Contributions to the Genetics of Tenebrio Molitor L

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Studies on the mode of action of a juvenile hormone on the mealworm Tenebrio molitor L. The morphology and histogenesis of the blood of the mealworm Tenebrio Molitor L. Host induced alteration of eastern equine encephalomyelitis virus in Tenebrio molitor L. The effects of the natural fats of tenebrio molitor on the tyrosinase-melanin reaction. Ein beitrag zur kenntnis der tyrosinase von tenebrio molitor.

The olfactory sense of the adult meal-worm beetle Tenebrio molitor Linn. Skip to main Skip to similar items. HathiTrust Digital Library. Search full-text index. Available Indexes Full-text Catalog Full view only. Advanced full-text search Advanced catalog search Search tips. Search HathiTrust. Tools Cite this Export citation file. Author Ferwerda, Feiko Pier. Published Males that are experiencing a non-infectious immune-challenge, e.

Indeed, the immune challenge may induce in males, the perception of a lower survival probability consequent to their simulated infection status, causing the insect to make a last attempt to achieve a maximized level of reproductive success. The underlying signaling may transit through juvenile hormone JH , a hormone secreted by the corpora allata that is involved in the control of morphogenesis and reproduction in insects, as T.

So far, comparable adjustment of the reproductive effort upon infection has never been reported in females. The insect integument forms a robust barrier that successfully prevents most parasites and pathogens from colonizing the hemocoel Moret and Moreau, It usually constitutes the first barrier between an insect and endogenous invaders. The integument includes an outer layer, called the cuticle, which is produced by a monolayer of epidermal cells.

This layer of cells, or epidermis, is separated from the underlying tissues by a thin matrix called the basal lamina. In addition, melanin is toxic to microorganisms and has potent antimicrobial activity Soderhall and Ajaxon, In the mealworm beetle, the degree of cuticular melanization is a strong indicator of resistance to the entomopathogenic fungus, Metarhizium anisopliae. Indeed, darker beetles are more resistant than lighter ones Barnes and Siva-Jothy, Insect growth and development involve a series of molts during which the old cuticle is partially digested, while a new cuticle is formed and the remnant is discarded.

In addition to allowing insect growth, molting may serve as a defense mechanism by reducing the negative effects of a wound or a parasite invasion. For instance, molting quickly in response to a parasite exposure prevents parasites from remaining attached to the cuticle; subsequently, reducing the probability of a successful infection Duneau and Ebert, ; Kim and Roberts, The benefit of such molting could be exploited by the host inducing precocious molts in response to parasite early attachment Duneau and Ebert, ; Moret and Moreau, However, larvae grow through a variable number of molts from 8 to This suggests that the mealworm beetle can adjust its development in response to its environment.

Hence, it would be highly relevant to investigate the capacity of the mealworm to molt subsequently to the pressure caused by a wound or a pathogen attempting to invade the insect.

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Once a parasite or a pathogen has breached the integumental defenses, the insect has to produce a rapid and effective response that localizes and neutralizes the growth and development of the microbe. Like in other insects, hemocoelic defenses of T. Insect innate immune response relies mainly on those pathways, which, via their synergic actions, form efficient cellular and humoral responses. Cellular defenses primarily involve the action of immune cells called hemocytes, which drive phagocytosis, nodulation, and encapsulation of endogenous organisms.

Insects possess several types of circulating hemocytes that are morphologically and functionally distinct, and the prevalence of which is variable in the hemolymph. Plasmatocytes are large elongated cells that are likely involved in encapsulation. They are large oval cells with a centrally located nucleus and presumably produce enzymes of the melanization cascades.

Hemocyte phagocytosis is achieved upon the recognition of microbes, either directly or after their opsonization by thioester proteins TEPs , using Scavenger and Nimrod receptors or using the highly variable, alternatively spliced Dscam Cherry and Silverman, Particularly, T. When an endogenous object is too big to be phagocytized, the cellular immune response also relies on melanization and encapsulation processes.

Upon wounding or recognition of a foreign object by GNBPs and PGRPs, prophenoloxidase proPO , a zymogen present in some hemocytes and in the plasma, is cleaved through a cascade of serine proteases to liberate the active phenoloxidase PO. This enzyme catalyzes the production of melanin. In arthropods, levels of melanin and circulating proPO enzymes are used to evaluate immune functions and status. The plasticity of those traits could indicate a higher cost for the insect to maintain a more efficient immune system Barnes and Siva-Jothy, Unidentified trade-offs structuring insect life history traits may prevent the fixation of the darker cuticle phenotype in the wild.

Those intermediates are also part of a more systemic immune response as they are liberated in the insect hemolymph along with the inducible synthesis of AMPs produced by the fat body. These pathways are conserved in many insects including T. Contrary to the transient and immediate induction of cellular immune effectors, T. Interestingly, AMPs are induced in T. Moreover, the levels of immune gene expression in the eggs reach comparable levels to the expression in adults.

This suggests that eggs contain immunocompetent cells in addition to maternal effects to defend themselves against potential invaders. It is not known if T. Figure 1. Summary of the major pathways constituting T. Figure 2. Diversity of the hemocytes composing T. The risk for an individual to be infected with pathogens and parasites increases when it lives in a population with higher density.

Hence, it would be beneficial for individuals developing in such conditions to invest more in their defense mechanisms than individuals experiencing a low-density environment. This concept was first defined investigating the noctuid moth Spodoptera exempta , which presents a higher resistance to baculovirus when developing in high-density conditions Wilson and Reeson, This is especially supported in T.

Nevertheless, the plasticity of the melanization phenotypes in response to population density added to the absence of predominance of darker individuals among T. Figure 3. Factors influencing T. While population density influences insect melanization, the underlying molecular mechanisms governing DDP are still unclear. Nevertheless, DDP demonstrates that interaction between individuals can structure their development, including the immune defenses. A recent study investigated whether T. The authors did not report any evidence leading to the conclusion that social immunization exists in the mealworm beetle.

This suggests that T. Density- and infection-sensing can also modulate resistance mechanisms across generations, as shown by the water flea, Daphnia magna Michel and Hall, , and the cotton leafworm, Spodoptera littoralis Wilson and Graham, In those models, crowding the parental generation conditioned the immune response of the offspring associated to increased levels of parasite resistance.

No such result has been yet demonstrated in T. Hence, because the mealworm displays DDP, it would be highly relevant to investigate whether high-density conditions could lead to improve egg immunity. With the rising concern for climate change, a growing number of studies have focused on how temperature fluctuation impacts insect biology. One recent aspect of this field of investigations relates to the influence of temperature on insect immunity. Temperature stress triggers the production of heat-shock protein HSP that helps organisms to sustain said stress.

Interestingly, those proteins are also expressed in T. Altogether, these results show that temperature-related genes are intimately intricate with immune pathways, suggesting a potential influence of temperature on immune defenses. Conversely, the velvet bean caterpillar, Anticarsia gemmatalis , presents fewer hemocytes when developing at a higher temperature Silva and Elliot, As organisms evolve and build trade-offs between their life history traits influenced by their environment, it is expected that mechanisms underlying resistance or tolerance to stress correlate differently to the impacted life history traits.

It is especially relevant for insects, which, because they are ectothermic, must resist the variations of their environmental temperature. Moreover, while developing in warmer temperature conditions, the mealworm beetle experiences a shortened larval development and presents longer elytra. It shows that the insect biology in its whole is impacted by the temperature, which imposes trade-offs between different life history traits of an individual.

Contributions to the genetics of Tenebrio molitor L. - Research database - University of Groningen

While temperature stress impacts insect immune defenses, little is known about how and whether it also affects the immune system of offspring. This inquiry has been explored in T. In addition, a cold shock experienced by the mother or both parents induced higher PO activity in the offspring, while a heat shock of either parent, or both, reduced the PO activity of their offspring. In conclusion, temperature is an important parameter that can significantly influence the biology of individuals, including their immune system. Hence, it would be beneficial to further investigate how temperature relates to T.

Food quality and quantity are critical to immune defenses against parasites and pathogens. While leveraging food amount and quality for restricting or controlling pest populations is difficult, we may use nutrients that directly or indirectly improve the immune system of insects that we would like to maintain or mass rear. As immune functions require metabolic resources, food restriction can impair immune activity. For instance, adult T. Furthermore, following an immune challenge, T.

Hence, unsurprisingly, food supply is important to keep insects healthy. The same observation has been made for T. As a consequence of this diet shift, hemocyte circulation and antibacterial activity are enhanced in the hemolymph, which presumably maximizes resistance against bacterial infection. On the one hand, excess levels of PO activity could be dangerous, as uncontrolled activation of PO in the hemocoel would result in the production of toxic quinones and reactive oxygen species, which could harm self-tissues and organs Nappi and Vass, ; Sadd and Siva-Jothy, Therefore, preventing excessive diet-mediated upregulation of PO activity might be required.

On the other hand, PO is also involved in a large set of physiological functions independent of immunity Hiruma and Riddiford, Thus, preventing its excessive downregulation may help to maintain homeostasis of those other physiological functions. Interestingly, immune-challenged T. Hence, a relevant way to maximize growth and immunity of mealworm beetles would be to supply the insect with nutrient adjusted according to their physiological needs. The experimental supplementation of T. Interestingly, the cuticle was also thicker, but only in females, suggesting that males and females are allocating their tyrosine resources differently.

Insect immune activities are associated with the production and release of cytotoxic compounds such as reactive oxygen and nitrogen species ROS and RNS, respectively Nappi and Vass, While these toxic substances help to kill invading organisms, they also cause self-damage in T.

While insects rely on endogenous antioxidants to scavenge these free radicals, this process might be supported by dietary sources of antioxidants Chew and Park, Contrary to these general observations, life-time dietary supplementation of T.

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Such an alteration of the host metabolism may reduce the allocation of energetic resources to the immune system. If these receptors are conserved among taxa, similar regulatory effects may also occur in insects. These results suggest that supplying T. Hence, the use of this carotenoid might not be adequate when rearing this insect. By contrast, its immune-depressive effect could be used to improve the success of microbial insecticides, where the insect is detrimental Figure 4. Figure 4. Potential methods to weaken T. Like other invertebrates, T. However, the invertebrate immune system is capable of functional modulation similar to the acquired immune response of vertebrates Moret and Siva-Jothy, ; Moret, This suggests that immune priming originates, at least partially, from activation of immune defenses rather than solely from the presence of MAMPs.

First, it may involve a sustained response, corresponding to the long-lasting upregulation of the same immune effectors after the initial immune challenge. Second, a recalled response results in a faster and stronger response after a secondary infection in a way that is reminiscent of the vertebrate acquired immune response. Third, priming may induce an immune shift, involving different immune effector systems during the primary and the secondary immune responses. Current evidence suggests that individual immune priming in T. Therefore, individual priming responses induced by Gram-positive bacteria are stronger and more protective than those induced by Gram-negative bacteria in T.

However, while the maternal challenge with S. Hence, offspring immunity is affected differently through TGIP depending on the nature of the maternal challenge. Figure 5. TGIP enhances offspring resistance to pathogens if either the father left or the mother right has been primed. However, the sex of the parent triggering the TGIP produces different consequences on the offspring traits.

Offspring originated from a mother primed with either LPS blue , Gram-negative bacteria red , or Gram-positive bacteria green are also affected differently by the TGIP. Larval developmental time stopwatch is represented by the length of the arrows between larvae and pupae arbitrary scale. Weight of the pupae scale is represented by the size of the scheme at this stage arbitrary scale.

Contributions to the Genetics of Tenebrio Molitor L

Density of hemocytes and hemolymph phenoloxidase PO activity is represented by the relative abundance of their corresponding symbols in the circles originated from the offspring beetles. Although TGIP occurs in several invertebrate species, investigations on its molecular mechanisms have just begun. Interestingly, T. These results suggest that mechanisms regulating protection of eggs and adult offspring are probably different. Hence, TGIP likely involves independent mechanisms that are acting simultaneously or sequentially over the development of the insect. While hemocytes may play a role in immune memory, evidence is still scarce.

These siRNAs, secreted in exosome-like vesicles of immune cells, may represent the source of information storage. Similar processes are unknown in T. Epigenetic reprogramming was also proposed as an important process to support within and trans-generational immune priming Ottaviani, Epigenetic reprogramming of immune cells could be achieved through remodeling of DNA methylation patterns, changes in histone marks, modifications of chromatin structure, or changes in miRNA or lncRNA expression patterns. No global changes in DNA methylation resulting from either within or across generation immune priming were detected.

However, whether DNA methylation was affecting smaller relevant portions of the genomic DNA, for instance, targeting the regulatory regions of a restricted number of genes was not investigated. In addition, a low proportion of RNA methylation results from individual immune priming, indicating that RNA methylation could be involved in the process.

However, no such change results from TGIP. Further study is needed to identify the types of RNA involved in methylation and their implication in the individual priming process. The involvement of microRNA, lncRNA, and changes in chromatin structure has not been investigated in TGIP, despite their involvement in invertebrate immunity and host-pathogen interactions Asgari, Hence, considering the prominent role of epigenetics in many trans-generational adaptation processes in animals and its implication in the modulation of several immune response pathways, its involvement in immune priming, especially in TGIP, might be a promising avenue to explore in greater depth.

Immune priming, either within or across generation, is beneficial by enhancing individual immune protection against repeated infections. However, this process likely exerts energy-related costs that would constrain the expression of other important functions. These costs might be bearable upon high risks of repeated infection but could be heavy when re-infection is unlikely Tate, The cost of individual immune priming includes the cost of the initial immune response, upon a primary contact with the pathogen, and the additional cost of keeping the immune system upregulated for an extended period of time i.

The cost of TGIP is likely shared by both parents and offspring. On the one hand, parents, especially mothers, may support part of the cost of TGIP by producing and transferring immune substances to their eggs in addition to paying the usual immune activation costs resulting from the priming infection Moret and Schmid-Hempel, For instance, bacterially immune-challenged females of T. On the other hand, enhanced immunity in the offspring may compromise other important functions.

TGIP enhances immunity in the offspring of T. A prolonged larval development time increases the probability of mortality Bell, , especially in tenebrionid beetles, which exhibits cannibalism on juveniles Ichikawa and Kurauchi, However, such a cost in T. As pathogens may vary in the selective pressure they impose on hosts, T.

In other insects, primed offspring exhibit reduced fecundity at the adult stage Trauer and Hilker, and reduced resistance to a different parasite type to which the mother was exposed Sadd and Schmid-Hempel, Further investigations are needed to reveal whether T. These negative effects associated to TGIP may result from the offspring trading-off their immunity against other functions.

Alternatively, they may be the consequence of a reduced parental investment per offspring resulting from the cost of the parental immune challenge. However, recent evidence showed that immune-challenged T. This suggests that TGIP cost is likely to arise from offspring trade-offs and not from a reduced parental investment. Indeed, understanding the microbiota of insects that are used for consumption is an essential for identifying potential spoilage bacteria and food pathogens. The gut-associated microbiota is an important mediator of host development and growth.

While no such intimate interaction has yet been described between T. In addition, microbe-free T. As previously mentioned, another growing interest for T. While polystyrene foam decreases T. This makes the insect a relevant alternative to recycle polystyrene. Especially, the bacterium Exiguobacterium sp. This shows that specific members of the microbial community confer the mealworm its ability to digest polystyrene. Hence, targeting the microbial community of T. This could be achieved via isolation of bacteria originating from the mealworm microbiota that would be genetically engineered to produce polystyrene-degrading enzymes.

In addition to supporting insect growth, indigenous microbes can mediate the development and function of their host immune system. These examples demonstrate the intricate impact that the microbiota plays on host immune development. Such an association between T. Nevertheless, the enhanced immune response conferred by oral priming and TGIP demonstrates that immune mechanisms are adjustable according to T.

Also, it was suggested that microbiota influences oral priming in the red flour beetle T. Hence, exploring whether T. The microbiota of T. Thus, the presence of pathogens in mealworms would serve as an impediment to the use of this insect as a source of human and animal food. How the immune system could cope with controlling pathogens or modifying the microbiota structure is still an open question. However, the activation of the immune system through the production of antimicrobial peptides before processing the larvae could help to prevent an unwanted microbial community growing within insect-processed products.

In consequence, primed insects would incorporate antimicrobial peptides that prevent unwanted microbes from contaminating the mealworm-derived food and feed. Hence, insect farms have started to mass produced mealworms despite the risk of an infection outbreak. While supplementation of tyrosine could be easily achieved, increasing the rearing temperature would cause some deleterious effects on the insect immune system, which makes it a versatile parameter to account for. Immune priming could be an asset for the mass production of healthy insects while keeping in mind the deleterious effects on other traits of the offspring.

However, all the studies investigating immune priming in T. This may prove difficult in mass-reared insects due to their large number. Alternatively, managing individually the parental line to enhance offspring immune parameters would be an easier task than trying to apply a method to each mass-produced insect. Hence, applying such stress only to insects destined for reproduction could enhance the overall immunity of the colony Figure 5.

Immune priming may also have strong implications for the control of populations of pest insects, such as T. Indeed, when failing to kill the insects, biocontrol agents may subsequently enhance the insect resistance or tolerance, rendering their use less efficient over time. The control of unwanted populations might be even further complicated when, like in T. Furthermore, insects may not necessarily need to suffer from the infection by the pathogen to become primed, as the consumption of dead bacteria in the food could be sufficient to prime them, as shown for T.

Such an infection-free priming process may keep the insects vigorous enough to maintain prolific reproduction while becoming more immunocompetent. Optimizing the production of insects such as T. Given the broad spectrum activity exhibited by insect AMPs, their production in heterologous systems can reveal difficult.

However, T. Because the purification of AMPs could prove difficult, the use of a whole insect extract could be a viable alternative. It would be highly beneficial to optimize production of the insect, in combination with improving its digestive capacity via microbiota manipulation, as an alternative to conventional polystyrene recycling schemes. Fundamentally, T.

Recently, the insect immune system has been studied in the context of developing new tools for insect pest control. Recently, this method was applied to downregulate the expression of genes involved in T. RNAi-driven knockdown of cactus leads to the death of the insect, validating the relevance of targeting this gene as a novel control method. However, as cactus , and more globally the Toll pathway, is required for dorsoventral patterning in Drosophila melanogaster Belvin and Anderson, , the observed effect on T. As developmental genes are usually highly conserved across taxa, targeting genes specifically involved in the immune system of an organism under infection could prevent such an effect.

Knockdown of immune genes could be combined with the use of T. AV and YM conceived the ideas.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank Dr. Brian Weiss for his critical review of the manuscript and the reviewers for their constructive criticisms. Altincicek, B. Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum. Andersen, S. Insect cuticular sclerotization: a review. Insect Biochem. Armitage, S. Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity 94, — Arnaud, L.

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