Entomologia Experimentalis et Applicata90: 61–67, 1999.© 1999Kluwer Academic Publishers. Printed in the Netherlands.

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Host size induced variation in progeny sex ratio of an aphid parasitoidLysiphlebia mirzai

Sharmila Pandey & Rajendra SinghAphid Biocontrol Laboratory, Department of Zoology, DDU Gorakhpur University, Gorakhpur 273 009, India

Accepted: November 3, 1998

Key words: Lysiphlebia mirzai, Rhopalosiphum maidis, sex ratio, host size, biocontrol, aphid, parasitoid,Braconidae, Aphididae

Abstract

A study aimed at determining the effect of host size on the pattern of sex allocation by an aphid parasitoidLysiphlebia mirzaiShuja-Uddin (Hymenoptera: Braconidae: Aphidiinae) was undertaken to test the validity of thefollowing three hypotheses: (1) larger hosts will yield a greater proportion of daughters, (2) differential mortalityof the sexes of the parasitoid during development is a function of host-size, and (3) daughters emerging fromlarger hosts are more fecund. The results suggested a propensity in the parasitoid to deposit fertilised (diploid)eggs in large hosts (third instar nymph) and unfertilised (haploid) eggs in small hosts (first and second instarnymphs). Unpreferred fourth instar nymphs and apterous aphid adults also received more haploid eggs despitebeing larger in size than the preferred third instar nymphs. However, the perception of host size by the motherwas dependent on the extent of temporal variation in the host size distribution and on her previous experience ofhost size. Developmental period, longevity, mating potential, fecundity and progeny sex ratio ofL. mirzaiemergingfrom small versus large hosts indicated that the host size affected the fitness of the daughters more than that of sons.No differential mortality of the sexes during development ofL. mirzai was observed in small versus large hosts.This shows thatL. mirzai, while ovipositing in growing stages of the host, adjusts progeny sex ratio accordingto the host size and by doing so she tends to contribute maximally to progeny fitness without knowing about thefuture host quality.

Introduction

Lysiphlebia mirzaiShuja-Uddin (Hymenoptera: Bra-conidae: Aphidiinae) is a cereal aphid parasitoid andis reported to be a promising biocontrol agent againstpearl-millet aphid,Rhopalosiphum maidis(Fitch) inIndia (Tripathi & Singh, 1990; 1995). It reproducesarrhenotokously, i.e., sons develop from unfertilisedhaploid eggs by parthenogenesis while daughters de-velop from fertilised (diploid) eggs. Thus the female isable to influence the progeny sex ratio (proportion ofmales in the population) at oviposition by regulatingfertilisation of the eggs. Among several factors thatcan affect the progeny sex ratio in aphid parasitoids(Singh & Pandey, 1997), host size has attracted muchattention from theoretical as well as experimental bi-ologists (Charnov et al., 1981; Singh & Pandey, 1986;

King, 1988, 1989, 1990, 1994, 1996; Cloutier et al.,1991; Srivastava & Singh, 1995). The size of aphidhosts varies with age, but an increase in host size (=age) does not necessarily imply the improvement ofhost quality. Mackauer & Kambhampati (1988) andSrivastava & Singh (1995) demonstrated that aphidsize determines the parasitoid size and fitness. Ex-perimental evidence strengthens the prediction of sexratio models reflecting deposition of a greater propor-tion of fertilised eggs in larger hosts. This predictionwas expected only in parasitoids which oviposit innon-growing and non-feeding host stages (idiobioticparasitoids) where the host size is considered to be agood predictor of host resources at the time of ovipo-sition (Nechols & Kikuchi, 1985). However, Wellingset al. (1986) assumed that parasitoids that develop andoviposit inside growing host stages (koinobiotic para-

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sitoids), would not have the skill to assess the host’sfuture quality at oviposition and thus in them, hostsize related progeny sex ratio should not be expected.However, they made a logical error in defending thehypothesis by stating that in order for koinobiotic par-asitoids to evolve manipulation of sex ratio in responseto host size, the female would have to be able to as-sess, at oviposition, the host’s future rate of resourceacquisition. They felt that it was unlikely that koino-bionts would have this knowledge. However, there isno reason that females need this knowledge. Whatis necessary is a consistent relationship between hostsize at oviposition and resources available to the devel-oping parasitoids (King, 1989). Differential mortalityof the male and female progeny during developmentin relation to host size was proposed as an alternativeexplanation for shifts of progeny sex ratio in para-sitoid wasps (Waage, 1986); therefore, the host sizemodel should also include such information. Thereare only few laboratory studies that deal with hostsize related progeny sex ratio in aphid parasitoids. No-table amongst them are those of Cloutier et al. (1991)for Ephedrus californicusBaker, a parasitoid of peaaphid,Acyrthosiphon pisum(Harris) and Srivastava &Singh (1995) forLysiphlebus delhiensis(Subba Rao& Sharma), a parasitoid of corn aphid,Melanaphissacchari (Zehntner). With a view to enhance ourknowledge on this aspect of aphid parasitoid biology,our investigations concerning variation in progeny sexratio of L. mirzaicaused by host size examined (i) theprediction that a greater proportion of daughters willemerge from larger hosts, (ii) the occurrence of dif-ferential mortality of the sexes during development asa function of host size and (iii) the assumption thathost size has a greater positive effect on the fitness(reproductive success) of daughters.

Materials and methods

Colonies of the aphidR. maidisand the parasitoidsL.mirzai were reared in the laboratory on seedlings ofSorghum bicolorpotted in clay pots at 22± 1◦C inscreened (625 mesh/cm2) cages (45× 45× 60 cm)(Tripathi & Singh, 1990) at 16 h photoperiod, 1000–1500 lux light intensity and 60–80% r.h. Only freshlyemerged (0–12 h old) parasitoids fed on a dietary mix-ture consisting of honey, honeydew and water in theratio of 30:30:40 (v/v) were used in the experiments.In trials requiring mated females, each female waspaired with one (virgin) male in a 5 ml glass vial.

All experiments were conducted at the same en-vironmental condition as adopted for maintenance ofhost-parasitoid cultures in the laboratory. The testswere carried out inside cages (similar to those usedin the laboratory cultures) having potted seedlingsof S. bicolor with 4–5 leaves (20–25 days old) toserve as supporting food plants. After their exposureto the parasitoids, the aphids (hosts) were reared onthe food plant until the emergence of the adult par-asitoids (progeny population), which were then sexedand counted and compared with size difference, if any,of the parasitised host. Mortality of the hosts was alsorecorded in relation to such size variation. The dataobtained were expressed as proportion for host accep-tance and progeny sex ratio. The data were subjectedto statistical analyses (e.g., ANOVA or pairedt-test).

A: Effect of host size on the progeny sex ratio of theparasitoid

Test type 1 (no-choice condition).Individual femaleparasitoids were introduced into the cages harbouringapproximately 100 aphid nymphs of either of first, sec-ond, third, fourth instars and apterous adults on thefood plant. After 24 h, the females were removed fromthe cages and were transferred to other cages whereinthey were confined for 4 successive days with freshgroups of similar number of aphids of the same stageoffered per day. Five replicates were performed.

Test type 2 (choice conditions).The layout of the ex-periment and the replications were basically the sameas described above for type 1 with the difference thata single female was given simultaneously access to20 individuals each of first, second, third and fourthinstar aphid nymphs as well as of apterous adults foronly 24 h. Thereafter, the hosts were separated stagewise and were placed gently on the leaves of pottedyoung seedlings ofS. bicolorfor further developmentuntil the emergence of the adult parasitoids.

Test type 3. To separate maternal effects, if any, fromhost-size effect on progeny sex ratio ofL. mirzai, thehost size was categorised into small and large classesfor the ANOVAs. A single female wasp was first re-leased into the cage having 50 small hosts (first instar)on the food plant for only 4 h. Thereafter, the para-sitoid was removed, fed and re-introduced after halfan hour into another cage having 50 large hosts (thirdinstar) on the food plant for another 4 h (Set 1). Areversal in this sequence of parasitoid’s exposure to

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the host constituted Set 2 of this test type. In each ofthese two sets, tests were arranged with five separatefemales of the same parent.

B: Effect of host size on mortality and fitness of maleand female progeny during development

Differential mortality of the sexes was determined bycomparing progeny production of mated versus virginmothers. If there is differential mortality, total progenyproduction will differ, because mated mothers pro-duce both sons and daughters whereas virgin mothersproduce only sons. This test for differential mortalityassumes that mated and virgin mothers parasitise thesame number of hosts (King, 1988). For this purpose,10 mated/virgin females obtained from the same par-ents were individually given access to 100 first or thirdinstar nymphs of the aphids, as described earlier, forparasitisation. Fresh lots of same number and stageof nymphal individuals were provided to each suchfemale at the end of every 24 h till her death. Total de-velopmental period of successfully emerged male andfemale individuals of the parasitoid was determined.

Mating ability of sons as well as fecundity andprogeny sex ratio of daughters that emerged fromdifferent test situations outlined above were also as-sessed. After mating, the sons were removed andallowed to rest for an hour and were then again pairedwith another set of female-sibs. This exercise was re-peated until the sons died. The frequency of each ofthe four possible mating outcomes were noted: (1) sonfrom a small host× daughter from a small host,(2) son from a small host× daughter from a largehost, (3) son from a large host× daughter from asmall host and (4) son from a large host× daughterfrom a large host. Five mated daughters (separatelyfor all four possible crosses of the above experiment)were individually introduced into the cages, each hav-ing a young seedling harbouring approximately 100third instar hosts throughout their life-span to measurefecundity and progeny sex ratio.

The longevity of both sons and daughters resultingfrom the above experiments was also determined for50 individuals of each sex. For this, the adults were putindividually in glass vials (10×150 mm) with a regularfood supply (a mixture of honey, honeydew and waterin the ratio of 3:3:4).

Table 1. Progeny sex ratio ofL. mirzai in smalland large hosts (R. maidis) classified by order ofhost size that was encountered first. Values areexpressed as mean± SE estimated from five ob-servations. Prior to the statistical analysis, datawere arcsine transformed

Host size first Small host Large host

encountered

Small host 0.55± 0.05 0.21± 0.02

Large host 0.77± 0.06 0.29± 0.02

Fsequence 1,17 = 10.94, P< 0.001;

Fhost size1,17 = 74.64, P< 0.001.

Results

A: Effect of host size on progeny sex ratio

In no-choice as well as choice situations, the femaleparasitoidL. mirzaiattacked all the different nymphalinstars and apterous adults irrespective of size varia-tion of the host (Fig. 1). However, third instar nymphswere significantly preferred to first or fourth instarindividuals or apterous adults in both experimental sit-uations. The mothers allocated more daughters intothe third, fourth and second instars than in apterousadult and first instar in both cases (Figure 1). Sig-nificant negative correlations were obtained betweenpercentage of hosts accepted and progeny sex ratio(rno−choice = −0.935∗, rchoice = −0.965∗; ∗P <

0.01).Progeny sex ratio varied significantly when either

small (first instar) or large (third instar) hosts wereexposed first to the naive female for 4 h followed byexposure to large or small hosts for the same duration,respectively (Table 1). Experienced mothers depositedmore fertilised eggs into large hosts when they werepreviously exposed to small hosts. The progeny sexratio was significantly higher in small hosts when themothers were offered large hosts first. This impliesthat the experience of host size gained by the mothersduring the first few ovipositions influences their de-cision for depositing fertilised (female producing) orunfertilised eggs (male producing).

B: Effect of host size on mortality and fitness of maleand female progeny during development

To eliminate any possible maternal effect (genetic orotherwise) on developmental period, mortality of de-

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Figure 1. Host stage preference and progeny sex ratio ofL. mirzai parasitising nymphs belonging to different developmental stages (I toIV instar) or apterous adults (AA) of the hostR. maidiswhen given separately to the female parasitoid for four successive days (no choicecondition) or when offered simultaneously to the female parasitoid during the first 24 h (choice experiments). Mean differences followed bycommon letters (small letters for no choice and capital letters for choice experiments) are not significantly different (P>0.05, Duncan’s multiplerange test, the data were subjected to arcsin transformation before statistical analyses).

velopmental stages of the parasitoid inside the hostand longevity of adult progeny, ANOVA was used foreach sex to separate maternal effects from host-sizeeffects.

The ANOVA does not provide any evidence ofdifferential mortality of progeny individuals belong-ing to either sex as the number of progeny producedby mated females was not significantly different fromthe number produced by virgin females whether givenlarge hosts or small hosts (Table 2). However, all fe-males produced significantly more progeny in largehosts than in small hosts (mated females: 231.6±12.4(SE) progeny in large hosts and 133.2± 9.3 progenyin small hosts,t = 6.34, P< 0.001; virgin females:209.4± 10.5 progeny in large hosts and 127.0± 8.6progeny in small host,t = 6.07, P< 0.001).

Male L. mirzai required the same number of daysto develop in small hosts (13.6± 0.43 (SE) days) asin large hosts (12.6±0.34 days) (F1,98 = 3.67, P>0.05), however, females took significantly longer todevelop in small hosts (15.2 ± 0.43 days) than inlarge hosts (13.0 ± 0.34 days) (F1,98 = 16.34, P< 0.001). Both male and female progeny survivedsignificantly longer when emerged from large hosts(female: 10.2±0.47 days; male: 8.7±0.43 days) thanemerged from small hosts (female: 7.2±0.48 days;male: 6.2± 0.29 days) (Fmale1,98= 23.50, P< 0.001;

Ffemale1,98 = 27.27, P< 0.001). Daughters survivedsignificantly longer than sons only when they emergedfrom large hosts (t = 3.23, P< 0.01).

Irrespective of host size from which malesemerged, their mating ability with female-sibs emerg-ing from small hosts did not significantly vary (Ta-ble 3). However, the number of successful matingswith the female-sibs that had emerged from large hostsincreased significantly.

Although, both sons and daughters were largerwhen they developed on large hosts, the host size sig-nificantly influenced only the size of daughters (1.70±0.02 mm emerged from small hosts; 2.01± 0.04 mmemerged from large hosts;F1,9 = 65.97, P< 0.001)and not the sons which were always smaller (1.58±0.19 mm emerged from small hosts; 1.64±0.03 mmemerged from large hosts;F1,9 = 3.65, P> 0.05).

The size of the host significantly affected the fe-cundity of the progeny ofL. mirzai. Females devel-oped in small hosts were smaller and yielded fewerprogeny than those developed in large hosts (109.4±11.2 (SE) progeny/female in small hosts, 231.2±18.3progeny/female in large hosts,t = 5.68, P< 0.01)and the progeny sex ratio was significantly higher forthose mothers that developed in small hosts than inlarge hosts (0.44± 0.03 in small hosts, 0.32± 0.02 inlarge hosts,t = 3.19, P< 0.02).

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Table 2. Analysis of variance of the number of progeny produced byvirgin and mated females and progeny sex ratio ofL. mirzai∗ parasitis-ing small or large hosts (R. maidis). ∗ Females emerged from largehosts.

Source of variation d.f. MS F Significance

A: Number of progeny

Host size 1 81721.6 70.38 P< 0.001

Maternal identity 1 2016.4 1.74 P> 0.05

(mated/virgin)

Error 37 1161.0

B: Progeny sex ratio

Host size 1 0.154 15.02 P< 0.001

Maternal identity 1 3.091 302.02 P< 0.001

(mated/virgin)

Error 37 0.010

Table 3. Effect of host size on mating ability of the progeny ofL. mirzai. Valuesare expressed as mean± SE estimated from five observations.

Size of the host Number of mating successes of males emerged from

from which female Small host Large host t-values

progeny emerged

Small 4.2± 0.5 6.4± 0.9 2.27 NS

Large 13.6± 1.4 20.0± 1.5 3.11∗t-values 6.30∗ 7.93∗

∗ P<0.02; NS = Non-significant

Discussion

Aphids are patchily distributed on their food plantsand all developmental stages are simultaneouslypresent in various proportions. Therefore, during hostsearching a female parasitoid encounters all thesestages. Like other aphid parasitoids,L. mirzai prefersthird instar nymphs as host (Tripathi & Singh, 1995).Despite being a koinobiont, host size at oviposi-tion still seems to affect the progeny sex ratio ofthis parasitoid since a higher proportion of femaleswas observed emerging from large hosts (third in-star nymphs). This is consistent with the observationsmade for other aphid parasitoids (Cloutier et al., 1981,1991; Singh & Pandey, 1986; Srivastava & Singh,1995) and is at variance with the hypothesis of Waage(1986) which postulates absence of any relationshipbetween host size and progeny sex ratio in koino-biotic parasitoids. Further, it supports the host sizemodel of Charnov et al. (1981) for idiobiotic para-

sitoids wherein a lower progeny sex ratio in large hostsis predicted. But presence of fewer fertilised eggs inmuch larger fourth instar nymphs and apterous adultssuggests that host size alone does not determine thedecision of this parasitoid to deposit diploid or hap-loid eggs. Other qualities (maximum life expectancy,least physiological immunity as well as behaviouraldefence and greatest potential for parasitoid growth)of the host stage irrespective of its size, as reported bySrivastava & Singh (1995) might have contributed tothe preference for third instar nymphs. Emergence ofmore sons from simultaneously offered first, second,fourth instar and apterous adults demonstrated that theperception of host size byL. mirzai is not absolute.Similar observations were reported by Srivastava &Singh (1995) in the case ofL. delhiensis. Cloutieret al. (1991) and Srivastava & Singh (1995) statedthat previous host size experience of the females in-fluenced distribution of sons/daughters in the progenyof aphid parasitoids. This implies that host size per-

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ception by femaleL. mirzai is a temporally- and anexperience-related phenomenon.

The fitness of the progeny is generally measuredby its development time, larval and progeny survival,progeny size, mating ability, fecundity and progenysex ratio. The faster development of daughters in largehosts decreases generation time (T ) which is inverselyrelated with the growth rate (rm) of the parasitoid pop-ulation [T = Ro/rm, whereRo =net fecundity rateof the parasitoid (total female progeny per female)and rm =intrinsic rate of natural increase] (Tripathi& Singh, 1990). If the value ofRo of a parasitoidis constant, any decrease in generation time will in-crease the value of its growth rate and thus enhanceits fitness. The shorter development time may also re-duce the time it is vulnerable to hyperparasitism orto other causes of mortality. InL. mirzai, as withother aphid parasitoids (Mackauer, 1986; Srivastava &Singh, 1995), daughters developed faster in large hoststhan in small hosts. However, the sons and daughtersdevelop approximately at the same rate in large hosts.Early emergence of sons in small hosts is an addedadvantage for the parasitoid in preventing ovipositionby virgin females (Biswas & Singh, 1995).

The longevity of the progeny of both sexes ofL.mirzai was significantly less if they emerged fromsmall hosts. These findings agree with Wellings et al.(1986) and Srivastava & Singh (1995) but differ fromCloutier et al. (1991). The mating success of maleL.mirzai with female-sibs emerging from large hosts isgreater than that of those emerging from small hosts.Such an effect of host size on the mating ability ofmales in other koinobionts has been shown by van denAssem (1976), Charnov et al. (1981) and Srivastava& Singh (1995). A similar effect of host size was alsoobserved on the fecundity of females. The results thusdemonstrate that host size had a greater effect on thereproductive success of females than on that of males.

Differential mortality of the sexes in hosts of dif-ferent size has usually been proposed as an alternativeexplanation causing shifts in progeny sex ratio. As inother studies (Kraaijeveld & van Alphen, 1986; King,1988, 1990), the present study could not provide anyevidence of differential mortality of either sex ofL.mirzai in small versus large hosts. The absence of dif-ferential mortality clearly shows that while ovipositingin the growing stages of an aphid,L. mirzai doesexhibit maternal manipulation of progeny sex ratio ac-cording to the host size. However, the significance ofthe host size model goes beyond understanding the sexratio in aphidiine parasitoids because it is only a part

of the more general phenomenon of a facultative sexratio in response to environmental conditions (Singh& Pandey, 1997). However, such information is nec-essary for maximising the number of potential femalesin mass-cultures for releases as well as for laboratoryuse. The significance of the present study is that, al-though the host size model predicts progeny sex ratioin relation to host size in mostly idiobiotic parasitoids,L. mirzai, being a koinobiont, is also able to responddifferentially to host size for sex allocation.

Acknowledgements

The authors are thankful to Prof. R. A. Agarwal, Headof the Department of Zoology, DDU Gorakhpur Uni-versity for providing necessary facilities; to Prof. S. S.Krishna, Entomological Research Institute, LoyolaCollege, Chennai for critical suggestions and linguis-tic improvement and to CSIR, New Delhi for financialassistance (Project No. 37(0853)/94/EMR-II).

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