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University of Zurich

Zurich Open Repository and Archive

Winterthurerstr. 190 CH-8057 Zurich http://www.zora.uzh.ch

Year: 2008

Limited scope for maternal effects in aphid defence against

parasitoids

Vorburger, C; Gegenschatz, S E; Ranieri, G; Rodriguez, P

Vorburger, C; Gegenschatz, S E; Ranieri, G; Rodriguez, P (2008). Limited scope for maternal effects in aphid defence against parasitoids. Ecological Entomology, 33(2):189-196.

Postprint available at: http://www.zora.uzh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch

Originally published at:

Ecological Entomology 2008, 33(2):189-196.

Vorburger, C; Gegenschatz, S E; Ranieri, G; Rodriguez, P (2008). Limited scope for maternal effects in aphid defence against parasitoids. Ecological Entomology, 33(2):189-196.

Postprint available at: http://www.zora.uzh.ch

Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch

(2)

Limited scope for maternal effects in aphid defence against

parasitoids

Abstract

1. A mother's environment frequently affects her offspring's phenotype. Such maternal effects may be adaptive, in particular with respect to pathogens or parasites, for example if maternal exposure increases offspring resistance. 2. In aphids, maternal effects are likely to occur as a result of their telescoping generations. This study investigated whether maternal effects influence the susceptibility of the

peach-potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), to its parasitoid Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiinae). 3. In a first experiment, susceptibility was

compared among offspring of aphid mothers that had either no contact to parasitoids, had contact but were not attacked, or were attacked but not mummified. Mothers from the last group had successfully resisted the parasitoid. 4. In a second experiment using two different clones, maternal and progeny environment were manipulated by rearing each generation either on a benign (radish) or a more stressful host plant (silver beet) before progeny exposure to parasitoids. 5. The first experiment revealed no significant effect of the maternal treatment on offspring susceptibility to parasitoids and thus no evidence for trans-generational defence. In the second experiment, maternal environment effects were also weak, yet with a trend towards less susceptible offspring of aphid mothers reared on the more stressful plant. However, there was a significant difference among clones and a strong clone × progeny host plant interaction, illustrating that the outcome of a parasitoid attack may be determined by a complex interplay of genetic and environmental factors. 6. Overall, the results suggest that there is limited scope for maternal effects in aphid defence against parasitoids.

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Limited scope for maternal effects in aphid defence against parasitoids

CHRISTOPH VORBURGER1,SILVAN E.GEGENSCHATZ2,GIULIA RANIERI3&PAULA RODRIGUEZ4

Institute of Zoology, University of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland

Running title: Maternal effects on resistance to parasitoids

1Correspondence: Dr. Christoph Vorburger, Institute of Zoology, University of Zürich,

Winterthurerstrasse 190, 8057 Zürich, Switzerland. E-mail: [email protected]

2Present address: SVS Naturschutzzentrum Neeracherried, Postfach, 8173 Neerach,

Switzerland

3Present address: University Hospital Zürich, Dermatology, Gloriastrasse 31, 8091 Zürich,

Switzerland

4Present address: Institute of Systematic Botany, University of Zürich, Zollikerstrasse 107,

(4)

Abstract. 1. A mother's environment frequently affects her offspring's phenotype. Such 1

maternal effects may be adaptive, in particular with respect to pathogens or parasites, e.g. if 2

maternal exposure increases offspring resistance. 3

2. In aphids, maternal effects are likely to occur due to their telescoping generations. 4

This study investigated whether maternal effects influence the susceptibility of the peach-5

potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), to its parasitoid Diaeretiella

6

rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiinae). 7

3. In a first experiment, susceptibility was compared among offspring of aphid mothers 8

that had either no contact to parasitoids, had contact but were not attacked, or were attacked 9

but not mummified. Mothers from the last group had successfully resisted the parasitoid. 10

4. In a second experiment using two different clones, maternal and progeny environment 11

were manipulated by rearing each generation either on a benign (radish) or a more stressful 12

host plant (silver beet) before progeny exposure to parasitoids. 13

5. The first experiment revealed no significant effect of the maternal treatment on 14

offspring susceptibility to parasitoids and thus no evidence for trans-generational defence. In 15

the second experiment, maternal environment effects were also weak, yet with a trend towards 16

less suceptible offspring of aphid mothers reared on the more stressful plant. However, there 17

was a significant difference among clones and a strong clone × progeny host plant interaction, 18

illustrating that the outcome of a parasitoid attack may be determined by a complex interplay 19

of genetic and environmental factors. 20

6. Overall, the results suggest that there is limited scope for maternal effects in aphid 21

defence against parasitoids. 22

23

Keywords.Diaeretiella rapae, host plant, maternal effects, Myzus persicae, obligate 24

parthenogenesis, parasitoids, resistance, trans-generational defence 25

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Introduction

26 27

The environment a mother experiences often affects her offsprings' phenotype. Such 28

environmental maternal effects have also been termed 'trans-generational phenotypic 29

plasticity' (Mousseau & Dingle, 1991). Although it is not always easy to distinguish between 30

adaptive and nonadaptive plasticity (Gotthard & Nylin, 1995), some adaptive maternal effects 31

undoubtedly exist. Adaptive maternal effects are expected to evolve when the mother's 32

environment provides reliable cues about the progeny's environment (Mousseau & Fox, 33

1998). In aphids, maternal or even grand-maternal effects are particularly likely to occur 34

because they exhibit telescoping of generations. During the parthenogenetic phase of the 35

aphid life-cycle, the viviparous females bear developing embryos which themselves already 36

contain embryos. Any physiological response of a mother to her environment will thus be 37

directly experienced by her daughters or even grand-daughters. Indeed, the induction of 38

winged progeny in response to maternal crowding is one of the textbook examples of an 39

adaptive maternal effect (Dixon, 1977). 40

Other environmental challenges against which maternal effects may provide large benefits 41

are natural enemies like predators, parasites or pathogens. A nice example with respect to 42

predators is provided by the trans-generational induction of helmet formation in the water flea 43

Daphnia cucullata (Sars). Triggered by kairomones, these water fleas grow helmets as an 44

induced defence against predators, which in turn leads to the production of helmeted and thus 45

better protected offspring via a maternal effect (Agrawal et al., 1999). With respect to 46

pathogens, it is known that vertebrates can transfer acquired immune factors like antibodies to 47

offspring and thereby reduce their susceptibility to disease (Grindstaff et al., 2003). In 48

invertebrates, which have long been assumed to lack any adaptive or specific immunity, such 49

transgenerational defences have only recently been demonstrated. Examples include increased 50

(6)

antimicrobial activity in offspring of immune-challenged mothers in bumblebees and 51

mealworm beetles (Moret, 2006; Sadd et al., 2005), and even the maternal transfer of strain-52

specific immunity against a pathogenic bacterium in waterfleas (Little et al., 2003). 53

Apart from exposure to parasites or pathogens, the nutritional quality of the maternal 54

environment may also affect offspring susceptibility. Mitchell and Read (2005) showed that 55

in Daphnia magna (Straus), offspring produced by mothers in crowded conditions with low 56

food availability were more resistant to parasites than offspring produced under good 57

conditions. This maternal effect may well be adaptive (exposure to parasites tends to increase 58

with crowding), although this is yet to be demonstrated. 59

In aphid populations, substantial mortality is caused by parasitoids, which may even be 60

their most important natural enemies (Schmidt et al., 2003). A number of studies have shown 61

that aphid populations exhibit clonal variation for the susceptibility to parasitoids, e.g. in the 62

pea aphid, Acyrthosiphon pisum (Harris) (Henter & Via, 1995), and in the peach-potato aphid, 63

Myzus persicae (von Burg et al., in press). The mechanisms with which the aphid immune 64

system attacks parasitoid eggs or larvae are poorly understood and appear to be distinct from 65

the well-known encapsulation response employed by many other insects (Henter & Via, 66

1995). It is known that aphid susceptibility to parasitoids may be strongly reduced if the 67

aphids harbour certain facultative endosymbiotic bacteria (Oliver et al., 2003). What is not 68

known is whether susceptibility to parasitoids is also influenced by maternal environmental 69

effects in aphids. Given that transgenerational defences would seem highly beneficial and – 70

due to the telescoping of generations – could evolve easily in aphids, this study tested for the 71

presence of maternal effects on resistance to parasitoids in M. persicae. Two questions were 72

addressed: (1) Do offspring of aphid mothers that successfully defended themselves against a 73

parasitoid exhibit increased resistance? (2) Does the quality of the maternal environment (here 74

manipulated by different host plants) affect offspring resistance? 75

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Material and methods 76 77 Study organisms 78 79

The peach-potato aphid, Myzus persicae, is an economically important pest with a 80

worldwide distribution. Cyclical parthenogens of this polyphagous species are host-81

alternating between the primary host peach (Prunus persica L.) and a large number of 82

secondary host plants belonging to > 40 families (Blackman & Eastop, 2000). However, in 83

mild temperate and warmer climate zones, M. persicae reproduces predominantly by obligate 84

parthenogenesis and is thus independent of its primary host (Blackman, 1974; Vorburger et 85

al., 2003a). In the present study, three clones of M. persicae were used, one from Switzerland 86

and two from Australia (Table 1). They differ in their microsatellite multilocus genotypes 87

(Table 1), which were reconfirmed before the start of the experiments. None of these three 88

clones harbours any of the endosymbiotic bacteria known to affect resistance to parasitoids 89

(unpublished data). The two Australian clones have been used in a number of previous studies 90

on life-history variation (Vorburger, 2005), host specialization (Vorburger & Ramsauer, in 91

press), and the quantitative genetics of resistance against parasitoids (von Burg et al., in 92

press). Since their collection, clones of M. persicae have been maintained on seedlings of 93

either radish (Raphanus sativus) or cabbage (Brassica oleracea). They grow in 0.072 l plastic 94

pots fitted with cages made of perspex plastic tubes that have one end covered with fine 95

gauze. Colonies are maintained in plant growth chambers at 20 °C and a 16 h photoperiod 96

with a light intensity of approx. 550 µmolm-2s-1. The long photoperiod ensures continuous 97

apomictic parthenogenesis. The same standard rearing conditions were also used for both 98

experiments reported below. 99

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The solitary koinobiont endoparasitoid Diaeretiella rapae is an important natural enemy of 100

M. persicae (e.g. Kavallieratos et al., 2004; e.g. Starý, 1970). After oviposition of a single egg 101

into aphid nymphs, the larva develops inside the living aphid, eventually killing its host and 102

pupating inside its dried remains. This forms a characteristic mummy from which the adult 103

wasp emerges after metamorphosis. The parasitoids used in this study were kindly provided 104

by Martin Torrance from IACR Rothamstead, UK, from a laboratory colony founded with 105

wasps from two sites in England. At the University of Zürich they are maintained as a large 106

cage population on Swiss clones of M. persicae. 107

108

Experiment 1: Effect of maternal exposure to parasitoids

109 110

This experiment was designed to test whether offspring of aphid mothers that successfully 111

defended themselves against a parasitoid (i.e. aphids that suffered oviposition by the 112

parasitoid but were not mummified) are better defended against the same parasitoid than 113

offspring of mothers that were not attacked. Because it is feasible that the perceived risk of 114

parasitism alone might trigger an increased defence ability, a third treatment was included in 115

which aphids were not attacked but had contact with parasitoids. In this treatment, aphids had 116

the possibility to detect the presence of parasitoids either directly or via alarm signals of their 117

clone mates. 118

The experiment was started with a total of 490 four-day-old nymphs of a single Swiss 119

clone (Mp5) of M. persicae. In groups of 11-15 individuals, these nymphs were placed in 120

Petri dishes of 3.5 cm diameter. A single female of D. rapae was then added and the dishes 121

were continuously monitored. When oviposition by the parasitoid was observed, the attacked 122

aphid was immediately removed and assigned to the 'parasitised' treatment. After 123

approximately two thirds of the aphid nymphs had been attacked and removed from the dish, 124

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the wasp was also removed and the remaining aphids were assigned to the 'contact' treatment. 125

To account for possible effects of handling and time off the host plant, the nymphs assigned 126

to the 'control' treatment were also placed in Petri dishes for the same time as parasitoid 127

exposures lasted, yet without parasitoid contact. After the nymphs had been subject to their 128

respective treatments, they were reared on radish seedlings (five individuals per seedling) 129

until the mummies in the 'parasitized' treatment were clearly visible. At this time, surviving 130

aphids from all three treatments were adult and reproducing. From these adults the mothers 131

for the next generation were haphazardly selected and caged in groups of four individuals on 132

new seedlings, where they were allowed to reproduce for 24 h and then discarded. This 133

procedure produced batches of offspring of similar age on individual seedlings that 134

represented the replicates for testing offspring susceptibility to parasitoids. The number of 135

offspring produced per female served as an estimate of fecundity for aphid mothers from the 136

three treatments. When they were between 72 and 96 h old, the nymphs on each seedling were 137

exposed to parasitoids. Two female D. rapae were added to each cage, allowed to attack the 138

aphids for 5 h and then removed. The same assay was successfully used by von Burg et al. (in 139

press) and proved sensitive enough to detect clonal variation in susceptibility. Nine days after 140

exposure to parasitoids, when mummies were clearly visible, the number of mummified and 141

surviving aphids was determined on each plant. 142

Due to non-homogeneous error variances, the fecundity of aphid mothers from the three 143

treatments was compared with a non-parametric Kruskal-Wallis test. To compare the 144

susceptibility of their offspring to parasitoids, the proportion of individuals mummified was 145

analysed using a generalised linear model with the logit link function and – due to 146

overdispersion – quasibinomial errors in R 2.3.1 (R Development Core Team, 2006). Apart 147

from the treatment effect, the number of nymphs exposed to parasitoids was included as a 148

covariate to account for unequal numbers of individuals among replicates. Following the 149

(10)

recommendation of Crawley (2005) for quasibinomial fits, F-tests rather than χ2-tests were 150

used to compare models with and without the effects to be tested. The same analysis was also 151

applied to the proportion of aphids surviving. The proportion mummified and the proportion 152

surviving do not necessarily add up to 1 because some aphids simply died after exposure to 153

parasitoids without getting mummified. 154

155

Experiment 2: Effect of maternal host plant

156 157

This experiment tested whether the maternal host plant and the host plant on which 158

progeny are reared affect the susceptibility of M. persicae to the parasitoid D. rapae. The two 159

host plants used were radish (Raphanus sativus, var. 'Eiszapfen'), a very benign host for M.

160

persicae (Vorburger et al., 2003b), and silver beet (Beta vulgaris, var. 'Grüner Schnitt'), a 161

more challenging host on which the reproductive rate of M. persicae is much reduced 162

compared to radish (C. Vorburger, personal observation). For this experiment, two Australian 163

clones of M. persicae were used (6.21 and 7.10, see Table 1). These clones were chosen 164

because they were shown to differ in their susceptibility to D. rapae in a previous study 165

comparing a total of 17 clones (von Burg et al., in press) and thus served as an internal control 166

that the experimental protocol indeed allowed the detection of known differences. 167

For the maternal generation, each clone was split into 30 replicate lines, 15 on radish and 168

15 on silver beet. Lines were started by placing three adult female aphids on a seedling of the 169

respective plant, where they were allowed to reproduce for two days and then discarded. The 170

resulting cohorts of offspring represented the maternal generation of the experiment. When 171

the maternal generation reached adult ecdysis and started to reproduce, each maternal line was 172

split into two progeny lines, one on radish and one on silver beet. This procedure created 60 173

progeny lines for each clone comprising 15 replicates of the four combinations of maternal 174

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host plant/progeny host plant: radish/radish, radish/silver beet, silver beet/radish, and silver 175

beet/silver beet. To start the progeny generation, either five (when mothers were reared on 176

radish) or ten adults (when mothers were reared on silver beet) were placed on seedlings and 177

allowed to reproduce for 24 h. The different numbers were used to compensate for the lower 178

fecundity of aphid mothers reared on silver beet in order to obtain similar-sized progeny 179

cohorts for exposure to parasitoids. However, for some replicates fewer than ten mothers from 180

silver beet were available. It is unlikely that the different numbers of aphid mothers markedly 181

affected host plant condition. Even ten individuals are a minor challenge to the plants and 182

they only remained on the plants for 24 h. After their removal from the seedlings, aphid 183

mothers were weighed to the nearest microgram on a Mettler MX5 microbalance and their 184

progeny were counted to assess the effect of the maternal host plant on fecundity and body 185

size. When the progeny were between three and four days old, they were exposed to D. rapae

186

in the same way as in experiment 1, i.e. to two female wasps for 5 h. Due to time constraints 187

these exposures were split over three consecutive days (= experimental blocks, five replicates 188

of each treatment combination per block). Nine days after exposure to parasitoids, when 189

mummies were clearly visible, the number of mummified and surviving aphids was counted. 190

Two variables were measured to assess the condition of the maternal generation aphids: 191

body size (adult mass) and daily fecundity (offspring produced per mother within 24 h). Adult 192

mass was analysed with an ANOVA, testing for the effects of block, host plant, clone, and the 193

host × clone interaction. Because the two clones were deliberately chosen to represent 194

different levels of resistance, clone was treated as a fixed effect like all the other factors. 195

Daily fecundity was analysed with ANOVA as well, but the model also included the progeny 196

host plant (and its interactions with other factors), since aphid mothers reared on either 197

maternal host were transferred to both progeny hosts to produce the experimental cohorts of 198

offspring. Their susceptibility to D. rapae (i.e. the proportion mummified) was again analysed 199

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using a generalised linear model with logit link and quasibinomial errors, testing for the 200

effects of block, maternal host, progeny host and clone, as well as their interactions. The 201

number of offspring exposed did not contribute to the variation in mummification in this 202

experiment (F1, 114 = 0.519, P = 0.472) and was therefore omitted from the model. The same

203

analysis was repeated for the proportion of aphids surviving. 204 205 Results 206 207 Experiment 1 208 209

Out of 311 nymphs that were observed to be stung by parasitoids (the 'parasitised' 210

treatment), 86 (27.7%) died before mummies were visible, 112 (36.0%) were mummified, and 211

113 (36.3%) survived. In the control treatment, 19 out of 85 individuals died (22.4%) within 212

the same time, and 13 out of 94 individuals died in the 'contact' treatment (13.8 %). A single 213

individual from the 'contact' treatment was mummified, thus one oviposition event in the Petri 214

dish must have escaped our notice. Mortality did not differ significantly between the 'contact' 215

and 'control' treatments (χ21 = 2.21, P = 0.137), but the mortality in these two treatments was

216

lower than the mortality that occurred in addition to mummification in the 'parasitised' 217

treatment (χ21 = 5.94, P = 0.015).

218

A comparison of the number of offspring produced within 24 h by the surviving females 219

revealed a significant difference between the three treatments (Kruskal-Wallis test, P < 220

0.001), showing that parasitoid attack also had a negative effect on the fecundity of the 221

surviving aphids (Fig. 1). On average, females from the 'control' and 'contact' treatments 222

produced almost two offspring more per day than females that had survived a parasitoid 223

attack. However, the maternal treatments had no significant effect on their offsprings' 224

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susceptibility to parasitoids. The proportion of individuals mummified tended to decrease 225

with the number of nymphs exposed to the parasitoids (F1, 55 = 3.376, P = 0.072), but it did

226

not differ significantly among treatments (F2, 55 = 0.783, P = 0.462) (Fig. 2). The analysis of

227

the proportion of individuals surviving mirrored that of the proportion mummified: survival 228

increased non-significantly with the number of nymphs exposed (F1, 55 = 2.992, P = 0.089),

229

but did not differ among treatments (F2, 55 = 0.258, P = 0.773).

230 231

Experiment 2

232 233

The host plant on which they were reared had strong effects on the body size and fecundity 234

of the maternal-generation aphids. Individuals grown on radish were substantially heavier 235

(Fig. 3, Table 2), yet there was no significant difference among the two clones and no 236

interaction between host plant and clone (Table 2). In accordance with their larger body size, 237

aphids reared on radish were also more fecund (Fig. 4). Apart from this highly significant 238

effect of maternal host, there was also a significant effect of progeny host (Table 3), i.e. the 239

host to which aphid mothers were transferred to produce the cohort of progeny used for assays 240

of parasitoid resistance. Aphid mothers reared on either host produced more offspring on 241

radish (Fig. 4). The fecundity of the two clones was not significantly different, nor were there 242

any significant interaction effects (Table 3). 243

Despite the fact that host plants had strong effects on the condition of their mothers, this 244

did not translate into a significant maternal effect on the offspring's susceptibility to the 245

parasitoid D. rapae. Offspring of aphid mothers reared on radish were mummified at slightly 246

higher rates than offspring of mothers reared on silver beet (Fig. 5), but this difference was 247

not significant (Table 4). As expected from previous data (von Burg et al., in press), there was 248

a highly significant difference among clones (Table 4), with clone 7.10 being mummified at a 249

(14)

higher proportion than clone 6.21 (Fig. 5). Interestingly, there was also a significant clone ×

250

progeny host interaction (Table 4), mainly reflecting the fact that clone 6.21 suffered from 251

higher rates of mummification when progeny developed on radish, whereas a similar 252

difference was not evident for clone 7.10 (Fig. 5). 253

The analysis of the proportion of aphids surviving gave similar results, but in this case did 254

reveal a significant effect of the maternal environment (Table 4). On average, more offspring 255

of aphid mothers reared on silver beet survived than offspring of mothers reared on radish 256

(Fig. 5). Again, there was a significant difference among clones and a significant clone ×

257

progeny host interaction (Table 4). 258

259

Discussion

260 261

This study reports two experiments testing for maternal effects on aphid susceptibility to 262

parasitoids. The main finding of the first experiment is that offspring of aphid mothers that 263

have successfully defended themselves against parasitoids are not better defended against the 264

same parasitoids than offspring of mothers that have not been attacked. This implies that 265

trans-generational immune priming, which has been shown to improve offspring resistance to 266

microbial pathogens in some insects and crustaceans (Little et al., 2003; Moret, 2006; Sadd et 267

al., 2005), is unlikely to play an important role in aphid defence against parasitoids. 268

A potential problem with this experiment is that parasitoid attacks may not always be 269

successful and result in oviposition. Maternal-generation aphids were assigned to the 270

'parasitised' treatment based on one observed parasitoid attack. If these aphids survived not 271

because they successfully prevented the parasitoid's development, but because no egg had 272

been present in the first place, the lack of a maternal effect on offspring resistance would be a 273

trivial outcome. However, a study on the aphid parasitoid Aphidius ervi showed that after a 274

(15)

single attack, the difficult-to-find eggs could be recovered from more than 90% of the aphids 275

(Bensadia et al., 2006), indicating that oviposition attempts are rarely unsuccessful. In the 276

present experiment, 36.3% of the maternal-generation aphids survived the observed parasitoid 277

attack, suggesting that at least a large fraction of aphid mothers from the 'parasitised' 278

treatment had indeed successfully prevented parasitoid development. 279

The observed lack of a trans-generational defence against parasitoids is somewhat 280

unexpected for two reasons. Firstly, it would seem that mechanisms to convey trans-281

generational defence could evolve easily in aphids due to the telescoping of generations. 282

Secondly, the benefits of trans-generational defence would appear to be large in aphids 283

because the relatedness between a mother and her clonal daughter is 1, and because being 284

attacked by a parasitoid should be a reliable indicator of the risk of parasitism for the 285

offspring. This is because female parasitoids start ovipositing very soon upon hatching from 286

the mummy, often within the same aphid colony from which they emerged (C. Vorburger, 287

personal observation). It will be interesting to see whether future studies on other aphids will 288

also fail to find evidence for trans-generational defence against parasitoids, and if yes, to find 289

out what it is that prevents the evolution of what would seem to be a highly beneficial trait. 290

As a side result, this experiment has shown very clearly that even if an aphid is able to 291

prevent parasitoid development, the attack alone has substantial costs in terms of reduced 292

fecundity. This is likely to be a consequence of parasitoid-derived agents for host regulation 293

that are injected at oviposition, like venom proteins (reviewed in Beckage & Gelman, 2004). 294

Possibly, being attacked compromises not only on the number of offspring a female can still 295

produce, but also their physical condition. Speculatively, this could be put forward as an 296

explanation why offspring of attacked mothers did not show increased resistance. 297

The outcome of the second experiment was less straightforward. The data on maternal 298

mass and fecundity clearly showed that creating a benign and a stressful environment by 299

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manipulating the host plant was successful, yet there was at most a weak effect of the 300

maternal host plant on the proportion of offspring mummified by D. rapae. Offspring of aphid 301

mothers reared on silver beet suffering slightly lower rates of mummification. On the other 302

hand, there was a significant effect of the maternal host plant on offspring survival, apparently 303

because more offspring of mothers reared on radish died without being mummified (Fig. 5). 304

Insofar as some of the mortality on top of mummification is likely to also result from 305

parasitoid attacks (see Experiment 1), this significant difference in survival could cautiously 306

be interpreted as a maternal environmental effect on susceptibility to parasitoids, even though 307

the evidence from rates of mummification is at best suggestive. It is interesting to note that 308

the direction of the effect is consistent with that found in Daphnia by Mitchell and Read 309

(2005): it is the more stressful and not the more benign maternal environment that decreases 310

offspring susceptibility. In the case of Daphnia, it was proposed that this effect may occur 311

because mothers reared under poor conditions shift investment from offspring quantity to 312

offspring quality to produce larger, better provisioned offspring, which in turn may be better 313

able to resist pathogens (Mitchell & Read, 2005). In the case of aphids, this kind of 314

explanation is unlikely to apply because mothers reared on challenging host plants produce 315

much smaller offspring than mothers reared on benign hosts (Vorburger & Ramsauer, in 316

press). 317

Unlike the study by Mitchell and Read (2005) on Daphnia, where a benign progeny 318

environment resulted in reduced rates of infection, the present study revealed no consistent 319

effect of the progeny environment on mummification. Instead, the effect of the progeny host 320

plant was dependent on the aphid clone, as evident from the significant clone × progeny host 321

interaction (Table 4). The plant had no obvious effect in the more susceptible clone 7.10, but 322

the more resistant clone 6.21 was mummified at a lower rate on silver beet (the more 323

challenging host) than on radish (the more benign host). The reasons for this difference are 324

(17)

unknown, yet it illustrates how the outcome of a parasitoid attack can be determined by a 325

complex interaction between genetic and environmental factors. At least for some aphid 326

genotypes, the host on which reproduction is maximised may not be the same as the host on 327

which susceptibility to parasitoids is minimised. This could affect the host selection behaviour 328

of aphids under differential risks of parasitism. 329

In summary, this study provided no evidence for trans-generational defence against a 330

parasitoid in the aphid M. persicae and at best a weak indication that an aphid's susceptibility 331

to parasitoids can be affected by the host plant on which its mother developed. Thus in 332

contrast to other invertebrate systems where maternal effects may account for a large fraction 333

of the variation in offspring rates of infection (Little et al., 2003; Mitchell & Read, 2005; 334

Moret, 2006; Sadd et al., 2005), there appears to be limited scope for maternal effects on 335

susceptibility in the aphid-parasitoid system studied here. 336

337

Acknowledgements

338 339

We thank S. von Burg for her assistance with the execution of experiment 1 and M. Torrance 340

for sending us D. rapae. This work was supported through grants from the Swiss National 341

Science Foundation (nr. 3100A0-109266) and from the Forschungskredit of the University of 342 Zürich (nr. 57202802) to CV. 343 344 References 345 346

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19

Collection inform

ation and m

icrosatel

lite genotypes of the three clones of

Myzus persica e used in the present stud y (-- indic ates m issing data). Micros atellite Locus Collection site Collection date M37 M40 M63 M86 M107 myz2 myz9 Steinm aur, Switzerland 07.07.2004 -- 122 122 171 175 130 134 137 141 -- 194 202

Bacchus Marsh, Australia

13.03.2003 153 153 120 126 163 169 094 134 137 137 177 189 208 222

Bacchus Marsh, Australia

22.04.2003 153 153 122 126 163 187 128 132 137 137 177 205 220 222

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Table 2. Analysis of variance results for adult mass of the maternal-generation aphids in experiment 2. Effect d.f. MS F P Block 2 0.221 20.175 < 0.001 Maternal host 1 0.514 46.988 < 0.001 Clone 1 0.008 0.689 0.408

Maternal host × clone 1 0.010 0.909 0.342

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Table 3. Analysis of variance results for fecundity (offspring produced in 24 h) of the

maternal-generation aphids in experiment 2. Maternal host is the host plant on which these aphids were reared, progeny host is the host plant on which fecundity was measured, i.e. the host to which these aphids were transferred to produce the cohort of offspring used in resistance tests. Effect d.f. MS F P Block 2 6.358 5.289 0.006 Maternal host 1 304.015 252.904 0.000 Progeny host 1 26.555 22.090 0.000 Clone 1 0.111 0.092 0.762

Maternal host × progeny host 1 3.658 3.043 0.084

Maternal host × clone 1 2.874 2.391 0.125

Progeny host × clone 1 0.036 0.030 0.864

Maternal host × progeny host × clone 1 0.010 0.008 0.928

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22

Analysis of deviance tables for the propor

tion of progeny-generati

on aphids mumm

if

ied by

Diaeretiella rapae

and the proportion of

progeny-experim

ent 2. The model was a qua

si-likelihood fit using

the logit link and binom

ial errors (see

Material and Methods).

Proportion of aphids m

ummified

Proportion of aphids surviving

Deviance F P d.f. Deviance F P 2 11.41 2.18 0.118 2 12.37 2.14 0.123 host 1 6.19 2.36 0.127 1 19.01 6.56 0.012 host 1 2.00 0.76 0.384 1 0.71 0.25 0.621 1 40.16 15.32 < 0.001 1 47.43 16.37 < 0.001 al ho st × progeny host 1 5.00 1.91 0.170 1 1.03 0.36 0.553 al ho st × clon e 1 0.26 0.10 0.753 1 2.52 0.87 0.353 × clon e 1 24.06 9.18 0.003 1 33.11 11.43 0.001 al ho st × progeny host × clon e 1 2.62 1.00 0.320 1 0.27 0.09 0.760 272.33 106 332.68

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Figure legends

Fig. 1. Box plot depicting the fecundity of maternal-generation aphids from the three

treatments used in experiment 1. The boxes span the 25th to 75th percentiles, the line within the box depicts the median, and the upper and lower whiskers indicate the 90th and 10th percentiles. Values above and below the 90th and 10th percentiles are represented by filled circles. Fecundity is expressed as offspring per female produced within 24 h, but replication was at the level of groups of four females caged on a single plant. N = 16, 20 and 24 replicate groups for the 'control', 'contact' and 'parasitised' treatment, respectively.

Fig. 2. Relationship between the proportion of individuals mummified and the number of

offspring-generation nymphs exposed to the parasitoid in each replicate assay in experiment 1. Different shadings are used for the three maternal treatments.

Fig. 3. Mean mass of adult Myzus persicae from the maternal generation in experiment 2,

separately for both clones and maternal host plants. Each point represents the mean of 30 replicates and for each replicate a mean of 5 individual aphids were weighed.

Fig. 4. Daily fecundity of maternal-generation Myzus persicae in experiment 2. Separate

means are given for the two maternal host plants and the two progeny hosts on which fecundity was assayed. Each point represents the mean of 30 replicates and each replicate consisted of 1-10 (mean = 5) females caged on individual plants.

Fig. 5. Stacked bar plot of the fate of offspring-generation Myzus persicae after exposure to

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and the four combinations of maternal host plant → progeny host plant. Each bar depicts mean proportions of 12 – 15 replicate cohorts of offspring (mean N = 14.5).

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References

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