Alvin M. Simmons

Metabolic Coevolution in the Bacterial Symbiosis of Whiteflies and Related Plant Sap-Feeding Insects

Genomic decay is a common feature of intracellular bacteria that have entered into symbiosis with plant sap-feeding insects. This study of the whitefly Bemisia tabaci and two bacteria (Portiera aleyrodidarum and Hamiltonella defensa) cohoused in each host cell investigated whether the decay of Portiera metabolism genes is complemented by host and Hamiltonella genes, and compared the metabolic traits of the whitefly symbiosis with other sap-feeding insects (aphids, psyllids, and mealybugs). Parallel genomic and transcriptomic analysis revealed that the host genome contributes multiple metabolic reactions that complement or duplicate Portiera function, and that Hamiltonella may contribute multiple cofactors and one essential amino acid, lysine. Homologs of the Bemisia metabolism genes of insect origin have also been implicated in essential amino acid synthesis in other sap-feeding insect hosts, indicative of parallel coevolution of shared metabolic pathways across multiple symbioses. Further metabolism genes coded in the Bemisia genome are of bacterial origin, but phylogenetically distinct from Portiera, Hamiltonella and horizontally transferred genes identified in other sap-feeding insects. Overall, 75% of the metabolism genes of bacterial origin are functionally unique to one symbiosis, indicating that the evolutionary history of metabolic integration in these symbioses is strongly contingent on the pattern of horizontally acquired genes. Our analysis, further, shows that bacteria with genomic decay enable host acquisition of complex metabolic pathways by multiple independent horizontal gene transfers from exogenous bacteria. Specifically, each horizontally acquired gene can function with other genes in the pathway coded by the symbiont, while facilitating the decay of the symbiont gene coding the same reaction.

The detectability half‐life in arthropod predator–prey research: what it is, why we need it, how to measure it, and how to use it

Molecular gut‐content analysis enables detection of arthropod predation with minimal disruption of ecosystem processes. Most assays produce only qualitative results, with each predator testing either positive or negative for target prey remains. Nevertheless, they have yielded important insights into community processes. For example, they have confirmed the long‐hypothesized role of generalist predators in retarding early‐season build‐up of pest populations prior to the arrival of more specialized predators and parasitoids and documented the ubiquity of secondary and intraguild predation. However, raw qualitative gut‐content data cannot be used to assess the relative impact of different predator taxa on prey population dynamics: they must first be weighted by the relative detectability periods for molecular prey remains for each predator–prey combination. If this is not carried out, interpretations of predator impact will be biased towards those with the longest detectabilities. We review the challenges in determining detectability half‐lives, including unstated assumptions that have often been ignored in the performance of feeding trials. We also show how detectability half‐lives can be used to properly weight assay data to rank predators by their importance in prey population suppression, and how sets of half‐lives can be used to test hypotheses concerning predator ecology and physiology. We use data from 32 publications, comprising 97 half‐lives, to generate and test hypotheses on taxonomic differences in detectability half‐lives and discuss the possible role of the detectability half‐life in interpreting qPCR and next‐generation sequencing data.

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

BackgroundThe whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) is among the 100 worst invasive species in the world. As one of the most important crop pests and virus vectors, B. tabaci causes substantial crop losses and poses a serious threat to global food security.ResultsWe report the 615-Mb high-quality genome sequence of B. tabaci Middle East-Asia Minor 1 (MEAM1), the first genome sequence in the Aleyrodidae family, which contains 15,664 protein-coding genes. The B. tabaci genome is highly divergent from other sequenced hemipteran genomes, sharing no detectable synteny. A number of known detoxification gene families, including cytochrome P450s and UDP-glucuronosyltransferases, are significantly expanded in B. tabaci. Other expanded gene families, including cathepsins, large clusters of tandemly duplicated B. tabaci-specific genes, and phosphatidylethanolamine-binding proteins (PEBPs), were found to be associated with virus acquisition and transmission and/or insecticide resistance, likely contributing to the global invasiveness and efficient virus transmission capacity of B. tabaci. The presence of 142 horizontally transferred genes from bacteria or fungi in the B. tabaci genome, including genes encoding hopanoid/sterol synthesis and xenobiotic detoxification enzymes that are not present in other insects, offers novel insights into the unique biological adaptations of this insect such as polyphagy and insecticide resistance. Interestingly, two adjacent bacterial pantothenate biosynthesis genes, panB and panC, have been co-transferred into B. tabaci and fused into a single gene that has acquired introns during its evolution.ConclusionsThe B. tabaci genome contains numerous genetic novelties, including expansions in gene families associated with insecticide resistance, detoxification and virus transmission, as well as numerous horizontally transferred genes from bacteria and fungi. We believe these novelties likely have shaped B. tabaci as a highly invasive polyphagous crop pest and efficient vector of plant viruses. The genome serves as a reference for resolving the B. tabaci cryptic species complex, understanding fundamental biological novelties, and providing valuable genetic information to assist the development of novel strategies for controlling whiteflies and the viruses they transmit.

Analysis based on RAPD and ISSR markers reveals closer similarities among Citrullus and Cucumis species than with Praecitrullus fistulosus (Stocks) Pangalo

A cucurbit species named Praecitrullus fistulosus (Stocks) Pangalo, which thrives in India, is considered to be a distant relative of watermelon. Recent experiments indicated that it has mild resistance to whiteflies (Bemisia tabaci). However, our attempts to cross various US plant introductions (PIs) of P. fistulosus with watermelon or other Citrullus PIs have not been successful. Thus, to determine genetic relatedness among those species, phylogenetic analysis [based on simple sequence repeat (SSR)–anchored (also termed ISSR), and randomly amplified polymorphic DNA (RAPD) markers] was conducted among PIs of P. fistulosus, Citrullus lanatus var. lanatus (watermelon), C. lanatus var. citroides and the wild Citrullus colocynthis. Phylogenetic relationships were also examined with Cucumis melo (melon), Cucumis sativus (cucumber), and wild Cucumis species including C. africanus, C. metuliferus, C. anguria, C. meeusei, and C. zeyheri. Wide genetic distance exists between Citrullus and Cucumis groups (8% genetic similarity). Phylogenetic relationships among Citrullus species and subspecies are closer (25–55% genetic similarity) as compared with those among most Cucumis species (14–68% genetic similarity). P. fistulosus appeared to be distant from both Cucumis and Citrullus species (genetic similarity between P. fistulosus and Cucumis or Citrullus groups is less than 3%). Although wide genetic differences and reproductive barriers exist among cucurbit species examined in this study, they are still considered as potential germplasm source for enhancing watermelon and melon crops using traditional breeding and biotechnology procedures.

Attractancy and Ovipositional Response of Adult Bemisia argentifolii (Homoptera: Aleyrodidae) to Type IV Trichome Density on Leaves of Lycopersicon hirsutum Grown in Three Day-Length Regimes

Clonal plants of six accessions of Lycopersicon hirsutum Humb. and Bonpl., a wild relative of tomato, were grown in three day-length regimes. Clones of an accession grown in different day-length re...

Forty-nine new host plant species for Bemisia tabaci (Hemiptera: Aleyrodidae)

The sweetpotato whitefly, Bemisia tabaci (Gennadius), is a worldwide pest of numerous agricultural and ornamental crops. In addition to directly feeding on plants, it also acts as a vector of plant viruses of cultivated and uncultivated host plant species. Moreover, host plants can affect the population dynamics of whiteflies. An open‐choice screening experiment was conducted with B‐biotype B. tabaci on a diverse collection of crops, weeds, and other indigenous plant species. Five of the plant species were further evaluated in choice or no‐choice tests in the laboratory. The results reveal 49 new reproductive host plant species for B. tabaci. This includes 11 new genera of host plants (Arenaria, Avena, Carduus, Dichondra, Glechoma, Gnaphalium, Molugo, Panicum, Parthenocissus, Trianthema, and Triticum) for this whitefly. All species that served as hosts were acceptable for feeding, oviposition, and development to the adult stage by B. tabaci. The new hosts include three cultivated crops [oats (Avena sativa L.), proso millet (Panicum miliaceum L.), and winter wheat (Triticum aestivum L.)], weeds and other wild species, including 32 Ipomoea species, which are relatives of sweetpotato [I. batatas (L.) Lam.)]. Yellow nutsedge, Cyperus esculentus L., did not serve as a host for B. tabaci in either open‐choice or no‐choice tests. The results presented herein have implications for whitefly ecology and the numerous viruses that B. tabaci spreads to and among cultivated plants.

High frequency oligonucleotides: targeting active gene (HFO-TAG) markers revealed wide genetic diversity among Citrullus spp. accessions useful for enhancing disease or pest resistance in watermelon cultivars

There is a continuous need to enhance watermelon cultivars for disease and pest resistance. Different U.S. Plant Introductions (PIs) of Citrullus lanatus subsp. lanatus var. lanatus [also known as C. lanatus (Thunb.) Matsum. et Nakai subsp. lanatus var. citroides (Bailey) Mansf. ex Greb.] (CLC) collected in southern Africa are a useful source for enhancing disease or pest resistance in watermelon cultivars. They are also valuable as rootstocks for grafted watermelon, particularly in fields infested with root-knot nematodes or Fusarium wilt. However, there is little information about genetic relationships among these PIs. In this study, genetic diversity was examined among 74 CLC PIs collected from their center of origin in southern Africa. Also, 15 Citrullus lanatus subsp. lanatus (CLL) PIs and the American heirloom cultivars Charleston Gray and Black Diamond (Citrullus lanatus subsp. vulgaris (Schrader ex Eckl. et Zeyh.) Fursa) (CLV) and five Citrullus colocynthis (L.) Schrader (CC) PIs collected in different locations throughout the world were used as out-groups in the phylogenetic analysis for the CLC PIs. Twenty-three high frequency oligonucleotides—targeting active gene (HFO-TAG) primers were used in polymerase chain reaction (PCR) experiments to produce a total of 562 polymorphic markers among the Citrullus PIs and cultivars. Cluster and multidimensional scaling plot analysis produced distinct groups of CLC, CLL, and CC PIs. Several PIs that were designated as CLC or CLL were in transitional positions, indicating that they are the result of gene flow between the major Citrullus groups or subgroups. Population structure analysis indicated that CLC comprises two subgroups; each containing a set of unique alleles. Also, unique alleles exist in the CLL and the CC genotypes. Overall, broad genetic diversity exists among the Citrullus PIs. The data in this study should be useful for identifying PIs with a wide genetic distance between them that could be used in breeding programs aiming to develop heterotic F1 hybrid rootstock lines for grafted watermelon.

Natural Enemies of Bemisia tabaci: Predators and Parasitoids

Arthropod parasitoids and predators are ubiquitous and operate continuously on all life stages of the whitefly, functioning as control factors in the process. The goal of biological control is to better exploit this behavior in order to more effectively manage pests and reduce insecticide use. Biological control of whiteflies and other pests has been pursued through observation and utilization of natural enemy activity (e.g., Albajes et al. 2003), through search for and introduction of natural enemies (e.g., Gould et al. 2008; Nomikou et al.

PREY PREFERENCE BY DELPHASTUS CATALINAE (COLEOPTERA: COCCINELLIDAE) ON BEMISIA ARGENTIFOLII (HOMOPTERA: ALEYRODIDAE): EFFECTS OF PLANT SPECIES AND PREY STAGES

Abstract Plant species and insect stages were studied for their effects on feeding by predator Delphastus catalinae (Horn) (Coleoptera: Coccinellidae) on the silverleaf whitefly (Bemisia argentifolii Bellows and Perring) (Homoptera: Aleyrodidae). To study the influence of plant species, immature whitefly prey were presented simultaneously to starved predator adults on leaf cuttings of five different plant species: cotton (Gossypium hirsutum L.), tomato (Lycopersicon esculentum Miller), hibiscus (Hibiscus rosa-sinensis L.), cowpea (Vigna unguiculata [L.], Walpers ssp. unguiculata), and collard (Brassica oleracea var. acephala DC). Percentage predation over 24 h was significantly highest on cotton, followed in rank order by collards, cowpea, tomato, and hibiscus. Different predation rates may have been caused by differential response to volatile secondary compounds released by the leaf cuttings. Host stage preference was studied by presenting individual adult predators with equal numbers of prey (200 per replicate) in three aggregate life stages: eggs, small nymphs (1st to 3rd instars) and large nymphs (4th instar to pupae). Adults consumed significantly higher numbers of eggs in a 24-h predation period compared with small or large nymphs. These findings suggest that among the plant species tested, Delphastus catalinae may be most effective on early-season cotton or immediately after whitefly infestation when eggs are predominant.

Survival and Predation of Delphastus catalinae (Coleoptera: Coccinellidae), a Predator of Whiteflies (Homoptera: Aleyrodidae), After Exposure to a Range of Constant Temperatures

Abstract Delphastus catalinae (Horn) is a predator of whiteflies that has shown promise as a tool in pest management strategies. Exposure to short-term temperature extremes can affect the survival of predators in a greenhouse or field environment. The B-biotype sweetpotato whitefly, Bemisia tabaci (Gennadius), survives the winters of mild climates (where temperatures are commonly above 0°C), but it is not known if D. catalinae can survive such winters. The influence of constant temperature on the survival of D. catalinae was determined in the laboratory using eggs and nymphs of the B-biotype B. tabaci. Over 90% of the adult beetles exposed to temperature regimens of 5, 10, 15, 20, 25, 30, and 35°C for 24 h survived when confined with hosts. The lower and upper thresholds for survival over that duration were around 0 and 40°C, respectively; ∼1% of the insects survived temperatures beyond these extremes. Survival of D. catalinae pupae was similar to that of adults. Adult D. catalinae survived up to 5.8 mo when confined on a plant infested with whitefly eggs and nymphs and held at 25°C; 50% of the cohort survived for 3.4 mo. Those held in a similar test at 35°C lived up to 0.6 mo. The number of immature whiteflies consumed during 24 h by adult D. catalinae generally increased with temperatures of 14–30°C. This study provides information on temperatures that may affect the survival of D. catalinae during commercial shipment and after release for biological control in the field or greenhouse, and it may help in the understanding of their ability to survive mild winters.