New Results

Wolbachia both aids and hampers the performance of spider mites on different host plants

Flore Zélé, Joaquim L. Santos, Diogo Prino Godinho, Sara Magalhães
doi: https://doi.org/10.1101/344143

Abstract

In the last decades, many studies had revealed the potential role of arthropod bacterial endosymbionts in shaping the host range of generalist herbivores and their performance on different host plants, which, in turn, might affect endosymbiont distribution in herbivores populations. We tested this by measuring the prevalence of endosymbionts in natural populations of the generalist spider mite Tetranychus urticae on different host plants. Focusing on Wolbachia, we then analysed how symbionts affected mite life-history traits on the same host-plants in the laboratory. Overall, the prevalences of Cardinium and Rickettsia were low, whereas that of Wolbachia was high, with the highest values on bean and eggplant and the lowest on purple, tomato and zuchini. Although most mite life-history traits were affected by the plant species only, Wolbachia infection was detrimental for egg hatching rate on purple and zucchini, and led to a more female-biased sex ratio on purple and eggplant. These results suggest that endosymbionts may affect the host range of polyphagous herbivores, both by aiding and hampering their performance, depending on the host plant and on the life-history trait that affects performance the most. Conversely, endosymbiont spread may be facilitated or hindered by the plants on which infected herbivores occur.

INTRODUCTION

Although generalist herbivores are able to colonize several host plants, their performance on different host plants is variable. Whereas some studies suggest that the host range of herbivores is mostly determined by geographical location (Calatayud et al., 2016), others suggest that this range is determined by host-plant nutritional quality (Schoonhoven et al., 2005) or host-plant defences (Becerra, 1997). Still, the proximate mechanisms allowing populations to colonize particular host plants remain elusive.

Herbivores harbour a rich community of microorganisms, ranging from their gut microbiota and intracellular vertically-transmitted endosymbionts to plant bacteria and viruses of which they serve as vectors, and there is growing evidence of the impact of such communities on herbivore performance on plants (Hosokawa et al., 2007, Clark et al., 2010, Frago et al., 2012, Hansen & Moran, 2014, Oliver & Martinez, 2014, Zhu et al., 2014, Shikano et al., 2017). Obvious candidates to influence plant colonization by herbivorous arthropods are their heritable endosymbionts (Clark et al., 2010, Feldhaar, 2011, Ferrari & Vavre, 2011, Frago et al., 2012, Jaenike, 2015). Due to their vertical mode of transmission, the fitness of such symbionts is tightly linked to that of their host and they are likely to benefit their host in order to increase their own transmission (Fine, 1975). Indeed, endosymbionts have been shown to affect the host-plant range of herbivorous arthropods (Hosokawa et al., 2007, Tsuchida et al., 2011, Sugio et al., 2015, Wagner et al., 2015, Giron et al., 2017) or to increase performance on certain plant species (Wilkinson et al., 2001, Leonardo & Muiru, 2003, Ferrari et al., 2004, Tsuchida et al., 2004, Ferrari et al., 2007, Hosokawa et al., 2007, Su et al., 2013, Su et al., 2015, Wagner et al., 2015), while decreasing performance on others (Chen et al., 2000, Leonardo & Muiru, 2003, Ferrari et al., 2007, Chandler et al., 2008, McLean et al., 2011, Wagner et al., 2015). In some cases, increased host performance is due to endosymbionts acting as nutritional mutualists, directly supplying their arthropod hosts with nutrients or enzymes that are missing in their plant diet (reviewed by Chaves et al., 2009, Douglas, 2009), or displaying compensatory effects during periods of nutritional deficiency (Su et al., 2014). Finally, endosymbionts may also enable arthropods to manipulate phytohormonal profiles (Kaiser et al., 2010, Body et al., 2013), resource allocation (Hackett et al., 2013), and anti-herbivory defences (Barr et al., 2010, Su et al., 2015). Conversely, symbiont-mediated decreased host performance on particular plants might be due to the nutrient profile (e.g., specific amino acids and nitrogen content) of these plants, which promotes deleterious symbiont traits and disturbs the host control over bacterial abundance (Wilkinson et al., 2007, Chandler et al., 2008).

Such variable effects of endosymbionts on herbivore plant use may contribute to variation in the abundance and distribution of herbivorous arthropods (Douglas, 2009, Hansen & Moran, 2014). Conversely, as symbiont-herbivore interactions may differ according to the host plant, and nutrition of herbivore host can affect the within-host symbiont density (Wilkinson et al., 2001, Wilkinson et al., 2007, Chandler et al., 2008, Zhang et al., 2016), the host plant can also affect endosymbiont distribution in the field (Leonardo & Muiru, 2003, Simon et al., 2003, Ferrari et al., 2004, Tsuchida et al., 2004, Chandler et al., 2008, Ahmed et al., 2010, Brady & White, 2013, Pan et al., 2013, Guidolin & Consoli, 2017). However, most studies addressing these questions have been conducted on sap-feeding insects and whether symbiont prevalence and their effects on their herbivorous host vary with the host plant remains unstudied in other systems.

The two-spotted spider mite Tetranychus urticae, a cosmopolitan agricultural and horticultural pest that feeds on cell content, is a highly polyphagous arthropod, feeding on more than 1100 plant species (Migeon & Dorkeld, 2006-2017). This generalist herbivore rapidly adapts to novel host plants (Fry, 1990, Agrawal, 2000, Magalhães et al., 2007), sometimes forming host races (Magalhães et al., 2007), and may harbour several endosymbiontic bacteria with variable prevalence among populations (Enigl & Schausberger, 2007, Gotoh et al., 2007, Staudacher et al., 2017). Among them, Wolbachia is the most prevalent (Liu et al., 2006, Gotoh et al., 2007, Ros & Breeuwer, 2009, Zhang et al., 2016, Zélé et al., 2018) and induces variable fitness effects in spider mites. For instance, it can decrease (Perrot-Minnot et al., 2002, Suh et al., 2015), not affect (Breeuwer, 1997, Vala et al., 2000, Perrot-Minnot et al., 2002, Vala et al., 2002, Gotoh et al., 2007), or increase (Vala et al., 2002, Gotoh et al., 2007, Xie et al., 2011) their fecundity. Given these variable effects, it is as yet unclear whether Wolbachia will facilitate or hamper host-plant colonization by spider mites.

Here, we measured the prevalence of the three most prevalent endosymbionts of T. urticae, namely Wolbachia, Cardinium, and Rickettsia, on five different host plants in Portugal. Subsequently, we explored whether the effect of Wolbachia on the performance of T. urticae hinges on the plant that is being colonized. Finally, we discuss the importance of possible mechanisms leading to our results as well as the potential adaptive significance of the presence of Wolbachia for plant colonization by T. urticae.

MATERIALS AND METHODS

Effect of the host plant on endosymbiont prevalence in the field

To determine whether the prevalence of Wolbachia, Cardinium and Rickettsia in natural T. urticae populations varied with the host plant, spider mites were collected on bean (Phaseolus vulgaris, Fabaceae), eggplant (Solanum melongena, Solenaceae), purple morning glory (Ipomoea purpurea, Convolvulaceae, hereafter “purple”), zucchini (Cucurbita pepo, Cucurbitaceae), and tomato (Solanum lycopersicum, Solenaceae) across 12 different locations (Table 1). These plants were selected because they are part of the natural host range of T. urticae but belong to different families. Sampling sites consisted of open fields, greenhouses or organic vegetable gardens, while being insecticide/pesticide free to avoid this potential confounding effect. Infested leaves were detached and placed in closed plastic boxes that were brought to the laboratory. On the same day, 50 adult females were haphazardly picked from each population and their species determined at the individual level based on morphological characteristics under a binocular microscope. These females were then placed on 2 cm2 leaf discs of the same plant species on which they were found, and allowed to lay eggs for 4 days. Subsequently, 20 of these females were randomly selected and individually tested for the presence of Wolbachia, Cardinium and Rickettsia on entire mites without DNA extraction by multiplex PCR using genus-specific primers as described in (Zélé et al., 2018). Subsequently, for each population, the DNA of a pool consisting of one daughter from each of these females was extracted, then a PCR-based method to identify the mite species was performed by multiplex PCR as described in (Zélé et al., 2018). If a pool could not be assigned unambiguously to T. urticae (see Table S1 in Additional file 1), all data concerning endosymbiont prevalence were discarded. This process was repeated until obtaining endosymbiont prevalence data for 5 populations per plant, except for purple, for which we could obtain only 2 populations of T. urticae due to the weak infestation rate of this plant by this spider-mite species, and despite a large sampling effort (Table S1).

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Table 1.

Tetranychus urticae populations collected on five different host plants across 12 different locations in June-July 2015 and used to study the plant effect on the prevalence of Wolbachia, Cardinium and Rickettsia.

Effect of Wolbachia, the host plant, and their interaction on the performance of spider mites

Spider mite populations, tetracycline treatment and population rearing

The spider-mite population used was originally collected on Datura plants at Aldeia da Mata Pequena, Portugal, in November 2013 and kept in a mass-rearing environment (>5 000 individuals) on bean plants (var. Enana), under controlled conditions (25°C, photoperiod of 16L:8D) since then. This population, hereafter called Wi, was found uninfected by Rickettsia, Spiroplasma or Arsenophonus but fully infected by Wolbachia in the field (Zélé et al., 2018). Although this population was also slightly infected by Cardinium (Zélé et al., 2018), this endosymbiont has been rapidly lost following laboratory rearing (unpublished data). To obtain a Wolbachia-uninfected (Wu) population with a similar genetic background, roughly 3 months after collection 30 adult females of the Wi population were placed in petri dishes containing bean leaf fragments placed on cotton with a tetracycline solution (0.1 %, w/v). This treatment was applied continuously for three successive generations (Breeuwer, 1997), then the population was maintained in a mass-rearing environment without antibiotics for c.a. 12 generations before the experiment to avoid (or limit) potential side effects of the antibiotic treatment (e.g. O’Shea & Singh, 2015) and allow mites to recover potential loss of gut. Before use, up to 20 individual females and pools of 100 females were checked by PCR to confirm the absence and presence of Wolbachia infection in Wu and Wi populations, respectively.

Performance of Wolbachia-infected and uninfected females on different host plant

To determine the effect of Wolbachia infection and of the host plant, as well as their possible interaction, on the performance of T. urticae, we measured life history traits of individuals from Wi or Wu populations when placed on the same plant species as those from which mites were collected in the field study (bean: var. Enana, eggplant: var. Larga Morada, purple: var. Vigorous, zucchini: var. Bellezza Negra, and tomato: var. Money Maker). To control for age, 100 females were allowed to lay eggs for three days on detached bean leaves placed on water-soaked cotton, and the adult females resulting from those eggs were used in the experiments. Fifty mated females (10-13 days old) were haphazardly picked from either Wi or Wu cohorts and placed individually on a 2 cm2 leaf disc from one of the 5 different host plants. The replicates were distributed along 5 temporal blocks (10 replicates per treatment per day during 5 consecutive days). Females that were alive after 3 days were transferred to new leaf discs where they could lay eggs for another 3 days. Their survival (S) and the proportion of drowned females in the water-soaked cotton (i.e. accidental death of females trying to escape the leaf discs; PD) were followed daily during six days. The fecundity of each female was measured at days 3 and 6 and the average female daily fecundity was estimated taking into account their daily mortality (DF = total number of eggs laid per female / number of days the female was alive). The number of unhatched eggs was counted 5 days later (i.e. days 8 and 11, respectively) to estimate the hatching rate (HR = hatched eggs / total number of eggs). Adult offspring (F1 females + F1 males) was counted after 6 additional days (i.e. days 14 and 17, respectively) and used to estimate juvenile mortality (JM = [total number of eggs - number of unhatched eggs - number of F1 adults]/ total number of eggs), F1 sex ratio (SR = number of F1 males/number of F1 adults) and the number of viable offspring (VO = total number of adult offspring per female per treatment observed at the end of the experiment on each plant). The entire experiment was repeated three months later (hereafter called blocks 1 and 2) except for replicates involving tomato plants. Indeed, given a very high proportion of drowned females (88 ± 3.3 %; data not shown) and because the surviving females laid on average less than 1 egg per day (0.32 ± 0.05; data not shown) on this plant, subsequent traits could not be measured and we decided to exclude it from this experiment.

Statistical analyses

Analyses were carried out using the R statistical package (v. 3.3.2). The different statistical models built to analyse the effect of host-plant on endosymbiont prevalence in field-collected spider-mite populations and the effects of Wolbachia on different host plants are described in the electronic supplementary material (Additional file 1), Table S2.

To analyse the effect of host plants on endosymbiont prevalence in field-collected mites, the prevalence of Wolbachia (model 1), Cardinium (model 2) and Rickettsia (model 3) were fit as binary response variables, the host plant on which mites were collected as fixed explanatory variable, and the location as random explanatory variable. Because of quasi-complete separation of some of our data, which usually causes problems with estimated regression coefficients, analyses were conducted using a mixed model bglmer procedure (blme package) with a binomial error distribution (Pasch et al., 2013). When the variable “plant” was significant, a stepwise a posteriori procedure (Crawley, 2007) to determine differences between plants was carried out by aggregating factor levels together and by testing the fit of the simplified model using a likelihood ratio test (LRT), which is approximately distributed as a χ2 distribution (Bolker, 2008). Because none of the mites collected in this study were singly infected by Cardnium or Rickettsia, and the prevalence of each type of coinfection was very low (cf. Results), we did not have enough statistical power to study the effect of the host plants on the prevalence of coinfections.

To analyse the effect of Wolbachia, the host plant, and their interaction on the performance of spider mites, the infection status of females (i.e. Wi: infected or Wu: uninfected) and the host plants tested were fit as fixed explanatory variables, whereas block and day were fit as random explanatory variables (day nested within block). Survival data (S; model 4) were analysed using a Cox proportional hazards mixed-effect model (coxme, kinship package). Hazard ratios were obtained from this model as an estimate of the difference in mortality rate (Crawley, 2007) between our control (Wi population on bean) and each of the other factor levels. PD, a binary response variable (drowned or not; model 5), was analysed using a generalized linear mixed model with a binomial distribution (glmer, lme4 package). DF, a continuous response variable (model 6) was analysed using linear mixed-effect models (lmer, nlme package). The other proportion variables HR, SR and JM (models 7, 8, and 9, respectively) were computed using the function cbind (e.g. number of hatched eggs, males, or dead juveniles vs. number of unhatched eggs, females, or alive juveniles, respectively). However, due to the low daily fecundity of spider mites, these variables, as well as VO (model 10) were greatly over-dispersed. One way of handling this over-dispersion is by using quasibinomial or negative binomial pseudo distributions (Crawley, 2007) but, to our knowledge, this is not possible within the usual mixed model glmer procedure. Thus, we used instead a mixed model glmmadmb procedure (glmmADMB package) with zero-inflated binomial error distribution for HR, SR and JM, and zero-inflated negative binomial error distribution for VO. When a statistically significant interaction between the variables “Wolbachia” (Wi or Wu) and “plant” was found, the effect of Wolbachia was analysed for each plant separately. When only the variable “plant” was significant, a posteriori contrasts between host plants were performed as before.

For all analyses, maximal models were simplified by sequentially eliminating non-significant terms to establish a minimal model (Crawley, 2007), and the significance of the explanatory variables was established using χ2-tests or F-tests to account for overdispersion (Bolker, 2008). The significant values given in the text are for the minimal model, while non-significant values correspond to those obtained before deletion of the variable from the model (Crawley, 2007). Full datasets are given in Additional files 2 and 3.

RESULTS

Effect of the host plant on endosymbiont prevalence in the field

The prevalence of Wolbachia was overall high (92.7 ± 1.2 %), while that of Cardinium (2.5 ± 0.7 %) and Rickettsia (2.0 ± 0.7 %) were low (Fig. 1). In addition, while 89.3 ± 1.5 % of the mites collected in this study were infected by Wolbachia only, none were infected by Cardinium or by Rickettsia only. 1.4 ± 0.6 % were coinfected by Wolbachia and Cardinium, 0.9 ± 0.5 % were coinfected by Wolbachia and Rickettsia, and 1.14 ± 0.5 % where infected by these three endosymbionts (see Fig. S1 in Additional file 1 for infection statuses at the individual level). The prevalence of Wolbachia and of Rickettsia were affected by the plant on which T. urticae females were collected (Χ24=14.79, p=0.005; model 1, and Χ24=12.71, p=0.01; model 3, respectively; Fig. 1). Contrast analyses revealed that the prevalence of Wolbachia was higher on bean and eggplant (97.0 ± 1.7 %; contrast bean vs eggplant: Χ21=0.51, p=0.47) than on the 3 other plants (89.2 ± 2.0 %; Contrast purple vs tomato vs zucchini: Χ22=0.39, p=0.82; Contrast between the two groups of plants: Χ21=14.34, p=0.0002), and that of Rickettsia differed only on purple (12.5 ± 5.3 %) compared to all other plants (1.0 ± 0.5 %; contrast bean vs eggplant vs tomato vs zucchini: Χ23=2.95, p=0.40; Contrast between this group of plants and purple: Χ21=9.76, p=0.002). Finally, the prevalence of Cardinium, similarly to that of Rickettsia, tended to be higher on purple (12.5 ± 5.3 %) compared to the other plants (1.5 ± 0.6 %), but this effect was re not statistically significant (Χ24=1.61, p=0.81; model 2).

Figure 1.
Figure 1. Endosymbiont prevalence in T. urticae females collected on different host plants.

Bars represent the mean (± s.e.) infection frequencies by Wolbachia (light grey), Cardinium (dark grey), and Rickettsia (black) for several spider mite populations collected on bean (n=5), eggplant (n=5), purple (n=2), tomato (n=5), and zucchini (n=5).

Effect of Wolbachia, the host plant, and their interaction on the performance of spider mites

Overall, there was no significant effect of Wolbachia (Χ21= 0.73, p=0.39), of host plants (Χ23= 6.84, p=0.07), or of their interaction (Χ23= 3.34, p=0.34; model 4; Table 1 and Fig. S2 in Additional file 1) on survival (S) over the 6 first days of the experiment. However, host plants affected significantly the proportion of drowned mites (PD; Χ23= 23.14, p<0.0001), regardless of Wolbachia infection (Wolbachia effect: Χ21= 1.35, p=0.25; Wolbachia-plant interaction: Χ23=0.70, p=0.87; model 5; Table 2).

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Table 2. Effect of Wolbachia and of host plants on the performance of spider mites.

Mean (± s.e.) values of both Wolbachia-infected (Wi) and uninfected (Wu) T. urticae on the different plants studied (bean, purple, zucchini and eggplant) are represented for each one of the performance traits measured in this study. For hatching rate, juvenile mortality and sex ratio, estimates were obtained from the GLMM statistical models and take into account variation among females, as well as the correction for zero-inflation and day within block as random effect.

Daily fecundity (DF) was significantly affected by host plants (Χ23=129.33, p<0.0001), but not by Wolbachia (Χ21=2.06, p=0.15) or its interaction with the plant (Χ23=1.21, p=0.75; model 6; table 2). Contrast analyses revealed that DF was similar on purple and zucchini (3.37 ± 0.11 eggs per day; contrast purple vs zucchini: Χ21=1.03, p=0.31), but higher on bean (4.60 ± 0.19 eggs per day; contrast purple-zucchini vs bean: Χ21=40.14, p<0.0001), and lower on eggplant (2.10 ± 0.13; Contrast eggplant vs purple-zucchini: Χ21=42.77, p<0.0001).

The effect of Wolbachia on egg hatching rate (HR) depended on the host plant tested (Wolbachia-plant interaction: F3,697=5.47, p=0.001; model 7; Table 1 and Fig. 2). Indeed, Wolbachia reduced HR on purple (F1,172=10.05, p=0.002) and on zucchini (F1,177=19.74, p<0.0001), but had no effect on bean and eggplant (F1,181=1.42, p=0.24 and F1,158=1.56, p=0.21, respectively).

Figure 2.
Figure 2. Effects of different host plants and of Wolbachia on the hatching rate of T. urticae eggs.

Bars represent the mean (± s.e.) proportions of hatched eggs laid by Wolbachia-infected (Wi; grey bars) and uninfected (Wu; white bars) females on different host plants. Estimates were obtained from the GLMM statistical model that takes into account variation of fecundity among females, day within block as random effect, and corrects for zero-inflation. Standard errors were obtained from the upper and lower confidence intervals given by the model.

Juvenile mortality (JM) was not significantly affected by Wolbachia (F1,692=0.01, p=0.92; model 8; Table 2), and this was consistent across all host plants (Wolbachia-plant interaction: F3,689=1.85, p=0.14; model 8). However, host plant was a significant predictor of JM (F3,693=48.23, p<0.0001; model 8). Bean and zucchini did not differ significantly from each other (contrast bean vs zucchini: Χ21=0.72, p=0.40) and led to intermediate JM of 16.8 ± 0.9%, while purple decreased it by 5.2 ± 1.5% (contrast purple vs bean-zucchini: Χ21=53.82, p<0.0001), and eggplant increased it by 11.3 ± 2.1% (contrast bean-zucchini vs eggplant: Χ21=109.36, p<0.0001).

Wolbachia infection affected differently the sex ratio (SR) produced on the different plants (Wolbachia-plant interaction: F3,681=2.48, p=0.04; model 9; Table 2 and Fig. 3). Indeed, Wolbachia decreased the proportion of males on purple (F1, 168=5.51, p=0.02) and on eggplant (F1, 153=8.54, p=0.004). On bean and zucchini, however, SR did not differ significantly between Wi and Wu mites (F1,179=5.51, p=0.54 and F1,1726=2.28, p=0.13, respectively).

Figure 3.
Figure 3. Effects of different host plants and of Wolbachia on the offspring sex ratio produced by T. urticae females.

Bars represent the mean (± s.e.) proportions of male offspring produced by Wolbachia-infected (Wi; grey bars) and uninfected (Wu; white bars) females on different host plants. Estimates were obtained from the GLMM statistical model that takes into account variation of fecundity among females, day within block as random effect, and corrects for zero-inflation. Standard errors were obtained from the upper and lower confidence intervals given by the model.

Although we found a significant Wolbachia-plant interaction on HR and SR, Wolbachia did not significantly influence the average number of viable offspring (VO; F1,789=0.78, p=0.38), and this effect was independent of the host plant (Wolbachia-plant interaction: F3,786=0.70, p=0.55; model 10; Table 2 and Fig. 4). Nonetheless, host plant significantly explained this trait (F3,790=48.72, p<0.0001; model 10), with the highest values on bean, intermediate values on purple (contrast purple vs bean: Χ21=4.82, p=0.03) and zucchini (contrast zucchini vs purple: Χ21=5.12, p=0.02), and the lowest values on eggplant (contrast eggplant zucchini: Χ21=44, p<0.0001).

Figure 4.
Figure 4. Effects of different host plants and of Wolbachia on the average number of viable offspring per female.

Bars represent the mean (± s.e.) numbers of offspring (grey: sons; white: daughters) produced by Wolbachia-infected (Wi; grey bars) and uninfected (Wu; white bars) females on different host plants.

DISCUSSION

In this study, we confirmed that Wolbachia is highly prevalent in T. urticae in Portugal, while Cardinium and Rickettsia were found at low prevalences (Zélé et al., 2018). Moreover, this study suggests that endosymbiont prevalence varied with the host plant, Cardinium and Rickettsia being more prevalent on purple (although non-significantly for Cardinium) than on the other plants, and Wolbachia being more prevalent on bean and eggplant than on tomato, purple and zucchini. In the laboratory, Wolbachia-infected eggs had a lower hatching rate than uninfected ones on purple and zucchini, while this was not the case on bean and eggplant.

The prevalence of Wolbachia and Rickettsia in T. urticae females found in this study was relatively similar to that of an earlier study in the same geographical area (Zélé et al., 2018). However, the prevalence of Cardinium was about five times lower in the current study than in the former one (2.5 ± 0.7 % vs 13.6 ± 2.9 %, respectively). As the populations were sampled on comparable host plants in this previous study (except for one population collected on Datura stramonium, the others were collected on bean, eggplant, tomato and zucchini), the discrepancy observed for the overall Cardinium prevalence between the two studies may be attributed to the time of collection. Indeed, mites were collected between September and December in the previous study and in June-July in the current one. Several studies have shown that the sampling period might affect endosymbiont prevalence and/or density in host populations (Toju & Fukatsu, 2011, Dorfmeier et al., 2015, Martinez-Diaz et al., 2016, Sumi et al., 2017). This increase of Cardinium prevalence during summer is compatible with the hypothesis of an accumulation of this symbiont throughout the season via horizontal transfers (Zélé et al., 2018).

We found that Wolbachia prevalence was overall high, but significantly higher on bean and eggplant than on the other plants. Whereas some earlier studies have shown that Wolbachia prevalence in herbivores varies according to the host plant (Ahmed et al., 2010, Toju & Fukatsu, 2011, Guidolin & Consoli, 2017), including a recent study conducted in the spider mite Tetranychus truncatus (Zhu et al., 2018), others show no difference (Ji et al., 2015). Unfortunately, the scarcity of studies, along with the fact that they were mostly done in other systems, hampers a meaningful comparison among studies. In addition, it is extremely difficult to sample spider-mite populations on all the plants tested within the same locality (see Table S1 in Additional file 1). Consequently, this implies an important sampling effort to obtain only a very reduced number of populations that fit the criteria for such studies. For instance, despite a large sampling effort across 21 localities and 12 host plant species, Zhu et al. (2018) could assess the effect of three common host plants (soybean, corn, and tomato) from three different locations only. Still, they did find that the prevalence of Wolbachia was significantly affected by the host plant (about 30% higher in tomato than in corn). In our study, the amplitude of the observed effects is much lower, possibly due to a threshold effect since the prevalence of Wolbachia that we observed in T. urticae is overall much higher than that observed in T. truncates by Zhu et al. (2018). Clearly, differences in Wolbachia prevalence were not associated with plant phylogenetic distance, as it differed between the solanaceous plants used (eggplant and tomato). Moreover, the effect of an endosymbiont on arthropod-plant interactions may depend on both the genotype (or species) of symbiont (Leonardo & Muiru, 2003) and arthropod host (Chen et al., 2000, Ferrari et al., 2007, McLean et al., 2011, Wagner et al., 2015), and/or their interaction (Ferrari et al., 2007). More studies on plant-dependent symbiont prevalence may thus shed light on the potential factors underlying the pattern observed and on the ecological meaning of such effects.

Here, we hypothesize that the variation in endosymbiont prevalence according to the host plant is, at least partially, due to plant-specific effects of these symbionts on spider-mite performance. Although we did find some variation of Rickettsia and Cardinium prevalence according to the host plant, their prevalence was very low, so we opted for addressing this issue using Wolbachia only. Overall, we found a strong effect of the host plant on spider-mite performance, with the highest values observed on bean. This is not surprising, given that bean was the rearing environment of the population used, and is generally a host plant of high quality for spider mites (e.g. Magalhães et al., 2011). Conversely, the lowest performances were found on Solanaceous plants (eggplant and tomato), being so low on tomato (cf. Material and Methods) that we excluded these data from further analyses. In the other four plants, we found that some traits (proportion escaping, female fecundity, and juvenile survival) were not affected by Wolbachia whereas others (egg hatching rate and sex ratio) were affected in a plant-specific manner.

The plant-specific effects of Wolbachia, although of low amplitude, could be explained by several non-exclusive mechanisms. First, Wolbachia may impose a nutritional burden to its hosts, sequestering and using vital host nutrients for its own survival (Chandler et al., 2008, Caragata et al., 2014, Ponton et al., 2015), and this may vary with the host plant. Indeed, the nutrient composition of plant material is often poor or unbalanced for herbivores (Schoonhoven et al., 2005, Karban & Baldwin, 2007), and nutrient deficient diet may increase the competition for resources between hosts and symbionts. In turn, this may lead to a decreased ability of infected spider mites to allocate enough nutrients to ensure egg viability on plants of low quality. Increased host-symbiont competition on such low-quality plants could also lead to a biased sex ratio towards males because females are produced from bigger eggs than males in T. urticae (Macke et al., 2011). In addition, the slight Wolbachia-induced female-biased sex ratio observed on purple could be a consequence of the lower hatching rate observed on this plant, as larger eggs are generally more likely to hatch (Macke et al., 2011). However, if this hypothesis would hold true, one would expect a stronger cost of Wolbachia in spider mites on plants of lower quality for mites, and we did not find such pattern.

Second, Wolbachia may directly influence the metabolism of some plants, which in turn can affect the biology of its herbivorous hosts. For instance, Wolbachia infecting the leaf-mining moth Phyllonorycter blancardella might be responsible for an increased level of cytokinins (plant hormones mainly involved in nutrient mobilisation and inhibition of senescence) in infested apple trees, Malus domestica. In this system, Wolbachia thus helps its host to develop in photosynthetically active green patches in otherwise senescent leaves (Kaiser et al., 2010, Body et al., 2013). Interestingly, cytokinins have also been shown to be responsible for sex-ratio shift towards females in the sap-feeding insect Tupiocoris notatus (although this effect was not mediated by Wolbachia; Adam et al. 2017). As Wolbachia possess a key gene involved in cytokinin biosynthesis in their genomes (Kaiser et al., 2010), frequently infect the salivary glands of its hosts (Dobson et al., 1999) and are present in high density in the gnathosoma of spider mites (Zhao et al., 2013), one could speculate that the sex-ratio shift towards females observed in Wolbachia-infected mites on purple and eggplant in our study is mediated by increased cytokinin levels induced by Wolbachia in these two plants. Further research is thus needed to test this hypothesis. In particular, whether the Wolbachia present in spider mites also possess genes involved in cytokinin biosynthesis in their genomes is still unknown and the full genome of Wolbachia isolated from spider-mite hosts has, to our knowledge, not yet been sequenced.

Third, Wolbachia may interfere with the mites’ response toward plant defences. Indeed, endosymbionts found in herbivores, including Wolbachia, may directly manipulate the plant defenses to benefit their host (Frago et al., 2012, Hansen & Moran, 2014, Zhu et al., 2014, Sugio et al., 2015, Giron et al., 2017, Shikano et al., 2017), or have a detrimental effect on their host by increasing the level of induced plant defences. For instance, down-regulation of several defense genes of maize by the western corn rootworm Diabrotica virgifera has been shown to be mediated by Wolbachia (Barr et al., 2010, but see Robert et al., 2013). Moreover, in a recent study, Staudacher et al. (2017) found that feeding by mites coinfected with Spiroplasma and Wolbachia increased the accumulation of 12-oxo-phytodienoic acid (a precursor of jasmonic acid) in tomato plants, compared to Spiroplasma-infected or non-infected mites. However, the concentration of jasmonic, salicylic and abscisic acids were not affected and no causal link could be established between the changes in plant defenses and mite performance (although only fecundity and longevity have been studied). Whether the presence of Wolbachia in T. urticae can upregulate the defences of zucchini and purple, and whether this could explain the reduced egg hatchability observed here, thus remains to be tested.

Despite the weak plant-specific effects of Wolbachia on mite performance, and that they do not affect the total number of viable offspring, they seem to be correlated with Wolbachia prevalence on field populations of T. urticae collected on different host plants. Indeed, given that Wolbachia is costly on egg hatchability on zucchini, we would expect a lower prevalence of this symbiont on this plant. Conversely, as Wolbachia increases the proportion of females produced on eggplant, we could expect a higher prevalence on this plant. Indeed, Wolbachia being maternally transmitted, it should always benefit from a more female-biased sex ratio. Note that, although Wolbachia may induce cytoplasmic incompatibility in T. urticae (Gotoh et al., 2007, Xie et al., 2011, Suh et al., 2015), the effects observed in this study on spider-mite sex ratio cannot be attributed to this phenotype as it involves a cross between infected males and uninfected females, which was not performed here. On purple, we could expect the prevalence of Wolbachia to be intermediate, as the infection decreases egg hatchability but increases female proportion. Finally, bean being the plant on which spider mites have, overall, the best performance and that Wolbachia is not costly on this plant, we could expect its prevalence to be very high. Hence, by affecting the balance costs/benefits of Wolbachia on its spider-mite hosts, plants may affect Wolbachia prevalence. From the host perspective, however, although increased egg hatchability would probably benefit the spread of spider mites, it is not clear whether a female-biased sex ratio would benefit mites, as this is expected to depend on population structure (Hamilton, 1967, Macke et al., 2011). More studies are thus needed to shed light on the potential role of Wolbachia on the host plant range of spider mites, as done in other systems (Hansen & Moran, 2014, Sugio et al., 2015, Giron et al., 2017).

In conclusion, our results show plant-dependent effects of Wolbachia on spider mites egg hatchability and offspring sex ratio, two crucial traits for both spider-mite population dynamics and Wolbachia spread among host populations. Although the amplitude of these effects is relatively low, they may, at least partially, explain the prevalence of this symbiont in spider mite populations collected on these different host plants. Moreover, our study highlights the importance of studying different host plants and life history traits when addressing the effects of endosymbionts on the performance of their herbivorous arthropods. These results also raised important questions, such as: (i) whether the pattern observed in this study varies between host and/or symbiont genotype, (ii) whether host plants affect the maintenance and/or spread of endosymbionts within and among populations, and (iii) whether endosymbionts affect the host range of herbivores.

AUTHOR’S CONTRIBUTIONS

Experimental conception and design: FZ, SM; field collections: JS, DG; acquisition of data: JS; statistical analyses: FZ, JS; paper writing: FZ, SM, with input from all authors. All authors have read and approved the final version of the manuscript.

FUNDING

This work was funded by an FCT-ANR project (FCT-ANR//BIA-EVF/0013/2012) to SM and Isabelle Olivieri and by a FCT-Tubitak project (FCT-TUBITAK/0001/2014) to SM and Ibrahim Cakmak. FZ and DG were funded through FCT Post-Doc (SFRH/BPD/125020/2016) and PhD (PD/BD/114010/2015) fellowships, respectively. Funding agencies did not participate in the design or analysis of experiments.

Conflict of interest

None declared.

ACKNOWLEDGMENTS

We thank M. Bakırdöven, J. Denoyelle, L. Rodrigues, and Inês Santos for their help in spider-mite collection. We also thank IS for the maintenance of the plants and mite populations, Miguel Cruz, Nelson Martins, Jordi Moya Laraño and Susana Verala for advices in statistical analysis.

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Posted June 11, 2018.
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Wolbachia both aids and hampers the performance of spider mites on different host plants
Flore Zélé, Joaquim L. Santos, Diogo Prino Godinho, Sara Magalhães
bioRxiv 344143; doi: https://doi.org/10.1101/344143
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