Evolutionary Genetics of Insect Innate Immunity

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (31 January 2021) | Viewed by 22797

Special Issue Editor


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Guest Editor
Department of Biological Sciences, Institute for Biomedical Sciences, The George Washington University, Washington, DC 20052, USA
Interests: infection; immunity; symbiosis; host defense

Special Issue Information

Dear Colleagues,

Innate immunity in insects is constantly evolving to provide efficient protection against assaults by a wide range of microbial pathogens. Previous cutting-edge research using model insects together with genetic and genomic tools has led to the identification and characterization of distinct signaling pathways which are activated in response to microbial infections. These findings have led to a better understanding of the nature and regulation of insect innate immune processes that participate in the elimination of pathogens or the suppression of their virulence factors which are designed to evade immune surveillance. In turn, this crucial information has not only progressed the research field of insect innate immunity, but it has also rekindled interest in the innate immune system of mammals. The goal of the relevant scientific community is now to continue filling existing gaps in our knowledge about how microbial infections are sensed, how their presence is communicated both within and among cells and tissues of the insect host, and how they can be efficiently eradicated. This Special Issue in Genes on “Evolutionary Genetics of Insect Innate Immunity” will provide an excellent venue to report recent advances in this topic by publishing high-quality research articles and comprehensive reviews on current and future challenges.

Prof. Dr. Ioannis Eleftherianos
Guest Editor

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Keywords

  • Insect innate immunity
  • Immune recognition and responses
  • Insect antipathogen defense
  • Evolution and genetics of immunity
  • Physiopathology and insect immunity

Published Papers (7 papers)

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Editorial

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2 pages, 140 KiB  
Editorial
Editorial: “Evolutionary Genetics of Insect Innate Immunity”
by Ioannis Eleftherianos
Genes 2021, 12(5), 725; https://doi.org/10.3390/genes12050725 - 13 May 2021
Viewed by 1745
Abstract
The insect innate immune system is under strong selection pressure to evolve resistance to pathogenic infections [...] Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)

Research

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17 pages, 5306 KiB  
Article
A Population Genomic Investigation of Immune Cell Diversity and Phagocytic Capacity in a Butterfly
by Naomi L. P. Keehnen, Lisa Fors, Peter Järver, Anna-Lena Spetz, Sören Nylin, Ulrich Theopold and Christopher W. Wheat
Genes 2021, 12(2), 279; https://doi.org/10.3390/genes12020279 - 16 Feb 2021
Cited by 5 | Viewed by 2007
Abstract
Insects rely on their innate immune system to successfully mediate complex interactions with their internal microbiota, as well as the microbes present in the environment. Given the variation in microbes across habitats, the challenges to respond to them are likely to result in [...] Read more.
Insects rely on their innate immune system to successfully mediate complex interactions with their internal microbiota, as well as the microbes present in the environment. Given the variation in microbes across habitats, the challenges to respond to them are likely to result in local adaptations in the immune system. Here we focus upon phagocytosis, a mechanism by which pathogens and foreign particles are engulfed in order to be contained, killed, and processed. We investigated the phenotypic and genetic variation related to phagocytosis in two allopatric populations of the butterfly Pieris napi. Populations were found to differ in their hemocyte composition and overall phagocytic capability, driven by the increased phagocytic propensity of each cell type. Yet, genes annotated to phagocytosis showed no large genomic signal of divergence. However, a gene set enrichment analysis on significantly divergent genes identified loci involved in glutamine metabolism, which recently have been linked to immune cell differentiation in mammals. Together these results suggest that heritable variation in phagocytic capacity arises via a quantitative trait architecture with variation in genes affecting the activation and/or differentiation of phagocytic cells, suggesting them as potential candidate genes underlying these phenotypic differences. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)
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17 pages, 2947 KiB  
Article
Overexpression of Activated AMPK in the Anopheles stephensi Midgut Impacts Mosquito Metabolism, Reproduction and Plasmodium Resistance
by Chioma Oringanje, Lillian R. Delacruz, Yunan Han, Shirley Luckhart and Michael A. Riehle
Genes 2021, 12(1), 119; https://doi.org/10.3390/genes12010119 - 19 Jan 2021
Cited by 8 | Viewed by 3588
Abstract
Mitochondrial integrity and homeostasis in the midgut are key factors controlling mosquito fitness and anti-pathogen resistance. Targeting genes that regulate mitochondrial dynamics represents a potential strategy for limiting mosquito-borne diseases. AMP-activated protein kinase (AMPK) is a key cellular energy sensor found in nearly [...] Read more.
Mitochondrial integrity and homeostasis in the midgut are key factors controlling mosquito fitness and anti-pathogen resistance. Targeting genes that regulate mitochondrial dynamics represents a potential strategy for limiting mosquito-borne diseases. AMP-activated protein kinase (AMPK) is a key cellular energy sensor found in nearly all eukaryotic cells. When activated, AMPK inhibits anabolic pathways that consume ATP and activates catabolic processes that synthesize ATP. In this study, we overexpressed a truncated and constitutively active α-subunit of AMPK under the control of the midgut-specific carboxypeptidase promotor in the midgut of female Anopheles stephensi. As expected, AMPK overexpression in homozygous transgenic mosquitoes was associated with changes in nutrient storage and metabolism, decreasing glycogen levels at 24 h post-blood feeding when transgene expression was maximal, and concurrently increasing circulating trehalose at the same time point. When transgenic lines were challenged with Plasmodium falciparum, we observed a significant decrease in the prevalence and intensity of infection relative to wild type controls. Surprisingly, we did not observe a significant difference in the survival of adult mosquitoes fed either sugar only or both sugar and bloodmeals throughout adult life. This may be due to the limited period that the transgene was activated before homeostasis was restored. However, we did observe a significant decrease in egg production, suggesting that manipulation of AMPK activity in the mosquito midgut resulted in the re-allocation of resources away from egg production. In summary, this work identifies midgut AMPK activity as an important regulator of metabolism, reproduction, and innate immunity in An. stephensi, a highly invasive and important malaria vector species. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)
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14 pages, 2285 KiB  
Article
Aquatic Exposure to Abscisic Acid Transstadially Enhances Anopheles stephensi Resistance to Malaria Parasite Infection
by Dean M. Taylor, Reagan S. Haney and Shirley Luckhart
Genes 2020, 11(12), 1393; https://doi.org/10.3390/genes11121393 - 24 Nov 2020
Cited by 1 | Viewed by 2253
Abstract
The ancient stress signaling molecule abscisic acid (ABA) is ubiquitous in animals and plants but is perhaps most well-known from its early discovery as a plant hormone. ABA can be released into water by plants and is found in nectar, but is also [...] Read more.
The ancient stress signaling molecule abscisic acid (ABA) is ubiquitous in animals and plants but is perhaps most well-known from its early discovery as a plant hormone. ABA can be released into water by plants and is found in nectar, but is also present in mammalian blood, three key contexts for mosquito biology. We previously established that addition of ABA to Anopheles stephensi larval rearing water altered immature development and life history traits of females derived from treated larvae, while addition of ABA to an infected bloodmeal increased resistance of adult female A. stephensi to human malaria parasite infection. Here we sought to determine whether larval treatment with ABA could similarly impact resistance to parasite infection in females derived from treated larvae and, if so, whether resistance could be extended to another parasite species. We examined nutrient levels and gene expression to demonstrate that ABA can transstadially alter resistance to a rodent malaria parasite with hallmarks of previously observed mechanisms of resistance following provision of ABA in blood to A. stephensi. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)
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Review

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21 pages, 1372 KiB  
Review
Insect Behavioral Change and the Potential Contributions of Neuroinflammation—A Call for Future Research
by Colleen A. Mangold and David P. Hughes
Genes 2021, 12(4), 465; https://doi.org/10.3390/genes12040465 - 24 Mar 2021
Cited by 8 | Viewed by 5088
Abstract
Many organisms are able to elicit behavioral change in other organisms. Examples include different microbes (e.g., viruses and fungi), parasites (e.g., hairworms and trematodes), and parasitoid wasps. In most cases, the mechanisms underlying host behavioral change remain relatively unclear. There is a growing [...] Read more.
Many organisms are able to elicit behavioral change in other organisms. Examples include different microbes (e.g., viruses and fungi), parasites (e.g., hairworms and trematodes), and parasitoid wasps. In most cases, the mechanisms underlying host behavioral change remain relatively unclear. There is a growing body of literature linking alterations in immune signaling with neuron health, communication, and function; however, there is a paucity of data detailing the effects of altered neuroimmune signaling on insect neuron function and how glial cells may contribute toward neuron dysregulation. It is important to consider the potential impacts of altered neuroimmune communication on host behavior and reflect on its potential role as an important tool in the “neuro-engineer” toolkit. In this review, we examine what is known about the relationships between the insect immune and nervous systems. We highlight organisms that are able to influence insect behavior and discuss possible mechanisms of behavioral manipulation, including potentially dysregulated neuroimmune communication. We close by identifying opportunities for integrating research in insect innate immunity, glial cell physiology, and neurobiology in the investigation of behavioral manipulation. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)
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15 pages, 961 KiB  
Review
Eicosanoid Signaling in Insect Immunology: New Genes and Unresolved Issues
by Yonggyun Kim and David Stanley
Genes 2021, 12(2), 211; https://doi.org/10.3390/genes12020211 - 1 Feb 2021
Cited by 44 | Viewed by 4083
Abstract
This paper is focused on eicosanoid signaling in insect immunology. We begin with eicosanoid biosynthesis through the actions of phospholipase A2, responsible for hydrolyzing the C18 polyunsaturated fatty acid, linoleic acid (18:2n-6), from cellular phospholipids, which is subsequently converted into arachidonic [...] Read more.
This paper is focused on eicosanoid signaling in insect immunology. We begin with eicosanoid biosynthesis through the actions of phospholipase A2, responsible for hydrolyzing the C18 polyunsaturated fatty acid, linoleic acid (18:2n-6), from cellular phospholipids, which is subsequently converted into arachidonic acid (AA; 20:4n-6) via elongases and desaturases. The synthesized AA is then oxygenated into one of three groups of eicosanoids, prostaglandins (PGs), epoxyeicosatrienoic acids (EETs) and lipoxygenase products. We mark the distinction between mammalian cyclooxygenases and insect peroxynectins, both of which convert AA into PGs. One PG, PGI2 (also called prostacyclin), is newly discovered in insects, as a negative regulator of immune reactions and a positive signal in juvenile development. Two new elements of insect PG biology are a PG dehydrogenase and a PG reductase, both of which enact necessary PG catabolism. EETs, which are produced from AA via cytochrome P450s, also act in immune signaling, acting as pro-inflammatory signals. Eicosanoids signal a wide range of cellular immune reactions to infections, invasions and wounding, including nodulation, cell spreading, hemocyte migration and releasing prophenoloxidase from oenocytoids, a class of lepidopteran hemocytes. We briefly review the relatively scant knowledge on insect PG receptors and note PGs also act in gut immunity and in humoral immunity. Detailed new information on PG actions in mosquito immunity against the malarial agent, Plasmodium berghei, has recently emerged and we treat this exciting new work. The new findings on eicosanoid actions in insect immunity have emerged from a very broad range of research at the genetic, cellular and organismal levels, all taking place at the international level. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)
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11 pages, 866 KiB  
Review
Transcriptomic Insights into the Insect Immune Response to Nematode Infection
by Ioannis Eleftherianos and Christa Heryanto
Genes 2021, 12(2), 202; https://doi.org/10.3390/genes12020202 - 30 Jan 2021
Cited by 10 | Viewed by 3000
Abstract
Insects in nature interact with a wide variety of microbial enemies including nematodes. These include entomopathogenic nematodes that contain mutualistic bacteria and together are able to infect a broad range of insects in order to complete their life cycle and multiply, filarial nematodes [...] Read more.
Insects in nature interact with a wide variety of microbial enemies including nematodes. These include entomopathogenic nematodes that contain mutualistic bacteria and together are able to infect a broad range of insects in order to complete their life cycle and multiply, filarial nematodes which are vectored by mosquitoes, and other parasitic nematodes. Entomopathogenic nematodes are commonly used in biological control practices and they form excellent research tools for understanding the genetic and functional bases of nematode pathogenicity and insect anti-nematode immunity. In addition, clarifying the mechanism of transmission of filarial nematodes by mosquitoes is critical for devising strategies to reduce disease transmission in humans. In all cases and in order to achieve these goals, it is vital to determine the number and type of insect host genes which are differentially regulated during infection and encode factors with anti-nematode properties. In this respect, the use of transcriptomic approaches has proven a key step for the identification of insect molecules with anti-nematode activity. Here, we review the progress in the field of transcriptomics that deals with the insect response to nematode infection. This information is important because it will expose conserved pathways of anti-nematode immunity in humans. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Insect Innate Immunity)
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