Trichoderma virens and Pseudomonas chlororaphis Differentially Regulate Maize Resistance to Anthracnose Leaf Blight and Insect Herbivores When Grown in Sterile versus Non-Sterile Soils.

Soil-borne Trichoderma spp. have been extensively studied for their biocontrol activities against pathogens and growth promotion ability in plants. However, the beneficial effect of Trichoderma on inducing resistance against insect herbivores has been underexplored. Among diverse Trichoderma species, consistent with previous reports, we showed that root colonization by T. virens triggered induced systemic resistance (ISR) to the leaf-infecting hemibiotrophic fungal pathogens Colletotrichum graminicola. Whether T. virens induces ISR to insect pests has not been tested before. In this study, we investigated whether T. virens affects jasmonic acid (JA) biosynthesis and defense against fall armyworm (FAW) and western corn rootworm (WCR). Unexpectedly, the results showed that T. virens colonization of maize seedlings grown in autoclaved soil suppressed wound-induced production of JA, resulting in reduced resistance to FAW. Similarly, the bacterial endophyte Pseudomonas chlororaphis 30-84 was found to suppress systemic resistance to FAW due to reduced JA. Further comparative analyses of the systemic effects of these endophytes when applied in sterile or non-sterile field soil showed that both T. virens and P. chlororaphis 30-84 triggered ISR against C. graminicola in both soil conditions, but only suppressed JA production and resistance to FAW in sterile soil, while no significant impact was observed when applied in non-sterile soil. In contrast to the effect on FAW defense, T. virens colonization of maize roots suppressed WCR larvae survival and weight gain. This is the first report suggesting the potential role of T. virens as a biocontrol agent against WCR.

Maize OPR2 and LOX10 Mediate Defense against Fall Armyworm and Western Corn Rootworm by Tissue-Specific Regulation of Jasmonic Acid and Ketol Metabolism.

Foliage-feeding fall armyworm (FAW; Spodoptera frugiperda) and root-feeding western corn rootworm (WCR; Diabrotica virgifera virgifera) are maize (Zea mays L.) pests that cause significant yield losses. Jasmonic acid (JA) plays a pivotal defense role against insects. 12-oxo-phytodienoic acid (12-OPDA) is converted into JA by peroxisome-localized OPDA reductases (OPR). However, little is known about the physiological functions of cytoplasmic OPRs. Here, we show that disruption of ZmOPR2 reduced wound-induced JA production and defense against FAW while accumulating more JA catabolites. Overexpression of ZmOPR2 in Arabidopsis enhanced JA production and defense against beet armyworm (BAW; Spodoptera exigua). In addition, lox10opr2 double mutants were more susceptible than either single mutant, suggesting that ZmOPR2 and ZmLOX10 uniquely and additively contributed to defense. In contrast to the defensive roles of ZmOPR2 and ZmLOX10 in leaves, single mutants did not display any alteration in root herbivory defense against WCR. Feeding on lox10opr2 double mutants resulted in increased WCR mortality associated with greater herbivory-induced production of insecticidal death acids and ketols. Thus, ZmOPR2 and ZmLOX10 cooperatively inhibit the synthesis of these metabolites during herbivory by WCR. We conclude that ZmOPR2 and ZmLOX10 regulate JA-mediated resistance in leaves against FAW while suppressing insecticidal oxylipin synthesis in roots during WCR infestation.

Root volatile profiles and herbivore preference are mediated by maize domestication, geographic spread, and modern breeding.

MAIN CONCLUSION: Domestication affected the abundances and diversity of maize root volatiles more than northward spread and modern breeding, and herbivore preference for roots was correlated with volatile diversity and herbivore resistance. Studies show that herbivore defenses in crops are mediated by domestication, spread, and breeding, among other human-driven processes. They also show that those processes affected chemical communication between crop plants and herbivores. We hypothesized that (i) preference of the herbivore (Diabrotica virgifera virgifera) larvae for embryonic roots of maize (Zea mays mays) would increase and (ii) root volatile diversity would decrease with the crop's domestication, northward spread to present-day USA, and modern breeding. We used Balsas teosinte (Zea mays parviglumis), Mexican and USA landrace maizes, and US inbred maize lines to test these hypotheses. We found that herbivore preference and volatile diversity increased with maize domestication and northward spread but decreased with modern breeding. Additionally, we found that the abundances of single volatiles did not consistently increase or decrease with maize domestication, spread, and breeding; rather, volatiles grouped per their abundances were differentially affected by those processes, and domestication had the greatest effects. Altogether, our results suggested that: the herbivore's preference for maize roots is correlated with volatile diversity and herbivore resistance; changes in abundances of individual volatiles are evident at the level of volatile groups; and maize domestication, but not spread and breeding, affected the abundances of some green leaf volatiles and sesquiterpenes/sesquiterpenoids. In part, we discussed our results in the context of herbivore defense evolution when resources for plant growth and defense vary across environments. We suggested that variability in relative abundance of volatiles may be associated with their local, functional relevance across wild and agricultural environments.

Genome sequencing reveals evidence of adaptive variation in the genus Zea.

Maize is a globally valuable commodity and one of the most extensively studied genetic model organisms. However, we know surprisingly little about the extent and potential utility of the genetic variation found in wild relatives of maize. Here, we characterize a high-density genomic variation map from 744 genomes encompassing maize and all wild taxa of the genus Zea, identifying over 70 million single-nucleotide polymorphisms. The variation map reveals evidence of selection within taxa displaying novel adaptations. We focus on adaptive alleles in highland teosinte and temperate maize, highlighting the key role of flowering-time-related pathways in their adaptation. To show the utility of variants in these data, we generate mutant alleles for two flowering-time candidate genes. This work provides an extensive sampling of the genetic diversity of Zea, resolving questions on evolution and identifying adaptive variants for direct use in modern breeding.

Novel Biopesticides Based on Nanoencapsulation of Azadirachtin with Whey Protein to Control Fall Armyworm.

Biopesticides have become a global trend in order to minimize the hazards derived from synthetic chemical pesticides and improve the safety, efficacy, and environmental friendliness of agricultural pest management. Herein, we report a novel biopesticide composite encapsulating azadirachtin with the size of 260.9 ± 6.8 nm and its effects on the insect pest Spodoptera frugiperda (fall armyworm). The nanocomposite biopesticide was produced via nano emulsification and freeze-drying process using whey protein isolate as a nanocarrier matrix to encapsulate azadirachtin, a natural insect-killing compound obtained from neem seed. We found that the nanocomposite biopesticide acted quicker and with greater efficacy than bulk azadirachtin treatment with corresponding LC50 values within 11 days of S. frugiperda larvae survival. Through confocal microscopy, we found the enhanced biodistribution of the nanocomposite to all parts of the insect body. Photodegradation assays revealed an enhanced UV stability facilitated by light-scattering stemming from the intrinsic nanostructure and UV scavenging vitamin-E component.

Improving Natural Enemy Selection in Biological Control through Greater Attention to Chemical Ecology and Host-Associated Differentiation of Target Arthropod Pests.

Host-associated differentiation (HAD) refers to cases in which genetically distinct populations of a species (e.g., herbivores or natural enemies) preferentially reproduce or feed on different host species. In agroecosystems, HAD often results in unique strains or biotypes of pest species, each attacking different species of crops. However, HAD is not restricted to pest populations, and may cascade to the third trophic level, affecting host selection by natural enemies, and ultimately leading to HAD within natural enemy species. Natural enemy HAD may affect the outcomes of biological control efforts, whether classical, conservation, or augmentative. Here, we explore the potential effects of pest and natural enemy HAD on biological control in agroecosystems, with emphases on current knowledge gaps and implications of HAD for selection of biological control agents. Additionally, given the importance of semiochemicals in mediating interactions between trophic levels, we emphasize the role of chemical ecology in interactions between pests and natural enemies, and suggest areas of consideration for biological control. Overall, we aim to jump-start a conversation concerning the relevance of HAD in biological control by reviewing currently available information on natural enemy HAD, identifying challenges to incorporating HAD considerations into biological control efforts, and proposing future research directions on natural enemy selection and HAD.

Comparative Screening of Mexican, Rwandan and Commercial Entomopathogenic Nematodes to Be Used against Invasive Fall Armyworm, Spodoptera frugiperda.

The fall armyworm (FAW), Spodoptera frugiperda Smith (Lepidoptera: Noctuidae) is an important pest of maize originating from the Americas. It recently invaded Africa and Asia, where it causes severe yield losses to maize. To fight this pest, tremendous quantities of synthetic insecticides are being used. As a safe and sustainable alternative, we explore the possibility to control FAW with entomopathogenic nematodes (EPN). We tested in the laboratory whether local EPNs, isolated in the invasive range of FAW, are as effective as EPNs from FAW native range or as commercially available EPNs. This work compared the virulence, killing speed and propagation capability of low doses of forty EPN strains, representing twelve species, after placing them with second-, third- and sixth-instar caterpillars as well as pupae. EPN isolated in the invasive range of FAW (Rwanda) were found to be as effective as commercial and EPNs from the native range of FAW (Mexico) at killing FAW caterpillars. In particular, the Rwandan Steinernema carpocapsae strain RW14-G-R3a-2 caused rapid 100% mortality of second- and third-instar and close to 75% of sixth-instar FAW caterpillars. EPN strains and concentrations used in this study were not effective in killing FAW pupae. Virulence varied greatly among EPN strains, underlining the importance of thorough EPN screenings. These findings will facilitate the development of local EPN-based biological control products for sustainable and environmentally friendly control of FAW in East Africa and beyond.

Aphelinus nigritus Howard (Hymenoptera: Aphelinidae) Preference for Sorghum Aphid, Melanaphis sorghi (Theobald, 1904) (Hemiptera: Aphididae), Honeydew Is Stronger in Johnson Grass, Sorghum halepense, Than in Grain Sorghum, Sorghum bicolor.

How aphid parasitoids of recent invasive species interact with their hosts can affect the feasibility of biological control. In this study, we focus on a recent invasive pest of US grain sorghum, Sorghum bicolor, the sorghum aphid (SA), Melanaphis sorghi. Understanding this pest's ecology in the grain sorghum agroecosystem is critical to develop effective control strategies. As parasitoids often use aphid honeydew as a sugar resource, and honeydew is known to mediate parasitoid-aphid interactions, we investigated the ability of SA honeydew to retain the parasitoid Aphelinus nigritus. Since SAs in the US have multiple plant hosts, and host-plant diet can modulate parasitoid retention (a major component in host foraging), we measured SA honeydew sugar, organic acid, and amino acid profiles, then assessed via retention time A. nigritus preference for honeydew produced on grain sorghum or Johnson grass, Sorghum halepense. Compared to a water control, A. nigritus spent more time on SA honeydew produced on either host plant. Despite similar honeydew profiles from both plant species, A. nigritus preferred honeydew produced on Johnson grass. Our results suggest the potential for SA honeydew to facilitate augmentation strategies aimed at maintaining A. nigritus on Johnson grass to suppress SAs before grain sorghum is planted.

Multi-locus phylogenetic analyses uncover species boundaries and reveal the occurrence of two new entomopathogenic nematode species, Heterorhabditis ruandica n. sp. and Heterorhabditis zacatecana n. sp.

Species of the nematode genus Heterorhabditis are important biological control agents against agricultural pests. The taxonomy of this group is still unclear as it currently relies on phylogenetic reconstructions based on a few genetic markers with little resolutive power, specially of closely related species. To fill this knowledge gap, we sequenced several phylogenetically relevant genetic loci and used them to reconstruct phylogenetic trees, to calculate sequence similarity scores, and to determine signatures of species- and population-specific genetic polymorphism. In addition, we revisited the current literature related to the description, synonymisation, and declaration as species inquirendae of Heterorhabditis species to compile taxonomically relevant morphological and morphometric characters, characterized new nematode isolates at the morphological and morphometrical level, and conducted self-crossing and cross-hybridization experiments. The results of this study show that the sequences of the mitochondrial cytochrome C oxidase subunit I (COI) gene provide better phylogenetic resolutive power than the sequences of nuclear rRNA genes and that this gene marker can phylogenetically resolve closely related species and even populations of the same species with high precision. Using this gene marker, we found two new species, Heterorhabditis ruandica n. sp. and Heterorhabditis zacatecana n. sp. A detailed characterization of these species at the morphological and morphometric levels and nematode reproduction assays revealed that the threshold for species delimitation in this genus, using COI sequences, is 97% to 98%. Our study illustrates the importance of rigorous morphological and morphometric characterization and multi-locus sequencing for the description of new species within the genus Heterorhabditis, serves to clarify the phylogenetic relationships of this important group of biological control agents, and can inform future species descriptions to advance our efforts towards developing more tools for sustainable and environmentally friendly agriculture.

Maize biochemistry in response to root herbivory was mediated by domestication, spread, and breeding.

MAIN CONCLUSION: With domestication, northward spread, and breeding, maize defence against root-herbivores relied on induced defences, decreasing levels of phytohormones involved in resistance, and increasing levels of a phytohormone involved in tolerance. We addressed whether a suite of maize (Zea mays mays) phytohormones and metabolites involved in herbivore defence were mediated by three successive processes: domestication, spread to North America, and modern breeding. With those processes, and following theoretical predictions, we expected to find: a change in defence strategy from reliance on induced defences to reliance on constitutive defences; decreasing levels of phytohormones involved in herbivore resistance, and; increasing levels of a phytohormone involved in herbivore tolerance. We tested those predictions by comparing phytohormone levels in seedlings exposed to root herbivory by Diabrotica virgifera virgifera among four plant types encompassing those processes: the maize ancestor Balsas teosinte (Zea mays parviglumis), Mexican maize landraces, USA maize landraces, and USA inbred maize cultivars. With domestication, maize transitioned from reliance on induced defences in teosinte to reliance on constitutive defences in maize, as predicted. One subset of metabolites putatively involved in herbivory defence (13-oxylipins) was suppressed with domestication, as predicted, though another was enhanced (9-oxylipins), and both were variably affected by spread and breeding. A phytohormone (indole-3-acetic acid) involved in tolerance was enhanced with domestication, and with spread and breeding, as predicted. These changes are consistent with documented changes in herbivory resistance and tolerance, and occurred coincidentally with cultivation in increasingly resource-rich environments, i.e., from wild to highly enriched agricultural environments. We concluded that herbivore defence evolution in crops may be mediated by processes spanning thousands of generations, e.g., domestication and spread, as well as by processes spanning tens of generations, e.g., breeding and agricultural intensification.

Impact of Metarhizium robertsii on Adults of the Parasitoid Diachasmimorpha longicaudata and Parasitized Anastrepha ludens Larvae.

Biological control of the Mexican fruit fly, Anastrepha ludens, is mainly carried out by releasing parasitoids, such as Diachasmimorpha longicaudata, and by applying entomopathogenic fungi (EPF), such as Metarhizium anisopliae, Beauveria bassiana, or Isaria fumosorosea, which can be applied to the soil or dispersed using infective devices. The combined use of two or more biocontrol agents could improve A. ludens control, but IGP between natural enemies, if it occurs, may have negative effects. We evaluated the effects of EPF on D. longicaudata. First, we determined the susceptibility of adults of D. longicaudata to strains of EPF (Metarhizium robertsii strain V3-160 and M. anisopliae strain MAAP1). We also evaluated the infection of these two fungi on A. ludens larvae parasitized by D. longicaudata. Finally, we determined sub-lethal effects on adults of D. longicaudata that emerged from larvae that had been exposed to low concentrations of M. robertsii. Both fungi caused moderate mortality to D. longicaudata adults. There were no adverse effects on the longevity of parasitoids that emerged from parasitized larvae exposed to M. robertsii. Based on these results, we argue that M. robertsii has the potential to be used for biocontrol of A. ludens, with limited risk to D. longicaudata adults.

Resistance and Tolerance to Root Herbivory in Maize Were Mediated by Domestication, Spread, and Breeding.

Plants may defend against herbivory and disease through various means. Plant defensive strategies against herbivores include resistance and tolerance, which may have metabolic costs that affect plant growth and reproduction. Thus, expression of these strategies may be mediated by a variety of factors, such as resource availability, herbivory pressure, and plant genetic variation, among others. Additionally, artificial selection by farmers and systematic breeding by scientists may mediate the expression of resistance and tolerance in crop plants. In this study, we tested whether maize defense against Western corn rootworm (WCR) was mediated by the crop's domestication, spread, and modern breeding. We expected to find a trend of decreasing resistance to WCR with maize domestication, spread, and breeding, and a trend of increasing tolerance with decreasing resistance. To test our expectations, we compared resistance and tolerance among four Zea plants spanning those processes: Balsas teosinte, Mexican landrace maize, US landrace maize, and US inbred maize. We measured the performance of WCR larvae as a proxy for plant resistance, and plant growth as affected by WCR feeding as a proxy for plant tolerance. Our results showed that domestication and spread decreased maize resistance to WCR, as expected, whereas breeding increased maize resistance to WCR, contrary to expected. Our results also showed that maize resistance and tolerance to WCR are negatively correlated, as expected. We discussed our findings in relation to ecological-evolutionary hypotheses seeking to explain defense strategy evolution in the contexts of plant resistance-productivity trade-offs, plant tolerance-resistance trade-offs, and varying resource availability vis-à-vis plant physiological stress and herbivory pressure. Finally, we suggested that defense strategy evolution in maize, from domestication to the present, is predicted by those ecological-evolutionary hypotheses.

Occurrence, Identification, and Virulence of Native Fungal Pathogens Isolated From Mexican Fruit Fly (Diptera: Tephritidae) Larvae From Soils of Three Cropping Systems.

The Mexican fruit fly, Anastrepha ludens Loew, is a significant pest in mango and citrus production areas of Mexico. In this study, we evaluated the effects of some geographic characteristics, rainfall period, soil micro-environmental, and soil coverage variables on the occurrence of entomopathogenic fungi (EPF) associated with A. ludens larvae in soils of mango, grapefruit and mixed crops in central Veracruz state, Mexico. EPF isolates were characterized morphologically and identified by sequence analysis of elongation factor (EF1-1018F, EF1-1620R). We recorded four species of EPF (Metarhizium robertsii J.F. Bisch, S.A. Rehner & Humber [Hypocreales: Cordycipitaceae], M. brunneum Petch [Hypocreales: Cordycipitaceae], M. pinghaense Q.T. Chen & H.L. Guo [Hypocreales: Cordycipitaceae], and Beauveria bassiana (Balsamo) Vuillemin [Hypocreales: Cordycipitaceae]), of which Metarhizium robertsii was the most abundant and the most virulent. Also, we found that rainfall period, organic matter, coverage of herbs and forbs, and calcium levels modulated EPF occurrence. We estimated lethal concentrations for A. ludens larvae of the four most promising isolates, V3-123, V3-160, V1-332, and V3-369. Our results suggest that M. robertsii obtained from agricultural soils holds potential as a biological control agent for A. ludens.

Association of Insect-Derived Ear Injury With Yield and Aflatoxin of Maize Hybrids Varying in Bt Transgenes.

Environmental factors have been associated with the production of aflatoxin in maize, Zea mays L., and it is inconclusive whether transgenic, Bacillus thuringiensis (Bt), maize has an impact on aflatoxin accumulation. Maize hybrids differing in transgenes were planted in two locations from 2014 to 2017. Yield, aflatoxin, and ear injury caused by corn earworm, Helicoverpa zea (Boddie), and fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), were measured across three groups of hybrids differing in transgenes including near-isogenic hybrids, and water-stressed conditions. The hybrid groups consisted of non-Bt hybrids with no Bt transgenes, a second group with one or more Cry-Bt transgenes, and the third group with vegetative insecticidal Bt protein and Cry-Bt transgenes (Cry/Vip-Bt). Across the six data sets derived from 11 experiments, the Cry-Bt and Cry/Vip-Bt hybrids had less ear injury and aflatoxin on average than non-Bt hybrids. The effects of ear injury on yield and aflatoxin were more prominent and consistent in Corpus Christi, TX, where hybrids experienced more water-limited conditions than in College Station, TX. The trend of increased aflatoxin among hybrids with increased ear injury was further resolved when looking at Cry-Bt and Cry/Vip-Bt isogenic hybrids in Corpus Christi. The results supported that the maize hybrids with the inclusion of Cry-Bt and Cry/Vip-Bt transgenes warrant further investigation in an integrated approach to insect and aflatoxin management in sub-tropical rain-fed maize production regions. Research outcomes may be improved by focusing on areas prone to water-stress and by using hybrids with similar genetic backgrounds.

Did maize domestication and early spread mediate the population genetics of corn leafhopper?

Investigating how crop domestication and early farming mediated crop attributes, distributions, and interactions with antagonists may shed light on today's agricultural pest problems. Crop domestication generally involved artificial selection for traits desirable to early farmers, for example, increased productivity or yield, and enhanced qualities, though invariably it altered the interactions between crops and insects, and expanded the geographical ranges of crops. Thus, some studies suggest that with crop domestication and spread, insect populations on wild crop ancestors gave rise to pestiferous insect populations on crops. Here, we addressed whether the emergence of corn leafhopper (Dalbulus maidis) as an agricultural pest may be associated with domestication and early spread of maize (Zea mays mays). We used AFLP markers and mitochondrial COI sequences to assess population genetic structuring and haplotype relationships among corn leafhopper samples from maize and its wild relative Zea diploperennis from multiple locations in Mexico and Argentina. We uncovered seven corn leafhopper haplotypes contained within two haplogroups, one haplogroup containing haplotypes associated with maize and the other containing haplotypes associated with Z. diploperennis in a mountainous habitat. Within the first haplogroup, one haplotype was predominant across Mexican locations, and another across Argentinean locations; both were considered pestiferous. We suggested that the divergence times of the maize-associated haplogroup and of the "pestiferous" haplotypes are correlated with the chronology of maize spread following its domestication. Overall, our results support a hypothesis positing that maize domestication favored corn leafhopper genotypes preadapted for exploiting maize so that they became pestiferous, and that with the geographical expansion of maize farming, corn leafhopper colonized Z. diploperennis, a host exclusive to secluded habitats that serves as a refuge for archaic corn leafhopper genotypic diversity. Broadly, our results help explain the extents to which crop domestication and early spread may have mediated the emergence of today's agricultural pests.

Do assortative mating and immigrant inviability help maintain population genetic structuring of an herbivore on a crop and a wild relative?

Population genetic structuring is common among herbivorous insects and frequently is associated with divergent host plants, such as crops and their wild relatives. Previous studies showed population genetic structuring in corn leafhopper Dalbulus maidis in Mexico, such that the species consists of two sympatric, host plant-associated populations: an abundant and widespread "pestiferous" population on maize (Zea mays mays), and a small and localized "wild" population on perennial teosinte (Zea diploperennis), a maize wild relative with a limited distribution. This study addressed whether assortative mating and immigrant inviability mediate genetic structuring of corn leafhopper by comparing the mating and reproductive successes of pestiferous and wild females that colonize their nonassociated host plants against the successes of females colonizing their associated host plants. Assortative mating was assessed by comparing mating frequencies and premating and mating times among females of each population on each host plant; immigrant inviability was assessed by comparing, across two generations, the fecundity, survival, development time, sex ratio, and population growth rate among leafhopper populations and host plants. Our results showed that on maize, and compared to resident, pestiferous females, wild females were more likely to mate, and greater proportions of their offspring survived to adult stage and were daughters; consequently, the per-generation population growth rate on maize was greater for immigrant, wild leafhoppers compared to resident, pestiferous leafhoppers. Our results suggested that wild leafhoppers emigrating to maize have a fitness advantage over resident, pestiferous leafhoppers, while immigrant pestiferous and resident wild leafhoppers on teosinte have similar fitnesses.

Nonsensical choices? Fall armyworm moths choose seemingly best or worst hosts for their larvae, but neonate larvae make their own choices.

Selecting optimal host plants is critical for herbivorous insects, such as fall armyworm (Spodoptera frugiperda), an important maize pest in the Americas and Africa. Fall armyworm larvae are presumed to have limited mobility, hence female moths are presumed to be largely responsible for selecting hosts. We addressed host selection by fall armyworm moths and neonate and older (3rd-instar) larvae, as mediated by resistance and herbivory in maize plants. Thus, we compared discrimination among three maize cultivars with varying degrees of resistance to fall armyworm, and between plants subjected or not to two types of herbivory. The cultivars were: (i) susceptible, and deficient in jasmonic acid (JA) production and green leaf volatiles (GLV) emissions (inbred line B73-lox10); (ii) modestly resistant (B73), and; (iii) highly resistant (Mp708). The herbivory types were: (i) ongoing (= fall armyworm larvae present), and; (ii) future (= fall armyworm eggs present). In choice tests, moths laid more eggs on the highly resistant cultivar, and least on the susceptible cultivar, though on those cultivars larvae performed poorest and best, respectively. In the context of herbivory, moths laid more eggs: (i) on plants subject to versus free of future herbivory, regardless of whether plants were deficient or not in JA and GLV production; (ii) on plants subject versus free of ongoing herbivory, and; (iii) on plants not deficient in compared to deficient in JA and GLV production. Neonate larvae dispersed aerially from host plants (i.e. ballooned), and most larvae colonized the modestly resistant cultivar, and fewest the highly resistant cultivar, suggesting quasi-directional, directed aerial descent. Finally, dispersing older larvae did not discriminate among the three maize cultivars, nor between maize plants and (plastic) model maize plants, suggesting random, visually-oriented dispersal. Our results were used to assemble a model of host selection by fall armyworm moths and larvae, including recommendations for future research.

Agriculture sows pests: how crop domestication, host shifts, and agricultural intensification can create insect pests from herbivores.

We argue that agriculture as practiced creates pests. We use three examples (Corn leafhopper, Dalbulus maidis; Western corn rootworm, Diabrotica virgifera virgifera; Cotton fleahopper, Pseudatomoscelis seriatus) to illustrate: firstly, how since its origins, agriculture has proven conducive to transforming selected herbivores into pests, particularly through crop domestication and spread, and agricultural intensification, and; secondly, that the herbivores that became pests were among those hosted by crop wild relatives or associates, and were pre-adapted either as whole species or component subpopulations. Two of our examples, Corn leafhopper and Western corn rootworm, illustrate how following a host shift to a domesticated host, emergent pests 'hopped' onto crops and rode expansion waves to spread far beyond the geographic ranges of their wild hosts. Western corn rootworm exemplifies how an herbivore-tolerant crop was left vulnerable when it was bred for yield and protected with insecticides. Cotton fleahopper illustrates how removing preferred wild host plants from landscapes and replacing them with crops, allows herbivores with flexible host preferences to reach pest-level populations. We conclude by arguing that in the new geological epoch we face, the Anthropocene, we can improve agriculture by looking to our past to identify and avoid missteps of early and recent farmers.

Maize Domestication and Anti-Herbivore Defences: Leaf-Specific Dynamics during Early Ontogeny of Maize and Its Wild Ancestors.

As a consequence of artificial selection for specific traits, crop plants underwent considerable genotypic and phenotypic changes during the process of domestication. These changes may have led to reduced resistance in the cultivated plant due to shifts in resource allocation from defensive traits to increased growth rates and yield. Modern maize (Zea mays ssp. mays) was domesticated from its ancestor Balsas teosinte (Z. mays ssp. parviglumis) approximately 9000 years ago. Although maize displays a high genetic overlap with its direct ancestor and other annual teosintes, several studies show that maize and its ancestors differ in their resistance phenotypes with teosintes being less susceptible to herbivore damage. However, the underlying mechanisms are poorly understood. Here we addressed the question to what extent maize domestication has affected two crucial chemical and one physical defence traits and whether differences in their expression may explain the differences in herbivore resistance levels. The ontogenetic trajectories of 1,4-benzoxazin-3-ones, maysin and leaf toughness were monitored for different leaf types across several maize cultivars and teosinte accessions during early vegetative growth stages. We found significant quantitative and qualitative differences in 1,4-benzoxazin-3-one accumulation in an initial pairwise comparison, but we did not find consistent differences between wild and cultivated genotypes during a more thorough examination employing several cultivars/accessions. Yet, 1,4-benzoxazin-3-one levels tended to decline more rapidly with plant age in the modern maize cultivars. Foliar maysin levels and leaf toughness increased with plant age in a leaf-specific manner, but were also unaffected by domestication. Based on our findings we suggest that defence traits other than the ones that were investigated are responsible for the observed differences in herbivore resistance between teosinte and maize. Furthermore, our results indicate that single pairwise comparisons may lead to false conclusions regarding the effects of domestication on defensive and possibly other traits.

Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding.

Plant defenses against herbivores are predicted to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus Zea (Poaceae). For this, we assessed performance of corn leafhopper (Dalbulus maidis) following colonization of one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual life cycle, the agricultural transition from wild annual grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance of corn leafhopper was measured through seven variables relevant to development speed, survivorship, fecundity, and body size. The plants included in our study were perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), a landrace maize (Zea mays mays), and a hybrid maize. Perennial teosinte is a perennial, iteroparous species, and is basal in Zea; Balsas teosinte is an annual species, and the progenitor of maize; the landrace maize is a primitive, genetically diverse cultivar, and is ancestral to the hybrid maize; and, the hybrid maize is a highly inbred, modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte and landrace maize, and best on hybrid maize, consistent with our expectation of declining defense from perennial teosinte to hybrid maize. Overall, our results indicated that corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and least with the domestication transition.