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A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology

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A special issue of Insects (ISSN 2075-4450). This special issue belongs to the section "Insect Physiology, Reproduction and Development".

Deadline for manuscript submissions: 30 April 2024 | Viewed by 20271

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Special Issue Editors

Dr. Geoffrey M. Attardo

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Guest Editor

Department of Entomology and Nematology, University of California, Davis, CA, USA
Interests: insect disease vectors; insect reproduction; vector/parasite interactions; reproductive physiology; male seminal secretions; symbiosis; lactation; nutrition; lipid metabolism; transcriptional regulation; comparative genomics; transcriptomics; proteomics and metabolomics

Prof. Dr. Serap Aksoy

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Guest Editor

Department of Epidemiology of Microbial Diseases, Yale School of Public Health, Yale University, New Haven, CT, USA
Interests: global health; trypanosomiasis; tsetse flies

Dr. Joshua B. Benoit

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Guest Editor

Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221, USA
Interests: insect stress tolerance; reproductive physiology; regulation of metabolism and aging
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The study of insect physiology allows us to explore the complex mechanisms underlying the adaptations that facilitate their amazing diversity and adaptive power. This knowledge allows us, as scientists, to understand the fundamental principles behind how life evolves to solve difficult environmental problems and persist and thrive in unique and sometimes hostile conditions. This can provide new insights into our own physiology, provide models with which we can study disease, and help us to develop new potential treatments. Having a detailed understanding of the physiological systems involved in pest and disease vectoring insects can also lead to new ways to control these insects that are more efficient with a decreased impact on the environment.

In this Special Issue, we recognize the immense contributions that Dr. David Denlinger has made across various topics in the field of insect physiology during his amazing career. Dave’s passion for insects began as a child and guided him to study fundamental and fascinating physiological questions such as “How can an insect survive in the extreme cold of the Antarctic? How does a fly lactate and give birth? How do insects know when to hibernate? How do organ systems in an insect communicate?”. In the process of investigating these questions, Dave has inspired, trained, and boosted the careers of many other insect physiologists who have gone on to make amazing discoveries of their own.

This issue highlights papers from researchers (many of whom trained under Dave) who continue to pursue topics such as viviparity, diapause, cold tolerance, circadian rhythms, and endocrinology and expand upon the foundational knowledge and systems established by Dave’s research.

Dr. Geoffrey M. Attardo
Prof. Dr. Serap Aksoy
Dr. Joshua B. Benoit
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Insects is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

Glossina
lactation
viviparity
trypanosomiasis
sub-Saharan Africa
symbiosis
diapause
cold tolerance
circadian rhythm
endocrinology

Published Papers (7 papers)

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Research

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11 pages, 1699 KiB

Open AccessArticle

The Impact of Climate on the Energetics of Overwintering Paper Wasp Gynes (Polistes dominula and Polistes gallicus)

by Helmut Kovac, Helmut Käfer, Iacopo Petrocelli, Astrid B. Amstrup and Anton Stabentheiner

Insects 2023, 14(11), 849; https://doi.org/10.3390/insects14110849 - 31 Oct 2023

Cited by 2 | Viewed by 1034

Abstract

Gynes of paper wasps (Polistes sp.) spend the cold season in sheltered hibernacles. These hibernacles protect against predators and adverse weather conditions but offer only limited protection against low temperatures. During overwintering diapause, wasps live on the energy they store. We investigated the hibernacles’ microclimate conditions of species from the Mediterranean (Italy, P. dominula, P. gallicus) and temperate (Austria, P. dominula) climates in order to describe the environmental conditions and calculate the energetic demand of overwintering according to standard metabolic rate functions. The temperatures at the hibernacles differed significantly between the Mediterranean and temperate habitats (average in Austria: 3.2 ± 5.71 °C, in Italy: 8.5 ± 5.29 °C). In both habitats, the hibernacle temperatures showed variance, but the mean hibernacle temperature corresponded closely to the meteorological climate data. Cumulative mass-specific energetic costs over the studied period were the lowest for the temperate P. dominula population compared with both Mediterranean species. The lower costs of the temperate species were a result of the lower hibernacle temperature and acclimation to lower environmental temperatures. Model calculations with an increased mean temperature of up to 3 °C due to climate change indicate a dramatic increase of up to 40% in additional costs. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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13 pages, 1369 KiB

Open AccessArticle

MicroRNA Expression Prior to Biting in a Vector Mosquito Anticipates Physiological Processes Related to Energy Utilization, Reproduction and Immunity

by Sarah Marzec, Alden Siperstein, Angela Zhou, Christina M. Holzapfel, William E. Bradshaw, Megan E. Meuti and Peter A. Armbruster

Insects 2023, 14(8), 700; https://doi.org/10.3390/insects14080700 - 10 Aug 2023

Cited by 1 | Viewed by 952

Abstract

Understanding the molecular and physiological processes underlying biting behavior in vector mosquitoes has important implications for developing novel strategies to suppress disease transmission. Here, we conduct small-RNA sequencing and qRT-PCR to identify differentially expressed microRNAs (miRNAs) in the head tissues of two subspecies of Culex pipiens that differ in biting behavior and the ability to produce eggs without blood feeding. We identified eight differentially expressed miRNAs between biting C. pipiens pipiens (Pipiens) and non-biting C. pipiens molestus (Molestus); six of these miRNAs have validated functions or predicted targets related to energy utilization (miR8-5-p, miR-283, miR-2952-3p, miR-1891), reproduction (miR-1891), and immunity (miR-2934-3p, miR-92a, miR8-5-p). Although miRNAs regulating physiological processes associated with blood feeding have previously been shown to be differentially expressed in response to a blood meal, our results are the first to demonstrate differential miRNA expression in anticipation of a blood meal before blood is actually imbibed. We compare our current miRNA results to three previous studies of differential messenger RNA expression in the head tissues of mosquitoes. Taken together, the combined results consistently show that biting mosquitoes commit to specific physiological processes in anticipation of a blood meal, while non-biting mosquitoes mitigate these anticipatory costs. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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14 pages, 1517 KiB

Open AccessArticle

Dehydration Alters Transcript Levels in the Mosquito Midgut, Likely Facilitating Rapid Rehydration following a Bloodmeal

by Christopher J. Holmes, Elliott S. Brown, Dhriti Sharma, Matthew Warden, Atit Pathak, Blaine Payton, Quynh Nguyen, Austin Spangler, Jaishna Sivakumar, Jacob M. Hendershot and Joshua B. Benoit

Insects 2023, 14(3), 274; https://doi.org/10.3390/insects14030274 - 09 Mar 2023

Cited by 1 | Viewed by 1605

Abstract

The mosquito midgut is an important site for bloodmeal regulation while also acting as a primary site for pathogen exposure within the mosquito. Recent studies show that exposure to dehydrating conditions alters mosquito bloodfeeding behaviors as well as post-feeding regulation, likely altering how pathogens interact with the mosquito. Unfortunately, few studies have explored the underlying dynamics between dehydration and bloodmeal utilization, and the overall impact on disease transmission dynamics remains veiled. In this study, we find that dehydration-based feeding in the yellow fever mosquito, Aedes aegypti, prompts alterations to midgut gene expression, as well as subsequent physiological factors involving water control and post-bloodfeeding (pbf) regulation. Altered expression of ion transporter genes and aquaporin 2 (AQP2) in the midgut of dehydrated mosquitoes as well as the rapid reequilibration of hemolymph osmolality after a bloodmeal indicate an ability to expedite fluid and ion processing. These alterations ultimately indicate that female A. aegypti employ mechanisms to ameliorate the detriments of dehydration by imbibing a bloodmeal, providing an effective avenue for rehydration. Continued research into bloodmeal utilization and the resulting effects on arthropod-borne transmission dynamics becomes increasingly important as drought prevalence is increased by climate change. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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17 pages, 1270 KiB

Open AccessArticle

Light Pollution Disrupts Seasonal Differences in the Daily Activity and Metabolic Profiles of the Northern House Mosquito, Culex pipiens

by Matthew Wolkoff, Lydia Fyie and Megan Meuti

Insects 2023, 14(1), 64; https://doi.org/10.3390/insects14010064 - 10 Jan 2023

Cited by 5 | Viewed by 8796

Abstract

The Northern House mosquito, Culex pipiens, is an important disease vector, and females are capable of surviving the winter in a state of overwintering diapause. This species’ diapause response has been extensively studied, and recent evidence suggests that the circadian clock is involved in measuring seasonal changes in daylength to initiate the diapause response. However, differences in the circadian activity of diapausing and non-diapausing Cx. pipiens have not been thoroughly investigated. Additionally, recent findings indicate that artificial light at night (ALAN) can disrupt mosquito diapause, potentially prolonging the mosquito biting season. We compared the circadian locomotor activity of mosquitoes reared in diapause-averting, long-day conditions and diapause-inducing, short-day conditions with and without ALAN to elucidate the interplay between circadian activity, diapause, and light pollution. We also uncovered metabolic differences between mosquitoes reared under diapausing and non-diapausing photoperiods with and without ALAN by measuring the concentration of protein, fructose, glycogen, water-soluble carbohydrates, and lipids. We found that ALAN exposure altered several diapause-associated phenotypes including slightly, but not significantly, increasing activity levels in short day-reared mosquitoes; and preventing some short day-reared mosquitoes from accumulating lipids. ALAN also significantly reduced glycogen and water-soluble carbohydrate levels in long day-reared mosquitoes. Based on our findings, light pollution may decrease insect fitness by perturbing metabolism, and may also impact several phenotypes associated with insect diapause, potentially extending the mosquito biting season and preventing insects in urban environments from overwintering successfully. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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11 pages, 1847 KiB

Open AccessArticle

Latent Genetic Effects of Past Selection on Blood Feeding: History Matters

by William E. Bradshaw, Piper Kizziar, Rudyard J. Borowczak, Ethan Kirsch and Christina M. Holzapfel

Insects 2022, 13(10), 939; https://doi.org/10.3390/insects13100939 - 16 Oct 2022

Cited by 1 | Viewed by 1405

Abstract

Conventional wisdom is that selection decreases genetic variation in populations, variation that should enable and be essential for population persistence in an ever-changing world. Basically, we find the opposite. Response to selection on biting in the pitcher-plant mosquito, Wyeomyia smithii, increases from 20 to 80% in 19 generations, but reverts back to the original 20% after seven generations of relaxed (not reversed) selection. At the same time, biting in the control line remains at the original 20% through 30 generations without blood feeding. Imposition of selection on biting in both lines elicits a rapid response in the previously selected line, but, importantly, not in the control line. Genetic variation for biting has increased, not decreased, as a consequence of long-term directional selection, contrary to expectations. Convergent phenotypes belie the underlying difference in future adaptive potential. Selection events over time in the background of individuals or populations will determine outcomes of applied research, be it in the fields of medicine, agriculture, or conservation. In short, history matters. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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Graphical abstract

18 pages, 1360 KiB

Open AccessArticle

Transcriptional Regulation of Reproductive Diapause in the Convergent Lady Beetle, Hippodamia convergens

by Emily A. W. Nadeau, Melise C. Lecheta, John J. Obrycki and Nicholas M. Teets

Insects 2022, 13(4), 343; https://doi.org/10.3390/insects13040343 - 31 Mar 2022

Cited by 3 | Viewed by 2499

Abstract

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. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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Review

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18 pages, 732 KiB

Open AccessReview

The Fallacy of Year-Round Breeding in Polyphagous Tropical Fruit Flies (Diptera: Tephritidae): Evidence for a Seasonal Reproductive Arrestment in Bactrocera Species

by Anthony R. Clarke, Peter Leach and Penelope F. Measham

Insects 2022, 13(10), 882; https://doi.org/10.3390/insects13100882 - 28 Sep 2022

Cited by 5 | Viewed by 2142

Abstract

The genus Bactrocera (Diptera: Tephritidae) is endemic to the monsoonal rainforests of South-east Asia and the western Pacific where the larvae breed in ripe, fleshy fruits. While most Bactrocera remain rainforest restricted, species such as Bactrocera dorsalis, Bactrocera zonata and Bactrocera tryoni are internationally significant pests of horticulture, being both highly invasive and highly polyphagous. Almost universally in the literature it is assumed that Bactrocera breed continuously if temperature and hosts are not limiting. However, despite that, these flies show distinct seasonality. If discussed, seasonality is generally attributed to the fruiting of a particular breeding host (almost invariably mango or guava), but the question appears not to have been asked why flies do not breed at other times of the year despite other hosts being available. Focusing initially on B. tryoni, for which more literature is available, we demonstrate that the seasonality exhibited by that species is closely correlated with the seasons of its endemic rainforest environment as recognised by traditional Aboriginal owners. Evidence suggests the presence of a seasonal reproductive arrest which helps the fly survive the first two-thirds of the dry season, when ripe fruits are scarce, followed by a rapid increase in breeding at the end of the dry season as humidity and the availability of ripe fruit increases. This seasonal phenology continues to be expressed in human-modified landscapes and, while suppressed, it also partially expresses in long-term cultures. We subsequently demonstrate that B. dorsalis, across both its endemic and invasive ranges, shows a very similar seasonality although reversed in the northern hemisphere. While high variability in the timing of B. dorsalis population peaks is exhibited across sites, a four-month period when flies are rare in traps (Dec–Mar) is highly consistent, as is the fact that nearly all sites only have one, generally very sharp, population peak per year. While literature to support or deny a reproductive arrest in B. dorsalis is not available, available data is clear that continuous breeding does not occur in this species and that there are seasonal differences in reproductive investment. Throughout the paper we reinforce the point that our argument for a complex reproductive physiology in Bactrocera is based on inductive reasoning and requires specific, hypothesis-testing experiments to confirm or deny, but we do believe there is ample evidence to prioritise such research. If it is found that species in the genus undergo a true reproductive diapause then there are very significant implications for within-field management, market access, and biosecurity risk planning which are discussed. Arguably the most important of these is that insects in diapause have greater stress resistance and cold tolerance, which could explain how tropical Bactrocera species have managed to successfully invade cool temperate regions. Full article

(This article belongs to the Special Issue A Commemorative Issue in Appreciation of Professor David L. Denlinger: Great Advances in Insect Physiology)

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