6urn:lsid:arphahub.com:pub:DE333E49-E4EE-5693-9BEF-D446E6301C98urn:lsid:zoobank.org:pub:55528528-5C97-4D79-A718-8B3D153B37CCJournal of Hymenoptera ResearchJHR1070-94281314-2607Pensoft Publishers10.3897/jhr.58.1276312763Research ArticleChalcidoideaGeneral ecologyAsiaInfluence of natal host and oviposition experience on sex allocation in a solitary egg parasitoid, Anastatusdisparis (Hymenoptera, Eupelmidae)LiuPeng-Cheng12WangJian-Jun3ZhaoBin1MenJin1WeiJian-Rongjrwei9@126.com1The College of Life Science, Hebei University, Baoding City, Hebei Province, ChinaHebei UniversityBaodingChinaThe College of Forestry, Nanjing Forestry University, Nanjing City, Jiangsu Province, ChinaNanjing Forestry UniversityNanjingChinaLiaoning Academy of Forestry Science, Shenyang, Liaoning Province, ChinaLiaoning Academy of Forestry ScienceShenyangChina
201731082017582940FF94FFC4-FF9A-B716-FFCF-FFDCFFE0F039C70246E4-97AE-42E8-9B65-90AA6C654BE48990731803201711072017Peng-Cheng Liu, Jian-Jun Wang, Bin Zhao, Jin Men, Jian-Rong WeiThis 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.http://zoobank.org/C70246E4-97AE-42E8-9B65-90AA6C654BE4
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. Anastatusdisparis Ruschka (Hymenoptera: Eupelmidae) is a solitary egg parasitoid of gypsy moth, Lymantriadispar (L.) (Lepidoptera: Lymantriidae), and several other lepidopteran forest pests. Here, we compared two different sized substitute hosts, the smaller one Dictyoplocajaponica Moore (Lepidoptera: Saturnidae) and the larger one Antheraeapernyi 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.
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
Introduction
Anastatusdisparis Ruschka (Hymenoptera: Eupelmidae) is a solitary egg parasitoid of several noxious lepidopteran forest pests, including the gypsy moth, Lymantriadispar (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 generations on L.dispar eggs annually in Northern China (Yao and Yan 1994). In our previous 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, Antheraeapernyi 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 manipulate 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, Charnov 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 species. 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 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 offspring 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 prefer 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. Two substitute host species of different sizes were evaluated: the smaller was Dictyoplocajaponica Moore (Lepidoptera: Saturnidae) and the larger was Antheraeapernyi Guerin-Meneville (Lepidoptera: Saturnidae).
Material and methodsInsect cultures
Pupae of Antheraeapernyi were purchased from a farmer in Qinglong Manchu Autonomous 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 extraction (see below); Dictyoplocajaponica 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 Anastatusdisparis colony was first established from a population developing 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.
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 replicate eggs were measured for each host species.
Sex allocation by Anastatusdisparis
One large experiment with six treatments was conducted to answer two primary questions, 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 relation 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 Anastatusdisparis 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, between maternal females that were either reared on Antheraeapernyi (treatment 1) or Dictyoplocajaponica (treatment 2) before being offered a choice of eggs from both lepidopteran 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, diameter: 5 cm) containing twenty A.pernyi eggs and twenty D.japonica eggs at 26±0.5 °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 28±0.5 °C until adult parasitoids emerged. The number and sex of offspring 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 maternal 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 species 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 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, diameter: 5 cm) containing twenty A.pernyi or D.japonica eggs (depending on treatment) at 26±0.5 °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 incubated for a further 24 hours at 26±0.5 °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.
Number of maternal replicates for each experimental treatment.
Host species on which the maternal parasitoid had been reared
Sequence of parasitism
First A.pernyi eggs then D.japonica eggs
First D.japonica eggs then A.pernyi eggs
A.pernyi eggs
73 (treatment 3)
77 (treatment 4)
D.japonica eggs
66 (treatment 5)
64 (treatment 6)
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 T-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%.
ResultsSizes of two host species
The eggs of A.pernyi (2.94±0.02 mm) were significantly larger than the eggs of D.japonica (2.31±0.02 mm; t=24.44, df=58, p<0.001).
Sex allocation by A.disparis when offered a choice of eggs from two different lepidopteran 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 offspring emerging from A.pernyi eggs was 9.35±1.87% 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 simultaneously (treatment 2), the results were similar: the proportion of male offspring emerging from A.pernyi eggs was 10.60±2.66% and the proportion emerging from D.japonica eggs was 30.60±7.02%. GLM with univariate analysis showed that offspring sex ratios 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 (Estimate=0.237, Wald Z=7.616, p<0.001).
Proportion of male offspring from maternal A.disparis when simultaneously presented with eggs 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).
https://binary.pensoft.net/fig/152973
The total number of offspring emerging from A.pernyi eggs parasitized by maternal A.disparis from host A.pernyi or D.japonica were 7.27±0.62 and 7.00±0.79, respectively. 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 treatments 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 parasitized host species (F=33.634, df=1, 116, p<0.001).
Sex allocation by A.disparis when the eggs of two different lepidopteran host species 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 (28.02±3.20%) than A.pernyi eggs (7.65±0.65%; 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 (34.37±3.42%) 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±0.93%) compared with the proportion emerging from A.pernyi eggs (8.93±0.93%; t=1.137, df=76, p>0.05).
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 proportion 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 experience 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 (34.37±3.42%; 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).
Proportion of male offspring from female A.disparis with different prior oviposition experience. 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.
https://binary.pensoft.net/fig/152974
When treatments 3-6 were put into a 2×2 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 (oviposition 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 subsequent 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.
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 species 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 experience. For instance, the proportion of male offspring emerging from D.japonica eggs parasitized by females with oviposition experience of A.pernyi eggs, was significantly higher than the proportion of males emerging from D.japonica eggs parasitized 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 second, 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.
Acknowledgements
Great thanks to Dr David Shuker for his very constructive suggestions on the manuscript, 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 Protection Station for their valuable help. This study was co-supported by grants from the State Forestry Administration (200904029) and Hebei University (2010-205).
ReferencesAlalouniUSchädlerMBrandlR (2013) Natural enemies and environmental factors affecting the population dynamics of the gypsy moth.137: 721–738. https://doi.org/10.1111/jen.12072BaarenJVBoivinG (1998) Learning affects host discrimination behavior in a parasitoid wasp.42: 9–16. https://doi.org/10.1007/s002650050406BennettDMHoffmannAA (1998) Effects of size and fluctuating asymmetry on field fitness of the parasitoid Trichogrammacarverae (Hymenoptera: Trichogrammatidae).67: 580–591. https://doi.org/10.1046/j.1365-2656.1998.00218.xCharnovEL (1979) The genetical evolution of patterns of sexuality: Darwinian fitness.113: 465–480. https://doi.org/10.1086/283407CharnovELLos-den HartoghRLJonesWTvan den AssemJ (1981) Sex ratio evolution in a variable environment.289: 27–33. https://doi.org/10.1038/289027a0CharnovELStephensDW (1988) On the evolution of host selection in solitary parasitoids.132: 707–722. https://doi.org/10.1086/284883CorteseroAMMongeJP (1994) Influence of pre-emergence experience on response to host and host plant odours in the larval parasitoid Eupelmusvuilleti.72: 281–288. https://doi.org/10.1111/j.1570-7458.1994.tb01828.xCrossmanSS (1925) Two imported egg parasites of the gipsy moth, Anastatusbifasciatus Fonsc and Schediuskuvanae Howard.30: 643–675.DauphinGCoquillardPColazzaSPeriEWajnbergÉ (2009) Host kairomone learning and foraging success in an egg parasitoid: a simulation model.34: 193–203. https://doi.org/10.1111/j.1365-2311.2008.01056.xDuttonALDornS (2000) Learning used as a strategy for host stage location in an endophytic host-parasitoid system.94: 123–132. https://doi.org/10.1046/j.1570-7458.2000.00612.xEllersJvan AlphenJJMSevensterJG (1998) A field study of size-fitness relationships in the parasitoid Asobaratabida.67: 318–324. https://doi.org/10.1046/j.1365-2656.1998.00195.xGandolfiMMattiacciLDornS (2003) Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp.270: 2623–2629. https://doi.org/10.1098/rspb.2003.2541GodfrayHCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton, NJ.GoubaultMKrespiLBoivinGPoinsotDNenonJPCorteseroAM (2004) Intraspecific variations in host discrimination behavior in the pupal parasitoid Pachycrepoideusvindemmiae Rondani (Hymenoptera: Pteromalidae).33: 362–369. https://doi.org/10.1603/0046-225X-33.2.362HastingsAGodfrayHCJ (1999) Learning, host fidelity, and the stability of host-parasitoid communities.153: 295–301.HeimpelGEde BoerJG (2008) Sex determination in the Hymenoptera.53: 209–230. https://doi.org/10.1146/annurev.ento.53.103106.093441JervisMAFernsPNHeimpelGE (2003) Body size and the timing of egg production in parasitoid wasps: a comparative analysis.17: 375–383. https://doi.org/10.1046/j.1365-2435.2003.00742.xKazmerDJLuckRF (1995) Field tests of the size-fitness hypothesis in the egg parasitoid Trichogrammapretiosum.76: 412–425. https://doi.org/10.2307/1941200KingBHCharnovEL (1988) Sex-ratio manipulation in response to host size by the parasitoid wasp Spalangiacameroni: a laboratory study.42: 1190–1198. https://doi.org/10.1111/j.1558-5646.1988.tb04179.xKingBHLeeHE (1994) Test of the adaptiveness of sex ratio manipulation in a parasitoid wasp.35: 437–443. https://doi.org/10.1007/BF00165847KurirA (1944) Anastatusdisparis Ruschka Eiparasit des Lymantriadispar L.30: 551–586. https://doi.org/10.1111/j.1439-0418.1944.tb00613.xLentzAJKesterKM (2008) Postemergence experience affects sex ratio allocation in a gregarious insect parasitoid.21: 34–45. https://doi.org/10.1007/s10905-007-9102-3LewisHMToshCRO’KeefeSShukerDMWestSAMayhewPJ (2010) Constraints on adaptation: explaining deviation from optimal sex ratio using artificial neural networks.23: 1708–1719. https://doi.org/10.1111/j.1420-9101.2010.02038.xLiBJLouJX (1992) Preliminary studies on Anastatusdisparis (Hymenoptera: Eupelmidae), an egg parasitoid of gypsy moth. Chinese Journal of Biological Control (3): 144. [In Chinese with English Summary]LiuPCWeiJRWangJJLiuJXDongLJ (2015) Relationship between the environmental temperatures and development of Anastatusdisparis (Ruschka) (Hymenoptera: Eupelmidae) and the sex ratio control of the offspring.34: 9–14. [In Chinese with English Summary]LiuPCMenJZhaoBWeiJR. (2017) Fitness-related offspring sex allocation of Anastatusdisparis, a gypsy moth egg parasitoid, on different-sized host species.163: 281–286. https://doi.org/10.1111/eea.12579MorrisRFellowesM (2002) Learning and natal host influence host preference, handling time and sex allocation behaviour in a pupal parasitoid.51: 386–393. https://doi.org/10.1007/s00265-001-0439-xNapoleonMEKingBH (1999) Offspring sex ratio response to host size in the parasitoid wasp Spalangiaendius.46: 325–332. https://doi.org/10.1007/s002650050626PapajDRVetLEM (1990) Odor learning and foraging success in the parasitoid, Leptopilinaheterotoma.16: 3137–3150. https://doi.org/10.1007/BF00979616PapajDRProkopyRJ (1989) Ecological and evolutionary aspects of learning in phytophagous insects.34: 315–350. https://doi.org/10.1146/annurev.en.34.010189.001531TriversRLWillardDE (1973) Natural selection of parental ability to vary the sex ratio of offspring.179: 90–92. https://doi.org/10.1126/science.179.4068.90TurlingsTCJLoughrinJHMcCallPJRoseUSRLewisWJTumlinsonJH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps.92: 4169–4174. https://doi.org/10.1073/pnas.92.10.4169VetLEMLewisWJCardéRT (1995) Parasitoid foraging and learning. In: CardéRTBellWJ (Eds) Chemical ecology of insects., 65–101. https://doi.org/10.1007/978-1-4615-1765-8_3VetLEMGroenewoldAW (1990) Semiochemicals and learning in parasitoids.16: 3119–3135. https://doi.org/10.1007/BF00979615VinsonSB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species.11: 79–96. https://doi.org/10.1006/bcon.1997.0601VisserMF (1994) The importance of being large: the relationship between size and fitness in females of the parasitoid Aphaeretaminuta (Hymenoptera: Braconidae).6: 963–978. https://doi.org/10.2307/5273WangJJLiuXBZhangYAWenCWeiJR (2014) The reproductive capability of Ooencyrtuskuvanae reared on eggs of the factitious host Antheraeapernyi.138: 267–272. https://doi.org/10.1111/jen.12080WestSA (2009) Sex allocation. Princeton University Press, Princeton, NJ. https://doi.org/10.1515/9781400832019WestSASheldonBC (2002) Constraints in the evolution of sex ratio adjustment.295: 1685–1688. https://doi.org/10.1126/science.1069043YanJJXuCHGaoWCLiGWYaoDFZhangPY (1989) China Forestry Publishing House, Beijing, China, 140 pp. [In Chinese]YaoDFYanJJ (1994) The parasitization dynamics of two egg parasites on gypsy moth.30: 334–337.