Current Research in Insect Science最新文献

{"title":"Unparalleled mitochondrial heteroplasmy and Wolbachia co-infection in the non-model bee, Amphylaeus morosus","authors":"Olivia K. Davies ,&nbsp;James B. Dorey ,&nbsp;Mark I. Stevens ,&nbsp;Michael G. Gardner ,&nbsp;Tessa M. Bradford ,&nbsp;Michael P. Schwarz","doi":"10.1016/j.cris.2022.100036","DOIUrl":"10.1016/j.cris.2022.100036","url":null,"abstract":"<div><p>Mitochondrial heteroplasmy is the occurrence of more than one type of mitochondrial DNA within a single individual. Although generally reported to occur in a small subset of individuals within a species, there are some instances of widespread heteroplasmy across entire populations. <em>Amphylaeus morosus</em> is an Australian native bee species in the diverse and cosmopolitan bee family Colletidae. This species has an extensive geographical range along the eastern Australian coast, from southern Queensland to western Victoria, covering approximately 2,000 km. Seventy individuals were collected from five localities across this geographical range and sequenced using Sanger sequencing for the mitochondrial cytochrome c oxidase subunit I (COI) gene. These data indicate that every individual had the same consistent heteroplasmic sites but no other nucleotide variation, suggesting two conserved and widespread heteroplasmic mitogenomes. Ion Torrent shotgun sequencing revealed that heteroplasmy occurred across multiple mitochondrial protein-coding genes and is unlikely explained by transposition of mitochondrial genes into the nuclear genome (NUMTs). DNA sequence data also demonstrated a consistent co-infection of <em>Wolbachia</em> across the <em>A. morosus</em> distribution with every individual infected with both bacterial strains. Our data are consistent with the presence of two mitogenomes within all individuals examined in this species and suggest a major divergence from standard patterns of mitochondrial inheritance. Because the host's mitogenome and the <em>Wolbachia</em> genome are genetically linked through maternal inheritance, we propose three possible hypotheses that could explain maintenance of the widespread and conserved co-occurring bacterial and mitochondrial genomes in this species.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100036"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387454/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40634791","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Investment in adult reproductive tissues is affected by larval growth conditions but not by evolution under poor larval growth conditions in Drosophila melanogaster","authors":"Rohit Kapila,&nbsp;Soumyadip Poddar,&nbsp;Neeraj Meena,&nbsp;Nagaraj Guru Prasad","doi":"10.1016/j.cris.2021.100027","DOIUrl":"10.1016/j.cris.2021.100027","url":null,"abstract":"<div><p>In many insects, the larval environment is confined to the egg-laying site, which often leads to crowded larval conditions, exposing the developing larvae to poor resource availability and toxic metabolic wastes. Larval crowding imposes two opposing selection pressures. On one hand, due to poor nutritional resources during developmental stages, adults from the crowded larval environment have reduced investment in reproductive tissues. On the other hand, a crowded larval environment acts as a cue for future reproductive competition inducing increased investment in reproductive tissues. Both these selection pressures are likely affected by the level of crowding. The evolutionary consequence of adaptation to larval crowding environment on adult reproductive investment is bound to be a result of the interaction of these two opposing forces. In this study, we used experimentally evolved populations of <em>Drosophila melanogaster</em> adapted to larval crowding to investigate the effect of adaptation to larval crowding on investment in reproductive organs (testes and accessory glands) of males. Our results show that there is a strong effect of larval developmental environment on absolute sizes of testes and accessory glands. However, there was no effect of the developmental environment when testis size was scaled by body size. We also found that flies from crowded cultures had smaller accessory gland sizes relative to body size. Moreover, the sizes of the reproductive organs were not affected by the selection histories of the populations. This study highlights that adaptation to two extremely different developmental environments does not affect the patterns of reproductive investment. We discuss the possibility that differential investment in reproductive tissues could be influenced by the mating dynamics and/or investment in larval survival traits, rather than just the developmental environment of the populations.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100027"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/a0/61/main.PMC9387493.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40439526","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Identification and profiling of stable microRNAs in hemolymph of young and old Locusta migratoria fifth instars","authors":"Stijn Van den Brande ,&nbsp;Marijke Gijbels ,&nbsp;Niels Wynant ,&nbsp;Paulien Peeters ,&nbsp;Yannick Gansemans ,&nbsp;Filip Van Nieuwerburgh ,&nbsp;Dulce Santos ,&nbsp;Jozef Vanden Broeck","doi":"10.1016/j.cris.2022.100041","DOIUrl":"10.1016/j.cris.2022.100041","url":null,"abstract":"<div><p>Since the discovery of the first microRNA (miRNA) in the nematode <em>Caenorhabditis elegans</em>, numerous novel miRNAs have been identified which can regulate presumably every biological process in a wide range of metazoan species. In accordance, several insect miRNAs have been identified and functionally characterized. While regulatory RNA pathways are traditionally described at an intracellular level, studies reporting on the presence and potential role of extracellular (small) sRNAs have been emerging in the last decade, mainly in mammalian systems. Interestingly, evidence in several species indicates the functional transfer of extracellular RNAs between donor and recipient cells, illustrating RNA-based intercellular communication. In insects, however, reports on extracellular small RNAs are emerging but the number of detailed studies is still very limited. Here, we demonstrate the presence of stable sRNAs in the hemolymph of the migratory locust, <em>Locusta migratoria</em>. Moreover, the levels of several extracellular miRNAs (ex-miRNAs) present in locust hemolymph differed significantly between young and old fifth nymphal instars. In addition, we performed a ‘proof of principle’ experiment which suggested that extracellularly delivered miRNA molecules are capable of affecting the locusts’ development.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100041"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/de/42/main.PMC9387440.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40634790","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Half a century of thermal tolerance studies in springtails (Collembola): A review of metrics, spatial and temporal trends","authors":"Pablo Escribano-Álvarez ,&nbsp;Luis R. Pertierra ,&nbsp;Brezo Martínez ,&nbsp;Steven L. Chown ,&nbsp;Miguel Á. Olalla-Tárraga","doi":"10.1016/j.cris.2021.100023","DOIUrl":"10.1016/j.cris.2021.100023","url":null,"abstract":"<div><p>Global changes in soil surface temperatures are altering the abundances and distribution ranges of invertebrate species worldwide, including effects on soil microarthropods such as springtails (Collembola), which are vital for maintaining soil health and providing ecosystem services. Studies of thermal tolerance limits in soil invertebrates have the potential to provide information on demographic responses to climate change and guide assessments of possible impacts on the structure and functioning of ecosystems. Here, we review the state of knowledge of thermal tolerance limits in Collembola. Thermal tolerance metrics have diversified over time, which should be taken into account when conducting large-scale comparative studies. A temporal trend shows that the estimation of ‘Critical Thermal Limits’ (CTL) is becoming more common than investigations of ‘Supercooling Point’ (SCP), despite the latter being the most widely used metric. Indeed, most studies (66%) in Collembola have focused on cold tolerance; fewer have assessed heat tolerance. The majority of thermal tolerance data are from temperate and polar regions, with fewer assessments from tropical and subtropical latitudes. While the hemiedaphic life form represents the majority of records at low latitudes, euedaphic and epedaphic groups remain largely unsampled in these regions compared to the situation in temperate and high latitude regions, where sampling records show a more balanced distribution among the different life forms. Most CTL data are obtained during the warmest period of the year, whereas SCP and ‘Lethal Temperature’ (LT) show more variation in terms of the season when the data were collected. We conclude that more attention should be given to understudied zoogeographical regions across the tropics, as well as certain less-studied clades such as the family Neanuridae, to identify the role of thermal tolerance limits in the redistribution of species under changing climates.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100023"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/90/42/main.PMC9387465.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40636753","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"An evaluation of common methods for comparing the scaling of vertical force production in flying insects","authors":"Nicholas P. Burnett,&nbsp;Emily L. Keliher,&nbsp;Stacey A. Combes","doi":"10.1016/j.cris.2022.100042","DOIUrl":"10.1016/j.cris.2022.100042","url":null,"abstract":"<div><p>Maximum vertical force production (F_vert) is an integral measure of flight performance that generally scales with size. Numerous methods of measuring F_vert and body size are accessible to entomologists, but we do not know whether method selection affects inter- and intraspecific comparisons of F_vert-size scaling. We compared two common techniques for measuring F_vert in bumblebees (<em>Bombus impatiens</em>) and mason bees (<em>Osmia lignaria</em>), and examined F_vert scaling using five size metrics. F_vert results were similar with incremental or asymptotic load-lifting, but scaling analyses were sensitive to the size metric used. Analyses based on some size metrics indicated similar scaling exponents and coefficients between species, whereas other metrics indicated coefficients that differed by up to 18%. Furthermore, F_vert showed isometry with body lengths and fed and starved masses, but negative allometry with dry mass. We conclude that F_vert can be measured using either incremental or asymptotic loading but choosing a size metric for scaling studies requires careful consideration.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100042"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387496/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40634794","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Are Signals of Local Environmental Adaptation Diluted by Laboratory Culture?","authors":"Elizabeth J. Huisamen,&nbsp;Minette Karsten,&nbsp;John S. Terblanche","doi":"10.1016/j.cris.2022.100048","DOIUrl":"10.1016/j.cris.2022.100048","url":null,"abstract":"<div><p>Insects have the ability to readily adapt to changes in environmental conditions, however the strength of local environmental adaptation signals under divergent conditions and the occurrence of trait inertia after relaxation of selection, remains poorly understood, especially for traits of climate stress resistance (CSR) and their phenotypic plasticity. The strength of environmental adaptation signals depend on several selection pressures present in the local environment, while trait inertia often occurs when there is a weakening or removal of a source of selection. Here, using <em>Drosophila melanogaster</em>, we asked whether signals of adaptation in CSR traits (critical thermal limits, heat and chill survival and, desiccation and starvation resistance) persist after exposure to laboratory culture for different durations (two vs. ten generations) across four climatically distinct populations. We show that culture duration has large effects on CSR traits and can both amplify or dilute signals of local adaptation. Effects were however dependent upon interactions between the source population, acclimation (adult acclimation at either 18 °C, 23 °C or 28 °C) conditions and the sex of the flies. Trait plasticity is markedly affected by the interaction between the source population, the specific acclimation conditions employed, and the duration in the laboratory. Therefore, a complex matrix of dynamic CSR trait responses is shown in space and time. Given these strong interaction effects, ‘snapshot’ estimates of environmental adaptation can result in misleading conclusions about the fitness consequences of climate variability.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100048"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/fd/31/main.PMC9846451.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10581053","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Life history strategy dictates thermal preferences across the diel cycle and in response to starvation in variable field crickets, Gryllus lineaticeps","authors":"Lisa A. Treidel ,&nbsp;Christopher Huebner ,&nbsp;Kevin T. Roberts ,&nbsp;Caroline M. Williams","doi":"10.1016/j.cris.2022.100038","DOIUrl":"https://doi.org/10.1016/j.cris.2022.100038","url":null,"abstract":"<div><p>Insects behaviorally thermoregulate across the diel cycle, and their preferred microhabitats change based on current resources available and the thermal performance optima of traits. Specific combinations of traits being prioritized are set by life history strategies, making life history an important intrinsic determinant of thermal preferences. However, we do not know how life history strategies shape plasticity of behavioral thermoregulation, limiting our ability to predict responses to environmental variability. We compared female variable field crickets (<em>Gryllus lineaticeps</em>) that are flight-capable (long-winged) and flightless (short-winged) to test the hypothesis that life history strategy determines plasticity of thermal preferences across the diel cycle and following starvation. Thermal preferences were elevated during the nocturnal activity period, and long-winged crickets preferred warmer temperatures compared to short-winged crickets across the diel cycle when fully fed. However, thermal preferences of starved crickets were reduced compared to fed crickets. The reduction in thermal preferences was greater in long-winged crickets, resulting in similar thermal preferences between starved long- and short-winged individuals and reflecting a more plastic response. Thus, life history does determine plasticity in thermoregulatory behaviors following resource limitations and effects of life history on thermal preferences are context dependent.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100038"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S2666515822000105/pdfft?md5=fac96cbe2ca4d280a9429ee893c5ffbf&pid=1-s2.0-S2666515822000105-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"91640335","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The P450 genes of the cat flea, Ctenocephalides felis: a CYPome in flux","authors":"René Feyereisen","doi":"10.1016/j.cris.2022.100032","DOIUrl":"10.1016/j.cris.2022.100032","url":null,"abstract":"<div><p>The genome of the cat flea, an ectoparasite of major veterinary importance and the first representative of the Siphonaptera, is highly unusual among arthropod genomes in showing a variable size and a very large number of gene duplications (Driscoll et al., 2020). The cat flea is the target of several classes of insecticides, justifying the description of its CYPome, the complement of P450s that are an important family of detoxification enzymes. 103 P450 genes were annotated on the nine chromosomes, with an additional 12 genes on small, extrachromosomal scaffolds. Only 34 genes were found as single sequences, with 47 duplicated two to four-fold. This included duplication of genes that are mostly single copy P450 genes in other arthropods. Large clusters of mitochondrial clan P450s were observed, resulting in a CYP12 bloom within this clan to 34 genes, a number of mitochondrial P450s not seen in other animals so far. The variable geometry of the cat flea CYPome poses a challenge to the study of P450 function in this species, and raises the question of the underlying causes of single copy control versus multicopy licence of P450 genes.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100032"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/0a/43/main.PMC9387431.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40439523","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Mosquito-larvicidal Binary (BinA/B) proteins for mosquito control programs —advancements, challenges, and possibilities","authors":"Mahima Sharma ,&nbsp;Vinay Kumar","doi":"10.1016/j.cris.2021.100028","DOIUrl":"10.1016/j.cris.2021.100028","url":null,"abstract":"<div><p>The increasing global burden of mosquito-borne diseases require targeted, environmentally friendly, and sustainable approaches for effective vector control without endangering the non-target beneficial insect population. Biological interventions such as biopesticides, Wolbachia-mediated biological controls, or sterile insect techniques are used worldwide. Here we review Binary or BinAB toxin—the mosquito-larvicidal component of WHO-recognized <em>Lysinibacillus sphaericus</em> bacterium employed in mosquito control programs. Binary (BinAB) toxin is primarily responsible for the larvicidal effect of the bacterium. BinAB is a single-receptor-specific toxin and is effective against larvae of Culex and Anopheles, but not against <em>Aedes aegypti</em>. The receptor in Culex, the Cqm1 protein, has been extensively studied. It is a GPI-anchored amylomaltase and is located apically in the lipid rafts of the larval-midgut epithelium. The interaction of the toxin components with the receptor is crucial for the mosquito larvicidal activity of the BinAB toxin. Here we extend support for the pore formation model of BinAB toxin internalization and the role of toxin-glycan interactions in the endoplasmic reticulum in mediating larval death. BinAB is phylogenetically safe for humans, as Cqm1-like protein is not expected in the human proteome. This review aims to initiate targeted R&amp;D efforts, such as applying fusion technologies (chimera of BinA, chemical modification of BinA), for efficient mosquito control interventions. In addition, the review also examines other areas such as bioremediation and cancer therapeutics, in which <em>L. sphaericus</em> is proving useful and showing potential for further development.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100028"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9387486/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40636754","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Ecdysteroid kinase-like (EcKL) paralogs confer developmental tolerance to caffeine in Drosophila melanogaster","authors":"Jack L. Scanlan ,&nbsp;Paul Battlay ,&nbsp;Charles Robin","doi":"10.1016/j.cris.2022.100030","DOIUrl":"10.1016/j.cris.2022.100030","url":null,"abstract":"<div><p>A unique aspect of metabolic detoxification in insects compared to other animals is the presence of xenobiotic phosphorylation, about which little is currently understood. Our previous work raised the hypothesis that members of the taxonomically restricted ecdysteroid kinase-like (EcKL) gene family encode the enzymes responsible for xenobiotic phosphorylation in the model insect <em>Drosophila melanogaster</em> (Diptera: Ephydroidea)—however, candidate detoxification genes identified in the EcKL family have yet to be functionally validated. Here, we test the hypothesis that EcKL genes in the rapidly evolving Dro5 clade are involved in the detoxification of plant and fungal toxins in <em>D. melanogaster</em>. The mining and reanalysis of existing data indicated multiple Dro5 genes are transcriptionally induced by the plant alkaloid caffeine and that adult caffeine susceptibility is associated with a novel naturally occurring indel in <em>CG31370</em> (Dro5-8) in the Drosophila Genetic Reference Panel (DGRP). CRISPR-Cas9 mutagenesis of five Dro5 EcKLs substantially decreased developmental tolerance of caffeine, while individual overexpression of two of these genes—<em>CG31300</em> (Dro5-1) and <em>CG13659</em> (Dro5-7)—in detoxification-related tissues increased developmental tolerance. In addition, we found Dro5 loss-of-function animals also have decreased developmental tolerance of the fungal secondary metabolite kojic acid. Taken together, this work provides the first compelling functional evidence that EcKLs encode detoxification enzymes and suggests that EcKLs in the Dro5 clade are involved in the metabolism of multiple ecologically relevant toxins in <em>D. melanogaster</em>. We also propose a biochemical hypothesis for EcKL involvement in caffeine detoxification and highlight the many unknown aspects of caffeine metabolism in <em>D. melanogaster</em> and other insects.</p></div>","PeriodicalId":34629,"journal":{"name":"Current Research in Insect Science","volume":"2 ","pages":"Article 100030"},"PeriodicalIF":0.0,"publicationDate":"2022-01-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://ftp.ncbi.nlm.nih.gov/pub/pmc/oa_pdf/26/44/main.PMC9387500.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"40439525","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}