Current Biology 20, 11821186, July 13, 2010 2010 Elsevier Ltd All rights reserved

DOI 10.1016/j.cub.2010.04.057

Report
Altruistic Colony Defense
by Menopausal Female Insects
Keigo Uematsu,1,* Mayako Kutsukake,2 Takema Fukatsu,2
Masakazu Shimada,1 and Harunobu Shibao1
1Department of General Systems Studies, University of Tokyo,
Tokyo 153-8902, Japan
2National Institute of Advanced Industrial Science
and Technology (AIST), Tsukuba 305-8566, Japan

Summary
Recent studies have suggested that an extended postreproductive life span, such as life after menopause in human
females, will evolve when the indirect (kin-selected) fitness
benefits from altruistic behavior are greater than the direct
fitness benefits from continuing reproduction [14]. Under
some conditions in which postreproductive altruism is
more beneficial and/or continuing reproduction is more
costly, the postreproductive life span can be shaped by
natural selection [5, 6]. However, indirect fitness benefits
during postreproductive survival have been documented
mainly in intelligent mammals such as humans and cetaceans, in which elder females possess enhanced social
knowledge through learning [710]. Here we show that postreproductive females of the gall-forming aphid Quadrartus
yoshinomiyai (Nipponaphidini) can gain indirect fitness
benefits through their altruistic colony defense. These
females cease reproduction around the time of gall opening
and defend the colony by sticking themselves to intruding
predators with a waxy secretion that is accumulated in their
body with aging. Our results suggest that the presence of an
age-related trait for altruistic behavior promotes the evolution of postreproductive altruism in this social insect via
kin selection under natural selection imposed by predators.
Results and Discussion
Experimental studies of postreproductive altruism in nonhuman species can be useful to reevaluate the evolutionary
theories of aging and provide a general framework for understanding the evolution of postreproductive life span [11].
However, postreproductive altruism that increases indirect
fitness has not been well documented outside of mammals.
Although a previous study suggested a long postreproductive
life span of poisonous moths for defending conspecifics [12],
there is no evidence that they aggregate in kin groups and
provide benefits exclusively for their kin. A possible reason
for the rarity of postreproductive altruism is the evolutionary
conflict due to genetic heterogeneity within kin groups [3, 13].
We examined gall-forming aphids to study the possibility of
postreproductive altruism in insects. Aphids reproduce via
parthenogenesis, without recombination for most of their life
cycles, giving rise to genetically identical offspring. In addition,
gall formation has been thought to promote the evolution of
sociality in aphids, because the galls provide defense-worthy
food-rich nest sites, facilitate antipredator behavior, and

*Correspondence: keigouematsu@gmail.com

encourage clonal integrity [14]. In social aphids, specialized

altruistic individuals termed soldiers [15] perform colony
defense, gall cleaning, and gall repair [14, 16, 17]. Considering
that many aphid species survive after ceasing reproduction
when reared under favorable laboratory conditions [18], postreproductive altruism could have evolved in gall-forming social
aphids, although their postreproductive life span and its
beneficial aspects have not yet been identified under natural
conditions [19].
Here, we report postreproductive altruism in the social
aphid Quadrartus yoshinomiyai, which forms conspicuous
large galls on its primary host plant, Distylium racemosum
(Figure 1A), and produces nonspecialized, monomorphic
first-instar defenders [20]. A closed gall is formed by a single
fundatrix (gall founder; see Table S1 available online). In the
gall, the mature fundatrix parthenogenetically produces viviparous offspring, which develop into wingless adults. The gall
matures and forms an exit hole in early to mid-April of
the second year. Winged adults, which are born from the wingless adults, escape from the open gall via the exit hole and
migrate to the secondary host plant, Quercus acutissima, on
which they found colonies [21] (Figure 1B). When disturbed,
wingless adults of Q. yoshinomiyai discharge a large quantity
of wax from their cornicles, a pair of tubular structures on
the abdomen (Figure 1C) [20]. The wax droplets are sticky
and promptly solidify (Movie S1). We observed in mature
galls that wingless adults of Q. yoshinomiyai were stuck to
predators by the waxy secretion, thereby immobilizing the
predators. The stuck wingless adults were unable to detach
themselves and were destined to die, suggesting that the
behavior is self-sacrificing and beneficial to their colony
members (Figure 1D; see also Figure S1).
In natural galls, wingless adults were preferentially found
around the exit holes (Figure 2A). The proportion of wingless
adults in the gall section around the exit hole was significantly
higher than that in the rest of the gall (generalized linear model
[GLM] with quasibinomial errors, F1,22 = 14.3, p = 0.0010;
Figure S2). These distribution patterns seem effective for
defending the colony from predators. A series of predator
introduction experiments were performed in the laboratory.
We prepared experimental galls in which wingless adults
around the exit hole were either removed or untouched, and
a ladybug (Harmonia axyridis) larva was introduced into each
of the galls. In the galls where the adults were removed, the
predators were more likely to get into the galls and less likely
to be stuck around the exit hole than were the predators in
the control galls (Fishers exact probability test, p = 0.0069;
Figure 2B). The adhesion of wingless adults had a significant
positive correlation with the proportion of predators being
immobilized (Fishers exact probability test, p = 0.0015;
Table S2). In this experiment, 57 wingless adults from 28 galls
were found stuck to the mouthparts (10 individuals) or legs
(47 individuals) of the predators, of which 21% (12 of 57) had
been eaten by the predators. These results indicate that wingless adults gather around the exit hole and prevent predators
from entering their galls in a self-sacrificing manner. In other
social aphids, defensive nymphs have been reported to gather
around the exit hole in a similar pattern [22].

Altruism by Menopausal Female Insects

1183

Figure 1. Life History and Behavior of the Aphid

Quadrartus yoshinomiyai
(A) Quadrartus yoshinomiyai gall. Arrow indicates
exit hole. Scale bar represents 10 mm.
(B) Galling stage in the life cycle of Q. yoshinomiyai. A closed gall is formed by a single fundatrix
(gall founder). In the gall, two to three generations
occur before April of the second year. The mature
gall contains about 50200 wingless adults and
5002000 winged or prewinged (i.e., with wing
buds) individuals. After the gall opens, winged
adults escape through the exit holes and
emigrate to their secondary host plants, Quercus
acutissima, to found colonies. All galls are dried
out before mid-June.
(C) Wingless adult discharging waxy droplets
(arrows). Scale bar represents 0.5 mm.
(D) Wingless adults (arrows) stuck with waxy
droplets to the legs of a predatory ladybug larva.

Next, we examined the reproductive potential of wingless

adults that showed defensive behavior in the field survey (16
individuals from two galls) and the laboratory experiments
(57 individuals from 28 galls). None (0 of 16) of the defending
wingless adults in the field survey contained mature embryos
(>0.2 mm long) in their abdomen, and only 5% (3 of 57) of the
defending wingless adults in the laboratory experiments did.
Because aphid embryos develop sequentially within ovarioles,
prereproductive and reproductive adults contain a number of
mature embryos in the abdomen. Hence, we concluded that
the adult defenders were mostly postreproductive individuals.
Field monitoring of the occurrence of wingless adults and
their fecundity revealed several interesting aspects in their

resource allocation across survival,

reproduction, and defense in an ecological context. In mid-April, an opening
appeared on each of the galls. After
exit hole formation, prewinged nymphs
reached a peak in number, winged
adults began to emerge, and the numbers of prewinged and winged insects
sharply declined as a result of migration
(Figure 3A). By contrast, the number of wingless adults
remained almost constant during the period (Figure 3A), indicating that the wingless adults survive and stay within the
open galls for a lengthy period. Inspection of dissected ovaries
revealed that the wingless adults in open galls contained
few mature embryos: on average, 84% of the wingless adults
in open galls were free of mature embryos (Figure 3B). By
contrast, in closed, immature galls collected on February 28
(n = 8), all dissected wingless adults (20 individuals per gall)
and all nymphs (third and fourth instar, 1352 individuals per
gall) contained embryos, suggesting that all wingless adults
originally have reproductive potential (Figure 3B). The prolonged life span and the substantial sterility of the wingless

Figure 2. Colony Defense by Wingless Adults of

Q. yoshinomiyai
(A) Wingless adults of Q. yoshinomiyai clustered
around the exit hole of a gall.
(B) Fate of predators (ladybug larvae) introduced
into galls. At 24 hr after introduction, each predator was examined for its position in the gall,
the presence or absence of attached wingless
adults, and its mobility. When wingless adults
around the exit hole were removed, the proportion of predators able to enter the galls (white
bars) increased, and the proportion of predators
stuck to wingless adults outside the galls (black
bars) decreased (n = 22 for each treatment, 2 3
3 Fishers exact probability test, p = 0.0069; see
also Table S2). Sample size is given in each bar.

Current Biology Vol 20 No 13

1184

Number of aphids

1400

Winged adults
Prewinged nymphs
Wingless adults

1200
1000
800
600
400
200

Proportion (%) of
embryo-lacking adults

Closed

Open

100
80
60
40
20
0
28-Feb
(n=8)

25-Mar
(12)

08-Apr
(12)

22-Apr
(12)

07-May
(12)

20-May
(10)

Date (year 2008)

C
Closed

Number of newborns

200

Open

150
100
50
0
09-Mar
(n=11)

06-Apr
(14)

22-Apr
(11)

09-May
(12)

Date (year 2009)

Figure 3. Temporal Changes in Colony Composition and Fecundity of Wingless Q. yoshinomiyai Adults in Mature Galls
Dashed lines distinguish between closed and open galls.
(A) Numbers of winged adults (mean + standard deviation [SD]), prewinged
nymphs (mean + SD), and wingless adults (mean 2 SD) in galls (n = 12 for
each sampling date, except for February 28 [n = 8] and May 20 [n = 10]). After
the galls opened, the number of prewinged nymphs reached a peak and
winged adults began to emerge, and the number then decreased sharply.
By contrast, wingless adults decreased slowly.
(B) The proportion of wingless adults lacking mature embryos increased
significantly with sampling date (F1,55 = 51.3, p < 0.0001). Twenty wingless
adults were randomly chosen from each gall and examined for the presence
of mature embryos in their ovarioles. Box plot shows median, quartiles, and
minimum and maximum values.
(C) Number of newborn nymphs produced by artificially reared wingless
adults. Wingless adults in cut galls (20 adults per gall) were reared at 15 C
for 14 days from the collection date. Number of newborn nymphs decreased
significantly with collection date (c2 = 150.8, p < 0.0001). The proportion of
galls in which no newborn nymphs were produced also increased with
collection date (c2 = 34.2, p < 0.0001; see also Table 1). Box plot shows
median, quartiles, and minimum and maximum values.

adults in open galls were confirmed by laboratory rearing of

the insects. We collected closed and open galls in the field,
manipulated the gall inhabitants to be 20 wingless adults per
gall, and maintained the experimental galls in an incubator.
In over 80% of the experimental open galls, no nymphs were
produced during 14 days of rearing (Figure 3C), in contrast to
6% of the experimental closed galls (Table 1). On average,
more than 90% of the wingless adults in both types of gall
survived for 14 days. Even after 24 days of rearing, many of
the insects were still alive (Table 1). These results indicate
that the wingless adults cease reproduction in mature, open
galls and survive for a lengthy period. Closed galls are resistant to attacks by predators. In maturity, however, galls must
open so that winged adults can migrate to the secondary
host plants, and this inevitably provides a route for predator
invasion. In other gall-forming social aphids, a correlation
between the intensity of gall defense and the length of the
emergence period of winged migrants has been reported
[23]. The timing of the shift from reproduction to defense in
the wingless adults is coincident with the ecological necessity
of the aphid colonies.
Histological examination of the wingless adults highlighted
the physiological basis of the shift from reproduction to
defense. In closed galls, the wingless adults contained many
embryos as well as a small amount of waxy defensive secretion in the abdomen (Figures 4A and 4C). In open galls, by
contrast, the abdomen of the winged adults was almost exclusively occupied by waxy defensive secretion (Figures 4B and
4D). Note that the size and shape of the abdomens were
similar, indicating resource allocation from embryo production
to secretion synthesis in the course of adult aging. Taken
together with the longevity of the wingless adults in open galls,
this suggests that reproductive cessation does not immediately result in debilitation and death of the insects but is
followed by active synthesis of secretion substances, leading
to physiological switching from reproduction to defense.
In conclusion, we have demonstrated the existence of postreproductive altruism in a gall-forming social aphid, providing
a documented invertebrate case of adult individuals gaining
indirect fitness during their postreproductive life span. Relevant to this phenomenon, previous studies have shown that
some social hymenopterans like paper wasps exhibit dominance interactions between reproductives, whereby inferior
individuals cease reproduction, function as workers, and
gain indirect fitness [13, 24]. In some sense, the parthenogenetic ant Pristomyrmex punctatus [25] may be regarded as
a hymenopteran proxy of Q. yoshinomiyai, in that clonal colony
members irreversibly switch their roles from reproduction to
foraging as they age [25]. The absence of kin-selected conflict
among clonal colony members is likely to have promoted
the evolution of postreproductive altruism [3]. The suicidal
behavior of wingless adults in Q. yoshinomiyai is reminiscent
of the explosion behavior of sterile walking bomb soldiers
in some ants and termites, which thereby spray adhesive
secretions on predators [26, 27]. The self-sacrificing gall
repairing in the nipponaphidine aphid Nipponaphis monzeni,
wherein body fluid discharged by soldier aphids solidifies
and plasters up gall breaches [16, 17], may be evolutionarily
relevant to the secretion-mediated defense in Q. yoshinomiyai.
In mammals, it is suggested that cultural information transmitted by older individuals leads to indirect fitness gain and
the evolution of prolonged postreproductive life span [7, 9,
28]. Our findings show that intelligence is not necessarily
involved in the evolution of postreproductive altruism,

Altruism by Menopausal Female Insects

1185

Table 1. Temporal Changes in Fecundity and Survival of Artificially Reared Wingless Q. yoshinomiyai Adults in Cut Galls

Collection
Date

Gall
Status

Galls with
Newborn Nymphs
after 14 Days

Galls without
Newborn Nymphs
after 14 Days

Average Number
of Newborn Nymphs
after 14 Days (Range)

Average Percent of
Surviving Wingless Adults
after 14 Days (Range)

Average Percent of
Surviving Wingless Adults
after 24 Days (Range)

3/9/2009
4/6/2009
4/22/2009
5/9/2009

closed
closed
open
open

11
12
2
1

0
2
9
11

143.9 (89211)
9.4 (024)
2.4 (018)
0.1 (01)

96.0 (85100)
96.1 (90100)
97.3 (90100)
90.5 (70100)

not observed
94.6 (85100)
93.2 (75100)
66.8 (2095)

In each cut gall, 20 wingless adults were incubated at 15 C for 1424 days. The proportion of galls in which no newborn nymphs were produced increased
with time (generalized linear model with binomial errors, c2 = 34.2, p < 0.0001).

providing a general framework for understanding complex

cooperative societies in animals.
Experimental Procedures
Materials
Quadrartus yoshinomiyai galls were found on Distylium racemosum trees in
the towns of Shinkiba and Wakasu (Koto-ku, Tokyo, Japan). Field observations were carried out from May 2006 to May 2009. Some galls were
collected, brought to the laboratory, and subjected to further analyses.
Defensive Behavior of Wingless Adults
Mature, open galls were cut with a razor and examined for the presence of
natural predators. If predators were present in the galls, then the defensive
behavior of wingless adults was observed.
Spatial Distribution of Wingless Adults within Galls
Twelve galls each with an exit hole (two galls from each of six trees) were
collected on April 10, 2007 in the field. Each gall was immediately removed

from the tree and cut into two sections: (1) the section around the exit hole,
located within 5 mm of this opening, and (2) the rest of the gall. Each section
was immediately preserved in 70% ethanol and brought to the laboratory.
The contents of each section were examined under a dissecting microscope, and the numbers of wingless adults and other aphids were recorded.
Predator Introduction Experiment in Galls with Wingless Adults
Removed
As test predators, first-instar larvae of the ladybug Harmonia axyridis, which
was previously reported as a natural predator of Q. yoshinomiyai [20], were
used. The larvae were offspring of three female adults that had been
collected from two silverberry trees (Elaeagnus sp.) at the Komaba campus
of the University of Tokyo on April 19, 2008. The ladybug larvae were reared
at 20 C 6 1 C in a chamber, fed Capitophorus hippophaes aphids, and then
deprived of food for 24 hr before the experiment.
A total of 22 pairs of galls, each of which had a single exit hole and more
than five wingless adults around this opening, were collected from three
D. racemosum trees between April 28 and May 7, 2008. Each pair was
obtained from the same branchs shoots and brought to the laboratory.
One of the pair was used as the treatment gall, from which wingless adults
were removed, and the other was used as the control gall. For each gall,
based on a previous study [29], a 0.5 ml open-ended centrifuge tube was
attached over the exit hole with warm paraffin wax so that the predator
could freely enter the gall. After attachment of the tube, all aphids around
the exit hole were gently removed from each treatment gall with tweezers,
and we confirmed under a dissecting microscope that wingless adults
visible around the exit hole had been completely removed. Each gall was
then placed with its opening directed upward; 5 min later, a predator
was introduced onto the gall through the attached tube, and the tube lid
was closed. After 24 hr, each predator was examined for its position, the
presence or absence of attached wingless adults, and its mobility in the
gall. Mobility was judged by whether the predator could move within 10 s
of being placed in the center of a Petri dish. Two accidentally injured predators were excluded from the mobility test. Experiments were conducted at
room temperature.
Fecundity of Wingless Adults Showing Defensive Behavior
Wingless adults showing defensive behavior in the field or in the laboratory
experiment were dissected and examined under a dissecting microscope
for the presence of mature embryos (>0.2 mm in length) in their ovarioles.

Figure 4. Histological Observations of Wingless Q. yoshinomiyai Adults

(A and B) Inner structure of the whole body of wingless adults in closed gall
(A) and open gall (B). The skins of the adults were made transparent by soaking them in ethanol. The whitish area indicates the organs containing waxy
defensive secretion (Wo); the darker area indicates embryos (Em).
(C and D) Sagittal cross-section of the abdomen of wingless adults in closed
gall (C) and open gall (D). Sections were stained with oil red O (red) and
hematoxylin (blue). The majority of the abdomen of wingless adults in
open galls was occupied by the highly developed defensive secretion
organs.
Scale bars represent 200 mm.

Temporal Changes in Colony Composition and Fecundity of Wingless

Adults
A total of 66 galls were collected from six trees from February to May 2008.
Each gall was examined for the presence of natural openings. Gall inhabitants were preserved in 70% ethanol and later examined under a dissecting
microscope for numbers of prewinged nymphs with wing buds, winged
adults, and wingless adults. From each gall, 20 randomly chosen wingless
adults were dissected and examined for the presence of mature embryos
in their ovarioles. In closed, immature galls collected on February 28, all
immature (third- and fourth-instar) wingless aphids (1352 individuals per
gall) were also dissected and examined for the presence of embryos.
Laboratory Rearing of Wingless Adults in Cut Galls
A total of 48 galls, together with the gall-bearing twigs, were collected from
three trees on March 9, April 6 and 22, and May 9, 2009. In the laboratory,
each gall was cut horizontally at a distance of 5 mm from its budding point.
All aphids were removed from the gall, and 20 wingless adults were placed
on the inner wall of the cut gall. Each cut gall and twig was completely sealed
with a stretched Parafilm sheet, and holes were made in the Parafilm with an

Current Biology Vol 20 No 13

1186

insect pin to ensure sufficient ventilation. Cotton wool soaked with distilled
water was wrapped around the cut end of the twig bearing each gall. Each
gall was placed in a plastic container and stored at 15 C in an incubator. For
each gall, the Parafilm sheet and cotton wool were renewed every 2 days, at
which time the number of newborn nymphs and the survival rate of wingless
adults were recorded. After each recording, all newborn nymphs were
removed from the gall.
Histological Examination
Wingless adults from the closed and open galls were fixed overnight in
freshly prepared 4% paraformaldehyde in phosphate-buffered saline
(PBS) at 4 C. They were then washed in PBS, incubated in 30% sucrose
in PBS at 4 C, and embedded in OCT compound. Frozen sections (15 mm
thick) of wingless adults were prepared on a cryostat, air dried, stained
with oil red O in 60% isopropanol, washed in 60% isopropanol, treated
with hematoxylin, and washed in PBS.
Data Analysis
The effects of removal of wingless adults and adhesion of wingless adults
on the fate of introduced predators were analyzed using Fishers exact
probability test. In other analyses, we used a GLM framework. For the relationships between the collection date of galls and the proportion of wingless
adults lacking mature embryos and between the position within galls and
the proportion of wingless adults, we used quasibinomial errors because
of overdispersion [30]. For the relationship between the collection date of
galls and the number of newborn nymphs produced by wingless adults in
the laboratory, we used the negative binomial error, which was selected
from among other error distributions (normal, Poisson, gamma, and inverse
normal) according to the Akaike information criterion. All statistical analyses
were performed with the software R v2.9.2 [31].
Supplemental Information
Supplemental Information includes two figures, two tables, and two movies
and can be found with this article online at doi:10.1016/j.cub.2010.04.057.
Acknowledgments
This research was supported by a 21st Center of Excellence Program of the
Research Center of Integrated Science at the University of Tokyo, financed
by the Ministry of Education, Culture, Sports, Science and Technology,
Japan. K.U. was supported by a Research Fellowship of the Japan Society
for the Promotion of Science for Young Scientists. We thank K. Niijima for
technical assistance in rearing ladybug larvae; A. Sedohara, K. Ohnuma,
and M. Asashima for assistance with the frozen sectioning procedure; and
T. Dixon and S. Dobata for comments on the manuscript.
Received: March 14, 2010
Revised: April 28, 2010
Accepted: April 28, 2010
Published online: June 17, 2010
References
1. Hawkes, K., OConnell, J.F., Jones, N.G.B., Alvarez, H., and Charnov,
E.L. (1998). Grandmothering, menopause, and the evolution of human
life histories. Proc. Natl. Acad. Sci. USA 95, 13361339.
2. Lee, R.D. (2003). Rethinking the evolutionary theory of aging: Transfers,
not births, shape senescence in social species. Proc. Natl. Acad. Sci.
USA 100, 96379642.
3. Bourke, A.F.G. (2007). Kin selection and the evolutionary theory of
aging. Annu. Rev. Ecol. Evol. Syst. 38, 103128.
4. Shanley, D.P., and Kirkwood, T.B.L. (2001). Evolution of the human
menopause. Bioessays 23, 282287.
5. Cant, M.A., and Johnstone, R.A. (2008). Reproductive conflict and the
separation of reproductive generations in humans. Proc. Natl. Acad.
Sci. USA 105, 53325336.
6. Cant, M.A., Johnstone, R.A., and Russell, A.F. (2009). Reproductive
conflict and the evolution of menopause. In Reproductive Skew in Vertebrates, R. Hager and C.B. Jones, eds. (Cambridge: Cambridge University Press), pp. 2450.
7. McAuliffe, K., and Whitehead, H. (2005). Eusociality, menopause and
information in matrilineal whales. Trends Ecol. Evol. 20, 650.

8. Lahdenpera, M., Lummaa, V., Helle, S., Tremblay, M., and Russell, A.F.
(2004). Fitness benefits of prolonged post-reproductive lifespan in
women. Nature 428, 178181.
9. Foster, K.R., and Ratnieks, F.L.W. (2005). A new eusocial vertebrate?
Trends Ecol. Evol. 20, 363364.
10. Dagg, A.I. (2009). The Social Behavior of Older Animals (Baltimore:
Johns Hopkins University Press).
11. Carey, J.R. (2008). Biodemography: Research prospects and directions.
Demogr. Res. 19, 17491758.
12. Blest, A. (1963). Longevity, palatability and natural selection in five
species of New World saturniid moth. Nature 197, 11831186.
13. Ratnieks, F.L.W., Foster, K.R., and Wenseleers, T. (2006). Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581608.
14. Pike, N., and Foster, W.A. (2008). The ecology of altruism in a clonal
insect. In Ecology of Social Evolution, J. Korb and J. Heinze, eds. (Berlin:
Springer), pp. 3657.
15. Aoki, S. (1977). Colophina clematis (Homoptera, Pemphigidae), an aphid
species with soldiers. Kontyu 45, 276282.
16. Kurosu, U., Aoki, S., and Fukatsu, T. (2003). Self-sacrificing gall repair by
aphid nymphs. Proc. Biol. Sci. 270 (Suppl 1), S12S14.
17. Kutsukake, M., Shibao, H., Uematsu, K., and Fukatsu, T. (2009). Scab
formation and wound healing of plant tissue by soldier aphid. Proc.
Biol. Sci. 276, 15551563.
18. Hamilton, W.D. (1966). The moulding of senescence by natural selection. J. Theor. Biol. 12, 1245.
19. Dixon, A.F.G. (1987). Parthenogenetic reproduction and the rate of
increase in aphids. In Aphids: Their Biology, Natural Enemies and
Control, Volume 2A, A. Minks and P. Harrewijn, eds. (Amsterdam: Elsevier), pp. 269287.
20. Uematsu, K., Kutsukake, M., Fukatsu, T., Shimada, M., and Shibao, H.
(2007). Altruistic defenders in a Japanese gall-forming aphid, Quadrartus yoshinomiyai (Homoptera: Aphididae: Hormaphidinae). Sociobiology 50, 711724.
21. Sorin, M. (2001). A new subspecies and little known Aphididae (Hemiptera) from Japan. Bull. Fac. Lit. Kogakkan Univ. 40, 127142.
22. Pike, N. (2007). Specialised placement of morphs within the gall of the
social aphid Pemphigus spyrothecae. BMC Evol. Biol. 7, 18.
23. Pike, N., Whitfield, J.A., and Foster, W.A. (2007). Ecological correlates of
sociality in Pemphigus aphids, with a partial phylogeny of the genus.
BMC Evol. Biol. 7, 185.
24. Reeve, H.K., and Keller, L. (2001). Tests of reproductive-skew models in
social insects. Annu. Rev. Entomol. 46, 347385.
25. Tsuji, K. (1990). Reproductive division of labor related to age in the Japanese queenless ant, Pristomyrmex pungens. Anim. Behav. 39, 843849.
26. Eisner, T., Eisner, M., and Siegler, M.V.S. (2005). Secret Weapons:
Defenses of Insects, Spiders, Scorpions, and Other Many-Legged Creatures (Cambridge, MA: Belknap Press of Harvard University Press).
27. Oster, G.F., and Wilson, E.O. (1978). Caste and Ecology in the Social
Insects (Princeton, NJ: Princeton University Press).
28. Gurven, M., and Kaplan, H. (2007). Longevity among hunter-gatherers:
A cross-cultural examination. Popul. Dev. Rev. 33, 321365.
29. Foster, W.A. (1990). Experimental evidence for effective and altruistic
colony defese against natural predators by soldiers of the gall-forming
aphid Pemphigus spyrothecae (Hemiptera, Pemphigidae). Behav.
Ecol. Sociobiol. 27, 421430.
30. Crawley, M.J. (2005). Statistics: An Introduction Using R (Chichester,
UK: Wiley).
31. R Development Core Team. (2009). R: A Language and Environment for
Statistical Computing (Vienna: R Foundation for Statistical Computing).