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JHR 58: 29—40 (2017) JOURNAL OF | 40eerriewed opevaccetsjoural
pape ies (4G) Hymenoptera

http://jhr.pensoft.net The Insertional Society of Hymenoptersts. RESEARCH

Influence of natal host and oviposition experience
on sex allocation in a solitary egg parasitoid,
Anastatus disparis (Hymenoptera, Eupelmidae)

Peng-Cheng Liu'”, Jian-Jun Wang’, Bin Zhao!, Jin Men', Jian-Rong Wei!

I The College of Life Science, Hebei University, Baoding City, Hebei Province, China 2 The College of Forestry,
Nanjing Forestry University, Nanjing City, Jiangsu Province, China 3 Liaoning Academy of Forestry Science,
Shenyang, Liaoning Province, China

Corresponding author: /ian-Rong Wei (jrwei9@126.com)

Academic editor: MZ. Shaw | Received 18 March 2017 | Accepted 11 July 2017 | Published 31 August 2017
http://zoobank.org/C70246E4-97AE-42E8-9B65-90AA6 C654BE4

Citation: Liu P-C, Wang J-J, Zhao B, Men J, Wei J—R (2017) Influence of natal host and oviposition experience on sex
allocation in a solitary egg parasitoid, Anastatus disparis (Hymenoptera, Eupelmidae). Journal of Hymenoptera Research
58: 29-40. https://doi.org/10.3897/jhr.58.12763

Abstract

Constraints on adaptation are a major topic in evolutionary biology. Sex allocation, in particular the ratio
of the sexes, has often been used as a key process for studying constraints on adaptation. Anastatus disparis
Ruschka (Hymenoptera: Eupelmidae) is a solitary egg parasitoid of gypsy moth, Lymantria dispar (L.)
(Lepidoptera: Lymantriidae), and several other lepidopteran forest pests. Here, we compared two differ-
ent sized substitute hosts, the smaller one Dictyoploca japonica Moore (Lepidoptera: Saturnidae) and the
larger one Antheraea pernyi Guerin-Meneville (Lepidoptera: Saturnidae), and investigated the influence of
natal host and oviposition experience on sex allocation by A. disparis. Results showed that natal host had
almost no impact on sex allocation by A. disparis, but oviposition experience did influence sex allocation
of A. disparis on D. japonica eggs. This suggests that information females obtain from the environment
influences how they allocate sex in their offspring. However, the sex ratios of A. disparis emerging from A.
pernyi eggs were consistent irrespective of oviposition experience of female A. disparis. This indicates that

the eggs of A. pernyi are large enough to maximize female progeny of A. disparis.

Keywords
Parasitoid, substitute host, learning, gypsy moth

Copyright Peng-Cheng Liu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

30 Peng-Cheng Liu et al. / Journal of Hymenoptera Research 58: 29-40 (2017)

Introduction

Anastatus disparis Ruschka (Hymenoptera: Eupelmidae) is a solitary egg parasitoid of
several noxious lepidopteran forest pests, including the gypsy moth, Lymantria dispar
(L.) (Lepidoptera: Lymantriidae) (Crossman 1925, Kurir 1944, Yan et al. 1989, Li and
Lou 1992, Alalouni et al. 2013, Liu et al, 2017). It can develop three to four genera-
tions on L. dispar eggs annually in Northern China (Yao and Yan 1994). In our previ-
ous research, we found that the offspring of A. disparis reared on egg masses of gypsy
moth were male-biased and small-bodied (Liu et al. 2017). However, when they were
reared on a larger host, Antheraea pernyi Guerin-Meneville (Lepidoptera: Saturnidae),
the offspring were female-biased and had a larger body size compared with those reared
from gypsy moth (Liu et al. 2017).

Sex allocation in haplodiploid arthropods has fitness-related implications and has
received much attention with regard to insect parasitoids (West 2009). In particular, an
important attribute of parasitoids is that they control the sex ratio of offspring in response
to environmental variables (Godfray 1994). In parasitoid wasps, mated females can ma-
nipulate the sex-ratio of progeny by controlling fertilization during oviposition. Males
develop from unfertilized eggs and are haploid, while females develop from fertilized
eggs and are diploid (Heimpel and de Boer 2008). In the case of solitary parasitoids, for
which only one individual develops in each host, the theory of host quality-dependent sex
allocation has been proposed to explain the sex ratio variation in this group of parasitic
Hymenoptera (Charnov 1979, Charnoyv et al. 1981). This theory states that the pattern
of sex allocation is determined depending on male- and female-fitness relationships with
host size; either female or male eggs could be allocated to higher quality hosts depending
on which sex benefits more from being large (Charnov et al. 1981, Napoleon and King
1999, West and Sheldon 2002). Both theoretical predictions and empirical studies show
that the sex (usually female) that benefits most from being larger, should be placed in a
larger host for its development (Charnov et al. 1981, King and Lee 1994). The size of
an emerging parasitoid is often positively correlated with the size of the natal host, as are
other fitness components such as longevity, fecundity, dispersal and patch-finding ability
in the field (King and Charnov 1988, King and Lee 1994, Visser 1994, Kazmer and Luck
1995, Bennett and Hoffmann 1998, Ellers et al. 1998, Jervis et al. 2003).

Learning and memory have been demonstrated in a large number of animal spe-
cies. Hymenopteran parasitoids can learn to recognize particular visual and olfactory
stimuli and use them to modify subsequent behaviours (Vet et al. 1995, Vinson 1998).
Learning may occur at any phase of the host selection process (Dauphin et al. 2009).
Therefore, learning includes ‘pre-imaginal learning’ at adult emergence (Cortesero and
Monge 1994, Gandolfi et al. 2003), ‘post-emergence learning’ or ‘early adult learning’
immediately after emergence (Lentz and Kester 2008), and ‘ovipositional learning’ at
oviposition (Turlings et al. 1995). Numerous studies have demonstrated the positive
effects of learning on host selection (Vet and Groenewold 1990, Hastings and Godfray
1999, Morris and Fellowes 2002), optimizing foraging efficiency (Vet and Groenewold

Influence of natal host and oviposition experience on sex allocation... 31

1990, Vet et al. 1995, Vinson 1998) and encountering suitable hosts (Papaj and Vet
1990, Baaren and Boivin 1998, Dutton and Dorn 2000).

Trivers and Wilard (1973) suggest that females should adjust the sex of their off-
spring in response to environmental conditions, and there is considerable empirical
evidence for such adjustments and deviations from optimal sex allocation strategies
(West and Sheldon 2002, Lewis et al. 2010). As a parasitoid, A. disparis can parasitize
small body-sized hosts through to large body-sized hosts, with females seeming to pre-
fer larger hosts which produce more female offspring (Liu et al. 2017). However, we
do not know whether natal host or oviposition experience influence the offspring sex
allocation of adults. For this reason, we devised a series of experiments aiming firstly
to determine whether natal host could influence sex allocation in female A. disparis,
and secondly whether a learning experience, in this case oviposition experience on one
host species, influences sex allocation by females during oviposition on a different host
species. Iwo substitute host species of different sizes were evaluated: the smaller was
Dictyoploca japonica Moore (Lepidoptera: Saturnidae) and the larger was Antheraea
pernyi Guerin-Meneville (Lepidoptera: Saturnidae).

Material and methods

Insect cultures

Pupae of Antheraea pernyi were purchased from a farmer in Qinglong Manchu Au-
tonomous County, Qinhuangdao City, Hebei Province, China; adults that emerged
from those pupae were maintained at 25—30 °C for less than two days prior to egg ex-
traction (see below); Dictyoploca japonica eggs were provided directly from the Forestry
Academy of Liaoning Province, China. Eggs of the two lepidopteran host species for
use in experiments were obtained by laparotomizing the adult females’ abdomen and
removing the eggs; these eggs were maintained at 0 °C prior to use, and for not longer
than 60 days (Wang et al. 2014).

An Anastatus disparis colony was first established from a population develop-
ing in L. dispar egg masses collected in Longhua County, Hebei Province (41°31'N,
117°74'E) in March, 2012, and was subsequently maintained on A. pernyi eggs in
several cylindrical rearing boxes (height: 5 cm, diameter: 5 cm) at 25+0.5°C, RH 60%,
14L:10D. Prior to experiments cohorts of A. disparis were also reared on D. japonica
eggs for three generations to provide the different treatments for the experiments (see
below). All adult female A. disparis had no experience of hosts or oviposition before
experiments began and were fed with honey water (honey: water=4: 6) on cotton balls
(Yan et al. 1989). The age of the females selected for the experiments ranged from 3 to
5 days because under standard conditions offspring sex ratio does not fluctuate widely
during this period (Liu et al. 2015). All females were placed with males for 24 hours to
ensure they were mated before each experiment.

32 Peng-Cheng Liu et al. / Journal of Hymenoptera Research 58: 29-40 (2017)

Measurement of egg sizes of different lepidopteran host species

The host egg sizes were determined from their length (Morris and Fellowes 2002),
which was measured using a light microscope (Leica M205A, Germany). Thirty repli-
cate eggs were measured for each host species.

Sex allocation by Anastatus disparis

One large experiment with six treatments was conducted to answer two primary ques-
tions, the first concerning sex-allocation by females offered a choice of different sized
hosts (treatments 1 and 2) and the second concerning females offered different sized
host sequentially (treatments 3-6; in all cases, they gained oviposition experience when
offered the first host which then had the potential to influence their behaviour in rela-
tion to the second host offered). All treatments were run at the same time but, to aid
interpretation, we describe them below in relation to the question being asked.

Sex allocation by Anastatus disparis when offered a choice of eggs from two different
lepidopteran host species presented at the same time

This question was answered by comparing between two treatments; specifically, be-
tween maternal females that were either reared on Antheraea pernyi (treatment 1) or
Dictyoploca japonica (treatment 2) before being offered a choice of eggs from both lepi-
dopteran species, for oviposition. One maternal adult (3—5 days) reared on either A.
pernyi or D. japonica was introduced into a cylindrical rearing box (height: 5 cm, diam-
eter: 5 cm) containing twenty A. pernyi eggs and twenty D. japonica eggs at 2640.5 °C.
After 24 hours, the eggs of both host species were collected and placed individually
into polyethylene tubes (height: 7.5 cm; diameter: 1 cm) plugged with cotton and
incubated at 2840.5 °C until adult parasitoids emerged. The number and sex of off-
spring was recorded after eclosion. Since A. disparis is haplodiploid, virgin females lay
100% unfertilized eggs, which develop into males, while mated females lay a mixture
of unfertilized and fertilized eggs, the latter of which develop into females. Therefore,
any replicates resulting in 100% male offspring were assumed to be from unmated ma-
ternal adults and were excluded from subsequent statistical analysis. Thirty replicates
of maternal adults were tested for each treatment (60 in total).

Sex allocation by A. disparis when eggs from two different lepidopteran host spe-
cies are presented separately and in sequence

This question was answered by comparing amongst four treatments in which maternal
females, reared either in A. pernyi or D. japonica, were offered eggs of one or other of the

Influence of natal host and oviposition experience on sex allocation... 33

Table |. Number of maternal replicates for each experimental treatment.

Sequence of parasitism

Host species on which the maternal

parasitoid had been seared First A. pernyi eggs then First D. japonica eggs then

D. japonica eggs A. pernyi eggs
77 (treatment 4)
64 (treatment 6)

A. pernyi eggs 73 (treatment 3)

D. japonica eggs 66 (treatment 5)

lepidopteran species in sequence, i.e. first A. pernyii eggs and then D. japonica eggs or vice
versa: all combinations (i.e. the four treatments, 3-6) and total replicates per treatment
combination can be seen in Table 1. Specifically: One maternal adult reared either on A.
pernyi or D. japonica, was introduced into a cylindrical rearing box (height: 5 cm, diam-
eter: 5 cm) containing twenty A. pernyi or D. japonica eggs (depending on treatment) at
2640.5 °C. Twenty-four hours later, all of the host eggs were collected and replaced by a
new batch of twenty eggs of A. pernyi or D. japonica (depending on treatment) and incu-
bated for a further 24 hours at 2640.5 °C. Parasitised host eggs from each treatment were
placed individually into polyethylene tubes (height: 7.5 cm; diameter: 1 cm) plugged
with cotton and incubated at 28+0.5 °C until adult parasitoids emerged. The number
and sex of offspring was recorded after eclosion. Results for maternal adults that had not
mated were excluded from the subsequent statistical analysis as described previously.

Statistical analysis

The sex ratio of the parasitoid offspring was represented as the proportion of males
(male divided by male+female). Sex ratios of offspring reared from the different host
species (for each treatment), and the egg sizes of the two different host species, were
compared using independent 7-tests in the statistical package SPSS version 20, after
arcsin (sqrt) transformation of the raw proportion data. For the whole experiment with
simultaneous presentation of both host species in treatment 1 and 2, sex ratios and
numbers of offspring reared from the different host species were compared by General
Linear Model (GLM) with Univariate tests and Generalised Linear Mixed Models
(GLMMs). For the effect of oviposition experience (hosts presented with different
sequences), results from the whole experiment (treatment 3-6) were analyzed by GLM
with Multivaritate tests. The confidence interval for all tests was set at 95%.

Results

Sizes of two host species

The eggs of A. pernyi (2.94+0.02 mm) were significantly larger than the eggs of D. japonica
(2.3140.02 mm; 1=24.44, d58, p<0.001).

34 Peng-Cheng Liu et al. / Journal of Hymenoptera Research 58: 29-40 (2017)

Sex allocation by A. disparis when offered a choice of eggs from two different lepi-
dopteran host species presented at the same time

When maternal A. disparis that had been reared on A. pernyi eggs encountered A.
pernyi and D. japonica eggs simultaneously (treatment 1), the proportion of male off-
spring emerging from A. pernyi eggs was 9.3541.87% and the proportion emerging
from D. japonica eggs was 44.53+8.34% (Fig. 1). When maternal A. disparis that had
been reared on D. japonica eggs encountered A. pernyi and D. japonica eggs simultane-
ously (treatment 2), the results were similar: the proportion of male offspring emerging
from A. pernyi eggs was 10.6042.66% and the proportion emerging from D. japonica
eges was 30.60+7.02%. GLM with univariate analysis showed that offspring sex ra-
tios of maternal adults from the two host species varied little (F=1.558; df=1, 116;
P=0.215), but when females made a choice between the two host species, the sex ratios
of offspring from A. pernyi eggs and D. japonica was significantly different (F=15.233;
df=1, 116; p<0.001) (Fig. 1). Analysis by GLMMs also showed that offspring sex ratios
of females from the two host species (natal influence) were not significantly different
(p>0.05), but their offspring differed when emerging from different host eggs (Esti-
mate=0.237, Wald Z=7.616, p<0.001).

The total number of offspring emerging from A. pernyi eggs parasitized by mater-
nal A. disparis from host A. pernyi or D. japonica were 7.27+0.62 and 7.00+40.79, re-
spectively. The total number of offspring emerging from D. japonica eggs parasitized by
maternal A. disparis from host A. pernyi or D. japonica were 3.53+0.69 and 2.97+0.55,
respectively. Analysis showed that the total offspring number laid by the two kinds of
females varied little (F=0.387, df=1, 116, p=0.535), This was consistent in the treat-
ments where eggs of the two hosts were presented sequentially and so we only report
total numbers here. However, there was a significant difference between the two para-

sitized host species (F=33.634, df=1, 116, p<0.001).

Sex allocation by A. disparis when the eggs of two different lepidopteran host spe-
cies were presented separately and in sequence

When maternal A. disparis reared on A. pernyi eggs were first offered A. pernyi eggs and
then D. japonica eggs (treatment 3) a significantly higher proportion of male offspring
emerged from D. japonica eggs (28.0243.20%) than A. pernyi eggs (7.6540.65%; t=-
6.640, df=72, p<0.001) (Fig. 2).

When maternal A. disparis reared on D. japonica eggs were first offered A. pernyi
eggs and then D. japonica eggs (treatment 5) a significantly higher proportion of male
offspring emerged from D. japonica eggs (34.3743.42%) than from A. pernyi eggs
(7.57+1.09%; t=-8.570, df=65, p<0.001).

When maternal A. disparis reared on A. pernyi eggs were first offered D. japonica
eggs and then A. pernyi eggs (treatment 4) there was no significant difference in the
proportion of male offspring emerging from D. japonica eggs (10.33+40.93%) com-

Influence of natal host and oviposition experience on sex allocation... 35

60
b O) Antheraea pernyi
— 50 | DO Dictvoploca japonica
a
=
Bl 40 b
a=
fs)
2 30
3
=
S
a 20
= q
5
a. 10 a:
o
aw
0
Antheraea pernyi Dictyoploca japonica

Host species on which the maternal adults had been reared

Figure |. Proportion of male offspring from maternal A. disparis when simultaneously presented with
eges of two host species. Bars with different lowercase letters are significantly different from each other
from the General Linear Models with Univariate test analysis (p<0.001).

Proportion of male offspring (%)

Maternal parasitoid from Antheraea Maternal parasitoid from Dictyoploca
pernyi egg japonica egg

Host species on which the offspring had been reared

Figure 2. Proportion of male offspring from female A. disparis with different prior oviposition experi-
ence. Bars with different lowercase letters are significantly different from each other from the General
Linear Models with Multivariate tests analysis (p<0.001). A3 and D3 represent host A. pernyi eggs and
D. japonica eggs in treatment 3, respectively; A4 and D4 represent two hosts in treatment 4; A5 and D5

represent two hosts in treatment 5; A6 and D6 represent two hosts in treatment 6.

36 Peng-Cheng Liu et al. / Journal of Hymenoptera Research 58: 29-40 (2017)

pared with the proportion emerging from A. pernyi eggs (8.9340.93%; t=1.137, df=76,
p>90.05).

When maternal A. disparis reared on D. japonica eggs were first offered D. japonica
eggs and then A. pernyi eggs (treatment 6) there was no significant difference in the pro-
portion of male offspring emerging from A. pernyi eggs (9.07+0.92%) compared with
the proportion emerging from D. japonica eggs (8.19+0.80%; t=-0.754, df=63, p>0.05).

In both treatments in which the maternal adults had been reared on A. pernyi eggs
(treatments 3 and 4), the proportion of A. disparis male offspring emerging from D.
japonica eggs was significantly higher when the female had previous oviposition experi-
ence on A. pernyi eggs (28.02+3.20%; treatment 3), than when they had no previous
oviposition experience (10.33+0.93%; t=5.02, df=148, p<0.001; treatment 4) (Fig. 2).
The results were similar for the maternal adults that had been reared on D. japonica
eggs: a significantly higher percentage of male offspring emerged from D. japonica eggs
parasitized by females with oviposition experience on A. pernyi eggs (34.3743.42%;
treatment 5), than when they had no previous oviposition experience (8.19+0.80%;
t=7.46, df=128, p<0.001; treatment 6) (Fig. 2).

When treatments 3-6 were put into a 2x2 GLM analysis, ie, the first factor being
mother (emerged from A. pernyi or D. japonica) and the second factor being ‘when
experienced’ (first or second order), and the offspring sex ratios of A. disparis from A.
pernyi eggs and D. japonica eggs were regarded as two dependent variables, respectively,
several interesting results were observed. The first was that the offspring sex ratios were
not different across the first and second broods, regardless of host species (F=0.494,
df=2, 275 p=0.61), i.e., mothers (natal experience) either from A. pernyi or D. japonica
had little influence on offspring sex ratios. The second was that the offspring sex ratios
differed for the D. japonica between different orders (F=6.944, df=1, 276, p<0.01), but
were similar for the A. pernyi regardless of the oviposition experience of the maternal
adult (F=1.480, df=1, 276, p=0.225). Moreover, host species (natal) and order (ovipo-
sition experience) interacted in above treatments (F=34.835, df=2, 275, p<0.001), and
the main contributor was D. japonica (F=62.773, df=1, 276 p<0.001).

Discussion

Natal host can influence parasitoid host preference, handling time and sex allocation
behaviour. Morris and Fellowes (2002) speculated that, in part, host size may be judged
by self-reference by the ovipositing female comparing host size with a component of
her own size, such as the time it takes to walk over the surface of the host. However,
we found that despite the fact that females emerging from A. pernyi were significantly
larger than those emerging from D. japonica this had no significant effect of their sub-
sequent sex allocation. We suggest that A. disparis may, therefore, have no self-reference
ability, i.e. it does not judge potential host size by comparing it with its own size.

Influence of natal host and oviposition experience on sex allocation... 37

In theory, the sex (usually female) that benefits most from larger size should be
placed in larger hosts (host quality-dependent sex allocation theory) (Charnov and
Stephens 1988, King and Lee 1994). We found strong support for this hypothesis as,
regardless of whether maternal A. disparis had themselves been reared on A. pernyi or
D. japonica, they all preferred to lay more female offspring in relatively larger host spe-
cies and more male offspring in relatively smaller host species when both host species
were supplied simultaneously. The difference in host size could be judged by direct
comparison using visual and tactile cues.

We also found that sex allocation in A. disparis was affected by oviposition ex-
perience. For instance, the proportion of male offspring emerging from D. japonica
eggs parasitized by females with oviposition experience of A. pernyi eggs, was signifi-
cantly higher than the proportion of males emerging from D. japonica eggs para-
sitized by females that had no oviposition experience. We speculate that females can
judge current host size from oviposition experience of previously parasitized hosts.
If females have laid eggs in A. pernyi eggs, then when they subsequently encounter
D. japonica eggs, the female would compare the host quality (host size) of the D.
japonica eggs with its stored oviposition memory of A. pernyi eggs (Goubault et al.
2004, Papaj and Prokopy 1989), and determine that the D. japonica egg is smaller.
If this is the case, then more male offspring would be laid in the D. japonica eggs if
the host quality-dependent sex allocation theory is correct (Charnov and Stephens
1988, King and Lee 1994). However, we did not find evidence for this when female
parasitoids were first offered D. japonica eggs and then A. pernyi eggs, when the
proportion of male offspring emerging from the A. pernyi eggs was not significantly
different from the proportion of males emerging from A. pernyi eggs that had been
parasitized by females that had no oviposition experience. Therefore, we supposed
that A. pernyi eggs were large enough for the parasitoid to achieve maximum female
progeny in nature.

In conclusion, sex allocation in A. disparis females fitted with the predictions of
condition-dependent sex allocation theory in parasitoids (Trivers and Willard 1973,
West and Sheldon 2002, Lewis et al. 2010). It also provided a nice test of experience
(i.e. context-dependence) in terms of sex allocation: when first presented with eggs
of the larger host, females produced a more male-biased clutch on a patch of the sec-
ond, smaller host eggs; however, when females experienced the small eggs first, the sex
ratios did not shift when they moved to larger hosts. This suggests that information
females obtain from the environment influences their sex allocation. The asymmetry
in response suggests that female-biased sex ratios on the larger host were optimal come
what may, whilst if only presented with the smaller host, female biased sex ratios are
optimal, but in the presence of (or experience of) larger hosts, then more males are
produced in the smaller hosts (Lewis et al. 2010).

Further studies with longer intervals between oviposition on different host species
should be performed to evaluate the effects of learning and memory in this species.

38 Peng-Cheng Liu et al. / Journal of Hymenoptera Research 58: 29-40 (2017)

Acknowledgements

Great thanks to Dr David Shuker for his very constructive suggestions on the manu-
script, especially on the statistical analysis. ‘Thanks also to Professor Yong-An Zhang of
the Chinese Academy of Forestry and Chuan-Zhen Wang of the Yantai Forest Protec-
tion Station for their valuable help. This study was co-supported by grants from the
State Forestry Administration (200904029) and Hebei University (2010-205).

References

Alalouni U, Schadler M, Brandl R (2013) Natural enemies and environmental factors affect-
ing the population dynamics of the gypsy moth. Journal of Applied Entomology 137:
721-738. https://doi.org/10.1111/jen.12072

Baaren JV, Boivin G (1998) Learning affects host discrimination behavior in a parasitoid wasp.
Behavioral Ecology & Sociobiology 42: 9-16. https://doi.org/10.1007/s002650050406

Bennett DM, Hoffmann AA (1998) Effects of size and fluctuating asymmetry on field fitness
of the parasitoid Trichogramma carverae (Hymenoptera: Trichogrammatidae). Journal of
Animal Ecology 67: 580-591. https://doi.org/10.1046/j.1365-2656.1998.00218.x

Charnov EL (1979) The genetical evolution of patterns of sexuality: Darwinian fitness. American
Naturalist 113: 465-480. https://doi.org/10.1086/283407

Charnov EL, Los-den Hartogh RL, Jones WT, van den Assem J (1981) Sex ratio evolution in a
variable environment. Nature 289: 27—33. https://doi.org/10.1038/289027a0

Charnov EL, Stephens DW (1988) On the evolution of host selection in solitary parasitoids.
American Naturalist 132: 707-722. https://doi.org/10.1086/284883

Cortesero AM, Monge JP (1994) Influence of pre-emergence experience on response to host
and host plant odours in the larval parasitoid Eupelmus vuilleti. Entomologia Experimenta-
lis et Applicata 72: 281-288. https://doi.org/10.1111/j.1570-7458.1994.tb01828.x

Crossman SS (1925) Two imported egg parasites of the gipsy moth, Anastatus bifasciatus Fonsc
and Schedius kuvanae Howard. Journal of Agricultural Research 30: 643-675.

Dauphin G, Coquillard P, Colazza S, Peri E, Wajnberg E (2009) Host kairomone learning
and foraging success in an egg parasitoid: a simulation model. Ecological Entomology 34:
193-203. https://doi.org/10.1111/j.1365-2311.2008.01056.x

Dutton AL, Dorn S (2000) Learning used as a strategy for host stage location in an endophytic
host-parasitoid system. Entomologia Experimentalis et Applicata 94: 123-132. https://
doi.org/10.1046/j.1570-7458.2000.00612.x

Ellers J, van Alphen JJM, Sevenster JG (1998) A field study of size-fitness relationships in
the parasitoid Asobara tabida. Journal of Animal Ecology 67: 318-324. https://doi.
org/10.1046/j.1365-2656.1998.00195.x

Gandolfi M, Mattiacci L, Dorn S (2003) Preimaginal learning determines adult response to
chemical stimuli in a parasitic wasp. Proceedings of the Royal Society B Biological Sciences

270: 2623-2629. https://doi.org/10.1098/rspb.2003.2541

Influence of natal host and oviposition experience on sex allocation... ao

Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University
Press, Princeton, NJ.

Goubault M, Krespi L, Boivin G, Poinsot D, Nenon JP, Cortesero AM (2004) Intraspecific
variations in host discrimination behavior in the pupal parasitoid Pachycrepoideus vindem-
miae Rondani (Hymenoptera: Pteromalidae). Environmental Entomology 33: 362-369.
https://doi.org/10.1603/0046-225X-33.2.362

Hastings A, Godfray HCJ (1999) Learning, host fidelity, and the stability of host-parasitoid
communities. American Naturalist 153: 295-301.

Heimpel GE, de Boer JG (2008) Sex determination in the Hymenoptera. Annual Review of
Entomology 53: 209-230. https://doi.org/10.1146/annurev.ento.53.103106.093441
Jervis MA, Ferns PN, Heimpel GE (2003) Body size and the timing of egg production in
parasitoid wasps: a comparative analysis. Functional Ecology 17: 375-383. https://doi.

org/10.1046/j.1365-2435.2003.00742.x

Kazmer DJ, Luck RF (1995) Field tests of the size-fitness hypothesis in the egg parasitoid
Trichogramma pretiosum. Ecology 76: 412-425. https://doi.org/10.2307/1941200

King BH, Charnov EL (1988) Sex-ratio manipulation in response to host size by the parasi-
toid wasp Spalangia cameroni: a laboratory study. Evolution 42: 1190-1198. https://doi.
org/10.1111/j.1558-5646.1988.tb04179.x

King BH, Lee HE (1994) Test of the adaptiveness of sex ratio manipulation in a parasitoid wasp.
Behavioral Ecology and Sociobiology 35: 437-443. https://doi.org/10.1007/BF00165847

Kurir A (1944) Anastatus disparis Ruschka Eiparasit des Lymantria dispar L. Journal of Applied
Entomology 30: 551-586. https://doi.org/10.1111/j.1439-0418.1944.tb00613.x

Lentz AJ, Kester KM (2008) Postemergence experience affects sex ratio allocation in a gregarious insect
parasitoid. Journal of Insect Behavior 21: 34-45. https://doi.org/10.1007/s10905-007-9 102-3

Lewis HM, Tosh CR, O’Keefe S, Shuker DM, West SA, Mayhew PJ (2010) Constraints on adap-
tation: explaining deviation from optimal sex ratio using artificial neural networks. Journal of
Evolutionary Biology 23: 1708-1719. https://doi.org/10.1111/j.1420-9101.2010.02038.x

Li BJ, Lou JX (1992) Preliminary studies on Anastatus disparis (Hymenoptera: Eupelmidae), an
ege parasitoid of gypsy moth. Chinese Journal of Biological Control (3): 144. [In Chinese
with English Summary]

Liu PC, Wei JR, Wang JJ, Liu JX, Dong LJ (2015) Relationship between the environmental
temperatures and development of Anastatus disparis (Ruschka) (Hymenoptera: Eupelmi-
dae) and the sex ratio control of the offspring. Forest pest and disease 34: 9-14. [In Chinese
with English Summary]

Liu PC, Men J, Zhao B, Wei JR. (2017) Fitness-related offspring sex allocation of Anastatus
disparis, a gypsy moth egg parasitoid, on different-sized host species. Entomologia Experi-
mentalis et Applicata 163: 281—286. https://doi.org/10.1111/eea.12579

Morris R, Fellowes M (2002) Learning and natal host influence host preference, handling time
and sex allocation behaviour in a pupal parasitoid. Behavioral Ecology and Sociobiology
51: 386-393. https://doi.org/10.1007/s00265-00 1-0439-x

Napoleon ME, King BH (1999) Offspring sex ratio response to host size in the parasitoid
wasp Spalangia endius. Behavioral Ecology and Sociobiology 46: 325-332. https://doi.
org/10.1007/s002650050626

40 Peng-Cheng Liu et al. / Journal of Hymenoptera Research 58: 29-40 (2017)

Papaj DR, Vet LEM (1990) Odor learning and foraging success in the parasitoid, Leptopilina
heterotoma. Journal of Chemical Ecology 16: 3137-3150. https://doi.org/10.1007/
BF00979616

Papaj DR, Prokopy RJ (1989) Ecological and evolutionary aspects of learning in phytophago-
us insects. Annual Review of Entomology 34: 315-350. https://doi.org/10.1146/annurev.
en.34.010189.001531

Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of
offspring. Science 179: 90-92. https://doi.org/10.1126/science.179.4068.90

Turlings TCJ, Loughrin JH, McCall PJ, Rose USR, Lewis WJ, Tumlinson JH (1995) How
caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proceedings of
the National Academy of Sciences of the United States of America 92: 4169-4174. https://
doi.org/10.1073/pnas.92.10.4169

Vet LEM, Lewis WJ, Cardé RT (1995) Parasitoid foraging and learning. In: Cardé RT, Bell
WJ (Eds) Chemical ecology of insects. Chapman & Hall, New York, 65-101. https://doi.
org/10.1007/978-1-4615-1765-8_3

Vet LEM, Groenewold AW (1990) Semiochemicals and learning in parasitoids. Journal of
Chemical Ecology 16: 3119-3135. https://doi.org/10.1007/BF00979615

Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a com-
parison of initial strategies utilized by larvaphagous and oophagous species. Biological
Control 11: 79-96. https://doi.org/10.1006/bcon.1997.0601

Visser MF (1994) ‘The importance of being large: the relationship between size and fitness in
females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). Journal of Animal
Ecology 6: 963-978. https://doi.org/10.2307/5273

Wang JJ, Liu XB, Zhang YA, Wen C, Wei JR (2014) The reproductive capability of Ooencyrtus
kuvanae reared on eggs of the factitious host Antheraea pernyi. Journal of Applied Entomology
138: 267-272. https://doi.org/10.1111/jen.12080

West SA (2009) Sex allocation. Princeton University Press, Princeton, NJ. https://doi.
org/10.1515/9781400832019

West SA, Sheldon BC (2002) Constraints in the evolution of sex ratio adjustment. Science 295:
1685-1688. https://doi.org/10.1126/science. 1069043

Yan JJ, Xu CH, Gao WC, Li GW, Yao DE Zhang PY (1989) Parasites and predators of forest
pest. China Forestry Publishing House, Beijing, China, 140 pp. [In Chinese]

Yao DE, Yan JJ (1994) ‘The parasitization dynamics of two egg parasites on gypsy moth. Scientia
Silvae Sinicae 30: 334-337.