Analysis of three leafminers' complete mitochondrial genomes

Liriomyza trifolii (Burgess), Liriomyza huidobrensis (Blanchard), and Liriomyza bryoniae (Kaltenbach), are three closely related and economically important leafminer pests in the world. This study examined the complete mitochondrial genomes of L. trifolii, L. huidobrensis and L. bryoniae, which were 16141 bp, 16236 bp and 16183 bp in length, respectively. All of them displayed 37 typical animal mitochondrial genes and an A + T-rich region. The genomes were highly compact with only 60–68 bp of non-coding intergenic spacer. However, considerable differences in the A + T-rich region were detected among the three species. Results of this study also showed the two ribosomal RNA genes of the three species had very limited variable sites and thus should not provide much information in the study of population genetics of these species. Data generated from three leafminers' complete mitochondrial genomes should provide valuable information in studying phylogeny of Diptera, and developing genetic markers for species identification in leafminers.     

Displacement in two invasive species of leafminer fly in different localities

Liriomyza sativae was displaced by L. trifolii in the USA probably due to the lower insecticide susceptibility of L. trifolii, but L. trifolii was displaced by L. sativae in Japan. To know the possible causes of the species displacement observed in Japan, differences in the insecticide susceptibility, fecundity, effects of natural enemies, and reproductive interference between L. trifolii and L. sativae were evaluated. As a result, the higher fecundity of L. sativae and differential effects of parasitoids on the two Liriomyza species are considered to be contributing factors.     

Invasion of Japan by exotic leafminers <Emphasis Type="Italic">Liriomyza</Emphasis> spp. (Diptera: Agromyzidae) and its consequences

Identifying patterns and causes of species displacement is important from the viewpoints of ecology and evolutionary biology as this phenomenon affects community structure. Here I review the species displacement between Liriomyza trifolii (Burgess) and Liriomyza sativae Blanchard (Diptera: Agromyzidae) in Japan. These two species and Liriomyza huidobrensis (Blanchard) originated from the New World and are considered to have invaded Japan from around 1990 to the early 2000s. During this period, L. trifolii was apparently displaced by L. sativae, but the direction of displacement in Japan has been contrary to that observed between the same two species in the USA and China. While the displacement of L. sativae by L. trifolii in these two countries can be attributed to the lower insecticide susceptibility of L. trifolii there, species displacement in the opposite direction in Japan is probably due to the relatively high fecundity of L. sativae and differential effects of the introduced parasitoid Dacnusa sibirica Telenga (Hymenoptera: Braconidae) on both Liriomyza species, except in the south of the country.     

Interspecific and intraspecific differences in two Liriomyzaleafminer species in California

In recent years, the pest status of Liriomyza trifolii (Burgess) and L. huidobrensis (Blanchard) (Diptera: Agromyzidae) has changed in California, as well as other areas of the world. In California, L. huidobrensis has become the predominant Liriomyza species in valleys along the central coast, while L. trifolii remains the predominant species in southern California. To investigate possible reasons for this change in status, differences in host plant use and reproductive success of intraspecific populations were examined for Liriomyza trifolii and L. huidobrensis from both central and southern California. The southern L. trifolii fed, oviposited and reproduced successfully on all five hosts tested, but the central population fed significantly less on all hosts and was restricted to reproducing on pepper only. With the exception of pepper, southern L. trifolii had significantly greater larval survival on all hosts than central L. trifolii. In contrast, the central L. huidobrensis population had greater reproductive success than the southern population of that species on all hosts plants tested. However, pepper was not a suitable host for either L. huidobrensis population. Both species showed positive assortative mating, with homotypic mating occurring more frequently than heterotypic mating; however, the difference between L. trifolii populations was much more pronounced than between L. huidobrensis populations. These data indicate that central and southern California populations of each species are distinct biotypes. Furthermore when coupled with previous genetic data, our results suggest the possible existence of cryptic species within L. trifolii.     

Identifying factors determining the altitudinal distribution of the invasive pest leafminers Liriomyza huidobrensis and Liriomyza sativae

Abiotic and biotic factors that change with altitude can influence the distribution of herbivorous insects. We examined factors influencing the distribution of the generalist leafminers Liriomyza sativae Blanchard and Liriomyza huidobrensis Blanchard (Diptera: Agromyzidae), two pests of agricultural crops, in the tropical Dieng mountainous area of Central Java, Indonesia. Liriomyza huidobrensis predominated at altitudes above 700 m a.s.l. and was the only species collected above 1 400 m a.s.l. In contrast, L. sativae predominated below 600 m a.s.l. and was not found above 1 200 m where the average temperature was 20.7 °C. Parasitoid diversity decreased with altitude, but parasitism did not change. The distribution of neither species was affected by parasitoids; L. huidobrensis predominant at high altitudes was preferred by Opius parasitoids common at these altitudes. Intra‐ and interspecific competition was detected in laboratory experiments where larval density was high, but led to coexistence rather than species displacement. No competition was detected in a field experiment when larval density was low. However, L. sativae failed to reproduce at the highest altitude, whereas L. huidobrensis established at all altitudes. Host composition varied with altitude and one host (faba beans) preferred by L. huidobrensis was common at high altitudes. By relating published data on the performance of the leafminer species to altitudinal temperature changes, we were partly successful in predicting the altitude at which the dominant species switched. Temperature plays an overriding influence on the altitudinal distribution of leafminers.     

Host range and genetic strains of leafminer flies (Diptera: Agromyzidae) in eastern Brazil reveal a new divergent clade of Liriomyza sativae

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Comparison of the suitability of Liriomyza chinensis and L. trifolii (Diptera: Agromyzidae) as hosts for Neochrysocharis okazakii (Hymenoptera: Eulophidae)

Effective parasitoid production or mass-rearing is one of the key components in practicing biological control with parasitoids. Selection of host species for rearing parasitoids is a major approach to improve the production efficiency. The stone leek leafminer Liriomyza chinensis (Kato) is a destructive pest of onion crops in many Asian countries, which is difficult to control with chemicals. The present study examined whether the production of Neochrysocharis okazakii Kamijo, a promising native biological agent of L. chinensis, could be effective if kidney bean-Liriomyza trifolii (Burgess) system was used as an alternative rearing procedure. The suitability of L. chinensis and L. trifolii as hosts of N. okazakii was investigated in the laboratory. Neochrysocharis okazakii completed its development on both two host species, and the total development time was similar on these hosts. Longevity of N. okazakii females provided with L. chinensis was longer than those on L. trifolii. There were no significant differences in fecundity and offspring sex ratio when females had been provided with these two host species. The adult parasitoids emerged from L. chinensis were significantly larger than those from L. trifolii. However, the intrinsic rate of increase was higher, and mean generation time was lower, for L. trifolii than L. chinensis. Thus, mean net reproductive rate (Ro) was higher when L. trifolii was used as host. Although the two host species were equally suitable as host for N. okazakii, our findings suggested that L. trifolii and kidney bean is an ideal system for N. okazakii production.     

The complete mitochondrial genome of the leafminer Liriomyza sativae (Diptera: Agromyzidae): great difference in the A+T-rich region compared to Liriomyza trifolii

The complete mitochondrial genome sequence of Liriomyza sativae Blanchard (15,551 bp) was determined and analyzed in this study. The circular genome contained 37 genes including 13 protein-coding genes, 22 tRNA genes, 2 rRNA genes and an A + T-rich region. The initiation codons of COI and ND1 were ‘ATCA’ and ‘GTG’, respectively. ND2 gene used the truncated termination codon ‘T’. All the tRNA genes had the typical cloverleaf secondary structures except for tRNA^Ser(AGN) gene, which was found with the absence of a DHU arm. In addition, a tRNA-like secondary structure (tRNA^Met) was found in the A + T-rich region. The great difference was that the length of L. sativae A + T-rich region was 597 bp shorter than that of Liriomyza trifolii (Burgess). Meanwhile, some minor differences such as ‘TATA’ block were also observed in L. sativae in contrast to ‘TACA’ block in L. trifolii. There were also some essential structure elements such as ‘TATA’ block, ‘G(A)_nT’ block, poly-T stretch and stem-and-loop structure in the A + T-rich region of L. sativae mitochondrial genome.     

Volatiles released from bean plants in response to agromyzid flies

Liriomyza sativae Blanchard and Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) are two invasive flies in China that have caused economical damage on vegetables and ornamental plants. In this article, we report the profiles of emitted volatiles from healthy, mechanically damaged, and leafminer-damaged bean, Phaseolus vulgaris L., plants. Among 25 emitted volatiles identified, (E)-2-hexen-1-al, (3E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), (Z)-3-hexenyl acetate, (Z)-3-hexen-1-ol, (syn)- and (anti)-2-methylpropanal oxime, (syn)-2-methylbutanal oxime, linalool, and (E,E)-α-farnesene were consistently released from damaged bean plants. Combined amounts of these nine compounds made up more than 70% of the total volatiles emitted from each treatment. No qualitative differences in volatile emission were found between bean plants damaged by the two fly species; however, amounts of several major compounds induced by L. huidobrensis damage were significantly higher than those from plants damaged by L. sativae. The mechanically damaged plants released a higher proportion of green leaf volatiles than plants in the other treatments, whereas leafminer-damaged plants produced more terpenoids and oximes. Furthermore, the volatile profiles emitted from plants, damaged by adult leafminers, by second instar larvae, and even the plants with empty mines left by leafminer larvae (the pupal stage) were significantly different. The identification of volatile oximes released from damaged plants was confirmed and is discussed in a behavioral and biological control context.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

A genome-wide phylogeny and the diversification of genus Liriomyza (Diptera: Agromyzidae) inferred from anchored phylogenomics

The genus Liriomyza Mik (Diptera: Agromyzidae) is a diverse and globally distributed group of acalyptrate flies. Phylogenetic relationships among Liriomyza species have remained incompletely investigated and have never been fully addressed using molecular data. Here, we reconstruct the phylogeny of the genus Liriomyza using various phylogenetic methods (maximum likelihood, Bayesian inference, and gene tree coalescence) on target-capture-based phylogenomic datasets (nucleotides and amino acids) obtained from anchored hybrid enrichment (AHE). We have recovered tree topologies that are nearly congruent across all data types and methods, and individual clade support is strong across all phylogenetic analyses. Moreover, defined morphological species groups and clades are well-supported in our best estimates of the molecular phylogeny. Liriomyza violivora (Spencer) is a sister group to all remaining sampled Liriomyza species, and the well-known polyphagous vegetable pests [L. huidobrensis (Blanchard), L. langei Frick, L. bryoniae. (Kaltenbach), L. trifolii (Burgess), L. sativae Blanchard, and L. brassicae (Riley)]. belong to multiple clades that are not particularly closely related on the trees. Often, closely related Liriomyza species feed on distantly related host plants. We reject the hypothesis that cophylogenetic processes between Liriomyza species and their host plants drive diversification in this genus. Instead, Liriomyza exhibits a widespread pattern of major host shifts across plant taxa. Our new phylogenetic estimate for Liriomyza species provides considerable new information on the evolution of host-use patterns in this genus. In addition, it provides a framework for further study of the morphology, ecology, and diversification of these important flies.     

Mass production of Diglyphus isaea (Hymenoptera: Eulophidae), a biological control agent of a Korean population of potato leaf miner Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae)

The potato leaf miner, Liriomyza huidobrensis (Blanchard), is an important pest of potato throughout the world, including Korea. A method was developed for mass rearing the parasitoid Diglyphus isaea (Walker) using faba bean, Vicia faba L. (Fabaceae), as the host‐plant and L. huidobrensis as the insect host. Faba bean plants were planted in pots and maintained in a greenhouse for about 15 d. Pots were then exposed to adult leaf miners in oviposition cages for 4 h. Plants containing late second to early third instar larvae were exposed to adult D. isaea in parasitoid cages for 24 h. The leaf area per pot after 15 d was 597.9 cm², which produced 103.33 larvae per pot. The number of adult parasitoids emerging per pot was 72.5; about 41% of these were female. The daily cost of parasitoid production was USD20.95 per 1000 individual parasitoids. The methodology developed for D. isaea could be used to rear other ectoparasitoids such as Hemiptarsenus spp. and Pnigalio sp. with different insect hosts like L. trifolii. This is why this mass‐rearing information is important for securing test insect materials for ecological and biological study of Liriomyza species, and also for developing a biological control for Liriomyza species other than L. huidobrensis by mass production of associated natural enemies. We are facing rapid agro‐ecosystem changes including pest systems. Continuous monitoring of Liriomyza in solanaceous crops is needed.     

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 February 2013–31 March 2013

This article documents the addition of 142 microsatellite marker loci to the Molecular Ecology Resources database. Loci were developed for the following species: Agriophyllum squarrosum, Amazilia cyanocephala, Batillaria attramentaria, Fungal strain CTeY1 (Ascomycota), Gadopsis marmoratus, Juniperus phoenicea subsp. turbinata, Liriomyza sativae, Lupinus polyphyllus, Metschnikowia reukaufii, Puccinia striiformis and Xylocopa grisescens. These loci were cross‐tested on the following species: Amazilia beryllina, Amazilia candida, Amazilia rutila, Amazilia tzacatl, Amazilia violiceps, Amazilia yucatanensis, Campylopterus curvipennis, Cynanthus sordidus, Hylocharis leucotis, Juniperus brevifolia, Juniperus cedrus, Juniperus osteosperma, Juniperus oxycedrus, Juniperus thurifera, Liriomyza bryoniae, Liriomyza chinensis, Liriomyza huidobrensis and Liriomyza trifolii.     

Allozymatic diagnosis of four economically important Liriomyza species (Diptera, Agromyzidae)

Liriomyza bryoniae, L. huidobrensis, L. sativae and L. trifolii are leafminers of great economic importance; morphologically they are difficult to separate, many being inseparable at the pre-adult stages. Horizontal starch gel electrophoresis of larvae, pupae and adults was carried out in order to search for diagnostic allozymic characters. Analysis of the variation patterns at 15 genetic loci reveals that each species can be identified at all three stages of the life cycle. A biochemical key is presented.     

三种外来入侵斑潜蝇种间竞争研究进展

美洲斑潜蝇、南美斑潜蝇、三叶斑潜蝇是危害蔬菜、花卉的世界性大害虫。不同种间相互更替或取代的现象时有发生。根据国内外相关研究报道,综述了对近年来3种斑潜蝇种间竞争的研究。对斑潜蝇种间更替和取代现象的分析显示,生殖干扰、新生物型的出现、天敌、生态位、寄主植物以及抗药性等因素可能是影响它们种间竞争的关键。以期为斑潜蝇种群演替研究及防治策略制定提供参考。     

The complete mitochondrial genome of the leafminer <Emphasis Type="Italic">Liriomyza trifolii</Emphasis> (Diptera: Agromyzidae)

Liriomyza trifolii (Diptera: Agromyzidae) is one of the most economically significant pests in the world. In this paper we present sequence data for the complete mitochondrial genome of L. trifolii. The circular genome is 16,141 bp long and contains one encoding region including 37 genes and one non-coding A+T-rich region. Gene numbers and organization is similar to that of the typical insect mitochondrial genomes except that two additional tRNA genes are found in the A+T-rich region (tRNA^Thr and tRNA^Leu(UUR)). All of the protein initiation codons are ATN, except ND1 which begins with GTG and COI which is initiated by the quadruplet ATCA. The 22 tRNA anticodons of L. trifolii match those observed in Drosophila yakuba, and all of tRNAs form the typical cloverleaf structure except for tRNA^Ser(AGN), which has lost the DHU-arm. The A+T-rich region of L. trifolii also contains two previously noted Diperan features—a highly conserved polyT stretch and a (TA)_n stretch.     

Host feeding experience affects host plant odour preference of the polyphagous leafminer Liriomyza bryoniae

Herbivorous insects use highly specific volatiles or blends of volatiles characteristic to particular plant species to locate their host plants. Thus, data on olfactory preferences can be valuable in developing integrated pest management tools that deal with manipulation of pest insect behaviour. We examined host plant odour preferences of the tomato leafminer, Liriomyza bryoniae (Kaltenbach) (Diptera: Agromyzidae), which is an economically important agricultural pest widespread throughout Europe. The odour preferences of leafminers were tested in dependence of feeding experiences. We ranked host plant odours by their appeal to L. bryoniae based on two‐choice tests using a Y‐tube olfactometer with five host plants: tomato, Solanum lycopersicum Mill.; bittersweet, Solanum dulcamara L.; downy ground‐cherry, Physalis pubescens L. (all Solanaceae); white goosefoot, Chenopodium album L. (Chenopodiaceae); and dead nettle, Lamium album L. (Lamiaceae). The results imply that ranking of host plant odours by their attractiveness to L. bryoniae is complicated due to the influence of larval and adult feeding experiences. Without any feeding experience as an adult, L. bryoniae males showed a preference for the airflow with host plant odour vs. pure air, whereas females did not display a preference. Further tests revealed that adult feeding experience can alter the odour choice of L. bryoniae females. After feeding experience, females showed a preference for host plant odour vs. pure air. Feeding experience in the larval stage influenced the choice by adults of both sexes: for males as well as females reared on bittersweet the odour of that plant was the most attractive. Thus, host feeding experience both in larval and/or adult stage of polyphagous tomato leafminer L. bryoniae influences host plant odour preference by adults.     

Biological studies withChrysocharis parksi [Hym.: Eulophidae] a parasite ofLiriomyza spp. [Dipt.: Agromyzidae]

Biological studies withChrysocharis parksi Crawford, a parasite of agromyzid leafminers, were conducted.C. parksi successfully parasitized the following species in the genusLiriomyza Mik.,L. huidobrensis (Blanchard),L. sativae Blanchard,L. trifolii (Burgess), andL. trifoliearum Spencer. Successful parasite development was recorded from 8 plant families and 16 genera. Host plants which were suitable for leafminer development to the adult stage were also suitable for parasite development. Mean immature developmental period (egg to adult, usingL. trifolii as the host) at 21.1°, 26.7°, and 32.2° C was (for both sexes) 23, 14, and 14 days, respectively. Longevity of females provided only water was inversely related to temperature; significantly longer survival occurred at 21.1° C (5.0 days) compared to 26.7° C and 32.2° C (3.2 and 2.1 days, respectively). The addition of honey to the diet significantly improved longevity of both sexes at all temperatures. Adult female parasites which were provided an average of 33.0L. trifolii larvae per day produced an average of 135 offspring at a constant 26.7° C.C. parksi host-fed on ca. 3.7 leafminer larvae per day over an 11-day adult lifespan.      

Simplified rapid differentiation of Liriomyza chinensis Kato (Diptera; Agromyzidae) genotypes A and B using PCR-RFLP

The stone leek leafminer Liriomyza chinensis Kato is one of the most important pests of Allium spp. In recent years, a new genotype of L. chinensis, genotype B, has been shown to cause more severe damage to Allium spp. compared with the native genotype A in Japan. Thus, identification of the genotypes is important for establishing L. chinensis control strategies. In this study, we developed a simple and rapid method of genotype identification using PCR-restriction fragment length polymorphism (RFLP). Primers were designed to mitochondria cytochrome oxidase subunit I gene (mtCOI) nucleotide sequences from both genotypes. Genotypes A and B were successfully identified using the restriction enzymes PvuI and DdeI, respectively. Using PCR-RFLP, we identified the genotype of L. chinensis samples (n = 108) collected in seven Japanese bunching onion fields in Ibaraki Prefecture, Japan. All individuals were shown to be genotype B, as expected.     

Morphological and genetic characteristics of Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) infesting potato crops in Korea

The pea leafminer fly, Liriomyza huidobrensis (Blanchard), was found infesting and damaging Korean potato crops during a 2012 field survey. Localized outbreaks of L. huidobrensis were observed in Miryang and Goryeong counties in the south of the Korean Peninsula. This paper describes the morphological and genetic characteristics of the Korean population of L. huidobrensis. The dorsal color pattern on the abdomen, and an array of microsetae on the thorax, were the main diagnostic characteristics of this species. On the basis of an analysis of a partial mitochondrial cytochrome c oxidase subunit 1 (COI) DNA sequence, we found that intraspecific variation in L. huidobrensis was negligible, and that the distance between L. huidobrensis and a closely related species, L. trifolii, was estimated to be 7.4–7.6 K2P. This is the first report of the infestation of field crops by the invasive leafminer L. huidobrensis in Korea.     

The occurrence of leafminers and their parasitoids on vegetables and weeds in Hangzhou area, Southeast China

Leafminers are the mostimportant insect pests of vegetables inHangzhou area, Zhejiang province, SoutheastChina as well as in the rest of China, but havenever been investigated for speciescomposition, relative abundance and theirassociated parasitoids. A survey was conductedin four localities of Hangzhou area during 1998–2000to determine the distribution ofleafminers and their parasitoids on vegetablecrops and weeds in the field. Over 20,000leafminers were collected and reared. Theleafminer species found were Liriomyzasativae, L. chinensis and Chromatomyia horticola, with C.horticola and L. sativae the mostabundant in spring and autumn, respectively.About 11,000 parasitoid adults were reared fromthe leafminers collected. In total 14hymenopteran species of four families (onebraconid, 10 eulophids, one megaspilid and onepteromalid) were found. Eleven species werereared from C. horticola, nine from L. sativae and seven from L. chinensis.Opius caricivorae and Chrysocharispentheus were the dominant species. Sevenspecies were recorded from L. chinensisfor the first time. Eleven parasitoid specieswere reared from leafminers on two weeds (Veronica undulata and Sonchusoleraceus). Parasitoids caused 48.5–68.8%parasitism on leafminers on crops and 83.7%parasitism on leafminers on weeds in the latergrowing season of vegetable crops. The resultssuggest that leafminer populations areregulated to a certain extent by their naturalenemies in the field.