, as indicated by the ANOVA F tests. Broad sense heritability estimates of all three characters were high. However, because these estimates are based on full-sib analyses, this may be due to dominance effects.
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Phenotypic correlations
Female longevity (mean 20.51 ± 0.686 days, N = 74) was
positively correlated with degree of polyandry across families, indicating
that polyandrous females allowed to mate freely can utilize male donations
more efficiently than females mating a fewer number of times. There was a
positive relationship between average longevity and average degree of
polyandry (rs =.568, p =.0008; 37
families). Similar results have previously been experimentally demonstrated in
this species (Wiklund et al.,
1993,
1998).
Contrary to prediction, there was no significant negative relationship between average lifetime fecundity of forced monandrous females and the average degree of polyandry of their sisters (rs = -.184, p =.195; 37 families). However, if forced to live monandrously, sisters from polyandrous families had a shorter life span than females from less polyandrous families. There was a negative correlation across families between the average longevity of forced monandrous females and the predicted degree of polyandry—that is, the average polyandry of their sisters (rs = -.313, p =.0344; 37 families; Figure 3). The reduction in longevity was larger for polyandrous families. There was a positive relationship between the average difference in longevity between polyandrous females and their singly mated sisters with the average degree of polyandry across families (rs =.612, p =.0002; 37 families; Figure 4), indicating that females from polyandrous families suffer a larger reduction in life span when singly mated compared to females from less polyandrous families. Longevity of monandrous females (mean 16.90 ± 0.689 days, N = 78) was not related to female body weight (r =.070; 39 families), nor was there any relationship between degree of polyandry and female body weight (rs =.065; 37 families).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Lifetime fecundity and polyandry
Lifetime fecundity in P. napi has a genetic component. Moreover, fecundity was under genetic control independent of variation in female body weight per se. Other studies of butterflies and moths have shown that female fecundity is under genetic control but is likely due to heritable variation in body size (e.g., Campbell, 1962
; Iyengar and Eisner,
1999). Not all previous studies of P. napi have found
that lifetime fecundity covaries with body weight in this species (e.g.,
Wiklund and Kaitala, 1995),
indicating that genetic variation in fecundity independent of body size
variation may be a better predictor of lifetime egg production in this
species.
Polyandry also appears to be under genetic control. To our knowledge, this
is the first study to demonstrate that female lifetime mating frequency has a
genetic component. In the field cricket Gryllus integer, the number
of matings performed by females during their first 10 days was found to be
heritable (Solymar and Cade,
1990), and in Drosophila melanogaster time to female
remating is under genetic control (Pyle
and Gromko, 1981). Male mating success has previously been shown
to be heritable in some species (e.g.,
Hughes, 1995;
Jones et al., 1998;
Oksanen et al., 1999;
Wedell and Tregenza, 1999).
The number of lifetime matings of females in this study (mean 2.14, range 1-5
matings, N = 74) is in good agreement with field estimates of this
species (mean 2.03, range 1-5 matings), as determined by spermatophore counts
of wild-caught females (Wiklund and
Forsberg, 1991). Variation in female mating frequency cannot
solely be explained by variation in female age, as demonstrated by old, singly
mated, wild-caught females (Wiklund and
Forsberg, 1991).
In this study, the heritability estimates of all traits were high. However,
because broad sense heritabilities are based on full-sib analyses, these
values may be inflated due to dominance effects. Heritability estimates from
full-sib analyses may include one-quarter of the dominance variance
(Falconer, 1989), suggesting
that full-sib analyses may not be appropriate for estimating heritability of
life history traits. If additive genetic variation in life history traits is
eroded at a faster rate than for other (i.e., morphological) traits, then the
dominance variance should also be greater in life history traits
(Crnokrak and Roff, 1995).
Despite these problems, heritability estimates gained from full-sib analyses
provide valuable information about the genetic basis of traits. Numerous
studies have found that the full-sib method in general does not tend to
overestimate narrow sense heritability (e.g.,
Hedrick, 1994;
Mousseau and Roff, 1987;
Roff, 1997). Moreover, in
P. napi variation in paternal nutrient contribution affects both
female fecundity and offspring body size and performance (Wedell, unpublished
data; Wiklund et al., 1998);
hence a half-sib analysis is not feasible due to males providing smaller
nutrient contribution to offspring with number of previous matings
(Wiklund et al., 1998).
In this study, the environmental effect was to some degree controlled by
standardized rearing condition of the larvae. All individuals were reared at
the same density and temperature and on the same larval host plant. However,
individuals from the same family used to score fecundity and degree of
polyandry were reared in different pots and experienced different mating cages
in order to reduce the effect of common environment on these traits. The
results may potentially also be confounded by variation in mating status of
the males (and therefore variation in nutrient donations) the wild-caught
females had mated with. However, we do not think that this affected our
results. This species is protandrous, with males emerging before females
(Wiklund and Forsberg, 1991),
and early emerging females have a high probability of mating with virgin
males. Collecting females flying in early spring minimizes the risk that these
females have mated with males of varying mating history and hence differed in
nutrient provisioning. Previous studies show assortative mating does not occur
in P. napi (apart from early emerging individuals having a higher
probability of mating with virgins), as females are unable to distinguish
between mated and virgin males (Kaitala
and Wiklund, 1995). Furthermore, if there was a nongenetic effect
of paternal nutrients on offspring fecundity and mating frequency in P.
napi, we expect this to manifest itself via an effect on offspring body
size, as variation in larval host plant quality and male donations result in
body size variation of adults (Wiklund and Wedell, unpublished data). However,
in this study the variables were either independent of body size (lifetime
fecundity), or unrelated to body size (polyandry). No study has demonstrated
an effect of variation in paternal nutrient provisioning on offspring mating
rate or fecundity in a paternally investing insect.
When allowed to mate freely, females from polyandrous families lived
considerably longer than females from less polyandrous families, indicating
that more polyandrous females may be adapted at utilizing male donations
efficiently. This suggests that multiple mating is only beneficial to females
from polyandrous families. It is therefore unlikely that female P.
napi can compensate for low resource allocation during the larval stage
by increasing their mating frequency to receive nutritious donations as
adults. This is because females from less polyandrous families are selected to
mate fewer times, instead relying on their own resources. This in turn
suggests that differences in maximum number of matings is mainly under genetic
control rather than due to variation in available larval resources in this
species. Moreover, female P. napi do not compensate poor larval
reserves by increasing their mating frequency (J. Bergström et al.,
submitted). This differs from findings in bushcrickets, for example, where
females under poor nutritional conditions compensate by increasing their
mating frequency to obtain nutritious male donations
(Gwynne, 1990). However, it
should be pointed out that the situation only applies to female green-veined
white butterflies allowed to mate freely (i.e., the maximum number of matings
performed). In most situations, it is likely that females of this species do
not have the opportunity to mate as many times as they want (see below).
Variation in female mating frequency is also not caused by female competition
for male donations, as females never solicit matings or interact with each
other and are unable to discriminate between males depending on their mating
status (Kaitala and Wiklund,
1995). Males are also not a limited resource because their
reproductive rate greatly exceeds that of females, resulting in a male-biased
operational sex ratio (Wiklund et al.,
1998).
Trade-off between polyandry and longevity
Females from polyandrous families live longer, but the ability to benefit
from male-derived nutrients appears to be traded off against shorter life span
if forced to be monandrous. Singly mated females from polyandrous families
lived significantly shorter than singly mated females from monandrous
families. There was also a tendency for singly mated females from polyandrous
families to suffer lower fecundity than singly mated genetically monandrous
females, although this was not significant.
The reduction in longevity was more pronounced for females from more
polyandrous families. The difference is as much as an 18-days-shorter life
span for the most polyandrous females, a reduction of more than twice the
average life span of freely mating females. This may indirectly affect the
reproductive success of these females, as reduced longevity translates to
shorter time for egg laying. Why do females from polyandrous families suffer
more in terms of reduced longevity by being prevented from remating than
females from less polyandrous families? It is possible that there are genetic
differences between females in their metabolic rate that could explain this
pattern. For polyandrous females to benefit from receiving male nutrient
donations by repeated matings, they have to have a higher reproductive rate to
process these nutrients and convert them into more eggs. The rate of egg
laying differs between singly and doubly mated females
(Wiklund et al., 1993),
suggesting that polyandrous females are better able to convert male nutrients.
The duration of larval development varies with degree of polyandry. There is a
negative correlation between the average larval development time (measured as
number of days from the egg was laid to adult emergence) and average degree of
polyandry across families (rs = -.385, p
=.0269; 34 families), so polyandrous females develop quicker, which may imply
they have a higher metabolic rate.
Polyandrous and monandrous lifestyles?
It is possible that having a lower metabolic and reproductive rate is, at
times, beneficial to females. In Sweden there are frequently periods of
unfavorable weather during spring and early summer, when it is too cold for
females to either forage for nectar or to lay eggs. A similar situation may
occur also late in the flight season. It is possible that having a lower
metabolic rate increases females' chances of surviving periods of cold weather
compared to polyandrous females with higher metabolic requirements, although
this needs to be experimentally examined.
There are also other implications of variation in metabolic rate. In Sweden the first generation of P. napi is protandrous (males emerge before females). This means that females emerging later in the season due to longer development time may not have the opportunity to mate as frequently as early emerging females, especially since males under optimal conditions live significantly shorter time than females, only about 14 days (Wedell, personal observation). This means that late-emerging females may have to rely on their own resources for egg production rather than on males' nuptial gifts. Finally, females may also vary in their migration tendencies, which could also affect the probability of multiple mating. Dispersing females again would have to rely on their own resources to a larger degree than nondispersing females.
This study shows that there is genetic variation in female mating frequency. Although females from polyandrous families, when given the opportunity to mate multiply, have significantly higher reproductive output than females from monandrous families, they suffer more in terms of reduced life span when denied this opportunity. In Sweden the risk of remaining singly mated is a real one, particularly in the spring and early summer due to cold weather. Additionally, by having a higher metabolic rate, polyandrous females may have a higher risk of dying during periods of unfavorable weather. The results of this study suggest that a trade-off between mating rate and reduced longevity, when remating is prevented, may explain part of the variation in female mating frequency in this species. Ideally, the opposite experiment should be performed, whereby females from monandrous families are mated multiply. However, because monandrous females cannot be forced to mate multiply, this is not possible.
A similar situation, with females adopting different mating strategies, may
occur in the polyandrous pollen-feeding butterfly Heliconius cydno.
In this species, females that mate more often and thus receive more
male-derived nutrients do not feed as much on pollen (which also increase
fecundity) as less polyandrous females
(Boggs, 1990). It is possible
that mating frequency is traded off against pollen intake in this species,
with some females specializing in pollen feeding with few matings and others
instead opting for a high mating rate and low pollen intake. This suggests
that, as in P. napi, different females in this species employ
different strategies: some females obtain nutrients from the male by frequent
mating, and others instead eat pollen. As yet, the underlying cause of this
difference among females is unknown (Boggs,
1990).
In conclusion, we envisage a scenario where, on one hand, the polyandrous lifestyle of P. napi may be advantageous under environmental circumstances where genetically polyandrous females are able to mate multiply. On the other hand, under different environmental circumstances in which genetically polyandrous females are unable to realize their polyandry, the monandrous lifestyle may be advantageous. Hence, in nature it is likely that environmental factors (e.g., weather conditions) influence female mating opportunity, thereby aiding variability in degree of polyandry in the green-veined white butterfly.
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ACKNOWLEDGEMENTS |
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We thank W. Blanckenhorn and A. Nilsson for discussion of genetics calculations and Tom Tregenza and the three referees for helpful comments on the manuscript. This study was supported by grants from the Swedish Natural Science Research Council to N.W. and C.W. and by the Royal Society (European Exchange Program) to P.C.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Arnqvist G, Nilsson T, 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60: 145-164.[Web of Science][Medline]
Birkhead TR, Møller AP, 1998. Sperm competition and sexual selection. London: Academic Press.
Boggs CL, 1990. A general model of the role of male-donated nutrients in female insects' reproduction. Am Nat 136: 598-617.[Web of Science]
Boggs CL, Gilbert LE, 1979. Male contribution to egg
production in butterflies: evidence for transfer of nutrients at mating.
Science 206:
83-84.
Campbell IM, 1962. Reproductive capacity in the genus Choristoneura Led. (Lepidoptera: Torticidae). I. Quantitative inheritance and genes as controllers of rates. Can J Genet Cytol 4: 272-288.[Web of Science]
Clutton-Brock TH, 1991. The evolution of parental care. Princeton, New Jersey: Princeton University Press.
Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L, 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373: 241-244.[Medline]
Crnokrak P, Roff DA, 1995. Dominance variance: associations with selection and fitness. Heredity 75: 530-540.[Web of Science]
Drummond BB, 1984. Multiple mating and sperm competition in the Lepidoptera. In: Sperm competition and the evolution of animal mating systems (Smith RL, ed). London: Academic Press; 547-572.
Falconer DS, 1989. Introduction to quantitative genetics. New York: Longman.
Gage MJG, 1994. Associations between body size, mating
patterns, testis size and sperm length across butterflies. Proc R Soc
Lond B 258:
247-254.
Gwynne DT, 1984. Courtship feeding increases female reproductive success in bushcrickets. Nature 307: 361-363.
Gwynne DT, 1990. Testing parental investment and the control of sexual selection in katydids: the operational sex ratio. Am Nat 136: 474-484.[Web of Science]
Hedrick AV, 1994. The heritability of mate-attractive traits: a case study on field crickets. In: Quantitative genetic studies of behavioral evolution (Boake RB, ed). Chicago: University of Chicago Press; 228-250.
Holland B, Rice WR, 1999. Experimental removal of
sexual selection reverses intersexual antagonistic coevolution and removes a
reproductive load. Proc Natl Acad Sci USA
96: 5083-5088.
Hughes KA, 1995. The evolutionary genetics of male life history characters in Drosophila melanogaster. Evolution 49: 521-537.[Web of Science]
Iyengar VK, Eisner T, 1999. Heritability of body mass,
a sexually selected trait, in an arctiid moth (Utetheisa ornatrix).
Proc Natl Acad Sci USA 96:
9169-9171.
Jones TM, Quinnell RJ, Balmford A, 1998. Fisherian
flies: benefits of female choice in a lekking sandfly. Proc R Soc Lond
B 265:
1651-1657.
Kaitala A, Wiklund C, 1994. Polyandrous females forage for matings. Behav Ecol Sociobiol 35: 385-388.[Web of Science]
Kaitala A, Wiklund C, 1995. Female mate choice and mating costs in the polyandrous butterfly Pieris napi. J Insect Behav 8: 355-363.
Kempenaers B, Verheyen GJ, Ban den Broeck M, Burke T, van Broekhoven C, Dhondt AA, 1992. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357: 494-496.
Mousseau TA, Roff DA, 1987. Natural selection and the heritability of fitness components. Heredity 59: 181-198.
Oksanen TA, Alatalo RV, Horne TJ, Koskela E, Mappes J, Mappes T, 1999. Maternal effort and male quality in the bank vole, Clethrionomys glareolus. Proc R Soc Lond B 266: 1495-1500.[Medline]
Pyle DW, Gromko MH, 1981. Genetic basis for repeated mating in Drosophila melanogaster. Am Nat 117: 133-146.[Web of Science]
Roff DA, 1997. Evolutionary quantitative genetics. London: Chapman & Hall.
Stjernholm F, Karlsson B, 2000. Nuptial gifts and the use of body resources for reproduction in the green-veined white butterfly Pieris napi. Proc R Soc Lond B 267: 807-811.[Medline]
Solymar BD, Cade WH, 1990. Heritable variation for female mating frequency in field crickets, Gryllus integer. Behav Ecol Sociobiol 26: 73-76.
Tregenza T, Wedell N, 1998. Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution 52: 1726-1730.[Web of Science]
Wedell N, Tregenza T, 1999. Successful fathers sire successful sons. Evolution 53: 620-625.[Web of Science]
Wiklund C, Forsberg J, 1991. Sexual size dimorphism in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60: 373-381.[Web of Science]
Wiklund C, Kaitala A, 1995. Sexual selection for large
male size in a polyandrous butterfly: the effect of body size on male versus
female reproductive success in Pieris napi. Behav Ecol
6: 6-13.
Wiklund C, Kaitala A, Lindfors V, Abenius J, 1993. Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.). Behav Ecol Sociobiol 33: 25-33.
Wiklund C, Kaitala A, Wedell N, 1998. Decoupling of
reproductive rates and parental expenditure in a polyandrous butterfly.
Behav Ecol 9:
20-25.
Zeh JA, Zeh DW, 1997. The evolution of polyandry. I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263: 1711-1717.
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