Rapid growth and the evolution of complete metamorphosis in insects.

More than 50% of all animal species are insects that undergo complete metamorphosis. The key innovation of these holometabolous insects is a pupal stage between the larva and adult when most structures are completely rebuilt. Why this extreme lifestyle evolved is unclear. Here, we test the hypothesis that a trade-off between growth and differentiation explains the evolution of this novelty. Using a comparative approach, we find that holometabolous insects grow much faster than hemimetabolous insects. Using a theoretical model, we then show how holometaboly evolves under a growth-differentiation trade-off and identify conditions under which such temporal decoupling of growth and differentiation is favored. Our work supports the notion that the holometabolous life history evolved to remove developmental constraints on fast growth, primarily under high mortality.

Multicellularity in animals: The potential for within-organism conflict.

Metazoans function as individual organisms but also as "colonies" of cells whose single-celled ancestors lived and reproduced independently. Insights from evolutionary biology about multicellular group formation help us understand the behavior of cells: why they cooperate, and why cooperation sometimes breaks down. Current explanations for multicellularity focus on two aspects of development which promote cooperation and limit conflict among cells: a single-cell bottleneck, which creates organisms composed of clones, and a separation of somatic and germ cell lineages, which reduces the selective advantage of cheating. However, many obligately multicellular organisms thrive with neither, creating the potential for within-organism conflict. Here, we argue that the prevalence of such organisms throughout the Metazoa requires us to refine our preconceptions of conflict-free multicellularity. Evolutionary theory must incorporate developmental mechanisms across a broad range of organisms-such as unusual reproductive strategies, totipotency, and cell competition-while developmental biology must incorporate evolutionary principles. To facilitate this cross-disciplinary approach, we provide a conceptual overview from evolutionary biology for developmental biologists, using analogous examples in the well-studied social insects.

The genetic determination of alternate stages in polyphenic insects.

Molt-based transitions in form are a central feature of insect life that have enabled adaptation to diverse and changing environments. The endocrine regulation of these transitions is well established, but an understanding of their genetic regulation has only recently emerged from insect models. The pupal and adult stages of metamorphosing insects are determined by the stage specifying transcription factors broad-complex (br) and Ecdysone inducible protein 93 (E93), respectively. A probable larval determinant, chronologically inappropriate metamorphosis (chinmo), has just recently been characterized. Expression of these three transcription factors in the metamorphosing insects is regulated by juvenile hormone with ecdysteroid hormones, and by mutual repression between the stage-specific transcription factors. This review explores the hypothesis that variations in the onset, duration, and tissue-specific expression of chinmo, br, and E93 underlie other polyphenisms that have arisen throughout insects, including the castes of social insects, aquatic stages of mayflies, and the neoteny of endoparasites. The mechanisms that constrain how chinmo, br, and E93 expression may vary will also constrain the ways that insect life history may evolve. I find that four types of expression changes are associated with novel insect forms: (1) heterochronic shift in the turnover of expression, (2) expansion or contraction of expression, (3) tissue-specific expression, and (4) redeployment of stage-specific expression. While there is more to be learned about chinmo, br, and E93 function in diverse insect taxa, the studies outlined here show that insect stages are modular units in developmental time and a substrate for evolutionary forces to act upon.

Coevolution of larval signalling and worker response can trigger developmental caste determination in social insects.

Eusocial insects belong to distinct queen and worker castes, which, in turn, can be divided into several morphologically specialized castes of workers. Caste determination typically occurs by differential nutrition of developing larvae. We present a model for the coevolution of larval signalling and worker task allocation-both modelled by flexible smooth reaction norms-to investigate the evolution of caste determination mechanisms and worker polymorphism. In our model, larvae evolve to signal their nutritional state to workers. The workers evolve to allocate time to foraging for resources versus feeding the brood, conditional on the larval signals and their body size. Worker polymorphism evolves under accelerating foraging returns of increasing body size, which causes selection to favour large foraging and small nursing workers. Worker castes emerge because larvae evolve to amplify their signals after obtaining some food, which causes them to receive more food, while the other larvae remain unfed. This leads to symmetry-breaking among the larvae, which are either well-nourished or malnourished, thus emerging as small or large workers. Our model demonstrates the evolution of nutrition-dependent caste determination and worker polymorphism by a self-reinforcement mechanism that evolves from the interplay of larval signalling and worker response to the signals.

Modeling insect growth regulators for pest management.

Insect growth regulators (IGRs) have been developed as effective control measures against harmful insect pests to disrupt their normal development. This study is to propose a mathematical model to evaluate the cost-effectiveness of IGRs for pest management. The key features of the model include the temperature-dependent growth of insects and realistic impulsive IGRs releasing strategies. The impulsive releases are carefully modeled by counting the number of implements during an insect's temperature-dependent development duration, which introduces a surviving probability determined by a product of terms corresponding to each release. Dynamical behavior of the model is illustrated through dynamical system analysis and a threshold-type result is established in terms of the net reproduction number. Further numerical simulations are performed to quantitatively evaluate the effectiveness of IGRs to control populations of harmful insect pests. It is interesting to observe that the time-changing environment plays an important role in determining an optimal pest control scheme with appropriate release frequencies and time instants.

Evaluating old truths: Final adult size in holometabolous insects is set by the end of larval development.

For centuries, it has been understood that the final size of adult holometabolous insects is determined by the end of the larval stage, and that once they transform to adults, holometabolous insects do not grow. Despite this, no previous study has directly tested these "old truths" across holometabolous insects. Here, we demonstrate that final adult size is set at the end of the last larval stage in species representing each of the four orders of holometabolous insects: the fruit fly Drosophila melanogaster (Diptera), the tobacco hornworm Manduca sexta (Lepidoptera), the dung beetle Onthophagus taurus (Coleoptera), and the Florida carpenter ant Camponotus floridanus (Hymenoptera). Furthermore, in both D. melanogaster and C. floridanus, we show that the size of adult individuals fluctuates but does not significantly change. Therefore, our study finally confirms these two basic assumptions in the biology of insects, which have for centuries served as the foundation for studies of insect growth, size, and allometry.

A hemipteran insect reveals new genetic mechanisms and evolutionary insights into tracheal system development.

The diversity in the organization of the tracheal system is one of the drivers of insect evolutionary success; however, the genetic mechanisms responsible are yet to be elucidated. Here, we highlight the advantages of utilizing hemimetabolous insects, such as the milkweed bug Oncopeltus fasciatus, in which the final adult tracheal patterning can be directly inferred by examining its blueprint in embryos. By reporting the expression patterns, functions, and Hox gene regulation of trachealess (trh), ventral veinless (vvl), and cut (ct), key genes involved in tracheal development, this study provides important insights. First, Hox genes function as activators, modifiers, and suppressors of trh expression, which in turn results in a difference between the thoracic and abdominal tracheal organization. Second, spiracle morphogenesis requires the input of both trh and ct, where ct is positively regulated by trh As Hox genes regulate trh, we can now mechanistically explain the previous observations of their effects on spiracle formation. Third, the default state of vvl expression in the thorax, in the absence of Hox gene expression, features three lateral cell clusters connected to ducts. Fourth, the exocrine scent glands express vvl and are regulated by Hox genes. These results extend previous findings [Sánchez-Higueras et al., 2014], suggesting that the exocrine glands, similar to the endocrine, develop from the same primordia that give rise to the trachea. The presence of such versatile primordia in the miracrustacean ancestor could account for the similar gene networks found in the glandular and respiratory organs of both insects and crustaceans.

The AMPK-PP2A axis in insect fat body is activated by 20-hydroxyecdysone to antagonize insulin/IGF signaling and restrict growth rate.

In insects, 20-hydroxyecdysone (20E) limits the growth period by triggering developmental transitions; 20E also modulates the growth rate by antagonizing insulin/insulin-like growth factor signaling (IIS). Previous work has shown that 20E cross-talks with IIS, but the underlying molecular mechanisms are not fully understood. Here we found that, in both the silkworm Bombyx mori and the fruit fly Drosophila melanogaster, 20E antagonized IIS through the AMP-activated protein kinase (AMPK)-protein phosphatase 2A (PP2A) axis in the fat body and suppressed the growth rate. During Bombyx larval molt or Drosophila pupariation, high levels of 20E activate AMPK, a molecular sensor that maintains energy homeostasis in the insect fat body. In turn, AMPK activates PP2A, which further dephosphorylates insulin receptor and protein kinase B (AKT), thus inhibiting IIS. Activation of the AMPK-PP2A axis and inhibition of IIS in the Drosophila fat body reduced food consumption, resulting in the restriction of growth rate and body weight. Overall, our study revealed an important mechanism by which 20E antagonizes IIS in the insect fat body to restrict the larval growth rate, thereby expanding our understanding of the comprehensive regulatory mechanisms of final body size in animals.

A Potential Lead for Insect Growth Regulator: Design, Synthesis, and Biological Activity Evaluation of Novel Hexacyclic Pyrazolamide Derivatives.

Ecdysone receptor (EcR) and chitinase play a critical role in the molting stage of insect pests. Each of them is considered a promising target for the development of novel insect growth regulators (IGRs). In the present paper, a total of 24 (23 novel) hexacyclic pyrazolamide derivatives were designed and synthesized by reducing the heptacycle and inserting small flexible linkers on the basis of the previously discovered dual-target compound D-27 acting simultaneously on EcR and Ostrinia furnacalis chitinase (OfChtI). Their insecticidal activities against Plutella xylostella, Spodoptera frugiperda, and Ostrinia furnacalis larvae were evaluated. The results revealed that the insecticidal activity was not significantly enhanced when the heptacycle on the pyrazole ring was reduced to a hexacycle. However, the insertion of an additional methylene spacer between the substituted phenyl ring and the amide bond can improve the insecticidal activity. Among the derivatives, the most potent compound, 6j, exhibited promising insecticidal activities against P. xylostella and S. frugiperda. Further protein binding assays and molecular docking indicated that 6j could target both EcR and OfChtI, and is a potential lead compound for IGRs. The present work provides valuable clues for the development of new dual-target IGRs.

Variability in plant nutrients reduces insect herbivore performance.

The performance and population dynamics of insect herbivores depend on the nutritive and defensive traits of their host plants. The literature on plant-herbivore interactions focuses on plant trait mean values, but recent studies showing the importance of plant genetic diversity for herbivores suggest that plant trait variance may be equally important. The consequences of plant trait variance for herbivore performance, however, have been largely overlooked. Here we report an extensive assessment of the effects of within-population plant trait variance on herbivore performance using 457 performance datasets from 53 species of insect herbivores. We show that variance in plant nutritive traits substantially reduces mean herbivore performance via non-linear averaging of performance relationships that were overwhelmingly concave down. By contrast, relationships between herbivore performance and plant defence levels were typically linear, with variance in plant defence not affecting herbivore performance via non-linear averaging. Our results demonstrate that plants contribute to the suppression of herbivore populations through variable nutrient levels, not just by having low average quality as is typically thought. We propose that this phenomenon could play a key role in the suppression of herbivore populations in natural systems, and that increased nutrient heterogeneity within agricultural crops could contribute to the sustainable control of insect pests in agroecosystems.

Transcriptomic basis and evolution of the ant nurse-larval social interactome.

Development is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to characterize the social interactome regulating ant larval development by collecting and sequencing the transcriptomes of interacting nurses and larvae across time. We find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development. We leverage this widespread nurse-larva gene co-expression to infer putative social gene regulatory networks acting between nurses and larvae. Genes with the strongest inferred social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. This includes interesting candidates such as the nurse-expressed giant-lens, which may influence larval epidermal growth factor signaling, a pathway known to influence various aspects of insect development. Finally, we find that genes with the strongest signatures of social regulation tend to experience relaxed selective constraint and are evolutionarily young. Overall, our study provides a first glimpse into the molecular and evolutionary features of the social mechanisms that regulate all aspects of social life.

Hox genes limit germ cell formation in the short germ insect Gryllus bimaculatus.

Hox genes are conserved transcription factor-encoding genes that specify the identity of body regions in bilaterally symmetrical animals. In the cricket Gryllus bimaculatus, a member of the hemimetabolous insect group Orthoptera, the induction of a subset of mesodermal cells to form the primordial germ cells (PGCs) is restricted to the second through the fourth abdominal segments (A2 to A4). In numerous insect species, the Hox genes Sex-combs reduced (Scr), Antennapedia (Antp), Ultrabithorax (Ubx), and abdominal-A (abd-A) jointly regulate the identities of middle and posterior body segments, suggesting that these genes may restrict PGC formation to specific abdominal segments in G. bimaculatus Here we show that reducing transcript levels of some or all of these Hox genes results in supernumerary and/or ectopic PGCs, either individually or in segment-specific combinations, suggesting that the role of these Hox genes is to limit PGC development with respect to their number, segmental location, or both. These data provide evidence of a role for this ancient group of genes in PGC development.

Growing Up in a Changing World: Environmental Regulation of Development in Insects.

All organisms are exposed to changes in their environment throughout their life cycle. When confronted with these changes, they adjust their development and physiology to ensure that they can produce the functional structures necessary for survival and reproduction. While some traits are remarkably invariant, or robust, across environmental conditions, others show high degrees of variation, known as plasticity. Generally, developmental processes that establish cell identity are thought to be robust to environmental perturbation, while those relating to body and organ growth show greater degrees of plasticity. However, examples of plastic patterning and robust organ growth demonstrate that this is not a hard-and-fast rule.In this review, we explore how the developmental context and the gene regulatory mechanisms underlying trait formation determine the impacts of the environment on development in insects. Furthermore, we outline future issues that need to be resolved to understand how the structure of signaling networks defines whether a trait displays plasticity or robustness.

Glycosyltransferases: the multifaceted enzymatic regulator in insects.

Glycosyltransferases (GTs) catalyse the reaction of glyco-conjugation of various biomolecules by transferring the saccharide moieties from an activated nucleotide sugar to nucleophilic glycosyl acceptor. In insects, GTs show diverse temporal and site-specific expression patterns and thus play significant roles in forming the complex biomolecular structures that are necessary for insect survival, growth and development. Several insects exhibit GT-mediated detoxification as a key defence strategy against plant allelochemicals and xenobiotic compounds, as well as a mechanism for pesticide cross-resistance. Also, these enzymes act as crucial effectors and modulators in various developmental processes of insects such as eye development, UV shielding, cuticle formation, epithelial development and other specialized functions. Furthermore, many of the known insect GTs have been shown to play a fundamental role in other physiological processes like body pigmentation, cuticular tanning, chemosensation and stress response. This review provides a detailed overview of the multifaceted functionality of insect GTs and summarizes numerous case studies associated with it.

Post-transcriptional regulation of insect metamorphosis and oogenesis.

Metamorphic transformation from larvae to adults along with the high fecundity is key to insect success. Insect metamorphosis and reproduction are governed by two critical endocrines, juvenile hormone (JH), and 20-hydroxyecdysone (20E). Recent studies have established a crucial role of microRNA (miRNA) in insect metamorphosis and oogenesis. While miRNAs target genes involved in JH and 20E-signaling pathways, these two hormones reciprocally regulate miRNA expression, forming regulatory loops of miRNA with JH and 20E-signaling cascades. Insect metamorphosis and oogenesis rely on the coordination of hormones, cognate genes, and miRNAs for precise regulation. In addition, the alternative splicing of genes in JH and 20E-signaling pathways has distinct functions in insect metamorphosis and oogenesis. We, therefore, focus in this review on recent advances in post-transcriptional regulation, with the emphasis on the regulatory role of miRNA and alternative splicing, in insect metamorphosis and oogenesis. We will highlight important new findings of miRNA interactions with hormonal signaling and alternative splicing of JH receptor heterodimer gene Taiman.

Comparison between sustained effects of spray and injection thiamethoxam on apple aphids and non-target insects in apple orchard.

Spray application is considered to be the most common method of insecticide use in apple orchard, while trunk injection has often be used in labor-intensive areas. Here, a comparison of both methods in aphid control efficiency and non-target effects was conducted. We evaluated the effects of thiamethoxam by either spray or injection on apple aphid Aphis citricola, and examined the temporal dynamic of thiamethoxam in leaves by using residue analysis. Results showed that thiamethoxam had a remarkable suppression effect on Aphis citricola, and both application methods had obvious control efficiency with the highest value above 90%. The control effect of spray method on Aphis citricola reached the maximum at 7 days after application, while that of injection method reached the maximum at 14 days after application. Moreover, the control effect of injection after 14 days and that of spray after 7 days were not significant, suggesting the spray method had a higher quick-acting effect than the injection method, and the two methods had a similar persistence effect. The population dynamics of non-target insects (ladybugs, parasitoid wasps and predatory bugs) showed basically the same as that of blank controlled. The control effect evaluation of thiamethoxam on Aphis citricola suggest that injection treatment was more effective in protecting natural enemies than spray treatment, and thiamethoxam didn't interfere with natural enemies to control Aphis citricola with both two application methods.

Nanoformulations and their mode of action in insects: a review of biological interactions.

While nanoparticles (NPs) can be used as insecticides by themselves, they can also be carriers for insecticidal chemicals. Existing literature suggests that the smaller the NP size, the greater the toxicity and penetration into the insect's body. Nonetheless, there is a lack of literature pertaining to the mode of action within insects. This review article summarizes the currently available entomological studies on the mechanisms of NP-insect interactions. Externally, NPs affect pigmentation and integrity of the cuticle, while internally they induce immune responses and alter gene expression leading to altered protein, lipid, and carbohydrate metabolism along with cellular toxicity that impairs development and reproduction of the insect. Consequently, insects are incapacitated due to the disruption of the nutrient intake, production of reactive oxygen species and altered biochemical activity while some NPs can promote growth and development as well as diminish the effects of nontarget toxicity.

Performance of the SSI development function compared with 33 other functions applied to 79 arthropod species' datasets.

The development rates of arthropods are temperature-dependent. Studies aiming to predict the dynamics of arachnid, crustacean, and insect populations in nature often require the derivation of development functions representing this phenomenon. A previous study (Quinn, B.K., 2017, J. Therm. Biol. 63, 65-77) identified 33 development functions commonly used in past studies on temperature-dependent development of arthropods, and illustrated that: (1) most of 99 past studies only applied one or few (2-5) development functions to their data without considering others; and (2) most of a subset of 79 studies' data were not fit with the actual best function for them, resulting in sometimes substantial differences in model performance and predictive ability. However, that study did not test the class of development functions based on theoretical enzyme thermodynamics, including the Sharpe-Schoolfield-Ikemoto (SSI) function. Herein, the meta-analyses done in that previous study were redone, after fitting all 79 reanalyzed datasets with the SSI function. Estimates of the intrinsic optimum temperature (TΦ) for development of each tested species were also derived using the SSI function and compared among taxa. Including the SSI function in analyses did not change the conclusions of the previous study concerning development function usage, choice, and consequences. Notably, the SSI function performed as well as or relatively better than other functions of comparable or lower complexity in terms of R2, AICC-based rankings, ΔAICC values, and prediction errors, which may recommend its more widespread use in future studies. Overall differences in TΦ were found among arthropod subphyla, as well as between most species pairs. Most TΦ estimates produced herein were novel, and could be used to make inferences about or comparisons among arthropod taxa in future studies.

Trichoderma as biological control agent: scope and prospects to improve efficacy.

A major current challenge is to increase the food production while preserving natural resources. Agricultural practices that enhance the productivity and progressively improve the soil quality are relevant to face this challenge. Trichoderma species are widely used in agriculture to stimulate the plant growth and to control different pathogens affecting crops, representing useful tools for sustainable food production. This mini-review summarizes applications of Trichoderma strains in agriculture to control fungal pathogens, nematodes and insects, the involved biocontrol mechanisms, efficacy and inoculation forms in greenhouse, field and post-harvest conditions. Aspects of Trichoderma handling that influence on biocontrol efficacy such as preventive treatments, frequency of applications and delivery methods are discussed. Strategies useful to improve the antagonistic performance such as the use of native strains, protoplast fusion, formulation, growth on pathogen cell wall medium and combination with other antagonists in integrated treatments are discussed. This mini-review provides practical knowledge to design safe and optimal biocontrol strategies based on Trichoderma and pose challenges to expand its antagonist performance.

Contribution to understanding the evolution of holometaboly: transformation of internal head structures during the metamorphosis in the green lacewing Chrysopa pallens (Neuroptera: Chrysopidae).

BACKGROUND: Metamorphosis remains one of the most complicated and poorly understood processes in insects. This is particularly so for the very dynamic transformations that take place within the pupal sheath of holometabolous insects. Only few studies address these transformations especially with regard to cranial structures of those holometabolous species where the larval and adult forms have a similar diet. It thus remains unclear to what extent the internal structures undergo histolysis and rebuilding. Here, the development of the brain and skeleto-muscular system of the head of Chrysopa pallens (Rambur, 1838) is studied. This species is a predator of aphids in the larval and adult stage. RESULTS: We used micro-computed-tomography (µ-CT) to study the transformations of the larval, prepupal and pupal head within the cocoon. We first assessed the morphological differences and similarities between the stages. We then determined the point in time when the compound eyes appear and describe the re-orientation of the head capsule which transforms the prognathous larva into a hypognathous adult. The internal head muscles are distinctly more slender in larvae than adults. In addition, the adults have a significantly larger brain which is likely needed for the processing of the signals obtained by the adults vastly expanded sensory organs that are presumably needed for dispersal and mating. Our study shows that the histolysis and modification of the inner muscles and skeletal elements take place within the prepupa. The central nervous system persists throughout metamorphosis but its morphology changes significantly. CONCLUSION: Our study reveals that not only the inner structures, but also the outer morphology continues to change after the final larval moult. The adult cuticle and internal structures form gradually within the cocoon. The histolysis and rebuilding begin with the skeletal elements and is followed by changes in the central nervous system before it concludes with modifications of the musculature. This order of events is likely ancestral for Holometabola because it is also known from Hymenoptera, Diptera, Mecoptera, and Coleoptera.