Holometabolous Insects Research Articles

The Correlation between Reproductive Behavior and Population Structure of Holometabolous Insects

The Correlation between Reproductive Behavior and Population Structure of Holometabolous Insects

Analysis of Life Cycle and Development Process of Holometabolous Insects

Analysis of Life Cycle and Development Process of Holometabolous Insects

The Dietary Diversity of Holometabolous Insects and the Construction of Food Webs

The Dietary Diversity of Holometabolous Insects and the Construction of Food Webs

The Chemical Composition and Attack Mechanism of the Venom of Holometabolous Insects

The Chemical Composition and Attack Mechanism of the Venom of Holometabolous Insects

Endoreplication in the Drosophila melanogaster prothoracic gland is dispensable for the critical weight checkpoint.

Critical weight (CW) attainment is a key life event in the development of holometabolous insects including Drosophila melanogaster. It indicates that sufficient growth has occurred to initiate the juvenile-to-adult transition. The prothoracic gland (PG), the major insect larval endocrine organ, is a polyploid tissue that plays a key role in the determination of CW via release of the steroid hormone ecdysone. Here we show that when the cells of the PG fail to make the mitotic-to-endocycle switch, but instead remain mitotic, the result is more but smaller cells. Nevertheless, they reach the same CW and produce healthy adults after only a moderate developmental delay. We propose that the CW checkpoint can be reached by either an endocycling or mitotic PG and may simply reflect the attainment of sufficient ecdysone biosynthetic capacity to initiate metamorphosis.

State-dependency of behavioural traits is a function of the life-stage in a holometabolous insect

State-dependency of behavioural traits is a function of the life-stage in a holometabolous insect

Uric acid metabolism modulates diet-dependent responses to intraspecific competition in Drosophila larvae.

Intraspecific competition drives ecological specialization, and niche expansion. In holometabolous insects, larval intraspecific competition ("crowding") has lasting fitness consequences for individuals and shapes adaptive responses. However, our understanding of the molecular profile of larval crowding responses remains allusive. Here, I used a genetic construct in Drosophila melanogaster with disrupted uric acid metabolism (uro -) to demonstrate the role of the uric acid metabolism-and its interactive effects with larval crowding, diet, and urea concentration-on female oviposition and larval development. Uro - larvae developed faster in sugar-rich diets. However, uro - larvae pupated at lower heights in protein- and sugar-rich diets in crowded larval conditions and showed slower development in protein-rich mixed-genotype environments. uro - did not affect female oviposition nor larval pupation success. Overall, this study provides the first step toward an integrated understanding of the molecular pathways underpinning the responses to intraspecific competition in holometabolous insects.

Modalities of aging in organisms with different strategies of resource allocation.

Although the progress of aging research relies heavily on a theoretical framework, today there is no consensus on many critical questions in aging biology. I hypothesize that a systematic analysis of the intersection of different evolutionary mechanisms of aging with diverse resource allocation strategies in different organisms may reconcile aging hypotheses. The application of disposable soma, mutation accumulation, antagonistic pleiotropy, and life-history theory is considered across organisms with asexual reproduction, organisms with sexual reproduction and indeterminate growth in different conditions of extrinsic mortality, and organisms with determinate growth, with endotherms/homeotherms as a subgroup. This review demonstrates that different aging mechanisms are complementary to each other, and in organisms with different resource allocation strategies they form aging modalities ranging from immortality to suicidal programs. It also revamps the role of growth arrest in aging. Growth arrest evolved in many different groups of organisms as a result of resource reallocation from growth to reproduction (e.g., semelparous animals, holometabolic insects), or from growth to nutrient storage (endotherms/homeotherms). Growth arrest in different animal lineages has similar molecular mechanisms and similar consequences for longevity due to the conflict between growth-promoting and growth-suppressing programs and suppression of regenerative capacity.

Thermal stress exposure of pupal oriental fruit fly has strong and trait‐specific consequences in adult flies

AbstractGlobal climate change is projected to increase the incidence of heat waves, their magnitude and duration resulting in insects experiencing increasing environmental stress in both natural and managed ecosystems. While studies on insect thermal tolerance are rapidly increasing, variation across developmental or juvenile stress cross‐stage effects within and across generations remain largely unexplored. Yet in holometabolous insects, heat stress at an early developmental stage may influence performance and survival during later stages. Here, we investigated the effects of pupal mild heat stress on the performance of laboratory‐reared adult Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) measured as longevity, critical thermal maximum (CTmax), critical thermal minima (CTmin), heat knockdown time (HKDT) and chill coma recovery time (CCRT). Pupal heat stress significantly influenced performance of B. dorsalis adults resulting in impaired longevity and heat tolerance (CTmax and HKDT) in both sexes with improved and compromised cold tolerance (CTmin and CCRT) in females and males, respectively. These findings highlight the role of juvenile stages in mediating stress responses at adult stages. For B. dorsalis, pupal heat stress largely compromised thermal tolerance implying that the species has limited potential to shift its geographic range in heat prone areas. Significant benefits in cold tolerance in females following heat stress may help in improving survival in the cold in the short‐term despite restricted activity to the same traits in males. This study suggests that basal heat tolerance and not short‐term compensatory thermal plasticity following heat stress may have aided the recent invasion of B. dorsalis in African landscapes.

Nutritional and metabolic process of the dung beetle Phelotrupes auratus depends on the plant ingredients that the herbivores eat

BackgroundThe dung beetle Phelotrupes auratus is a holometabolous insect belonging to the order Coleoptera, and it is widely distributed in Japan. The P. auratus habitat depends on herbivores. P. auratus eats the dung of the herbivores and carries it underground for its young. In this process, herbivore droppings disappear from the ground, not only keeping the ground hygienic but also maintaining good soil conditions for plant growth. In this way, a rich ecosystem is maintained. In recent years, the population of P. auratus has decreased, and the main cause has been the decrease in grazing land. It seems that Japanese dung beetles are mainly dependent on herbivores for nutrient sources. However, the physiological relationship between herbivores and P. auratus has not been well investigated. Here, we investigated the nutritional metabolism system of P. auratus by performing whole gene expression analysis of individuals collected from two areas where the ecosystem is occupied by different herbivores.ResultsWe obtained 54,635 transcripts from P. auratus from Nara Park and Cape Toi and identified 2,592 differentially expressed genes in the fat bodies of the Nara Park and Cape Toi groups. We annotated P. auratus transcripts using Homo sapiens and Drosophila melanogaster genes as references; 50.5% of P. auratus transcripts were assigned to H. sapiens genes, and 54.0% of P. auratus transcripts were assigned to D. melanogaster genes. To perform gene set enrichment analysis, we chose H. sapiens genes for P. auratus transcript annotation. Principal component analysis and gene set enrichment analysis revealed that the nutritional metabolism of P. auratus from Cape Toi might differ from that of P. auratus from Nara Park.ConclusionWe analyzed the nutritional metabolism system of P. auratus from Cape Toi and Nara Park and found that the characteristics of the nutritional metabolism process might depend on the plants consumed by the herbivores. Our findings will contribute to elucidating the relationships among habitat plants, herbivores, and dung decomposers and may aid in the maintenance of sustainable land health cycles.

Redox Imbalance and Oxidative Eustress during Larval-Pupal Transition in a Holometabolous Insect

Redox Imbalance and Oxidative Eustress during Larval-Pupal Transition in a Holometabolous Insect

How does access to water at different life-stages affect male investment in reproduction and survival?

Holometabolous insects have four distinct life-stages – eggs, larvae, pupae and adults. Active resource acquisition generally occurs during either or both the larval and adult stages. Previous research on the acquisition of food resources in holometabolous insects, has shown that resources acquired during each of these life-stages can differ in how they are allocated to different traits, and how they affect fitness. In addition to food, water is also an essential resource needed for a range of biological processes that enhance fitness. Yet, how water acquired at different life-stages affects key fitness traits is still not clear. Here, we manipulated both developmental and adult water availability of male seed beetles (Callosobruchus maculatus) to explore how water acquired at each life-stage affects a range of fitness related traits, including body mass, ejaculate weight, mating behavior and lifespan. Our results indicate that the juvenile environment had little effect on body weight, ejaculate weight, ejaculate replenishment or lifespan, but did influence male mating behavior in both early and late adult life. This contrasts with the adult environment, which had strong effects on weight loss, ejaculate size and lifespan but little effect on mating behavior. Males with access to water during adulthood transferred larger ejaculates during their first mating, lost less weight as they aged, and lived longer. These results suggest that water acquired during development and adulthood are allocated differently to a variety of fitness traits across life.

Recapitulation of the embryonic transcriptional program in holometabolous insect pupae

Holometabolous insects are predominantly motionless during metamorphosis, when no active feeding is observed and the body is enclosed in a hardened cuticle. These physiological properties as well as undergoing processes resemble embryogenesis, since at the pupal stage organs and systems of the imago are formed. Therefore, recapitulation of the embryonic expression program during metamorphosis could be hypothesized. To assess this hypothesis at the transcriptome level, we have performed a comprehensive analysis of the developmental datasets available in the public domain. Indeed, for most datasets, the pupal gene expression resembles the embryonic rather than the larval pattern, interrupting gradual changes in the transcriptome. Moreover, changes in the transcriptome profile during the pupa-to-imago transition are positively correlated with those at the embryo-to-larvae transition, suggesting that similar expression programs are activated. Gene sets that change their expression level during the larval stage and revert it to the embryonic-like state during the metamorphosis are enriched with genes associated with metabolism and development.

Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom.

Extraembryonic tissues: exploring concepts, definitions and functions across the animal kingdom.

The transcriptomic signature of responses to larval crowding in Drosophila melanogaster.

Intraspecific competition at the larval stage is an important ecological factor affecting life-history, adaptation and evolutionary trajectory in holometabolous insects. However, the molecular pathways underpinning these ecological processes are poorly characterized. We reared Drosophila melanogaster at three egg densities (5, 60, and 300 eggs/mL) and sequenced the transcriptomes of pooled third-instar larvae. We also examined emergence time, egg-to-adult viability, adult mass, and adult sex-ratio at each density. Medium crowding had minor detrimental effects on adult phenotypes compared to low density and yielded 24 differentially expressed genes (DEGs), including several chitinase enzymes. In contrast, high crowding had substantial detrimental effects on adult phenotypes and yielded 2107 DEGs. Among these, upregulated gene sets were enriched in sugar, steroid and amino acid metabolism as well as DNA replication pathways, whereas downregulated gene sets were enriched in ABC transporters, taurine, Toll/Imd signaling, and P450 xenobiotics metabolism pathways. Overall, our findings show that larval crowding has a large consistent effect on several molecular pathways (i.e., core responses) with few pathways displaying density-specific regulation (i.e., idiosyncratic responses). This provides important insights into how holometabolous insects respond to intraspecific competition during development.

Complete metamorphosis and microbiota turnover in insects.

The insects constitute the majority of animal diversity. Most insects are holometabolous: during complete metamorphosis their bodies are radically reorganized. This reorganization poses a significant challenge to the gut microbiota, as the gut is replaced during pupation, a process that does not occur in hemimetabolous insects. In holometabolous hosts, it offers the opportunity to decouple the gut microbiota between the larval and adult life stages resulting in high beta diversity whilst limiting alpha diversity. Here, we studied 18 different herbivorous insect species from five orders of holometabolous and three orders of hemimetabolous insects. Comparing larval and adult specimens, we find a much higher beta-diversity and hence microbiota turnover in holometabolous insects compared to hemimetabolous insects. Alpha diversity did not differ between holo- and hemimetabolous insects nor between developmental stages within these groups. Our results support the idea that pupation offers the opportunity to change the gut microbiota and hence might facilitate ecological niche shifts. This possible effect of niche shift facilitation could explain a selective advantage of the evolution of complete metamorphosis, which is a defining trait of the most speciose insect taxon, the holometabola.

The role of neuropeptides in regulating ecdysis and reproduction in the hemimetabolous insect Rhodnius prolixus.

In ecdysozoan animals, moulting entails the production of a new exoskeleton and shedding of the old one during ecdysis. It is induced by a pulse of ecdysone that regulates the expression of different hormonal receptors and activates a peptide-mediated signalling cascade. In Holometabola, the peptidergic cascade regulating ecdysis has been well described. However, very little functional information regarding the neuroendocrine regulation of ecdysis is available for Hemimetabola, which display an incomplete metamorphosis. We use Rhodnius prolixus as a convenient experimental model to test two hypotheses: (1) the role of neuropeptides that regulate ecdysis in Holometabola is conserved in hemimetabolous insects; and (2) the neuropeptides regulating ecdysis play a role in the regulation of female reproduction during the adult stage. The RNA interference-mediated reduction of ecdysis triggering hormone (ETH) mRNA levels in fourth-instar nymphs resulted in lethality at the expected time of ecdysis. Unlike in holometabolous insects, knockdown of eth and orcokinin isoform A (oka) did not affect oviposition in adult females, pointing to a different endocrine regulation of ovary maturation. However, eth knockdown prevented egg hatching. The blockage of egg hatching appears to be a consequence of embryonic ecdysis failure. Most of the first-instar nymphs hatched from the eggs laid by females injected with dsRNA for eclosion hormone (dsEH), crustacean cardioactive peptide (dsCCAP) and dsOKA died at the expected time of ecdysis, indicating the crucial involvement of these genes in post-embryonic development. No phenotypes were observed upon corazonin (cz) knockdown in nymphs or adult females. The results are relevant for evolutionary entomology and could reveal targets for neuropeptide-based pest control tools.

Larval crowding effects during early development in the Chinese oak silkmoth Antheraea pernyi (Lepidoptera: Saturniidae).

Chinese sericulture relies in part on the rearing of the Chinese oak silkmoth Antheraea pernyi, an insect with key cultural and ecological roles. While feeding primarily on oak, Antheraea species are known to accept alternative hosts such as birch Betula sp with little to no apparent negative fitness consequences. This opens up the range of hostplants that could be used for large‐scale rearing of A. pernyi for silk production and food, or used by this species in possible invasions. To date, however, the natural history and ecology of A. pernyi remain subject of investigation. For instance, we still do not know how individuals respond to crowding developmental environments, which is an important factor to consider for the ecology of the species as well as for commercial rearing. Here, I describe the implications of larval crowding to the survival and growth of A. pernyi larvae during early development. I show that higher crowding is associated with stronger negative effects on growth and survival, corroborating findings from other holometabolous insects. I then discuss the implications of this findings for our understanding of optimum larval crowding. Overall, the findings reveal important ecological information for an insect species key for provisioning and cultural ecosystem services.

Morphological adaptation for ectosymbiont maintenance and transmission during metamorphosis in Lagria beetles.

The diversity and success of holometabolous insects is partly driven by metamorphosis, which allows for the exploitation of different niches and decouples growth and tissue differentiation from reproduction. Despite its benefits, metamorphosis comes with the cost of temporal vulnerability during pupation and challenges associated with tissue reorganizations. These rearrangements can also affect the presence, abundance, and localization of beneficial microbes in the host. However, how symbionts are maintained or translocated during metamorphosis and which adaptations are necessary from each partner during this process remains unknown for the vast majority of symbiotic systems. Here, we show that Lagria beetles circumvent the constraints of metamorphosis by maintaining defensive symbionts on the surface in specialized cuticular structures. The symbionts are present in both sexes throughout larval development and during the pupal phase, in line with a protective role during the beetle’s immature stages. By comparing symbiont titer and morphology of the cuticular structures between sexes using qPCR, fluorescence in situ hybridization, and micro-computed tomography, we found that the organs likely play an important role as a symbiont reservoir for transmission to female adults, since symbiont titers and structures are reduced in male pupae. Using symbiont-sized fluorescent beads, we demonstrate transfer from the region of the dorsal symbiont-housing organs to the opening of the reproductive tract of adult females, suggesting that symbiont relocation on the outer surface is possible, even without specialized symbiont adaptations or motility. Our results illustrate a strategy for holometabolous insects to cope with the challenge of symbiont maintenance during metamorphosis via an external route, circumventing problems associated with internal tissue reorganization. Thereby, Lagria beetles keep a tight relationship with their beneficial partners during growth and metamorphosis.

Metabolite Changes in Orange Dead Leaf Butterfly Kallima inachus during Ontogeny and Diapause.

Holometabolism is a form of insect development which includes four life stages: egg, larva, pupa, and imago (or adult). The developmental change of whole body in metabolite levels of holometabolous insects are usually ignored and lack study. Diapause is an alternative life-history strategy that can occur during the egg, larval, pupal, and adult stages in holometabolous insects. Kallima inachus (Lepidoptera: Nymphalidae) is a holometabolous and adult diapausing butterfly. This study was intended to analyze metabolic changes in K. inachus during ontogeny and diapause through a non-targeted UPLC-MS/MS (ultra-performance liquid chromatograph coupled with tandem mass spectrometry) based metabolomics analysis. A variety of glycerophospholipids (11), amino acid and its derivatives (16), and fatty acyls (nine) are crucial to the stage development of K. inachus. 2-Keto-6-acetamidocaproate, N-phenylacetylglycine, Cinnabarinic acid, 2-(Formylamino) benzoic acid, L-histidine, L-glutamate, and L-glutamine play a potentially important role in transition of successive stages (larva to pupa and pupa to adult). We observed adjustments associated with active metabolism, including an accumulation of glycerophospholipids and carbohydrates and a degradation of lipids, as well as amino acid and its derivatives shifts, suggesting significantly changed in energy utilization and management when entering into adult diapause. Alpha-linolenic acid metabolism and ferroptosis were first found to be associated with diapause in adults through pathway analyses. Our study lays the foundation for a systematic study of the developmental mechanism of holometabolous insects and metabolic basis of adult diapause in butterflies.