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25 result(s) for "Teets, Nicholas M."
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Obligate diapause and its termination shape the life-cycle seasonality of an Antarctic insect
The Antarctic midge, Belgica antarctica , is a unique insect endemic to Antarctica. It has a 2-year life cycle, with larvae overwintering in two different instars and adults emerging the following summer. This seasonality is crucial for adaptation to Antarctica’s harsh climates and ephemeral growing seasons; however, the underlying mechanisms remain unclear. We found that, under summer-like conditions, larvae could develop from egg to the fourth-instar larval stage without interruption, but they never pupated. Spontaneous developmental arrest at this stage suggests that they overwinter in obligate diapause, a genetically determined period of dormancy. The winter cold can terminate this diapause, and long-term cold exposure is more effective. Although this species can utilise two alternative cold tolerance strategies with diapause for overwintering, freezing was more successful than cryoprotective dehydration in allowing survival and developmental resumption in our experimental conditions. In contrast, the first three larval instars continued their development under the same conditions as the fourth-instar larvae. Although we do not exclude the possibility of facultative diapause, they likely overwinter in a quiescent state, an immediate developmental arrest in response to adversity, to maximise exploitation of the short Antarctic summer. Diapause and quiescence ensure developmental and reproductive success in this extremophile insect.
Compact genome of the Antarctic midge is likely an adaptation to an extreme environment
The midge, Belgica antarctica , is the only insect endemic to Antarctica, and thus it offers a powerful model for probing responses to extreme temperatures, freeze tolerance, dehydration, osmotic stress, ultraviolet radiation and other forms of environmental stress. Here we present the first genome assembly of an extremophile, the first dipteran in the family Chironomidae, and the first Antarctic eukaryote to be sequenced. At 99 megabases, B. antarctica has the smallest insect genome sequenced thus far. Although it has a similar number of genes as other Diptera, the midge genome has very low repeat density and a reduction in intron length. Environmental extremes appear to constrain genome architecture, not gene content. The few transposable elements present are mainly ancient, inactive retroelements. An abundance of genes associated with development, regulation of metabolism and responses to external stimuli may reflect adaptations for surviving in this harsh environment. The Antarctic midge, Belgica antarctica , is the only insect endemic to Antarctica. Here, the authors sequence the B. antarctica genome, the smallest insect genome yet reported, and suggest that genes involved in development, metabolism and stimuli response may have had a role in how this insect adapted to survive in such a harsh environment.
Insect capa neuropeptides impact desiccation and cold tolerance
The success of insects is linked to their impressive tolerance to environmental stress, but little is known about how such responses are mediated by the neuroendocrine system. Here we show that the capability ( capa ) neuropeptide gene is a desiccation- and cold stress-responsive gene in diverse dipteran species. Using targeted in vivo gene silencing, physiological manipulations, stress-tolerance assays, and rationally designed neuropeptide analogs, we demonstrate that the Drosophila melanogaster capa neuropeptide gene and its encoded peptides alter desiccation and cold tolerance. Knockdown of the capa gene increases desiccation tolerance but lengthens chill coma recovery time, and injection of capa peptide analogs can reverse both phenotypes. Immunohistochemical staining suggests that capa accumulates in the capa-expressing Va neurons during desiccation and nonlethal cold stress but is not released until recovery from each stress. Our results also suggest that regulation of cellular ion and water homeostasis mediated by capa peptide signaling in the insect Malpighian (renal) tubules is a key physiological mechanism during recovery from desiccation and cold stress. This work augments our understanding of how stress tolerance is mediated by neuroendocrine signaling and illustrates the use of rationally designed peptide analogs as agents for disrupting protective stress tolerance. Significance Insects are among the most robust organisms on the planet, surviving in virtually all environments and capable of surmounting a range of environmental stresses including desiccation and cold. Although desiccation and cold tolerance share many common traits, potential mechanisms for such linked responses remain unclear. Here we show that an insect neuropeptide gene is associated with tolerance of both desiccation and cold in Drosophila melanogaster , suggesting a novel mechanism in renal tubule epithelia that enhances survival of both desiccation and cold. Also, we can reverse RNAi-induced stress tolerance phenotypes in intact flies using rationally designed peptide mimetic analogs. We thus demonstrate the power of intervention in physiological processes controlled by neuropeptides, with potential for insect pest control.
Calcium signaling mediates cold sensing in insect tissues
The ability to rapidly respond to changes in temperature is a critical adaptation for insects and other ectotherms living in thermally variable environments. In a process called rapid cold hardening (RCH), insects significantly enhance cold tolerance following brief (i.e., minutes to hours) exposure to nonlethal chilling. Although the ecological relevance of RCH is well-established, the underlying physiological mechanisms that trigger RCH are poorly understood. RCH can be elicited in isolated tissues ex vivo, suggesting cold-sensing and downstream hardening pathways are governed by brain-independent signaling mechanisms. We previously provided preliminary evidence that calcium is involved in RCH, and here we firmly establish that calcium signaling mediates cold sensing in insect tissues. In tracheal cells of the freeze-tolerant goldenrod gall fly, Eurosta solidaginis, chilling to 0 °C evoked a 40% increase in intracellular calcium concentration as determined by live-cell confocal imaging. Downstream of calcium entry, RCH conditions significantly increased the activity of calcium/calmodulin-dependent protein kinase II (CaMKII) while reducing phosphorylation of the inhibitory Thr306 residue. Pharmacological inhibitors of calcium entry, calmodulin activation, and CaMKII activity all prevented ex vivo RCH in midgut and salivary gland tissues, indicating that calcium signaling is required for RCH to occur. Similar results were obtained for a freeze-intolerant species, adults of the flesh fly, Sarcophaga bullata, suggesting that calcium-mediated cold sensing is a general feature of insects. Our results imply that insect tissues use calcium signaling to instantly detect decreases in temperature and trigger downstream cold-hardening mechanisms.
Editorial: Rising stars in insect physiology
The four original contributions in this Research Topic focus on molecular and/or biochemical insights into the physiology of mosquitoes.Keyes-Scott et al.demonstrated the role of two previously orphaned G protein-coupled receptors (GPCRs) in reproduction of Aedes aegypti.Bianco et al.found that diapause in Culex pipiens can be disrupted by feeding them royal jelly produced by honey bees (Apis mellifera), which is enriched with Major Royal Jelly Protein 1, or by knocking down the mRNA encoding the orthologous protein in C. pipiens.Picinic et al.characterized the localization of several aquaporin (AQP) proteins in the alimentary canal, fat body, and ovaries of A. aegypti and demonstrated that localization was impacted by blood feeding, providing insights into putative roles in water and/or metabolite transport in these tissues. [...]Sajadi and Paluzzicharacterized the molecular and immunochemical expression of an understudied insect neuropeptide (ion transport peptide, ITP) in A. aegypti and used RNAi to uncover putative roles in excretory physiology, reproduction, and blood feeding. [...]Vinauger and Chandrasegaranreview studies on A. aegypti that use laboratory, semi-field, and field experiments to elucidate potential interactions between mosquito physiology and behavior and highlight the complications of studying mosquito life history traits associated with variations in larval competition nutrition and competition.
Gene expression changes governing extreme dehydration tolerance in an Antarctic insect
Among terrestrial organisms, arthropods are especially susceptible to dehydration, given their small body size and high surface area to volume ratio. This challenge is particularly acute for polar arthropods that face near-constant desiccating conditions, as water is frozen and thus unavailable for much of the year. The molecular mechanisms that govern extreme dehydration tolerance in insects remain largely undefined. In this study, we used RNA sequencing to quantify transcriptional mechanisms of extreme dehydration tolerance in the Antarctic midge, Belgica antarctica, the world’s southernmost insect and only insect endemic to Antarctica. Larvae of B. antarctica are remarkably tolerant of dehydration, surviving losses up to 70% of their body water. Gene expression changes in response to dehydration indicated up-regulation of cellular recycling pathways including the ubiquitin-mediated proteasome and autophagy, with concurrent down-regulation of genes involved in general metabolism and ATP production. Metabolomics results revealed shifts in metabolite pools that correlated closely with changes in gene expression, indicating that coordinated changes in gene expression and metabolism are a critical component of the dehydration response. Finally, using comparative genomics, we compared our gene expression results with a transcriptomic dataset for the Arctic collembolan, Megaphorura arctica. Although B. antarctica and M. arctica are adapted to similar environments, our analysis indicated very little overlap in expression profiles between these two arthropods. Whereas several orthologous genes showed similar expression patterns, transcriptional changes were largely species specific, indicating these polar arthropods have developed distinct transcriptional mechanisms to cope with similar desiccating conditions.
Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males
The Sterile Insect Technique (SIT) is a successful autocidal control method that uses ionizing radiation to sterilize insects. However, irradiation in normal atmospheric conditions can be damaging for males, because irradiation generates substantial biological oxidative stress that, combined with domestication and mass-rearing conditions, may reduce sterile male sexual competitiveness and quality. In this study, biological oxidative stress and antioxidant capacity were experimentally manipulated in Anastrepha suspensa using a combination of low-oxygen conditions and transgenic overexpression of mitochondrial superoxide dismutase (SOD2) to evaluate their role in the sexual behavior and quality of irradiated males. Our results showed that SOD2 overexpression enhances irradiated insect quality and improves male competitiveness in leks. However, the improvements in mating performance were modest, as normoxia-irradiated SOD2 males exhibited only a 22% improvement in mating success compared to normoxia-irradiated wild type males. Additionally, SOD2 overexpression did not synergistically improve the mating success of males irradiated in either hypoxia or severe hypoxia. Short-term hypoxic and severe-hypoxic conditioning hormesis, per se, increased antioxidant capacity and enhanced sexual competitiveness of irradiated males relative to non-irradiated males in leks. Our study provides valuable new information that antioxidant enzymes, particularly SOD2, have potential to improve the quality and lekking performance of sterile males used in SIT programs.
Characterization of drought-induced rapid cold-hardening in the Antarctic midge, Belgica antarctica
Survival of the terrestrial midge, Belgica antarctica, on the Antarctic Peninsula is promoted, not only by their adaptations to prolonged exposures to seasonal stresses, but also by their ability to respond to unpredictable changes in their environments. Rapid cold-hardening (RCH) is an extremely swift acclimatory response of insects that occurs within minutes to hours. While the RCH response is most commonly induced by a brief exposure to mildly low temperatures, a similar rapid acclimatory response can also be elicited by exposure to drought. In this study, we characterized this drought-induced RCH in larvae of B. antarctica. Compared to fully hydrated larvae, those desiccated at various relative humidity (R.H.) conditions between 0 and 99% R.H. for 2 h had a significantly greater survival ( ~ 50%) to freezing at − 14 °C. The amount of water loss varied between 4 and 16% depending on R.H. conditions; however, all treatments were equally effective in eliciting the protective response against freezing stress, and its induction was evident within 30 min of desiccation. Lack of substantial changes in body-fluid osmolality or levels of major cryoprotectants suggest that accumulation of these protective solutes is not a primary mechanism of this response. Interestingly, the RCH protection induced by desiccation persisted after larvae were allowed to recover a significant portion of the lost water. Our results indicate that larval midges are highly sensitive to desiccation, capable of swiftly initiating physiological changes in response to a small reduction in their body water content.
Transcriptional Regulation of Reproductive Diapause in the Convergent Lady Beetle, Hippodamia convergens
Diapause is an alternate development program that synchronizes an insect’s life cycle with seasonally abundant resources and ensures survival in unfavorable conditions. The physiological basis of diapause has been well characterized, but the molecular mechanisms regulating it are still being elucidated. Here, we present a de novo transcriptome and quantify transcript expression during diapause in the convergent lady beetle Hippodamia convergens. H. convergens is used as an augmentative biocontrol agent, and adult females undergo reproductive diapause that is regulated by photoperiod. We sampled females at three stages (early, mid, and late diapause) and compared transcript expression to non-diapausing individuals. Based on principle component analysis, the transcriptomes of diapausing beetles were distinct from non-diapausing beetles, and the three diapausing points tended to cluster together. However, there were still classes of transcripts that differed in expression across distinct phases of diapause. In general, transcripts involved in muscle function and flight were upregulated during diapause, likely to support dispersal flights that occur during diapause, while transcripts involved in ovarian development were downregulated. This information could be used to improve biological control by manipulating diapause. Additionally, our data contribute to a growing understanding of the genetic regulation of diapause across diverse insects.
Alternative overwintering strategies in an Antarctic midge: freezing vs. cryoprotective dehydration
Cryoprotective dehydration is a relatively new addition to our understanding of freeze avoidance strategies employed by polar invertebrates. Although the underlying cellular processes associated with this strategy are similar to those of freeze tolerance, little is known about potential trade‐offs of overwintering in these physiological states. This study compares the potential of larvae of the terrestrial midge Belgica antarctica (Diptera, Chironomidae) to overwinter in these two states. As the only insect with the capacity to tolerate freezing and to cryoprotectively dehydrate, it is an ideal model to compare the benefits and costs of these strategies. Compared to summer‐acclimated larvae, supercooling points of winter‐acclimatized larvae were significantly depressed and were lower than observed minima for their microhabitat temperatures. Thus, if larvae avoid inoculative freezing from environmental ice, they could remain unfrozen via cryoprotective dehydration. Both frozen and cryoprotectively dehydrated larvae readily survived a 32‐day exposure to simulated overwintering temperatures. Freezing had little effect on larval body water content and haemolymph osmolality. In contrast, cryoprotective dehydration at −5 °C resulted in a progressive loss of body water, ultimately reducing larval water content by 62%. This level of dehydration corresponded to an increase in haemolymph osmolality to c. 2750 mOsm kg⁻¹, depressing the haemolymph melting point to −4·9 °C. Freezing and cryoprotective dehydration resulted in distinctly different patterns of glycogen breakdown. Whereas the glycogen content decreased only during the first 14 days in cryoprotectively dehydrated larvae, frozen larvae continued to break down glycogen throughout the 32‐day subzero exposure. However, after recovery at 0 °C for 5 days, glycogen levels were similar in these two groups, as were the levels of total lipids. Our results indicate that freezing and cryoprotective dehydration are both effective in promoting winter survival of larvae, with surprisingly few differences in energetic costs. Whether larvae freeze or become cryoprotectively dehydrated ultimately depends on the hydric condition of their microhabitat. The physiological flexibility of B. antarctica to overwinter in these alternative states likely contributed to its range distribution that extends further south than any other free‐living insect.