Effects of Tomato chlorosis virus on the performance of its key vector,Bemisia tabaci,in China

Tomato chlorosis virus (ToCV), which is a newly emerged and rapidly spreading plant virus in China, has seriously reduced tomato production and quality over the past several years. In this study, the effect of ToCV on the demography of the whitefly, Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae), fed on infected and healthy tomato plants was evaluated using the age‐stage, two‐sex life table. When reared on ToCV‐infected tomato plants, the fecundity, length of oviposition period and female adult longevity of B. tabaci biotype Q decreased significantly, while the pre‐adult duration significantly increased compared to controls reared on healthy tomatoes. Consequently, the intrinsic rate of increase (r) and finite of increase (λ) of B. tabaci biotype Q on ToCV‐infected tomato plants significantly decreased compared to those on healthy tomatoes. Population projection predicted that a population of B. tabaci biotype Q fed on ToCV‐infected tomatoes increases slower than on healthy plants. These findings demonstrated that ToCV infection decreased the performance of B. tabaci biotype Q on tomato plants.     

Settling preferences of the whitefly vector Bemisia tabaci on infected plants varies with virus family and transmission mode

Virus infection may change not only the host‐plant phenotypic (morphological and physiological) characteristics, but can also modify the behavior of their insect vector in a mutualistic or rather antagonistic manner, to promote their spread to new hosts. Viruses differ in their modes of transmission and depend on vector behavior for successful spread. Here, we investigated the effects of the semi‐persistently transmitted Tomato chlorosis virus (ToCV, Crinivirus) and the persistent circulative Tomato severe rugose virus (ToSRV, Begomovirus) on alighting preferences and arrestment behavior of their whitefly vector Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) Middle East Asia Minor 1 (MEAM1) on tomato plants (Solanum lycopersicum L. cv. Santa Clara, Solanaceae). The vector alighting preferences between infected and uninfected plants in choice assays were apparently influenced by the presence of ToCV and ToSRV in the whiteflies or by their previous exposure to infected plants. The observed changes in vector behavior do not seem to benefit the spread of ToCV: non‐viruliferous insects clearly preferred mock‐inoculated plants, whereas ToCV‐viruliferous insects landed on mock‐inoculated and ToCV‐infected plants, indicating a partial change in insect behavior – ToCV was able to directly affect the preference of its vector B. tabaci, but this change in insect behavior did not affect the virus spread because viruliferous insects landed on mock‐inoculated and infected plants indistinctly. In contrast, ToSRV‐viruliferous insects preferred to land on mock‐inoculated plants, a behavior that increases the probability of spread to new host plants. In the arresting behavior assay, the majority of the insects remained on mock‐inoculated plants when released on them. A greater number of insects moved toward mock‐inoculated plants when initially released on ToCV‐ or ToSRV‐infected plants, suggesting that these viruses may repel or reduce the nutritional quality of the host plants for B. tabaci MEAM1.     

Abundance of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and its parasitoids on vegetables and cassava plants in Burkina Faso (West Africa)

The whitefly Bemisia tabaci is a pest of many agricultural and ornamental crops worldwide and particularly in Africa. It is a complex of cryptic species, which is extremely polyphagous with hundreds of host plants identified around the world. Previous surveys in western Africa indicated the presence of two biotypes of the invasive MED species (MED‐Q1 and MED‐Q3) living in sympatry with the African species SSA and ASL. This situation constitutes one of the rare cases of local coexistence of various genetic entities within the B. tabaci complex. In order to study the dynamics of the distribution and abundance of genetic entities within this community and to identify potential factors that could contribute to coexistence, we sampled B. tabaci populations in Burkina Faso in 2015 and 2016 on various plants, and also their parasitoids. All four genetic entities were still recorded, indicating no exclusion of local species by the MED species. While B. tabaci individuals were found on 55 plant species belonging to eighteen (18) families showing the high polyphagy of this pest, some species/biotypes exhibited higher specificity. Two parasitoid species (Eretmocerus mundus and Encarsia vandrieschei) were also recorded with E. mundus being predominant in most localities and on most plants. Our data indicated that whitefly abundance, diversity, and rate of parasitism varied according to areas, plants, and years, but that parasitism rate was globally highly correlated with whitefly abundance suggesting density dependence. Our results also suggest dynamic variation in the local diversity of B. tabaci species/biotypes from 1 year to the other, specifically with MED‐Q1 and ASL species. This work provides relevant information on the nature of plant–B. tabaci‐parasitoid interactions in West Africa and identifies that coexistence might be stabilized by niche differentiation for some genetic entities. However, MED‐Q1 and ASL show extensive niche overlap, which could ultimately lead to competitive exclusion.     

Mixed Infection and Natural Spread of ‘Candidatus Phytoplasma asteris’ and Mungbean Yellow Mosaic India Virus Affecting Soya Bean Crop in India

Suspected phytoplasma and virus‐like symptoms of little leaf, yellow mosaic and witches’ broom were recorded on soya bean and two weed species (Digitaria sanguinalis and Parthenium hysterophorus), at experimental fields of Indian Agricultural Research Institute, New Delhi, India, in August–September 2013. The phytoplasma aetiology was confirmed in symptomatic soya bean and both the weed species by direct and nested PCR assays with phytoplasma‐specific universal primer pairs (P1/P6 and R16F2n/R16R2n). One major leafhopper species viz. Empoasca motti Pruthi feeding on symptomatic soya bean plants was also found phytoplasma positive in nested PCR assays. Sequencing BLASTn search analysis and phylogenetic analysis revealed that 16Sr DNA sequences of phytoplasma isolates of soya bean, weeds and leafhoppers had 99% sequence identity among themselves and were related to strains of ‘Candidatus Phytoplasma asteris’. PCR assays with Mungbean yellow mosaic India virus (MYMIV) coat‐protein‐specific primers yielded an amplicon of approximately 770 bp both from symptomatic soya bean and from whiteflies (Bemisia tabaci) feeding on soya bean, confirmed the presence of MYMIV in soya bean and whitefly. Hence, this study suggested the mixed infection of MYMIV and ‘Ca. P. asteris’ with soya bean yellow leaf and witches’ broom syndrome. The two weed species (D. sanguinalis and P. hysterophorus) were recorded as putative alternative hosts for ‘Ca. P. asteris’ soya bean Indian strain. However, the leafhopper E. motti was recorded as putative vector for the identified soya bean phytoplasma isolate, and the whitefly (B. tabaci) was identified as vector of MYMIV which belonged to Asia‐II‐1 genotype.     

Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor

Plant-mediated interactions between herbivorous arthropods and pathogens transmitted by herbivores are important determinants of the population dynamics of both types of organisms in the field. The role of plant defence in mediating these types of tripartite interactions have been recognized but rarely examined especially at the physiological and molecular levels. Our previous work shows that a worldwide invasive whitefly can establish mutualism with the begomovirus Tomato yellow leaf curl China virus (TYLCCNV) via crop plants. Here, we show that TYLCCNV and betasatellite co-infection suppresses jasmonic acid defences in the plant. Impairing or enhancing defences mediated by jasmonic acid in the plant enhances or depresses the performance of the whitefly. We further demonstrate that the pathogenicity factor βC1 encoded in the betasatellite is responsible for the initiation of suppression on plant defences and contributes to the realization of the virus-vector mutualism. By integrating ecological, mechanistic and molecular approaches, our study reveals a major mechanism of the plant-mediated mutualism between a virus and its vector. As the test plant is an important economic crop, the results also have substantial implications for developing novel strategies for management of crop viruses and the insect vectors associated with them.     

Lack of genetic isolation by distance,similar genetic structuring but different demographic histories in a fig‐pollinating wasp mutualism

Historical abiotic factors such as climatic oscillations and extreme climatic events as well as biotic factors have shaped the structuring of species' genetic diversity. In obligate species‐specific mutualisms, the biogeographic histories of the interacting species are tightly linked. This could be particularly true for nuclear genes in the Ficus‐pollinating wasp mutualistic association as the insects disperse pollen from their natal tree. In this study, we compare spatial genetic structure of plant and pollinator for the Ficus hirta–Valisia javana association throughout southeast China including Hainan Island, for both nuclear and cytoplasmic markers. We show that dispersal of the insect leads to plant and insect presenting similar signatures of lack of genetic isolation by distance for nuclear genes on the continent over a distance of 1000 km. But we also show that the demographic histories of plant and insect are strikingly different. This is in agreement with extreme climatic events leading to transient regional extinctions of the insects, associated with local survival of the plants. We also observe evidence of genetic differentiation for both wasps and fig‐tree between the continent and Hainan Island, although the Qiongzhou Strait is only on average 30 km wide, suggesting that geographic isolation by itself has not been sufficient to generate this differentiation. Hence, our results suggest that in highly dispersive mutualistic systems, isolation‐by‐dispersal limitation across a geographic barrier could be supplemented by isolation by adaptation, and maybe by coevolution, allowing further genetic divergence. In such systems, species may frequently be composed of a single population.     

Reversal of mutualism in a leafflower–leafflower moth association: the possible driving role of a third‐party partner

A major goal in the study of mutualism is to understand how co‐operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third‐party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co‐operation.     

Infiltration of a facultative ant–plant mutualism by the introduced Argentine ant: effects on mutualist diversity and mutualism benefits

1. Ant–plant mutualisms have been the focus of considerable empirical research, but few studies have investigated how introduced ants affect these interactions. Using 2 years of survey data, this study examines how the introduced Argentine ant [Linepithema humile (Mayr)] differs from native ants with respect to its ability to protect the extrafloral nectary‐bearing coast barrel cactus (Ferocactus viridescens) in Southern California. 2. Eighteen native ant species visited cacti in uninvaded areas, but cacti in invaded areas were primarily visited by the Argentine ant. The main herbivore of the coast barrel cactus present at the study sites is a leaf‐footed bug (Narnia wilsoni). 3. Herbivore presence (the fraction of surveys in which leaf‐footed bugs were present on individual cacti) was negatively related to ant presence (the fraction of surveys in which ants were present on individual cacti). Compared with cacti in uninvaded areas, those in invaded areas were less likely to have herbivores and when they did had them less often. 4. Seed mass was negatively related to herbivore presence, and this relationship did not differ for cacti in invaded areas versus those in uninvaded areas. 5. Although the Argentine ant might provide superior protection from herbivores, invasion‐induced reductions in ant mutualist diversity could potentially compromise plant reproduction. The cumulative number of ant species on individual cacti over time was lower in invaded areas and was associated with a shortened seasonal duration of ant protection and reduced seed mass. These results support the hypothesis that multiple partners may enhance mutualism benefits.     

Synergistic effects of floral phytochemicals against a bumble bee parasite

Floral landscapes comprise diverse phytochemical combinations. Individual phytochemicals in floral nectar and pollen can reduce infection in bees and directly inhibit trypanosome parasites. However, gut parasites of generalist pollinators, which consume nectar and pollen from many plant species, are exposed to phytochemical combinations. Interactions between phytochemicals could augment or decrease effects of single compounds on parasites. Using a matrix of 36 phytochemical treatment combinations, we assessed the combined effects of two floral phytochemicals, eugenol and thymol, against four strains of the bumblebee gut trypanosome Crithidia bombi. Eugenol and thymol had synergistic effects against C. bombi growth across seven independent experiments, showing that the phytochemical combination can disproportionately inhibit parasites. The strength of synergistic effects varied across strains and experiments. Thus, the antiparasitic effects of individual compounds will depend on both the presence of other phytochemicals and parasite strain identity. The presence of synergistic phytochemical combinations could augment the antiparasitic activity of individual compounds for pollinators in diverse floral landscapes.     

Host nuclear genotype influences phenotype of a conditional mutualist symbiont

Arthropods commonly carry maternally inherited intracellular bacterial symbionts that may profoundly influence host biology and evolution. The intracellular symbiont Rickettsia sp. nr. bellii swept rapidly into populations of the sweetpotato whitefly Bemisia tabaci in the south‐western USA. Previous laboratory experiments showed female‐bias and fitness benefits were associated with Rickettsia infection, potentially explaining the high frequencies of infection observed in field populations, but the effects varied with whitefly genetic line. Here, we explored whether host extranuclear or nuclear genes influenced the variation in the Rickettsia–host phenotype in two genetic lines of the whitefly host, each with Rickettsia‐infected and uninfected sublines. Introgression between the Rickettsia‐infected subline of one genetic line and the Rickettsia‐uninfected subline of the other was used to create two new sublines, each with the maternally inherited extranuclear genetic lineages of one line (Rickettsia, two other symbionts and the mitochondria) and the nuclear genotype of the other. Performance assays comparing the original and new lines showed that in addition to Rickettsia, the interaction of Rickettsia infection with host nuclear genotype influenced development time and the sex ratio of the progeny, whereas the extranuclear genotype did not. Host nuclear genotype, but not extranuclear genotype, also influenced the titre of Rickettsia. Our results support the hypothesis that differences in host nuclear genotype alone may explain considerable within‐population variation in host–symbiont phenotype and may contribute to the observed variation in Rickettsia–whitefly interactions worldwide.     

Phenological matching rather than genetic variation in host preference underlies geographical variation in host plants used by orange tip butterflies

An insect species that shows variation in host species association across its geographical range may do so either because of local adaptation in host plant preference of the insect or through environmentally or genetically induced differences in the plants, causing variation in host plant suitability between regions. In the present study, we experimentally investigate the host plant preference of Anthocharis cardamines (orange tip butterfly) in two populations from the UK and two from Sweden. Previous reports indicate that A. cardamines larvae are found on different host plant species in different regions of the UK, and some variation has been reported in Sweden. Host plant choice trials showed that females prefer to oviposit on plants in an earlier phenological stage, as well as on larger plants. When controlling for plant phenological stage and size, the host species had no statistically significant effect on the choice of the females. Moreover, there were no differences in host plant species preference among the four butterfly populations. Based on our experiment, the oviposition choice by A. cardamines mainly depends on the phenological stage and the size of the host plant. This finding supports the idea that the geographical patterns of host–plant association of A. cardamines in the UK and Sweden are consequences of the phenology and availability of the local hosts, rather than regional genetic differences in the host species preference of the butterfly.     

Inoculation of susceptible and resistant potato plants with the late blight pathogen Phytophthora infestans: effects on an aphid and its parasitoid

Plants are exposed to microbial pathogens as well as herbivorous insects and their natural enemies. Here, we examined the effects of inoculation of potato plants, Solanum tuberosum L. (Solanaceae), with the late blight pathogen Phytophthora infestans (Mont.) de Bary (Peronosporales: Pythiaceae) on an aphid species commonly infesting potato crops and one of the aphid's major parasitoids. We observed the peach‐potato aphid, Myzus persicae Sulzer (Hemiptera: Aphididae), and its natural enemy, the biocontrol agent Aphidius colemani Viereck (Hymenoptera: Braconidae), on potato either inoculated with water or P. infestans. Population growth of the aphid, parasitism rate of its natural enemy, and other insect life‐history traits were compared on several potato genotypes, the susceptible cultivar Désirée and genetically modified (GM) isogenic lines carrying genes conferring resistance to P. infestans. Effects of P. infestans inoculation on the intrinsic rate of aphid population increase and the performance of the parasitoid were only found on the susceptible cultivar. Insect traits were similar when comparing inoculated with non‐inoculated resistant GM genotypes. We also tested how GM‐plant characteristics such as location of gene insertion and number of R genes could influence non‐target insects by comparing insect performance among GM events. Different transformation events leading to different positions of R‐gene insertion in the genome influenced aphids either with or without P. infestans infection, whereas effects of position of R‐gene insertion on the parasitoid A. colemani were evident only in the presence of inoculation with P. infestans. We conclude that it is important to study different transformation events before continuing with further stages of risk assessment of this GM crop. This provides important information on the effects of plant resistance to a phytopathogen on non‐target insects at various trophic levels.     

Impact of plant and aphid stress history on infestation in arugula plants

Plants can activate inducible defence mechanisms against pests, pathogens, or chemical elicitors, such as ozone, mediated by reactive oxygen species (ROS), particularly hydrogen peroxide (H₂O₂). An unfavourable balance between ROS production and the plant antioxidant capacity seems to be responsible for the resulting susceptibility of the plant to insect attack. Arugula plants [Eruca sativa Mill. (Brassicaceae)] and green peach aphids, Myzus persicae (Sulzer) (Hemiptera: Aphididae), were used in this study to test the hypothesis that the growth of an aphid population depends on both plant and insect stress history. We investigated the impact of density and duration of a previous aphid infestation, and the time lag before re‐infestation, on aphid population growth. In a second experiment, we assessed the effect on aphid population growth of previous ozone exposure of arugula plants in open top chambers receiving a continuous O₃ fumigation of 100–120 p.p.b., 90 min per day during 3 days. A third experiment was conducted to study the effect of aphid density during a previous infestation on the population growth on an uninfested host. Both previous herbivory and ozone changed the oxidative status of plant tissues and facilitated aphid population growth, which increased with the duration and density of a previous infestation by aphids. Colonization success also depended on the aphids' own history. Aphids coming from high‐density populations and/or longer infestation periods produced larger populations on an (initially) uninfested plant. Pest outbreaks in a polluted environment might be expected to be modulated by the hosts' spatial‐temporal heterogeneity related to the ozone exposure and previous herbivory.     

The inter‐kingdom volatile signal indole promotes root development by interfering with auxin signalling

Recently, emission of volatile organic compounds (VOCs) has emerged as a mode of communication between bacteria and plants. Although some bacterial VOCs that promote plant growth have been identified, their underlying mechanism of action is unknown. Here we demonstrate that indole, which was identified using a screen for Arabidopsis growth promotion by VOCs from soil‐borne bacteria, is a potent plant‐growth modulator. Its prominent role in increasing the plant secondary root network is mediated by interfering with the auxin‐signalling machinery. Using auxin reporter lines and classic auxin physiological and transport assays we show that the indole signal invades the plant body, reaches zones of auxin activity and acts in a polar auxin transport‐dependent bimodal mechanism to trigger differential cellular auxin responses. Our results suggest that indole, beyond its importance as a bacterial signal molecule, can serve as a remote messenger to manipulate plant growth and development.     

Biogeography of mutualistic fungi cultivated by leafcutter ants

Leafcutter ants propagate co‐evolving fungi for food. The nearly 50 species of leafcutter ants (Atta, Acromyrmex) range from Argentina to the United States, with the greatest species diversity in southern South America. We elucidate the biogeography of fungi cultivated by leafcutter ants using DNA sequence and microsatellite‐marker analyses of 474 cultivars collected across the leafcutter range. Fungal cultivars belong to two clades (Clade‐A and Clade‐B). The dominant and widespread Clade‐A cultivars form three genotype clusters, with their relative prevalence corresponding to southern South America, northern South America, Central and North America. Admixture between Clade‐A populations supports genetic exchange within a single species, Leucocoprinus gongylophorus. Some leafcutter species that cut grass as fungicultural substrate are specialized to cultivate Clade‐B fungi, whereas leafcutters preferring dicot plants appear specialized on Clade‐A fungi. Cultivar sharing between sympatric leafcutter species occurs frequently such that cultivars of Atta are not distinct from those of Acromyrmex. Leafcutters specialized on Clade‐B fungi occur only in South America. Diversity of Clade‐A fungi is greatest in South America, but minimal in Central and North America. Maximum cultivar diversity in South America is predicted by the Kusnezov–Fowler hypothesis that leafcutter ants originated in subtropical South America and only dicot‐specialized leafcutter ants migrated out of South America, but the cultivar diversity becomes also compatible with a recently proposed hypothesis of a Central American origin by postulating that leafcutter ants acquired novel cultivars many times from other nonleafcutter fungus‐growing ants during their migrations from Central America across South America. We evaluate these biogeographic hypotheses in the light of estimated dates for the origins of leafcutter ants and their cultivars.     

The NIa‐Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector,Myzus persicae (green peach aphid)

Many plant viruses depend on aphids and other phloem‐feeding insects for transmission within and among host plants. Thus, viruses may promote their own transmission by manipulating plant physiology to attract aphids and increase aphid reproduction. Consistent with this hypothesis, Myzus persicae (green peach aphids) prefer to settle on Nicotiana benthamiana infected with Turnip mosaic virus (TuMV) and fecundity on virus‐infected N. benthamiana and Arabidopsis thaliana (Arabidopsis) is higher than on uninfected controls. TuMV infection suppresses callose deposition, an important plant defense, and increases the amount of free amino acids, the major source of nitrogen for aphids. To investigate the underlying molecular mechanisms of this phenomenon, 10 TuMV genes were over‐expressed in plants to determine their effects on aphid reproduction. Production of a single TuMV protein, nuclear inclusion a‐protease domain (NIa‐Pro), increased M. persicae reproduction on both N. benthamiana and Arabidopsis. Similar to the effects that are observed during TuMV infection, NIa‐Pro expression alone increased aphid arrestment, suppressed callose deposition and increased the abundance of free amino acids. Together, these results suggest a function for the TuMV NIa‐Pro protein in manipulating the physiology of host plants. By attracting aphid vectors and promoting their reproduction, TuMV may influence plant–aphid interactions to promote its own transmission.     

Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants

Plants can detect cues associated with the risk of future herbivory and modify defence phenotypes accordingly; however, our current understanding is limited both with respect to the range of early warning cues to which plants respond and the nature of the responses. Here we report that exposure to volatile emissions from plant tissues infested with herbivore eggs promotes stronger defence responses to subsequent herbivory in two Brassica species. Furthermore, exposure to these volatile cues elicited an apparent shift from growth to reproduction in Brassica nigra, with exposed plants exhibiting increased flower and seed production, but reduced leaf production, relative to unexposed controls. Our results thus document plant defence priming in response to a novel environmental cue, oviposition‐induced plant volatiles, while also showing that plant responses to early warning cues can include changes in both defence and life‐history traits.     

Evidence for adaptive divergence of thermal responses among Bemisia tabaci populations from tropical Colombia following a recent invasion

There is an increasing evidence that populations of ectotherms can diverge genetically in response to different climatic conditions, both within their native range and (in the case of invasive species) in their new range. Here, we test for such divergence in invasive whitefly Bemisia tabaci populations in tropical Colombia, by considering heritable variation within and between populations in survival and fecundity under temperature stress, and by comparing population differences with patterns established from putatively neutral microsatellite markers. We detected significant differences among populations linked to mean temperature (for survival) and temperature variation (for fecundity) in local environments. A Q_ST ? F_ST analysis indicated that phenotypic divergence was often larger than neutral expectations (Q_ST > F_ST). Particularly, for survival after a sublethal heat shock, this divergence remained linked to the local mean temperature after controlling for neutral divergence. These findings point to rapid adaptation in invasive whitefly likely to contribute to its success as a pest species. Ongoing evolutionary divergence also provides challenges in predicting the likely impact of Bemisia in invaded regions.