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Behavioral Ecology Vol. 13 No. 6: 742-749
© 2002 International Society for Behavioral Ecology
Phenotypic selection and function of reproductive behavior in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae)
Laboratory of Applied Zoology, Faculty of Agriculture, Hokkaido University, Sapporo, 060-8589 and Department of Biology, Naruto University of Education, Naruto, Tokushima, 772-8502 Japan
Address correspondence to S. Kudo, Naruto University of Education, Naruto, Tokushima, 772-8502 Japan. E-mail: skudo{at}naruto-u.ac.jp.
Received 25 July 2001; revised 25 January 2002; accepted 12 February 2002.
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ABSTRACT |
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To investigate the function of maternal care and determinants of reproductive success in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae), I used two different approaches, the measurement of phenotypic selection and female-removal experiments under conditions differing in biotic-environmental pressure. For two field populations, unattended eggs and younger nymphs consistently suffered severe predation pressure and attendance by parent females greatly enhanced their survival. In contrast, under enemy-excluded conditions, offspring performance was not reduced in broods without parent females, indicating that maternal care functions as a physical defense against predators. However, the determinant of female reproductive success in E. putoni in the field was not the care behavior alone. Selection gradient analysis showed that early season oviposition and larger clutch size, as well as a longer duration of care by a female, was favored during the breeding episode. This study is the first to evaluate phenotypic selection on parental care and other reproductive traits in arthropods.
Key words: Elasmucha, Heteroptera, parental care, phenotypic selection, reproductive success, subsociality.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Theories of life-history evolution and parental investment, including post-ovipositional parental care, generally assume that increased investment in current offspring provides fitness benefits to the offspring but also imposes costs in future survival and/or reproduction of the parent (e.g., Clutton-Brock, 1991
;
Roff, 1992;
Stearns, 1992). Optimal
parental care strategies have been considered to be designed to maximize
fitness gain of the parent under such reproductive trade-offs
(Grafen and Sibly, 1978;
Lazarus, 1990;
Maynard Smith, 1977;
Winkler, 1987;
Yamamura and Tsuji, 1993).
Parental care of eggs or young is not common among arthropods but has
evolved repeatedly in different lineages and resulted in current diverse forms
(Choe and Crespi, 1997;
Zeh and Smith, 1985). For a
variety of arthropod taxa, there has been an increasing number of empirical
studies that evaluate costs and benefits of parental care by different
research methods (reviewed in Tallamy and
Wood, 1986; Trumbo,
1996).
To quantify costs and benefits of parental behavior in arthropods,
experiments in which treatment groups with different investment in care
behavior are established by removing the parent from the offspring have
usually been employed (for benefits, see, e.g.,
Diesel, 1989;
Kudo et al., 1995;
Filippi-Tsukamoto et al.,
1995; Tallamy and Denno,
1981a; for costs, see, e.g.,
Fink, 1986;
Nalepa, 1988;
Tallamy and Denno, 1982). Such
an experimental approach provides quantitative evidence for the contribution
of care behavior to reproductive success of the parent, but it is not enough
to understand the determinants of reproductive success because reproductive
traits other than care behavior, such as clutch size, oviposition site
selection, and oviposition schedule, can also affect reproductive success.
Moreover, reproductive traits, including care behavior, are often correlated
with each other, and natural selection acts on individual phenotype through
the net effects of these traits. There have been only a few studies that
clarify how parental care behavior varies with other traits and affects
reproductive success of the parent in the field (e.g.,
Scott and Traniello, 1990).
Selection gradient analysis is a powerful tool to quantify phenotypic
selection on such correlated traits (Arnold
and Wade, 1984; Lande and
Arnold, 1983; reviewed in
Brodie et al., 1995). However,
to the best of my knowledge, there has been no attempt to apply this method to
understanding natural selection on reproductive traits of subsocial
arthropods. Such a regression analysis approach and an experimental approach
complement each other in the study of phenotypic evolution
(Mitchell-Olds and Shaw, 1987;
Wade and Kalisz, 1990): The
former will identify target traits and modes of selection in the study
population, and the latter will clarify the agent and the mechanism of the
detected selection on a particular trait.
Elasmucha bugs are well-known subsocial insects, and their
reproductive history and maternal care vary considerably among species (e.g.,
Kaitala and Mappes, 1997).
Elasmucha putoni Scott has two generations per year, each of which
depends on different host plants, and overwintered females breed on
fruit-bearing wild mulberry, Morus bombycis Koizumi
(Kudo, 1994). E.
putoni is semelparous in the field. Females lay single egg masses on the
underside of host leaves usually in early June. First-instar nymphs remain in
tight aggregations on natal leaves, and second- or later instar nymphs move
among the shoots to feed on fruit, maintaining their aggregations. The nymphal
feeding aggregations become smaller as the instars progress, and final (fifth)
instar nymphs often feed solitarily. Females attend their eggs and nymphs
until as late as the third instar on wild mulberry in the field
(Honbo and Nakamura, 1985;
Kudo, 1996). Honbo and
Nakamura (1985) have shown
that in an E. putoni population of central Japan, eggs suffer high
predation when the parent female is removed. However, the function of maternal
behavior has not been well studied. Moreover, potential environmental pressure
against offspring can vary temporally and spatially (e.g.,
Jeanne, 1979). Costs and
benefits of maternal care may also vary according to variation in selection
pressure among different populations.
In this study, I sought to clarify ecological and behavioral factors determining reproductive success of females on wild mulberry in E. putoni populations of northern Japan, using both experimental and regression analysis approaches.
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MATERIALS AND METHODS |
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Measurement of phenotypic selection
Data collection
I carried out field investigations from mid-May to July in 1991 using an E. putoni population of Misumai located in Sapporo, Hokkaido, northern Japan (42°57' N, 141°15' E). I censused branches of seven wild mulberry trees, which had been marked with colored tapes, and when first found, I marked individual females guarding eggs with quick-drying paint for later discrimination. At the first census on 21 May, no E. putoni adults were found on the wild mulberry. Copulating pairs were found first on 25 May, and the first oviposition occurred on 30 May. In total, 57 females with offspring were found and monitored every day or two until the collection of their families (see below).
I measured and recorded the following traits for each of the 57 females:
clutch size, duration of care (see below), the date when oviposition occurred
(30 May = 1), length of the oviposition leaf, relative position of the
oviposition leaf on a shoot (order of the leaf from the apex/no. leaves per
shoot; 1 = most basal position), number of leaves on the shoot with the
clutch, number of fruits on the shoot with the clutch, and the minimum
distance from the ground to the oviposition leaf along the tree surface. The
latter five traits are characters of oviposition-site selection by females.
The last trait, distance from the ground to the oviposition leaf, might
correlate significantly with ant predation because ants have often been
reported to be important predators of the offspring of Elasmucha bugs
(Kudo et al., 1989;
Mappes and Kaitala, 1995;
Melber et al., 1980). I
examined clutch size by removing the female temporarily from the clutch. This
female removal did not affect subsequent female behavior.
Two days after the time when broods molted into the second instar, I collected all of the broods and parent females, which were usually found on or near the natal shoot, and counted the number of surviving nymphs. It was difficult or impossible to identify the broods after that time: The later instar broods move away from natal sites and often split into different groups (or join again in other groups) through development. Thus, data on care duration did not cover its full range in the field, which sometimes extends to the third instar. The number of surviving nymphs in a brood was regarded as reproductive success for each parent female and was used in the selection analyses as a measure of fitness (see below). I measured the prothroax width of the collected females under a stereomicroscope using an ocular micrometer. Some females had left their broods before the collection and were subsequently caught when found solitary on wild mulberry trees. However, most of them had disappeared from the trees and were not discovered later. Their body size data are missing. Therefore, body size was not included in the following selection analyses.
Estimation of selection coefficients
I used multivariate statistical techniques for quantifying natural
selection acting on reproductive traits in a current population of E.
putoni (Lande and Arnold,
1983; Mitchell-Olds and Shaw,
1987; reviewed in Brodie et
al., 1995). Individual measures of fitness (reproductive success)
were converted to relative fitness with a mean value of 1 within a population.
Some trait variables were log- or square-root—transformed, and then all
of the variables were standardized to a mean zero and unit variance. Thus,
selection coefficients presented here are standardized selection coefficients.
The opportunity for selection, the upper limit of the strength of selection,
was calculated as the variance in relative fitness. I calculated linear
selection differentials, which describe changes in trait means, as the
covariance of trait values with relative fitness
(Lande and Arnold, 1983).
Significance tests of the differentials were made with Spearman's rank
correlation (Lande and Arnold,
1983). I estimated linear selection gradients, which describe
direct effects of a given trait on fitness adjusting for indirect effects of
other correlated traits, as the partial regression co-efficients in a linear
multiple regression model of relative fitness on all traits
(Lande and Arnold, 1983). In
multivariate regression, multicollinearity can lead to inflation of the
standard errors of the regression coefficients, thus reducing the power of the
analysis (Mitchell-Olds and Shaw,
1987). To assess the impact of multicollinearity on the results, I
examined the variance inflation factors for trait variables in the regression
model (Chatterjee and Price,
1977). The variance inflation factors for the linear selection
gradients were not high (1.2-1.6), indicating that the multicollinearity was
not problematic in the analysis. Residuals of relative fitness in the model
were approximately normally distributed (Kolmogorov-Smirnov one-sample test,
z = 1.33, p = .06).
Microenvironmental heterogeneity among host trees might affect reproductive
behavior of E. putoni, as suggested in E. grisea
(Mappes and Kaitala, 1995).
There was no significant difference in female reproductive success among seven
wild mulberry trees on which oviposition occurred (F6,50 =
0.67, p = .67). Trait variables, however, differed among the trees
(MANOVA: Pillai's trace = 1.71, F42,294 = 2.78, p
< .0001). To examine effects of the trees on female reproductive success, I
included those as dummy variables in the regression model
(Chatterjee and Price, 1977).
The effects of trees were not significant and thus were excluded from the
final model.
To detect nonlinear and correlational selection acting on trait variances and covariances, large sample size is ordinarily needed. In the preliminary analysis, neither quadratic nor correlational (cross-product) terms were significant in the full quadratic regression model (quadratic, F8,12 = 2.15, p = .11; cross-product, F28,12 = 1.26, p = .35). Moreover, as mentioned above, the present data do not completely cover the breeding episode of females, and this may cause underestimates of the nonlinear selection (see also the Discussion). Therefore, I omitted the detailed analysis.
Female-removal experiments
Under field conditions
I carried out field experiments at Nopporo (43°02' N,
141°30' E) in 1987 and at Misumai in 1990 and 1991. In early June, I
removed mothers from clutches randomly chosen on wild mulberry trees (the
female-removal group). Other females guarding clutches were kept intact as the
control group. I examined clutch size by temporarily removing the female from
the clutch. There were no significant differences in initial clutch size
between the female-removal and control groups in any of the experiments
conducted in the Nopporo (female-removal, n = 15, mean ± SD =
48.38 ± 4.91, control, n = 23, 46.33 ± 3.32;
t36 = -0.524, p = .60) and Misumai populations
(in 1990, n = 16, 48.38 ± 4.91, n = 25, 46.33
± 3.32; t39 = -0.294, p = .77; in 1991,
n = 18, 48.38 ± 4.91, n = 25, 46.33 ± 3.32;
t41 = -0.439, p = .66). I monitored the clutches
in the two experimental groups at 1-3 day intervals. Enemies attacking
clutches (or females) were identified.
When the oldest brood had molted into the second instar, I collected all of the experimental broods in 1987 in Nopporo and 1991 in Misumai. In 1990 in Misumai, broods were collected just before hatching. I compared the survival of offspring between the female-removal and the control groups.
Under enemy-excluded conditions
I conducted experiments using wild mulberry trees in the seri-cultural farm
of the Hokkaido University in 1990. Nineteen branches with many shoots bearing
fruit were selected and enclosed by cylindrical nylon nets (ca. 100 cm long,
40 cm diam). These enclosures contained a large amount of fruit to allow bugs
to complete development. I introduced a copulating pair which had been
collected from the Misumai population to each of the experimental branches.
Other arthropods were removed from the experimental branches before the
introduction of E. putoni pairs. I checked each branch daily to
confirm ovipositions. When an oviposition occurred, I measured clutch size by
temporarily removing the female from the clutch. Males were also removed from
the branch at this time.
The day after oviposition I removed the females from six randomly chosen clutches (the female-removal group). The other 13 females guarding clutches were kept intact as the control group. There was no significant difference in initial clutch size between the two groups (control, mean ± SD = 48.38 ± 4.91, female-removal, 46.33 ± 3.32; t17 = 0.69, p = .50). Conducting frequent censuses that involve opening the nylon-net enclosures could disturb females attending nymphs on shoots. Thus, I checked experimental branches only once or twice a week.
I compared the survival and the size of offspring (prothorax width) between the female-removal and the control groups when they had grown into adults. The development rate of offspring was not compared because oviposition did not occur simultaneously among females.
Statistics
Statistical analyses were performed with StatView 5.0
(SAS Institute, 1998), JMP 3.1
(SAS Institute, 1995), and SAS
program software (SAS Institute,
1990). I used a sequential Bonferroni correction
(Rice, 1989) to evaluate the
table-wide significance.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Variation of reproductive traits and phenotypic selection
A summary of the traits measured and phenotypic correlations among them (female body size excluded) are shown in Tables 1 and 2. As previously reported for this population in a different year and for another population (Kudo, 2001
), there was a
positive correlation between female body size and clutch size
(rs = .505, n = 45, p = .0008) in the
sample collected. No other significant correlations with body size were
detected (see also Materials and Methods).
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The mean reproductive success for 57 females, as measured by the number of surviving nymphs, was 36.88 ± 14.62 (SD), and the opportunity for selection was 0.157. Selection differentials for clutch size and care duration showed significant positive values (Table 3). Overall, females producing larger clutches and those taking care of offspring longer were favored during the breeding episode. The regression model was highly significant, and trait variables explained about 65% of the variance in female reproductive success (Table 3). Significant directional selection for clutch size, care duration, and oviposition date (positive values for the former two and a negative value for the latter) were detected. I conclude that earlier and larger clutch production with longer care by the female was selected directly during the breeding episode in the Misumai population.
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Experiments under field conditions
The survival of offspring decreased rapidly in the female-removal group in
the Nopporo population (Figure
1C). This was also the case for the Misumai population in
different years (Figure 1A, B). In all of the three experiments, there were significant differences in
offspring survival between the female-removal group and the control group
(Mann-Whitney U test: Nopporo, z corrected for ties = -4.01,
p < .0001; Misumai in 1990, z = -4.21, p <
.0001; in 1991, z = -5.13, p < .0001). Eggs and young
nymphs in the female-removal group were attacked by a variety of arthropod
enemies (Table 4).
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Some females in the control group (4 of 23 females in Nopporo, 2 of 25 in Misumai in 1990, 6 of 25 in 1991) had disappeared before the brood molted into the second instar. The reason for these disappearances was usually unknown, but four females were confirmed to be killed by spiders (by direct observations), indicating that even brooding females were not always free from predation. Excluding those orphaned broods from analysis, mean survival of offspring during experiments was high in all of the three control groups (Nopporo, mean ± SD = 87.16 ± 13.79%; Misumai in 1990, 98.55 ± 1.80%; in 1991, 86.12 ± 12.35%).
To investigate the effect of clutch-size on predation rate, I performed regressions of offspring survivorship on clutch size (data were arcsine square-root transformed before analysis). No significant relationships were detected in any of the experimental groups in the two populations (female-removal: Nopporo, r2 = .023, F1,13 = 0.30, p = .59; Misumai in 1990, r2 = .018, F1,14 = 0.26, p = .62; in 1991, r2 = .043, F1,16 = 0.71, p = .41; control: Nopporo, r2 = .001, F1,21 = 0.03, p = .87; Misumai in 1990, r2 = .022, F1,23 = 0.52, p = .48; in 1991, r2 = .035, F1,23 = 0.84, p = .37).
Experiments under enemy-excluded conditions
All of the 13 females in the control group continued to attend their nymphs
when they left natal leaves to feed on fruit. There were no significant
differences in bug density in enclosures between the female-removal and the
control groups (female removal, mean ± SD = 40.17 ± 9.62;
control, 38.15 ± 9.10; t test, t17 =
-0.44, p = .67), and thus crowding effects can be ignored. No
significant difference in offspring survival, measured as the proportion of
adults eclosing in each clutch, was detected between the female-removal and
the control groups (data were arcsine-root transformed, t test,
t17 = -1.18, p = .25;
Figure 2A). There were also no
significant differences in the body size of emerging adults in both sexes
between the two groups (nested ANOVA with clutch [treatment] as a random
variable: for males, treatment, F1,17.17 = 1.78,
p = .20, clutch, F17,347 = 69.67, p <
.0001; for females, treatment, F1,17.02 = 0.40, p
= .54, clutch, F17,350 = 74.04, p < .0001;
Figure 2B).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Since the comprehensive review of insect sociality by Wilson (1971
), many studies have
revealed that, in a variety of subsocial taxa, ecological factors such as
stress from the physical environment, food availability, competition, and
natural enemies are associated with the evolution of parental care (reviewed
in Eickwort, 1981;
Tallamy and Wood, 1986;
Trumbo, 1996). In hervivorous
insects, the most important factor leading to parental care is predation by
other arthropods (e.g., Kudo et al.,
1992; Nafus and Schreiner,
1988; Tallamy and Denno,
1981b; Windsor,
1987; Wood, 1976).
In subsocial acanthosomatid bugs, offspring are potentially exposed to severe
predation pressure, and parent females provide highly effective defense for
their offspring (Kudo et al.,
1989; Kudo and Nakahira,
1993; Mappes and Kaitala,
1994; Mappes et al.,
1997; Melber and Schmidt,
1975; Melber et al.,
1980).
There are only a few subsocial insects (e.g., Elasmucha grisea;
Mappes and Kaitala, 1994;
Melber and Schmidt, 1975;
Melber et al., 1980) in which
effects of the parental care on offspring survival have been evaluated in
different populations and/or different years, among which environmental
pressures against the offspring might vary. Furthermore, the previous studies
on insect parental care, with a few exceptions (e.g.,
Filippi et al., 2000;
Kudo et al., 1995;
Tallamy and Denno, 1981b),
have not used experiments conducted under enemy-excluded conditions to
evaluate the possible roles of the parent. Such experiments may provide
evidence of functions of parental attendance other than simple protection from
enemies if offspring survival and/or development is reduced in the
experimental group. The present study and that by Honbo and Nakamura
(1985) demonstrate that in
different populations of E. putoni, arthropod predators are
consistently important mortality agents of the offspring and that physical
defense by the parent female is essential to offspring survival.
The results of phenotypic selection analysis suggest that natural selection
is acting on maternal care behavior in the study population: Females that
leave their broods earlier had lower reproductive success. Although there is
no quantitative measurement of potential predation against late instar nymphs,
the defensive effectiveness of females against predators may be high. However,
it should be noted that the present analysis does not completely cover the
breeding episode of females; potential reproductive success of females with
longer care was not considered. E. putoni females usually leave their
broods during the period when the broods are in the second instar on wild
mulberry in the field, and only some of the females attend the third instar
broods (Honbo and Nakamura,
1985; Kudo, 1994,
1996, unpublished data).
E. putoni nymphs depend on host fruits (probably developing seeds)
for food (Kudo, 1994,
unpublished data). They usually maintain aggregations in early instars.
Forming an aggregation may provide benefits such as facilitating feeding for
nymphs, but it may also induce competition between nymphs, particularly in
later instars, for limiting food resources (e.g.,
Godfray, 1987). The optimal
feeding aggregation size for nymphs would change with their growth and
resource conditions. Wild mulberry has shoots bearing a small amount of fruits
(three or four fruits per shoot), and maturing fruits fall off during the
period when E. putoni nymphs are developing on them
(Kudo, 1994, unpublished
data). The fact that nymphal feeding aggregations on wild mulberry become
smaller in later instars and that nymphs cease aggregating if fruits are
experimentally removed from branches on which the nymphs are enclosed
(Kudo, 1994, unpublished data)
suggests growth-dependent competition for fruits among nymphs in aggregations.
But nymphs in aggregations can also have higher survival rates in the presence
of maternal defense. E. putoni females usually settle on the stems of
shoots which harbor nymphs feeding on fruit and face toward the base of the
shoot (Kudo, 1996). This
position and orientation of females attending nymphs is probably effective for
detecting predators approaching the nymphs by walking along the stem. Females
may keep their nymphs in aggregations on single shoots to provide better
physical defense.
As in some other Elasmucha species
(Kaitala and Mappes, 1997;
Kudo et al., 1989). E.
putoni is semelparous in the field, which is mediated by host-plant
phenology. Some females produce second clutches under laboratory conditions
(Kudo, 1994, unpublished
data). However, the experimental reduction of maternal care does not promote
second clutch production in terms of clutch size and recovery period before
oviposition (Kudo, 1994,
unpublished data). There is also no correlation between the first clutch size
and the recovery period. Even when females are removed from eggs and then
reared, they lay second clutches more than 6 weeks after the removal. Nymphs
derived from a second clutch cannot survive in the field because host fruits
become unavailable far before they complete the development
(Kudo, 1994, unpublished
data). In fact, I have found no females that produce the second clutch in the
field. Thus, E. putoni is considered a functionally semelparous
species (sensu Tallamy and Brown,
1999). In such species, females would be free from the cost of
parental care on their future survival and/or reproduction (e.g., Kudo et al.,
1989,
1995; see also
Tallamy and Brown, 1999).
In E. putoni on wild mulberry, the duration of maternal care is probably determined by the balance between fitness benefits and costs to current offspring; the former derived from enhanced survival by the defense against predators and the latter from sib competition in maintained aggregations. The self-defense capabilities of nymphs will increase with development, while competition for host fruit will also increase. It is possible that taking care of nymphs longer imposes costs on females through the reduction of performance of the nymphs, and consequently a stabilizing selection is acting on the duration of maternal care. The detected directional selection on care duration reported here may be a part of such a stabilizing selection. Further studies will be needed to confirm this possibility.
The determinant of female reproductive success in E. putoni was
not parental care behavior alone: Larger initial clutch-size and earlier
oviposition were also favored. If larger investment in egg production in a
single breeding opportunity imposes energetic costs on females (e.g.,
Monaghan et al., 1998),
females producing larger clutches might show shorter periods of care behavior
n. In the data reported here (Table
2), however, such a trade-off was not detected. Even when females
were monitored until they completed care, no correlation was detected between
clutch size and care duration (Kudo,
1994, unpublished data).
The offspring situated on the periphery of the clutch are more vulnerable
than those on the center in Elasmucha bugs as well as in other
subsocial insects in which parent females straddle their clutches to guard
them (e.g., Eberhard, 1975;
Mappes and Kaitala, 1994;
Mappes et al., 1997). Thus,
larger clutch size relative to female body size probably reduces defense
efficiency. Clutch size is positively correlated with female body size in
E. putoni (Kudo,
2001). Although effects of body size of females on their
reproductive success were not evaluated directly in the present analysis, body
size, as well as clutch size, may also be under positive directional
selection.
The mechanisms and agents responsible for selective advantages from early
oviposition are unclear. In phytophagous insects, the timing of oviposition is
often an important determinant for offspring performance through phenological
interactions of the insects and host plants (e.g.,
Keese and Wood, 1991). This
appears to be the case in E. putoni (see above). Wild mulberry trees
leaf in May in northern Japan, and E. putoni females begin
oviposition soon after completion of leaf expansion and flowering
(Kudo, 1994). When the second
instar broods were collected (20-28 June), many of the mulberry fruits were
mature and still remained on the tree. The total amount of mulberry fruit was
almost at the maximum. First-instar nymphs remain on natal leaves and take no
food (Honbo and Nakamura,
1985). Thus, at the time of the collection, the nymphs had fed on
fruit for only 2 days. It is unlikely that, within the observed variation in
the oviposition date, later oviposition had induced keen competition and high
mortality among the second-instar nymphs during the 2 days. Although females
that laid clutches later did not leave offspring earlier
(Table 2), clutches deposited
later suffered higher mortality; there was a significant negative correlation
between survival rates and oviposition date (rs = -.322,
p = .016). In E. putoni, maternal defense is highly
effective but not perfect: Under field conditions up to 20% of offspring were
lost in female-guarded broods at the time of collection. If predation pressure
increases rapidly with the breeding season of E. putoni, this could
explain the advantage of earlier oviposition.
In insects, there are a variety anti-enemy tactics other than parental
defense (e.g., Gross, 1993;
Mappes and Kaitala, 1995).
Heteropterans living in environments in which the offspring suffer high
mortality may adopt alternative reproductive strategies (e.g.,
Tallamy and Denno, 1981a).
Such alternatives may explain the current distribution of parental care in the
Heteroptera (Tallamy and Schaefer, 1996). The quantification of selection on
multiple reproductive traits in related species will promote our understanding
of the evolution and maintenance of the diversified reproductive
strategies.
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ACKNOWLEDGEMENTS |
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I thank S. Makino, M. Ohara, Y. Sakamaki, M. Sato, and K. Sayama for assistance in the field, and F. Ito, J. Ogura, Y. Saito, M. Suwa, and T. Yasunaga for identifying predators. T. Iizuka permitted me to use the sericultural farm. I also thank S. Akimoto, E. Kasuya, and H. Ueno for their suggestions for the analysis and M. E. Carter, A. F. G. Bourke, and two anonymous referees for their helpful comments on the manuscript. This study was supported in part by Grants-in-Aid (nos. 09740581, 11740430, 13440227) for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan.
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