Offspring nursing extends mother's longevity in a long-term maternal cared spider.

Females typically outlive males in animals, especially in species that provide long-term maternal care. However, life history theory predicts that investments in reproduction, such as lactation and offspring nursing, often shorten caretakers' longevity. Aiming to interpret this paradox, we selected the lactating jumping spider Toxeus magnus to investigate the effects of reproductive activities on longevity for two sexes. We found that: (1) although "milk" provisioning reduces female's longevity, mothers who cared for offspring (provisioned "milk" and nursing) lived the longest compared to virgins and those did not provide care; (2) copulation increased female's longevity but had no effects on males; and (3) the two sexes have comparable developmental duration, but the female adult's longevity was 2.1 times that of male's. This study suggests that the time requirement for offspring dispersal might act as a key selective force favoring females' adulthood extension, which ultimately generates the longer-lived females in maternal cared species.

The effects of prey lipid on female mating and reproduction of a wolf spider.

As predators, the macronutrients spiders extract from their prey play important roles in their mating and reproduction. Previous studies of macronutrients on spider mating and reproduction focus on protein, the potential impact of prey lipid content on spider mating and reproduction remains largely unexplored. Here, we tested the influence of prey varying in lipid content on female mating, sexual cannibalism, reproduction, and offspring fitness in the wolf spider Pardosa pseudoannulata. We acquired 2 groups of fruit fly Drosophila melanogaster that differed significantly in lipid but not protein content by supplementing cultural media with a high or low dose of sucrose on which the fruit flies were reared (HL: high lipid and LL: low lipid). Subadult (i.e., 1 molt before adult) female spiders that fed HL flies matured with significantly higher lipid content than those fed LL flies. We found that the mated females fed with HL flies significantly shortened pre-oviposition time and resulted in a significantly higher fecundity. However, there was no significant difference in female spiders varying in lipid content on other behaviors and traits, including the latency to courtship, courtship duration, mating, copulation duration, sexual cannibalism, offspring body size, and survival. Hence, our results suggest that the lipid content of prey may be a limiting factor for female reproduction, but not for other behavioral traits in the wolf spiders P. pseudoannulata.

Sulfoxaflor Alters Bemisia tabaci MED (Hemiptera: Aleyrodidae) Preference, Feeding, and TYLCV Transmission.

Many damaging agricultural pests can, in addition to their direct feeding damage, acquire and transmit plant pathogens. Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) is considered a 'supervector' of disease-causing plant pathogens and viruses. One of the most damaging of these is Tomato yellow leaf curl virus (TYLCV), a circulatively transmitted begomovirus than can extensively damage field and greenhouse crops. Because sustained feeding periods are necessary to acquire and transmit circulatively transmitted viruses, pesticides that, in addition to their direct lethality, suppress feeding in surviving individuals may be particularly effective in decreasing viral transmission. We assessed the impact of sulfoxaflor, a sulfoximine insecticide, on the settling preference, feeding, and viral transmission of TYLCV-carrying B. tabaci on tomato. We found that viruliferous B. tabaci avoided both settling and feeding on sulfoxaflor-treated plants, and that sulfoxaflor virtually eliminated the transmission of TYLCV by B. tabaci. The antifeedant properties of sulfoxaflor have previously been reported in other pest systems; our results document similar effects on viruliferous B. tabaci and demonstrate that this pesticide can reduce TYLCV transmission by surviving individuals.

Lethal and Sublethal Effects of Flupyradifurone on Bemisia tabaci MED (Hemiptera: Aleyrodidae) Feeding Behavior and TYLCV Transmission in Tomato.

Pesticides primarily affect target organisms via direct toxicity, but may also alter the feeding behaviors of surviving individuals in ways that alter their effect on host plants. The latter impact is especially important when pests can transmit plant pathogens. The Mediterranean (MED) population of the sweetpotato whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) transmits Tomato yellow leaf curl virus (TYLCV), a pathogen that can be economically devastating in field and greenhouse cropping systems. We first assessed the impact of sublethal (LC15) and label concentrations of flupyradifurone, a butenolide-derived insecticide, on the feeding behavior of TYLCV-infected MED on tomato. We next measured the effect of flupyradifurone on plant TYLCV load, vector transmission efficiency, and MED survival. Both the LC15 and label flupyradifurone concentrations dramatically altered MED feeding and caused the near cessation of both salivation and phloem ingestion (necessary for viral transmission and acquisition, respectively). Both concentrations also significantly reduced plant TYLCV load, and the label rate of flupyradifurone sharply decreased TYLCV transmission while killing >99% of MED. As the first report of pesticide-induced changes in the feeding behavior of viruliferous Bemisia, our findings highlight the potential importance of chemically driven feeding cessation in the control of TYLCV and other Bemisia-transmitted plant pathogens.

High-lipid prey reduce juvenile survivorship and delay egg laying in a small linyphiid spider Hylyphantes graminicola.

Prey proteins and lipids greatly impact predator life-history traits. However, life-history plasticity offers predators the opportunity to tune the life-history traits in response to the limited macronutrients to allocate among traits. A fast-growing predator species with a strict maturation time may be more likely to consume nutritionally imbalanced prey. Here, we tested this hypothesis by examining the effect of the protein-to-lipid ratio in prey on a small sheet web-building spider, Hylyphantes graminicola, with a short life span, using adult Drosophila melanogaster as the prey. By manipulating the macronutrient content of the prey to generate three prey types with different protein-to-lipid ratios (i.e. high, intermediate and low), we demonstrated that the majority of the spiders that consumed only these flies could reach full maturity. However, juvenile spiders that consumed high-lipid (low protein-to-lipid ratio) flies had a higher rate of mortality than those consuming medium-protein and high-protein flies. The prey protein-to-lipid ratio had no significant effects on the developmental duration and size at maturity. Although the prey protein-to-lipid ratio had no significant influence on mating behaviour and female fecundity, females reared on high-lipid flies exhibited a significant delay in oviposition compared with those reared on high-protein flies. We conclude that high-lipid prey has negative effects on the survival and reproductive function of H. graminicola Our study thus provides clear evidence that low plasticity with fast development to a certain size means a high nutritional requirement for protein at a cost of lower survival and prolonged time to egg laying when prey have low protein-to-lipid content in H. graminicola.

Influence of maternal diet on offspring survivorship, growth, and reproduction in a sheetweb spider.

Prey vary dramatically in quality, and maternal diet is generally assumed to substantially influence offspring survivorship, growth, and reproduction in spiders. Numerous studies that have tested this hypothesis have focused exclusively on parental generation or have considered relatively few fitness components of juvenile offspring. However, maternal diet may have a substantial effect on fitness performance beyond juvenile offspring. Here, we investigated the influence of one-time maternal feeding on multiple offspring fitness components, including the survival rate and growth of juvenile offspring as well as the mating and reproductive success of adult offspring in Hylyphantes graminicola, a sheetweb spider with an extremely short lifespan (∼1 month). We fed field-collected adult female spiders two different diets only once immediately before oviposition: midges (Tendipes sp.) only (MO) or flies (Drosophila melanogaster) only (FO). Juvenile offspring of MO females had significantly higher survival rate, faster growth, and larger male size at maturity than FO offspring. Although maternal diet did not significantly influence mating behavior or fecundity of female offspring overall, those of MO females laid eggs earlier and their eggs also hatched earlier and had a higher hatching rate than those of FO females. Intriguingly, one-time maternal feeding was sufficient to have such an influence on offspring fitness even beyond juvenile offspring in Hgraminicola This one-time maternal effect may be widespread in other spiders and other invertebrates with a short lifespan.This article has an associated First Person interview with the first author of the paper.

Tomato Yellow Leaf Curl Virus Infection Alters Bemisia tabaci MED (Hemiptera: Aleyrodidae) Vulnerability to Flupyradifurone.

The whitefly, Bemisia tabaci Gennadius, is a major phloem-feeding pest of agricultural crops that is also an important vector of many plant diseases. The B. tabaci Mediterranean ('MED') biotype is a particularly effective vector of Tomato yellow leaf curl virus (TYLCV), a devastating plant pathogen. Although insecticides play an important role in the control of MED and TYLCV, little is known about how TYLCV infection affects MED susceptibility to insecticides. We conducted research addressing how MED susceptibility to flupyradifurone, the first commercially available systemic control agent derived from the butenolide class of insecticides, was affected by TYLCV infection. We first conducted bioassays determining the LC15 and LC50 for control and viruliferous MED feeding on either water- or insecticide-treated plants. We next measured several demographic parameters of control and viruliferous MED exposed to either insecticide- or water-treated plants. TYLCV infection increased MED tolerance of flupyradifurone: the LC15 and LC50 of viruliferous MED were double that of uninfected MED. Viral infection also altered MED demographic responses to flupyradifurone, but in an inconsistent manner. Although the ability of TYLCV and other persistently transmitted viruses to benefit Bemisia via manipulation of host plant defense is well known, this appears to be the first example of virally mediated changes in vector susceptibility to an insecticide.

Feeding behavior explains the different effects of cabbage on MEAM1 and MED cryptic species of Bemisia tabaci.

MEAM1 (Middle East-Asia Minor 1, "B" biotype) and MED (Mediterranean, "Q" biotype) are the two most destructive cryptic species of the Bemisia tabaci complex on the planet. Our previous studies have shown that MEAM1 outcompetes MED on cabbage; the underlying mechanism is unknown. In the Brassicaceae family, the glucosinolate-myrosinase defense system plays a crucial role in deterring feeding, inhibiting growth, and causing acute toxicity against a wide range of generalist herbivores. In the present study, we first compared the survival of MEAM1 and MED exposed to sinigrin (a glucosinolate) and myrosinase (an enzyme that degrades glucosinolates); we found that survival of both species was high in response to sinigrin alone but was near zero in response to sinigrin + myrosinase. We then used electropenetrography (electrical penetration graphs, EPG) to assess the feeding behaviors of MEAM1 and MED whiteflies on cabbage. The EPG results revealed that the mean duration of each potential drop (pd, indicating an intracellular puncture) was substantially longer for MED than MEAM1 on cabbage, indicating that the exposure to the toxic hydrolysates of glucosinolate and myrosinase is greater for MED than for MEAM1. We therefore conclude that differences in penetrating behaviors may help explain the different effects of cabbage on MEAM1 and MED whitefly species.

Mating experience affects male mating success, but not female fecundity in the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae).

In a mating system in which females are monandrous and males are polygynous, females may incur a risk by mating with males with possible sperm depletion following consecutive matings. Here, we examined the effects of male mating history on male mating success and female reproductive fitness in the wolf spider Pardosa pseudoannulata by performing mating trials and sperm counting experiments. Results showed that male mating history had a significant negative impact on subsequent copulation success but had little effect on courtship duration and courtship intensity. In addition, neither male courtship intensity nor morphological measurements of males and females had significant effects on male mating success. Furthermore, male mating history had no obvious impact on the fecundity of inseminated females, with no significant differences observed in the oviposition rate of females, the numbers and the carapace width of the second-instar spiderlings between treatments. Results showed that the number of sperm decreased significantly after mating but could be replenished, with no significant differences observed between groups in which males had rested for 7 d. These findings suggest that polygynous male spiders may recharge their sperm during the mating season, but how females differentiate the mating status of males remains unknown.

Prolonged milk provisioning in a jumping spider.

Lactation is a mammalian attribute, and the few known nonmammal examples have distinctly different modalities. We document here milk provisioning in a jumping spider, which compares functionally and behaviorally to lactation in mammals. The spiderlings ingest nutritious milk droplets secreted from the mother's epigastric furrow until the subadult stage. Milk is indispensable for offspring survival in the early stages and complements their foraging in later stages. Maternal care, as for some long-lived vertebrates, continues after the offspring reach maturity. Furthermore, a female-biased adult sex ratio is acquired only when the mother is present. These findings demonstrate that mammal-like milk provisioning and parental care for sexually mature offspring have also evolved in invertebrates, encouraging a reevaluation of their occurrence across the animal kingdom, especially in invertebrates.

Persistently Transmitted Viruses Restrict the Transmission of Other Viruses by Affecting Their Vectors.

Diverse pathogens, plant hosts, insect vectors, and non-vector herbivores coexist and interact in natural systems. An example is the cooccurrence of insects Bemisia tabaci Q and Frankliniella occidentalis and the pathogens tomato yellow leaf curl virus (TYLCV) and tomato spotted wilt virus (TSWV) on the same plant. In addition, both TYLCV and TSWV are persistently transmitted in these insect species. However, TSWV reduces the fitness of B. tabaci Q; therefore, we investigated whether TSWV affects the transmission of TYLCV to tomato. Both TYLCV and TSWV are persistently transmitted. Although B. tabaci Q cannot transmit TSWV, we found that this insect species is able to acquire and retain this virus serotype, indicating that the effects of TSWV on TYLCV transmission in the current study result from effects on the vector. The acquisition, retention, and transmission of TYLCV by B. tabaci Q were reduced when the insect vector contained TSWV. Additionally, the TYLCV acquisition and transmission by B. tabaci Q were reduced when the host plant was inoculated with TSWV before TYLCV or simultaneously with TYLCV. We also found that F. occidentalis fecundity and transmission of TSWV were reduced when F. occidentalis contained TYLCV. Our findings are consistent with the hypothesis that persistently transmitted viruses can restrict the transmission of other viruses by affecting their insect vectors.

Seasonal variations in body melanism and size of the wolf spider Pardosa astrigera (Araneae: Lycosidae).

Variations in species morphology and life-history traits strongly correlate with geographic and climatic characteristics. Most studies on morphological variations in animals focus on ectotherms distributed on a large geographic scale across latitudinal and/or altitudinal gradient. However, the morphological variations of spiders living in the same habitats across different seasons have not been reported. In this study, we used the wolf spider, Pardosa astrigera, as a model to determine seasonal differences in adult body size, melanism, fecundity, and egg diameter both in the overwintering and the first generation for 2010 and 2016. The results showed that in 2010, both females and males of the overwintering generation were significantly darker than the first generation. Moreover, the overwintering females were markedly larger and produced more and bigger eggs than the first generation in both 2010 and 2016. Considering the overwintering P. astrigera experiencing low temperature and/or desiccation stress, these results suggest that substantially darker and larger body of the overwintering generation is adaptive to adverse conditions.

The ability to manipulate plant glucosinolates and nutrients explains the better performance of Bemisia tabaci Middle East-Asia Minor 1 than Mediterranean on cabbage plants.

The performance of herbivorous insects is greatly affected by host chemical defenses and nutritional quality. Some herbivores have developed the ability to manipulate plant defenses via signaling pathways. It is currently unclear, however, whether a herbivore can benefit by simultaneously reducing plant defenses and enhancing plant nutritional quality. Here, we show that the better performance of the whitefly Bemisia tabaci Middle East-Asia Minor 1 (MEAM1; formerly the "B" biotype) than Mediterranean (MED; formerly the "Q" biotype) on cabbage is associated with a suppression of glucosinolate (GS) content and an increase in amino acid supply in MEAM1-infested cabbage compared with MED-infested cabbage. MEAM1 had higher survival, higher fecundity, higher intrinsic rate of increase (rm), a longer life span, and a shorter developmental time than MED on cabbage plants. Amino acid content was higher in cabbage infested with MEAM1 than MED. Although infestation by either biotype decreased the levels of total GS, aliphatic GS, glucoiberin, sinigrin, glucobrassicin, and 4OH-glucobrassicin, and the expression of related genes in cabbage, MED infestation increased the levels of 4ME-glucobrassicin, neoglucobrassicin, progoitrin, and glucoraphanin. The GS content and expression of GS-related genes were higher in cabbage infested with MED than with MEAM1. Our results suggest that MEAM1 performs better than MED on cabbage by manipulating host defenses and nutritional quality.

Effects of Heat Shock on the Bradysia odoriphaga (Diptera: Sciaridae).

Bradysia odoriphaga is frequently subjected to heat shock during the summer in China. Although the effects of heat shock on insect ecology and physiology have been widely explored, the effects of heat shock on the life history parameters of Bradysia odoriphaga are largely unknown. In the present study, we investigated the effects of heat shock on B. odoriphaga survival and reproduction as well as on offspring development and sex ratio. We exposed adult B. odoriphaga to 31, 33, 35, or 37 °C for different durations (from 0 to 120 min). The results showed that the survival of both sexes declined with the increase in temperature and exposure time, especially at 33, 35, and 37 °C. Longevity was markedly greater for males than females across all treatments. Fecundity generally declined as temperature and exposure time increased, and no eggs hatched when females were exposed to 37 °C for >75 min. The development of offspring larvae was significantly delayed when the parent female and male had been exposed to ≥31 °C for ≥30 min. In addition, the sex ratio of F1 progeny derived from heat-shocked parental adults was increasingly skewed to female as exposure time and temperature treatment increased. Overall, the results indicate that heat shock negatively influences B. odoriphaga.

Genome sequencing of the sweetpotato whitefly Bemisia tabaci MED/Q.

The sweetpotato whitefly Bemisia tabaci is a highly destructive agricultural and ornamental crop pest. It damages host plants through both phloem feeding and vectoring plant pathogens. Introductions of B. tabaci are difficult to quarantine and eradicate because of its high reproductive rates, broad host plant range, and insecticide resistance. A total of 791 Gb of raw DNA sequence from whole genome shotgun sequencing, and 13 BAC pooling libraries were generated by Illumina sequencing using different combinations of mate-pair and pair-end libraries. Assembly gave a final genome with a scaffold N50 of 437 kb, and a total length of 658 Mb. Annotation of repetitive elements and coding regions resulted in 265.0 Mb TEs (40.3%) and 20 786 protein-coding genes with putative gene family expansions, respectively. Phylogenetic analysis based on orthologs across 14 arthropod taxa suggested that MED/Q is clustered into a hemipteran clade containing A. pisum and is a sister lineage to a clade containing both R. prolixus and N. lugens. Genome completeness, as estimated using the CEGMA and Benchmarking Universal Single-Copy Orthologs pipelines, reached 96% and 79%. These MED/Q genomic resources lay a foundation for future 'pan-genomic' comparisons of invasive vs. noninvasive, invasive vs. invasive, and native vs. exotic Bemisia, which, in return, will open up new avenues of investigation into whitefly biology, evolution, and management.

Natal Host Plants Can Alter Herbivore Competition.

Interspecific competition between herbivores is widely recognized as an important determinant of community structure. Although researchers have identified a number of factors capable of altering competitive interactions, few studies have addressed the influence of neighboring plant species. If adaptation to/ epigenetic effects of an herbivore's natal host plant alter its performance on other host plants, then interspecific herbivore interactions may play out differently in heterogeneous and homogenous plant communities. We tested wether the natal host plant of a whitefly population affected interactions between the Middle-east Asia Minor 1 (MEAM1) and Mediterranean (MED) cryptic species of the whitefly Bemisia tabaci by rearing the offspring of a cabbage-derived MEAM1 population and a poinsettia-derived MED population together on three different host plants: cotton, poinsettia, and cabbage. We found that MED dominated on poinsettia and that MEAM1 dominated on cabbage, results consistent with previous research. MED also dominated when reared with MEAM1 on cotton, however, a result at odds with multiple otherwise-similar studies that reared both species on the same natal plant. Our work provides evidence that natal plants affect competitive interactions on another plant species, and highlights the potential importance of neighboring plant species on herbivore community composition in agricultral systems.

Differing Behavioural Responses of Bemisia tabaci MEAM1 and MED to Cabbage Damaged by Conspecifics and Heterospecifics.

The whitefly Bemisia tabaci is a serious pest with an extensive host range. Previous research has shown that B. tabaci is a species complex with many cryptic species or biotypes and that the two most important species are MEAM1 (Middle East-Minor Asia 1) and MED (Mediterranean genetic group). MEAM1 and MED are known to differ in their preference for cabbage, Brassica oleracea, as a host plant, however, the mechanism underlying this preference is unknown. In the current study, a host choice experiment showed that MED prefers to settle and oviposit on undamaged cabbage plants rather than MED-damaged cabbage plants. However, MEAM1 prefers MED-damaged cabbage plants to undamaged plants and does not exhibit a significant preference for undamaged or MEAM1-damaged cabbage plants. On the basis of gas chromatography-mass spectrometry (GC-MS) analysis, the following volatiles were released in larger quantities from Q-damaged cabbage plants than from undamaged plants: 2-ethyl-1-hexanol, benzenemethanol, (E)-2-decenol, benzaldehyde, nonanal, acetic acid geraniol ester, 4-hydroxy-4-methyl-2-pentanone, decane, and α-longipinene. Only one volatile, 4-hydroxy-4-methyl-2-pentanone, was released in greater quantities from MEAM1-damaged cabbage plants than from undamaged plants. Our results suggest that differences in herbivore-induced host volatile release may help explain the differences between the preference of B. tabaci MEAM1 and MED for cabbage as a host.

Transcriptome analysis of host-associated differentiation in Bemisia tabaci (Hemiptera: Aleyrodidae).

Host-associated differentiation is one of the driving forces behind the diversification of phytophagous insects. In this study, host induced transcriptomic differences were investigated in the sweetpotato whitefly Bemisia tabaci, an invasive agricultural pest worldwide. Comparative transcriptomic analyses using coding sequence (CDS), 5' and 3' untranslated regions (UTR) showed that sequence divergences between the original host plant, cabbage, and the derived hosts, including cotton, cucumber and tomato, were 0.11-0.14%, 0.19-0.26%, and 0.15-0.21%, respectively. In comparison to the derived hosts, 418 female and 303 male transcripts, respectively, were up-regulated in the original cabbage strain. Among them, 17 transcripts were consistently up-regulated in both female and male whiteflies originated from the cabbage host. Specifically, two ESTs annotated as Cathepsin B or Cathepsin B-like genes were significantly up-regulated in the original cabbage strain, representing a transcriptomic response to the dietary challenges imposed by the host shifting. Results from our transcriptome analysis, in conjunction with previous reports documenting the minor changes in their reproductive capacity, insecticide susceptibility, symbiotic composition and feeding behavior, suggest that the impact of host-associated differentiation in whiteflies is limited. Furthermore, it is unlikely the major factor contributing to their rapid range expansion/invasiveness.

Effects of plant virus and its insect vector on Encarsia formosa, a biocontrol agent of whiteflies.

In this study, we investigated the tritrophic interactions among a persistently transmitted plant virus, Tomato yellow leaf curl virus (TYLCV), its insect vector, the sweetpotato whitefly Bemisia tabaci, and a parasitoid, Encarsia formosa Gahan, one of the most extensively used biological control agents. As an emerging invasive pest worldwide, the two most damaging whiteflies are B. tabaci B and Q cryptic species. On healthy tomato plants, parasitoid-induced mortality was significantly higher in B. tabaci B than in Q. In contrast, similar mortality levels of B and Q were observed on TYLCV-infected plants. A higher rate of parasitism was consistently observed in B, independent of the TYLCV infection. Similarly, the life history traits of E. formosa were influenced by both TYLCV and the two cryptic species of B. tabaci. Specifically, E. formosa parasitizing B had a greater adult longevity and shorter developmental time on healthy plants, whereas the parasitoids developing from Q has a greater adult longevity on TYLCV-infected plants. The emergence rate of E. formosa was unaffected by either B. tabaci cryptic species or the virus. These results suggest that the vector-borne pathogen can manipulate the host suitability of a parasitoid and hence the parasitoid-host interactions.