Behavioral Ecology Vol. 13 No. 5: 690-695
© 2002 International Society for Behavioral Ecology
Siblicide and life-history evolution in parasitoids
Department of Biology, University of York, PO Box 373, York YO10 5YW, UK
Address correspondence to J.J. Pexton. E-mail: jjp100{at}york.ac.uk.
Received 24 September 2001; revised 30 January 2002; accepted 12 February 2002.
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ABSTRACT |
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Parasitoid wasps exhibit a stark dichotomy in larval behavior and developmental mode. In gregarious species, siblings developing together tolerate each other; hence more than one individual can successfully complete development. In contrast, solitary species have intolerant larvae that will engage in siblicide, leading to only one individual successfully completing development. Previous theoretical and empirical work has suggested that females from species with intolerant larvae should reduce their relative investment in reproduction. We tested this prediction by measuring investment in survival and reproduction in a pair of sister species from the genus Aphaereta (Hymenoptera: Braconidae). With increasing body size, divergent patterns of investment exist in the two species. Females of the solitary A. genevensis allocate additional resources almost exclusively toward greater fat reserves, resulting in enhanced longevity. Females of the gregarious A. pallipes invest relatively more in reproduction and hence have lower fat reserves, reduced longevity, and greater egg loads than A. genevensis. These differences reflect a trend toward greater investment in survival relative to reproduction in the solitary species, as predicted. We discuss the implications of these findings for the development of sibling rivalry and life-history theory.
Key words: Alysiinae, Callosobruchus, fecundity, optimal investment, parasitoids, resource allocation, trade-offs.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The behavior of siblings toward each other, and the effects on parents, is a topic of enduring interest for evolutionary biologists (Cheplick, 1992
;
Elgar and Crespi, 1992;
Mock and Parker, 1997). The
behavior of family members toward each other may include conflict between
offspring (Mock and Parker,
1997) and conflict between parents and offspring
(Godfray, 1995;
Trivers, 1974). Previously the
main challenge has been to determine the conditions that facilitate either
cooperation or conflict between relatives. In this article, our focus is on
the consequences of parent—offspring conflict and sibling rivalry on the
evolution of life-history traits.
Parasitoids are insects that develop by feeding on the bodies of other
arthropods. The completion of feeding inevitably kills the host. The adult
parasitoid is free-living, and the main task of females is finding new hosts
for the next generation (Godfray,
1994; Quicke,
1997).
Parasitoids are classic examples of nursery species, in which siblings are
required to share a limited space and set of resources. Sibling rivalry and
parent—offspring conflict is particularly acute in many species of
parasitoids. Parasitoids can be solitary, with only one larva developing
successfully from an individual host, or they can be gregarious if several
individuals successfully develop together
(Mayhew et al., 1998). The
majority of parasitoids develop solitarily, although gregarious development is
taxonomically widespread and is probably the derived state
(Mayhew, 1998). The larvae of
solitary species engage in lethal fighting or physiological suppression until
only one individual remains to consume the host
(Godfray, 1994;
Salt, 1961). This behavior has
been described as "ultrasiblicide"
(Mock and Parker, 1997). The
siblicidal behavior of developing wasps is an extreme example of
parent—offspring conflict over clutch size and implicitly the level of
parental investment received, with the offspring determining the outcome. In
this article, we examine the life-history consequences of siblicide that feed
back to adult parasitoids. Predictions come from both general life-history
theory and from more specific work on parasitoids, which we review briefly
below.
The general theoretical framework and empirical evidence suggest that
sibling rivalry should have direct consequences on the allocation of resources
to survival and reproduction in adults. Optimal investment models (e.g.,
Roff, 1992;
Smith, 1991;
Stearns, 1992;
Young, 1990) predict that
reduced instantaneous investment in reproduction and greater investment in
survival will be favored by any factor that increases the value of adults over
juveniles. These factors include increases in the mean and variance in
juvenile mortality, which devalues reproduction relative to adult survival.
Siblicide is a cause of juvenile mortality, and so should select for greater
investment in survival (Smith,
1991).
Comparisons between populations and species of bruchid beetles from the
genus Callosobruchus are consistent with the above prediction. As in
parasitoids, juveniles of these beetles share a limiting resource during
development (a seed), and populations differ in their larval behavior with
tolerant and intolerant larvae, giving rise to scramble and contest
competition, respectively. Species with fighting larvae may suffer high
juvenile mortality relative to those with tolerant larvae. Beetles with
tolerant larvae also have higher numbers of eggs on eclosion and reduced
longevity compared to strains and species with contest competition
(Giga and Smith, 1983;
Thanthianga and Mitchell,
1990; Smith,
1991).
Research on investment in survival and reproduction in parasitoids has
focused on the effects of internal (physiological) state or of habitat
characteristics, such as the distribution and abundance of hosts (see
Ellers et al., 2000, and
references therein), and the likelihood of host survival during the
development of juveniles (Price,
1974).
Price's (1974) balanced
mortality hypothesis is a potential framework for understanding patterns of
investment in reproduction and survival observed in parasitoids. It is based
on the empirical observation that potential fecundity in some parasitoid
assemblages is positively correlated with host abundance and the risk of
extrinsic environmental mortality for hosts (see
Price, 1974:
Figure 1). Parasitoid species
attacking hosts during an early life-stage (when the host is abundant, but it
experiences low survivorship rates) compensate for the resultant high level of
juvenile mortality by producing more eggs and attacking more hosts. In
contrast, those species attacking hosts at a later life-stage have reduced
potential fecundity. The balance thus is shifted away from investment in
reproduction when juvenile mortality is low. However, Price's hypothesis is
not directly supported by explicit theory and gives predictions in relation to
juvenile mortality that are at odds with general life-history models (see
above). An alternative interpretation of the data, which is not at odds with
theory, is that it is not juvenile mortality but host density that controls
investment in this case and that would select for increasing adult survival
when hosts are old but rare (see below). We return to these two alternative
selection pressures in the Discussion.
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Recent parasitoid models, and some empirical data, do in fact suggest that
increasing host-patch density and quality will favor investment in
reproduction rather than survival (Ellers
et al., 2000). Studies of the alysiine parasitoid Asobara
tabida have compared populations from different geographic locations.
Those from northern Europe allocate relatively more resources toward survival
than those from southern Europe, as predicted from the properties of the
habitats in those two regions (Ellers and
van Alphen, 1997). In this article we provide a similar but
contrasting study, comparing two sister species taken from the same geographic
location. Differences in allocation cannot then be due to geographical
characteristics and instead represent different intrinsic properties of the
species. We use these species to assess for the first time relative
instantaneous investment in reproduction and survival as a likely function of
parent—offspring conflict in parasitoids.
Our study species, the sister species Aphaereta genevensis and
Aphaereta pallipes (Hymenoptera: Braconidae: Alysiinae) are close
relatives of A. tabida and are extremely similar to each other: They
can both use the same host species, are almost indistinguishable
morphologically, and have similar developmental periods and trajectories. The
species both use hosts (such as Drosophila spp.) which congregate on
discrete, empheral patches such as rotten fruit. These patches represent not
only a set of reproductive opportunities but the substrate also represents a
potential source of food for adults. During dispersal females must in all
likelihood survive periods without food and use energy in flight. A.
genevensis larvae display siblicidal behavior and develop solitarily,
whereas the larvae of A. pallipes are tolerant of each other and
develop gregariously (Mayhew and van
Alphen, 1999). Here we test the hypothesis that the two species
also have contrasting strategies with respect to relative investment in
survival and reproduction at adult eclosion that reflect the difference in the
resolution of parent—offspring conflict. We predict that the solitary
species invests relatively more resources to survival, as predicted by
ecological theory (see Roff,
1992; Smith, 1991;
Stearns, 1992;
Young, 1990).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Cultures
We used laboratory populations of A. genevensis and A. pallipes in this study. The cultures were collected in New York state, USA, during 1995 and 1996, in a region where the species are sympatric (see Mayhew and van Alphen, 1999
).
Since 1997, both species have been reared on Drosophila virilis. The
hosts were reared in glass bottles on standard yeast-based medium. Wasps were
reared in 5-cm diam glass jars with foam stoppers. A 2-cm layer of nutrient
agar was poured into the base of a jar and allowed to set. Several 5- to
8-day-old D. virilis larvae were added along with a dab of viscous
yeast medium. Groups of mated females (2-5 females) with no prior experience
of hosts were introduced to the jars and left until death. We placed jars in
secure plastic boxes to ensure that both species were kept separate within a
single culturing room. The cultures were maintained at 20°C under constant
light and ambient humidity. All experiments described in this study were also
performed under these environmental conditions. All experiments and
observations were performed simultaneously with respect to both species over
the course of the year 2000.
Longevity experiments
To test our hypothesis of differential survival in these species, we
observed female longevity in both species with and without food (representing
survival in favorable and unfavorable conditions). Pupae containing developing
wasps were gently washed out from culture jars with lukewarm water and placed
into specimen tubes to ensure no feeding before experimental treatments. We
checked these rearing tubes every 24 h for newly emerged females.
Upon emergence, females of both species were randomly assigned to one of two treatments: with food or without food. Females were individually placed into 75 x 25 mm specimen tubes. Tubes in the feeding treatment contained a cotton-wool ball moistened with a 35% sucrose solution. Tubes in the control (nonfeeding) treatment contained a cotton-wool ball moistened with distilled water. We checked tubes every 24 h and recorded longevity for each female. The food or water resources were refreshed every 1-2 days, as needed, to ensure a constant supply of sugar solution or water. Upon death, we recorded hind tibia length. Specimens were then dried continuously at 70°C for 4 days and weighed.
Fat reserves upon emergence
We investigated the likely mechanistic basis for any differences in
longevity between the species by quantifying investment in survival as
measured by fat reserves upon eclosion. Pupae containing developing wasps were
placed into rearing tubes as in the longevity experiment, except that a
cotton-wool ball moistened with 35% sucrose solution was placed in the rearing
tube to ensure no decrease in fat reserves due to starvation. Previous work in
the closely related species A. tabida has shown that feeding on sugar
does not increase fat reserves but can significantly slow their rate of
decrease (Ellers, 1996). We
checked the tubes every hour during the working day and immediately upon the
start of the next working day. This ensured that the oldest wasps were at most
only 12 h old. Females were killed upon emergence by placement in a freezer at
-20°C. We measured hind tibia length after death had occurred.
We measured fat content using ether extraction. Specimens were dried at 70°C for 4 days and then weighed. Whole females were placed into sealed vials with 3 ml of diethyl ether [(C2H5)2O, water content < 0.001%] and left in a fume cupboard. After 24 h the ether was removed and replaced with 3 ml of fresh ether. This was repeated for 3 days, after which specimens were dried again for 4 days at 70°C and weighed. We calculated the size of the fat reserves by subtracting the dry weight after ether extraction from the dry weight before ether extraction.
Egg number and size upon emergence
Pupae were placed into rearing tubes as above and killed in the same manner
upon emergence. After hind tibia length had been recorded, we carefully
dissected the eggs out from females placed into a drop of Ringer's solution on
a glass slide under a light microscope. A coverslip was placed over the
droplet, and eggs were then counted using a compound microscope (480x
magnification). We measured the maximum length and width of the first five
individual eggs found using an eyepiece graticule. Because egg width showed
little observable variation (the eggs are elongated), we used the mean egg
length as a measure of egg size.
Statistical analysis
We analyzed the longevity results by fitting a Weibull distribution to the
data in the GLIM statistical package. The Weibull distribution is
two-parameter model with the exponential as a special case. The two parameters
are 
and 
, the shape of the hazard function and the rate
parameter, respectively. If = 1 (the exponential distribution), then
the hazard (risk of death) is constant. If > 1, the hazard
increases with age, and for < 1 the hazard declines with age. The
rate parameter is a linear combination of explanatory variables
(Crawley, 1993). In the case of
a Weibull distribution, a chi-square approximation is used to assess whether
the removal of variables from the model significantly increases the deviance.
We analyzed the fat reserve data and the egg load/egg size data using standard
techniques within SPSS.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Longevity
Average (± SE) female life span from eclosion in A. genevensis was 16.94 ± 1.12 days (n = 36) with food and 12.5 ± 0.88 days (n = 36) without food. In A. pallipes average female life span from eclosion was 16.64 ± 1.06 days (n = 33) with food and 5.8 ± 0.43 days (n = 40) without food. In addition, dry weight upon death was reduced in both feeding treatments compared to the dry weights of newly emergent females (ANOVA; A. genevensis, F2,103 = 49.54, p < .001; A. pallipes, F2,107 = 34.03, p < .001). Post-host tests (Student-Newman-Keuls) indicated that dry weight in all three groups (feeding, non-feeding, and newly emerged females) were significantly different from each other within both species (p < 0.05 in all comparisons), a trend consistent with previous findings in Asobara tabida that feeding reduced the rate of fat loss (Ellers, 1996
). This is a
problem because it means that dry weight upon death does not accurately
reflect size at emergence, which is the most objective way to estimate total
resources available to wasps that have just completed development. Regressions
were therefore performed to calculate what the dry weights of females of both
species in the longevity treatments would have been if those individuals had
been newly emergent (A. genevensis: dry weight [mg] = 0.853 x
hind tibia [mm] - 0.445, R2 = .77; A. pallipes:
dry weight [mg] = 0.563 x hind tibia [mm] - 0.258,
R2 = .86). These calculated dry weight measurements
("size" in the GLIM analysis) allowed for genuine comparisons of
the influence of dry weight on longevity.
Using the Weibull distribution was justified in all the models because it
significantly improved each of the model's explanatory power. The shape
parameter was > 1 for all models, indicating that the risk of death
increased over time (Figure 1).
Fed wasps lived significantly longer than unfed wasps in both species (A.
genevensis, 
12 = 10.63, p < .01;
A. pallipes, 12 = 69.38, p <
.001). Size also significantly increased longevity in both species
(Figure 2; A.
genevensis, 12 = 38.6, p < .001;
A. pallipes, 12 = 8.91, p <
.005). In the no-food treatment, there was a significant interaction between
species and size, indicating that longevity (under unfavorable conditions) in
the two species responded differently to increases in size, with A.
genevensis living longer than A. pallipes of the same size
(Figure 2;
12 = 6.92, p < .01).
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Fat reserves upon emergence
Fat reserves increased with total dry weight upon emergence
(F1,68 = 635.77, p < .001), and there was a
significant interaction between dry weight and species, with A.
genevensis having more fat for a given body size than A.
pallipes. The difference increased at larger body sizes
(Figure 3;
F1,68 = 48.23, p < .001).
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Egg number and egg size upon emergence
Egg number (upon eclosion) increased with size (F1,56 =
107.86, p < .001), and there was a significant interaction between
size and species, indicating that the rate of increase in egg number (upon
eclosion) with size differed between species, with A. pallipes having
more eggs than A. genevensis of the same size, the difference being
greatest at large body sizes (Figure
4; F1,56 = 71.31, p < .001). Egg
size increased with body size (F1,56 = 84.11, p
< .001), but there was no significant effect of species on egg size and no
significant interaction of body size and species (F1,56 =
2.98, 1.68, respectively). Egg size was positively associated with egg number
across all individuals (F1,56 = 13.12, p <
.01). There was no evidence for a negative egg size/egg number trade-off in
either species.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The primary finding of this study is that female A. genevensis and A. pallipes exhibit contrasting investment patterns in survival and reproduction at adult eclosion, as would be expected from life-history theory. Small-bodied individuals of both species display similar allocation. With increasing body size, the solitary A. genevensis invests relatively more in fat and relatively less in eggs than the gregarious A. pallipes. Upon emergence A. pallipes has consistently more eggs and has much less fat than A. genevensis. These differences in fat are reflected in differences in longevity; in the absence of food A. pallipes live for only a few days, whereas A. genevensis live for a much longer period. Thus, A. genevensis invests considerably more resources at eclosion in survival relative to reproduction compared to its sister species A. pallipes, as predicted by theory.
In this study, we used a pair of sister species to test the prediction that
solitary species should allocate more resources to survival than gregarious
species. Our data are consistent with this hypothesis and contribute to
previous comparative evidence in bruchid beetles
(Smith, 1991), demonstrating
that sibling rivalry and lethal fighting between developing larvae are
associated with increased allocation to survival. In comparative terms, our
data represent a single independent contrast
(Harvey and Pagel, 1991) and
cannot alone confirm or reject the hypothesis, but together with other studies
on similar systems will eventually make possible a broader test. Thus, our
study should be viewed as one step toward this longterm strategic goal. As
with most comparative studies, we can say nothing firm about the actual causes
of the differences we observe in a single comparison. However, we speculate
below on exactly which intrinsic properties may have been influential.
Causes of differences in investment
In previous work on bruchid beetles, differences in allocation between
populations were attributed to differences in juvenile mortality caused by
different types of larval competition
(Smith, 1991). In the present
study, differences in juvenile mortality may also play a direct role, but we
urge caution. One reason for caution is that the extent of juvenile mortality
is also determined by clutch size. In solitary species, small clutches are
generally laid that minimize wastage of investment in offspring that
inevitably fail to complete development
(Mayhew and Glaizot, 2001;
Skinner, 1985;
Waage and Godfray, 1985).
A. genevensis generally lays only one egg per clutch, and in fact
only suffers higher juvenile mortality than A. pallipes when several
females oviposit in the same host (superparasitism) or if a single female lays
a multiple clutch (Mayhew and van Alphen,
1999). The extent of superparasitism in the field is currently
unknown. It is at least possible that juvenile mortality does not directly
contribute to the present observations. However, the reduction in clutch size
seen in solitary parasitoids will be to a large extent a consequence of
parent—offspring conflict; therefore the possibility of juvenile
mortality indirectly influences the differences in allocation. We mention here
two other possible differences between the species that might be responsible
for the differences in allocation to reproduction and survival. These
differences may have evolved in response to differences in larval
behavior.
The first such factor is clutch size. The effect of clutch size on the
degree of investment in reproduction and survival across parasitoid
populations has not, to our knowledge, been investigated theoretically, but
intuitively we would expect larger clutch sizes to result in reduced
allocation to survival. Previous parasitoid investment theory has shown that
increasing patch quality selects for reduced investment in survival
(Ellers et al., 2000).
Producing many offspring per host is equivalent, in some respects, to
experiencing greater patch quality because more offspring can be produced
within a patch. Hence, we expect increasing clutch size to lead to increased
allocation to reproduction at the expense of survival.
The second possible factor may be the degree of host specialization.
Allocation models in parasitoids have suggested that as host availability
increases, species should invest more in reproduction and less in survival.
Hence, our results might be explained if A. pallipes is more
generalist and thus experiences an environment rich in reproductive
opportunities. Anecdotal evidence suggests that this is indeed the case.
Little is known about the range of host species of A. genevensis.
However, 20 different species of North American Diptera have been recorded as
being parasitized by A. pallipes
(Whistlecraft et al., 1984),
which for an alysiine is a relatively large range of host species
(Wharton, 1984). Large numbers
of host species may also be a general feature of gregarious alysiines
(Shaw and Huddleston, 1991).
Decreased oviposition specificity is also found in bruchid beetles with
tolerant larvae (Smith,
1991).
The reasons for the apparent decrease in host specialization in gregarious
species have not been addressed in earnest. We suggest two potential reasons
for decrease in host specialization. First, systematically laying large
clutches of eggs may make previously unsuitable hosts suitable, perhaps by
overwhelming a host's immune response or allowing larger-bodied hosts to be
fully consumed, examples of Allee effects. Effects of this type have been
reported in parasitoids (Ode and
Rosenheim, 1998; Streams,
1971). Second, reduced oviposition selectivity is predicted if
expected life span is short (e.g., Fletcher
et al., 1994; Mangel and
Clark, 1988; Roitberg et al.,
1992,
1993;
Sirot et al., 1997). If true
for this system, the degree of oviposition-site selectivity and investment in
survival and reproduction may feed back positively on each other, enhancing
the difference in allocation.
Conclusions
Finally, we consider briefly the wider implications of our data. The fact
that A. genevensis invests relatively more in fat reserves (resulting
in enhanced survival) suggests that it hardly ever runs out of eggs and hence
that it is severely time limited. In contrast, A. pallipes invests in
both time and eggs; hence, given extra life span, it is more likely to run out
of eggs (egg limited). Though the idea requires more specific testing, we
suggest that intraspecific allometric variation in investment strategy may
indicate whether a species is relatively time or egg limited.
The present, although still somewhat limited, picture of insects with a parasitoid-like life history is one in which the degree of sibling rivalry is correlated with, and has likely affected, several other traits. Some of these traits are expected to feed back on each other, enhancing the observable variation. This raises the possibility that in other systems where siblicide has evolved, such as many birds, carnivores, and ovipositing invertebrates, siblicide may account for a large fraction of the variation in life-history parameters. Such systems would seem ripe for investigation of this type.
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ACKNOWLEDGEMENTS |
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J.J.P. was supported by Natural Environment Research Council studentship GT 04/99/TS/300. We thank Pete Chabora for providing the original wasp and fly cultures, Leo Beukeboom and Gé Boskamp for keeping cultures alive while P.J.M. was in transit, and Jacintha Ellers and Lex Kraaijeveld for advising on ether extraction protocols. We also thank Nick Colegrave, Jacintha Ellers, Charles Godfray, Jay Rosenheim, and two anonymous referees for their thoughtful comments on previous versions of the manuscript.
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