{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T05:51:04Z","timestamp":1790401864736,"version":"4.1.0"},"reference-count":135,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2025,9,2]],"date-time":"2025-09-02T00:00:00Z","timestamp":1756771200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science Foundation (NSF)","award":["IOS-1936843"],"award-info":[{"award-number":["IOS-1936843"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Insects"],"abstract":"<jats:p>In most mosquito species, reproduction requires mating between the female and the male, followed by the female blood-feeding, completing oogenesis, and laying eggs. Warmer environmental temperature and aging both reduce mosquito fecundity and fertility, and warmer temperature accelerates the aging-dependent decline in reproduction such that reproductive impairment manifests earlier in life. To shed light on how this warming-based acceleration of reproductive senescence occurs, we investigated how temperature (27 \u00b0C, 30 \u00b0C, and 32 \u00b0C) and aging interactively shape female and male reproductive tissue size in the African malaria mosquito, Anopheles gambiae. In blood-fed females, we discovered that warmer temperature accelerates the aging-dependent decrease in the size of the ovaries but not the spermatheca. In males, we discovered that warmer temperature lessens and delays the aging-dependent increase in the size of the male accessory glands but not the testes. Next, we measured the expression of reproductive genes in females and males. In female reproductive tissues, warmer temperature accelerates the aging-dependent decrease in the expression of vitellogenin and the aging-dependent increase in the expression of MISO and HPX15. In male reproductive tissues, warmer temperature accelerates an aging-dependent decrease in the expression of Plugin, TGase3, phLP, and CYP315A1. Altogether, these data shed light on how physical and transcriptional changes underpin the warming-based acceleration of an aging-dependent decline in mosquito fecundity and fertility.<\/jats:p>","DOI":"10.3390\/insects16090921","type":"journal-article","created":{"date-parts":[[2025,9,2]],"date-time":"2025-09-02T16:05:22Z","timestamp":1756829122000},"page":"921","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Warmer Temperature Accelerates the Aging-Dependent Decrease in Female Ovary Size, Delays Male Accessory Gland Development, and Accelerates Aging-Dependent Changes in Reproductive Gene Expression in Anopheles gambiae Mosquitoes"],"prefix":"10.3390","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0009-0007-3329-0955","authenticated-orcid":false,"given":"Lindsay E.","family":"Martin","sequence":"first","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37232, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4671-8766","authenticated-orcid":false,"given":"Tania Y.","family":"Est\u00e9vez-Lao","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37232, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Megan I.","family":"Grant","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37232, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-3456-4284","authenticated-orcid":false,"given":"Norbu Y.","family":"Shastri","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37232, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3178-0201","authenticated-orcid":false,"given":"Juli\u00e1n F.","family":"Hillyer","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, Vanderbilt University, Nashville, TN 37232, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2025,9,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1016\/j.ibmb.2005.02.013","article-title":"Nutritional regulation of vitellogenesis in mosquitoes: Implications for anautogeny","volume":"35","author":"Attardo","year":"2005","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1590\/S0074-02761987000700019","article-title":"The cell biology of mosquito vitellogenesis","volume":"82","author":"Raikhel","year":"1987","journal-title":"Mem\u00f3rias Inst. Oswaldo Cruz"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Wu, Z., Yang, L., He, Q., and Zhou, S. (2021). Regulatory mechanisms of vitellogenesis in insects. Front. Cell Dev. Biol., 8.","DOI":"10.3389\/fcell.2020.593613"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1365-3032.1984.tb00675.x","article-title":"Ovarian development in mosquitoes: Stages of growth and arrest, and follicular resorption","volume":"9","author":"Clements","year":"1984","journal-title":"Physiol. Entomol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/bs.aiip.2016.05.004","article-title":"Regulation of reproductive processes in female mosquitoes","volume":"Volume 51","author":"Raikhel","year":"2016","journal-title":"Advances in Insect Physiology"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1016\/j.jinsphys.2012.05.005","article-title":"The fate of follicles after a blood meal is dependent on previtellogenic nutrition and juvenile hormone in Aedes aegypti","volume":"58","author":"Clifton","year":"2012","journal-title":"J. Insect Physiol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Hern\u00e1ndez-Mart\u00ednez, S., Cardoso-Jaime, V., Nouzova, M., Michalkova, V., Ramirez, C.E., Fernandez-Lima, F., and Noriega, F.G. (2019). Juvenile hormone controls ovarian development in female Anopheles albimanus mosquitoes. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-38631-6"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s13071-020-04558-5","article-title":"20-Hydroxyecdysone (20E) signaling as a promising target for the chemical control of malaria vectors","volume":"14","author":"Ekoka","year":"2021","journal-title":"Parasites Vectors"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Hansen, I.A., Attardo, G.M., Rodriguez, S.D., and Drake, L.L. (2014). Four-way regulation of mosquito yolk protein precursor genes by juvenile hormone-, ecdysone-, nutrient-, and insulin-like peptide signaling pathways. Front. Physiol., 5.","DOI":"10.3389\/fphys.2014.00103"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"867","DOI":"10.1016\/0022-1910(86)90102-2","article-title":"Juvenile hormone and juvenile hormone esterase in adult females of the mosquito Aedes aegypti","volume":"32","author":"Shapiro","year":"1986","journal-title":"J. Insect Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/0016-6480(82)90199-X","article-title":"Juvenile hormone and the development of ovarian responsiveness to a brain hormone in the mosquito, Aedes aegypti","volume":"46","author":"Shapiro","year":"1982","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"E2173","DOI":"10.1073\/pnas.1305293110","article-title":"Juvenile hormone and its receptor, methoprene-tolerant, control the dynamics of mosquito gene expression","volume":"110","author":"Zou","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1002\/(SICI)1520-6327(1997)35:4<491::AID-ARCH10>3.0.CO;2-5","article-title":"Endocrine aspects of mosquito reproduction","volume":"35","author":"Klowden","year":"1997","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"ref_14","first-page":"433","article-title":"Hormonal control of reproductive processes","volume":"Volume 3","author":"Raikhel","year":"2005","journal-title":"Reproductive Biology of Invertebrates, Vol. 12, Part B: Progress in Vitellogenesis"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/j.cois.2018.07.010","article-title":"Juvenile hormone signaling in insect oogenesis","volume":"31","author":"Santos","year":"2019","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"De Carvalho, S.S., Rodovalho, C.M., Gaviraghi, A., Mota, M.B.S., Jablonka, W., Rocha-Santos, C., Nunes, R.D., S\u00e1-Guimar\u00e3es, T.D.E., Oliveira, D.S., and Melo, A.C.A. (2021). Aedes aegypti post-emergence transcriptome: Unveiling the molecular basis for the hematophagic and gonotrophic capacitation. PLoS Neglected Trop. Dis., 15.","DOI":"10.1371\/journal.pntd.0008915"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/bs.aiip.2016.04.005","article-title":"The role of juvenile hormone in mosquito development and reproduction","volume":"Volume 51","author":"Raikhel","year":"2016","journal-title":"Advances in Insect Physiology"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1016\/j.jinsphys.2006.08.009","article-title":"Role of juvenile hormone and allatotropin on nutrient allocation, ovarian development and survivorship in mosquitoes","volume":"53","author":"Mayoral","year":"2007","journal-title":"J. Insect Physiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"2685","DOI":"10.1242\/jeb.01093","article-title":"Reduced juvenile hormone synthesis in mosquitoes with low teneral reserves reduces ovarian previtellogenic development in Aedes aegypti","volume":"207","author":"Caroci","year":"2004","journal-title":"J. Exp. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"19631","DOI":"10.1073\/pnas.0809264105","article-title":"Anopheles gambiae males produce and transfer the vitellogenic steroid hormone 20-hydroxyecdysone to females during mating","volume":"105","author":"Pondeville","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1179\/2047773212Y.0000000016","article-title":"Function and composition of male accessory gland secretions in Anopheles gambiae: A comparison with other insect vectors of infectious diseases","volume":"106","author":"Baldini","year":"2012","journal-title":"Pathog. Glob. Health"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Baldini, F., Gabrieli, P., South, A., Valim, C., Mancini, F., and Catteruccia, F. (2013). The interaction between a sexually transferred steroid hormone and a female protein regulates oogenesis in the malaria mosquito Anopheles gambiae. PLoS Biol., 11.","DOI":"10.1371\/journal.pbio.1001695"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"16353","DOI":"10.1073\/pnas.1410488111","article-title":"Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae","volume":"111","author":"Gabrieli","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Pondeville, E., Puchot, N., Lang, M., Cherrier, F., Schaffner, F., Dauphin-Villemant, C., Bischoff, E., and Bourgouin, C. (2019). Evolution of sexually-transferred steroids and mating-induced phenotypes in Anopheles mosquitoes. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-41094-4"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"S6","DOI":"10.1074\/mcp.RA118.001067","article-title":"Proteins, transcripts, and genetic architecture of seminal fluid and sperm in the mosquito Aedes aegypti","volume":"18","author":"Degner","year":"2019","journal-title":"Mol. Cell. Proteom."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1038\/s41586-022-04908-6","article-title":"A male steroid controls female sexual behaviour in the malaria mosquito","volume":"608","author":"Peng","year":"2022","journal-title":"Nature"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1146\/annurev.en.37.010192.001245","article-title":"Accumulation of yolk proteins in insect oocytes","volume":"37","author":"Raikhel","year":"1992","journal-title":"Annu. Rev. Entomol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1242\/jcs.s2-65.259.395","article-title":"The development of the ovary and ovarian egg of a mosquito, Anopheles maculipennis, Meig","volume":"S2-65","author":"Nicholson","year":"1921","journal-title":"J. Cell Sci."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Airs, P.M., Nazarchyk, M.J., Tucker, B.J., and Bartholomay, L.C. (2023). Characterizing oogenesis and programmed cell death in the eastern tree hole mosquito Aedes (Protomacleaya) triseriatus. Front. Insect Sci., 2.","DOI":"10.3389\/finsc.2022.1073308"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1080\/00034983.1963.11686197","article-title":"Observations on nulliparous and parous rates in some common East African mosquitoes","volume":"57","author":"Gillies","year":"1963","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Martin, L.E., Est\u00e9vez-Lao, T.Y., McCabe, T.C., and Hillyer, J.F. (2025). Warmer temperature accelerates reproductive senescence in mosquitoes. Front. Physiol., 16.","DOI":"10.3389\/fphys.2025.1610310"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1016\/S0925-5214(00)00169-1","article-title":"Physiological responses of insects to heat","volume":"21","author":"Neven","year":"2000","journal-title":"Postharvest Biol. Technol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1086\/648567","article-title":"Thermodynamic effects on organismal performance: Is hotter better?","volume":"83","author":"Angilletta","year":"2010","journal-title":"Physiol. Biochem. Zool."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Martin, L.E., Ruiz, M., and Hillyer, J.F. (2024). Senescence of humoral antimicrobial immunity occurs in infected mosquitoes when the temperature is higher. J. Exp. Biol., 227.","DOI":"10.1242\/jeb.248149"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"104525","DOI":"10.1016\/j.jinsphys.2023.104525","article-title":"Temperature and age, individually and interactively, shape the size, weight, and body composition of adult female mosquitoes","volume":"148","author":"Barr","year":"2023","journal-title":"J. Insect Physiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1186\/s12979-024-00465-w","article-title":"Warmer environmental temperature accelerates aging in mosquitoes, decreasing longevity and worsening infection outcomes","volume":"21","author":"Barr","year":"2024","journal-title":"Immun. Ageing"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1093\/jme\/tjac046","article-title":"Effects of elevated temperatures on the growth and development of adult Anopheles gambiae (s.l.) (Diptera: Culicidae) mosquitoes","volume":"59","author":"Agyekum","year":"2022","journal-title":"J. Med. Entomol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Martin, L.E., and Hillyer, J.F. (2024). Higher temperature accelerates the aging-dependent weakening of the melanization immune response in mosquitoes. PLoS Pathog., 20.","DOI":"10.1371\/journal.ppat.1011935"},{"key":"ref_39","first-page":"3357","article-title":"Complex effects of temperature on mosquito immune function","volume":"279","author":"Murdock","year":"2012","journal-title":"Proc. R. Soc. Lond. B Biol. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1690","DOI":"10.1111\/ele.13335","article-title":"Thermal biology of mosquito-borne disease","volume":"22","author":"Mordecai","year":"2019","journal-title":"Ecol. Lett."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Agyekum, T.P., Botwe, P.K., Arko-Mensah, J., Issah, I., Acquah, A.A., Hogarh, J.N., Dwomoh, D., Robins, T.G., and Fobil, J.N. (2021). A systematic review of the effects of temperature on Anopheles mosquito development and survival: Implications for malaria control in a future warmer climate. Int. J. Environ. Res. Public Health, 18.","DOI":"10.20944\/preprints202105.0054.v1"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Huxley, P.J., Murray, K.A., Pawar, S., and Cator, L.J. (2021). The effect of resource limitation on the temperature dependence of mosquito population fitness. Proc. R. Soc. Lond. B Biol. Sci., 288.","DOI":"10.1098\/rspb.2020.3217"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1603\/ME13003","article-title":"The effect of temperature on life history traits of Culex mosquitoes","volume":"51","author":"Ciota","year":"2014","journal-title":"J. Med. Entomol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13071-019-3391-1","article-title":"The role of temperature in affecting carry-over effects and larval competition in the globally invasive mosquito Aedes albopictus","volume":"12","author":"Ezeakacha","year":"2019","journal-title":"Parasites Vectors"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1590\/S0085-56262010000300021","article-title":"Impact of small variations in temperature and humidity on the reproductive activity and survival of Aedes aegypti (Diptera, Culicidae)","volume":"54","author":"Costa","year":"2010","journal-title":"Rev. Bras. Entomol."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Gandara, A.C.P., and Drummond-Barbosa, D. (2023). Chronic exposure to warm temperature causes low sperm abundance and quality in Drosophila melanogaster. Sci. Rep., 13.","DOI":"10.1038\/s41598-023-39360-7"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"231949","DOI":"10.1098\/rsos.231949","article-title":"Experimental heatwaves reduce the effectiveness of ejaculates at occupying female reproductive tracts in a model insect","volume":"11","author":"Sales","year":"2024","journal-title":"R. Soc. Open Sci."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"4771","DOI":"10.1038\/s41467-018-07273-z","article-title":"Experimental heatwaves compromise sperm function and cause transgenerational damage in a model insect","volume":"9","author":"Sales","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"art170","DOI":"10.1890\/ES15-00094.1","article-title":"Malaria control and senescence: The importance of accounting for the pace and shape of aging in wild mosquitoes","volume":"6","author":"Ryan","year":"2015","journal-title":"Ecosphere"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/1742-4933-10-12","article-title":"Immunosenescence in vertebrates and invertebrates","volume":"10","author":"Pawelec","year":"2013","journal-title":"Immun. Ageing"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1111\/1365-2435.13399","article-title":"Senescence in wild insects: Key questions and challenges","volume":"34","author":"Zajitschek","year":"2020","journal-title":"Funct. Ecol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"111","DOI":"10.4269\/ajtmh.2007.76.111","article-title":"Mosquitoes do senesce: Departure from the paradigm of constant mortality","volume":"76","author":"Styer","year":"2007","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Som\u00e9, B.M., Guissou, E., Da, D.F., Richard, Q., Choisy, M., Yameogo, K.B., Hien, D.F., Yerbanga, R.S., Ouedraogo, G.A., and Dabir\u00e9, K.R. (2024). Mosquito ageing modulates the development, virulence and transmission potential of pathogens. Proc. R. Soc. B Biol. Sci., 291.","DOI":"10.1098\/rspb.2023.2097"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1111\/j.1462-5822.2004.00430.x","article-title":"Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers","volume":"7","author":"Hillyer","year":"2005","journal-title":"Cell. Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"105396","DOI":"10.1016\/j.dci.2025.105396","article-title":"Cellular immune senescence in mosquitoes accelerates when the temperature is warmer","volume":"168","author":"Barr","year":"2025","journal-title":"Dev. Comp. Immunol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1111\/j.1948-7134.2009.00024.x","article-title":"Age modifies the effect of body size on fecundity in Culex quinquefasciatus Say (Diptera: Culicidae)","volume":"34","author":"McCann","year":"2009","journal-title":"J. Vector Ecol."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Petersen, M.T., Silveira, I.D.d., T\u00e1tila-Ferreira, A., David, M.R., Chouin-Carneiro, T., Van den Wouwer, L., Maes, L., and Maciel-de-Freitas, R. (2018). The impact of the age of first blood meal and Zika virus infection on Aedes aegypti egg production and longevity. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0200766"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"104570","DOI":"10.1016\/j.jinsphys.2023.104570","article-title":"The effects of female age on blood-feeding, insemination, sperm storage, and fertility in the dengue vector mosquito Aedes aegypti (Diptera: Culicidae)","volume":"150","author":"Avila","year":"2023","journal-title":"J. Insect Physiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1603\/ME12041","article-title":"Effects of age and size on Anopheles gambiae s.s. male mosquito mating success","volume":"50","author":"Sawadogo","year":"2013","journal-title":"J. Med. Entomol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1093\/jmedent\/44.3.422","article-title":"Age and body size influence male sperm capacity of the Dengue vector Aedes aegypti (Diptera: Culicidae)","volume":"44","author":"Ponlawat","year":"2007","journal-title":"J. Med. Entomol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1111\/j.1570-7458.1994.tb01814.x","article-title":"Age effects on the insemination rate of Anopheles gambiae s.l. in the laboratory","volume":"72","author":"Verhoek","year":"1994","journal-title":"Entomol. Exp. Appl."},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Meuti, M.E., and Short, S.M. (2019). Physiological and environmental factors affecting the composition of the ejaculate in mosquitoes and other insects. Insects, 10.","DOI":"10.3390\/insects10030074"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1111\/1744-7917.12446","article-title":"Male age and strain affect ejaculate quality in the Mexican fruit fly","volume":"25","author":"Abraham","year":"2018","journal-title":"Insect Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"a025593","DOI":"10.1101\/cshperspect.a025593","article-title":"Anopheline reproductive biology: Impacts on vectorial capacity and potential avenues for malaria control","volume":"7","author":"Mitchell","year":"2017","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"e69630","DOI":"10.7554\/eLife.69630","article-title":"How will mosquitoes adapt to climate warming?","volume":"10","author":"Couper","year":"2021","journal-title":"eLife"},{"key":"ref_66","unstructured":"P\u00f6rtner, H.O., Roberts, D.C., Tignor, M., Poloczanska, E.S., Mintenbeck, K., Alegr\u00eda, A., Craig, M., Langsdorf, S., L\u00f6schke, S., and M\u00f6ller, V. (2022). IPCC, 2022: Climate Change 2022: Impacts, Adaptation, and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1186\/s12936-024-04982-3","article-title":"The behaviour of adult Anopheles gambiae, sub-Saharan Africa\u2019s principal malaria vector, and its relevance to malaria control: A review","volume":"23","author":"Takken","year":"2024","journal-title":"Malar. J."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1186\/1475-2875-10-135","article-title":"Laboratory selection for an accelerated mosquito sexual development rate","volume":"10","author":"Oliva","year":"2011","journal-title":"Malar. J."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"S20","DOI":"10.1016\/j.actatropica.2013.07.023","article-title":"Analysis of the genitalia rotation in the male Anopheles funestus (Diptera: Culicidae)","volume":"132","author":"Dahan","year":"2014","journal-title":"Acta Trop."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1093\/aesa\/54.6.896","article-title":"Rotation of male terminalia in Aedes taeniorhynchus (Diptera: Culicidae) as affected by temperature","volume":"54","author":"Provost","year":"1961","journal-title":"Ann. Entomol. Soc. Am."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"S8","DOI":"10.1186\/1475-2875-8-S2-S8","article-title":"Male mating biology","volume":"8","author":"Howell","year":"2009","journal-title":"Malar. J."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v112.i01","article-title":"Parsimoniously fitting large multivariate random effects in glmmTMB","volume":"112","author":"McGillycuddy","year":"2025","journal-title":"J. Stat. Softw."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"378","DOI":"10.32614\/RJ-2017-066","article-title":"glmmTMB balances speed and flexibility among packages forzero-inflated generalized linear mixed modeling","volume":"9","author":"Brooks","year":"2017","journal-title":"R J."},{"key":"ref_74","unstructured":"Hartig, F. (DHARMa: Residual Diagnostics for Hierarchical (Multi-Level\/Mixed) Regression Models, 2024). DHARMa: Residual Diagnostics for Hierarchical (Multi-Level\/Mixed) Regression Models, v0.4.7."},{"key":"ref_75","first-page":"1","article-title":"Beta regression in R","volume":"34","author":"Zeileis","year":"2010","journal-title":"J. Stat. Softw."},{"key":"ref_76","unstructured":"Lenth, R.V. (Emmeans: Estimated Marginal Means, Aka Least-Squares Means, 2022). Emmeans: Estimated Marginal Means, Aka Least-Squares Means, 1.8.3."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_78","unstructured":"Kolde, R. (Pheatmap: Pretty Heatmaps, 2019). Pheatmap: Pretty Heatmaps, v1.0.12."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.zool.2016.12.001","article-title":"The insect spermatheca: An overview","volume":"121","author":"Pascini","year":"2017","journal-title":"Zoology"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"5854","DOI":"10.1073\/pnas.1401715111","article-title":"Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae","volume":"111","author":"Shaw","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Pascini, T.V., Ramalho-Ortig\u00e3o, M., Ribeiro, J.M., Jacobs-Lorena, M., and Martins, G.F. (2020). Transcriptional profiling and physiological roles of Aedes aegypti spermathecal-related genes. BMC Genom., 21.","DOI":"10.1186\/s12864-020-6543-y"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1038\/244103a0","article-title":"Ovarian control of vitellogenin synthesis by the fat body in Aedes aegypti","volume":"244","author":"Hagedorn","year":"1973","journal-title":"Nature"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"e220143","DOI":"10.1590\/0074-02760220143","article-title":"Vitellogenin genes are transcribed in Culex quinquefasciatus ovary","volume":"118","author":"Moura","year":"2023","journal-title":"Mem\u00f3rias Inst. Oswaldo Cruz"},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Itoe, M.A., Shaw, W.R., Stryapunina, I., Vidoudez, C., Peng, D., Du, E.W., Rinvee, T.A., Singh, N., Yan, Y., and Hulai, O. (2024). Maternal lipid mobilization is essential for embryonic development in the malaria vector Anopheles gambiae. PLoS Biol., 22.","DOI":"10.1371\/journal.pbio.3002960"},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Gondim, K.C., and Majerowicz, D. (2024). Lipophorin: The lipid shuttle. Lipophorin: The Lipid Shuttle, Springer International Publishing. Advances in Experimental Medicine and Biology.","DOI":"10.1007\/5584_2024_806"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Pinch, M., Mitra, S., Rodriguez, S.D., Li, Y., Kandel, Y., Dungan, B., Holguin, F.O., Attardo, G.M., and Hansen, I.A. (2021). Fat and happy: Profiling mosquito fat body lipid storage and composition post-blood meal. Front. Insect Sci., 1.","DOI":"10.3389\/finsc.2021.693168"},{"key":"ref_87","doi-asserted-by":"crossref","unstructured":"Zhao, Y., Liu, W., Zhao, X., Yu, Z., Guo, H., Yang, Y., Moussian, B., Zhu, K.Y., and Zhang, J. (2023). Lipophorin receptor is required for the accumulations of cuticular hydrocarbons and ovarian neutral lipids in Locusta migratoria. Int. J. Biol. Macromol., 236.","DOI":"10.1016\/j.ijbiomac.2023.123746"},{"key":"ref_88","first-page":"E2709","article-title":"Hormone and receptor interplay in the regulation of mosquito lipid metabolism","volume":"114","author":"Wang","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"2121","DOI":"10.1073\/pnas.0608407104","article-title":"Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae","volume":"104","author":"DeJong","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_90","doi-asserted-by":"crossref","unstructured":"Diaz-Albiter, H., Mitford, R., Genta, F.A., Sant\u2019Anna, M.R., and Dillon, R.J. (2011). Reactive oxygen species scavenging by catalase is important for female Lutzomyia longipalpis fecundity and mortality. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0017486"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1016\/j.jinsphys.2011.01.012","article-title":"Catalase and superoxide dismutase-2 enhance survival and protect ovaries during overwintering diapause in the mosquito Culex pipiens","volume":"57","author":"Sim","year":"2011","journal-title":"J. Insect Physiol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1093\/jmedent\/47.5.769","article-title":"Reproduction-longevity trade-off in Anopheles gambiae (Diptera: Culicidae)","volume":"47","author":"Dao","year":"2010","journal-title":"J. Med. Entomol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"4844","DOI":"10.1074\/jbc.M112.435347","article-title":"Characterization of Anopheles gambiae transglutaminase 3 (AgTG3) and Iits native substrate plugin","volume":"288","author":"Le","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_94","doi-asserted-by":"crossref","unstructured":"Rogers, D.W., Baldini, F., Battaglia, F., Panico, M., Dell, A., Morris, H.R., and Catteruccia, F. (2009). Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito. PLoS Biol., 7.","DOI":"10.1371\/journal.pbio.1000272"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1111\/1744-7917.13084","article-title":"Juvenile hormone acts on male accessory gland function via regulating l-asparaginase expression and triacylglycerol mobilization in Aedes aegypti","volume":"30","author":"Lyu","year":"2023","journal-title":"Insect Sci."},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Stanley, D., and Kim, Y. (2019). Prostaglandins and other eicosanoids in insects: Biosynthesis and biological actions. Front. Physiol., 9.","DOI":"10.3389\/fphys.2018.01927"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Pondeville, E., David, J.-P., Guittard, E., Maria, A., Jacques, J.-C., Ranson, H., Bourgouin, C., and Dauphin-Villemant, C. (2013). Microarray and RNAi analysis of P450s in Anopheles gambiae male and female steroidogenic tissues: CYP307A1 is required for ecdysteroid synthesis. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0079861"},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Hu, J., Medison, R.G., Zhang, S., Ma, P., and Shi, C. (2022). Impacts of non-lethal high-temperature stress on the development and reproductive organs of Bradysia odoriphaga. Insects, 13.","DOI":"10.3390\/insects13010074"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"dev200149","DOI":"10.1242\/dev.200149","article-title":"Warm and cold temperatures have distinct germline stem cell lineage effects during Drosophila oogenesis","volume":"149","author":"Gandara","year":"2022","journal-title":"Development"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1111\/j.1570-7458.2005.00316.x","article-title":"Temperature-dependent ovariole and testis maturation in the yellow dung fly","volume":"116","author":"Blanckenhorn","year":"2005","journal-title":"Entomol. Exp. Appl."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1016\/j.stem.2007.09.010","article-title":"Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary","volume":"1","author":"Pan","year":"2007","journal-title":"Cell Stem Cell"},{"key":"ref_102","doi-asserted-by":"crossref","unstructured":"Michalkova, V., Benoit, J.B., Attardo, G.M., Medlock, J., and Aksoy, S. (2014). Amelioration of reproduction-associated oxidative stress in a viviparous insect is critical to prevent reproductive senescence. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0087554"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"100114","DOI":"10.1016\/j.cris.2025.100114","article-title":"Antioxidants, oxidative stress and reactive oxygen species in insects exposed to heat","volume":"7","author":"Montoya","year":"2025","journal-title":"Curr. Res. Insect Sci."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"802","DOI":"10.1111\/brv.12588","article-title":"Insect responses to heat: Physiological mechanisms, evolution and ecological implications in a warming world","volume":"95","author":"Villalobos","year":"2020","journal-title":"Biol. Rev. Camb. Philos. Soc."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1093\/jmedent\/27.5.839","article-title":"Fecundity, metabolism, and body size in Anopheles (Diptera: Culicidae), vectors of malaria","volume":"27","author":"Briegel","year":"1990","journal-title":"J. Med. Entomol."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/0022-1910(90)90118-Y","article-title":"Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti","volume":"36","author":"Briegel","year":"1990","journal-title":"J. Insect Physiol."},{"key":"ref_107","doi-asserted-by":"crossref","unstructured":"Stryapunina, I., Itoe, M.A., Trinh, Q., Vidoudez, C., Du, E., Mendoza, L., Hulai, O., Kauffman, J., Carew, J., and Shaw, W.R. (2024). Precise coordination between nutrient transporters ensures fertility in the malaria mosquito Anopheles gambiae. PLoS Genet., 20.","DOI":"10.1371\/journal.pgen.1011145"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1275","DOI":"10.1016\/S0965-1748(02)00090-5","article-title":"Molecular biology of mosquito vitellogenesis: From basic studies to genetic engineering of antipathogen immunity","volume":"32","author":"Raikhel","year":"2002","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1603\/ME10071","article-title":"Male mating history and body size influence female fecundity and longevity of the Dengue vector Aedes aegypti","volume":"48","author":"Helinski","year":"2011","journal-title":"J. Med. Entomol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1111\/1365-2435.12515","article-title":"Developmental environment mediates male seminal protein investment in Drosophila melanogaster","volume":"30","author":"Wigby","year":"2016","journal-title":"Funct. Ecol."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"10626","DOI":"10.1073\/pnas.0403460101","article-title":"Target of rapamycin-mediated amino acid signaling in mosquito anautogeny","volume":"101","author":"Hansen","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/0531-5565(80)90061-3","article-title":"Metabolic changes in ageing Drosophila melanogaster","volume":"15","author":"Driver","year":"1980","journal-title":"Exp. Gerontol."},{"key":"ref_113","doi-asserted-by":"crossref","unstructured":"Costanzo, K., and Occhino, D. (2023). Effects of temperature on blood feeding and activity levels in the tiger mosquito, Aedes albopictus. Insects, 14.","DOI":"10.3390\/insects14090752"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1111\/tmi.13732","article-title":"Effects of elevated temperatures on the development of immature stages of Anopheles gambiae (s.l.) mosquitoes","volume":"27","author":"Agyekum","year":"2022","journal-title":"Trop. Med. Int. Health"},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1186\/s41936-018-0045-3","article-title":"Influence of rearing-water temperature on life stages\u2019 vector attributes, distribution and utilisation of metabolic reserves in Culex quinquefasciatus (Diptera: Culicidae): Implications for disease transmission and vector control","volume":"79","author":"Ukubuiwe","year":"2018","journal-title":"J. Basic Appl. Zool."},{"key":"ref_116","doi-asserted-by":"crossref","unstructured":"Klepsatel, P., G\u00e1likov\u00e1, M., Xu, Y., and K\u00fchnlein, R.P. (2016). Thermal stress depletes energy reserves in Drosophila. Sci. Rep., 6.","DOI":"10.1038\/srep33667"},{"key":"ref_117","doi-asserted-by":"crossref","unstructured":"Dittmer, J., Alafndi, A., and Gabrieli, P. (2019). Fat body\u2013specific vitellogenin expression regulates host-seeking behaviour in the mosquito Aedes albopictus. PLoS Biol., 17.","DOI":"10.1371\/journal.pbio.3000238"},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1093\/jmedent\/30.6.975","article-title":"Multiple blood meals as a reproductive strategy in Anopheles (Diptera: Culicidae)","volume":"30","author":"Briegel","year":"1993","journal-title":"J. Med. Entomol."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1093\/jmedent\/35.5.639","article-title":"Articles: Effect of body size on host seeking and blood meal utilization in Anopheles gambiae sensu stricto (Diptera: Culicidae): The disadvantage of being small","volume":"35","author":"Takken","year":"1998","journal-title":"J. Med. Entomol."},{"key":"ref_120","first-page":"11","article-title":"Reproductive physiology of Anopheles gambiae and Anopheles atroparvus","volume":"30","author":"Fernandes","year":"2005","journal-title":"J. Vector Ecol."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"1825","DOI":"10.1016\/0022-1910(67)90018-2","article-title":"The fine structure of the spermathecae and their ducts in the mosquito Aedes aegypti","volume":"13","author":"Clements","year":"1967","journal-title":"J. Insect Physiol."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1603\/AN13079","article-title":"The fine structure of the spermatheca in Anopheles aquasalis (Diptera: Culicidae)","volume":"106","author":"Pascini","year":"2013","journal-title":"Ann. Entomol. Soc. Am."},{"key":"ref_123","doi-asserted-by":"crossref","unstructured":"Pereira, J., Rios, T., Amorim, J., Faria-Reis, A., de Almeida, E., Neves, M., Santos-Ara\u00fajo, S., Selim, L., Bertuci, F., and Silva, M.B. (2025). Functional characterization of vitellogenin unveils novel roles in RHBP uptake and lifespan regulation in the insect vector Rhodnius prolixus. Insect Biochem. Mol. Biol., 180.","DOI":"10.1016\/j.ibmb.2025.104301"},{"key":"ref_124","doi-asserted-by":"crossref","unstructured":"Chen, D., Han, H.-L., Li, W.-J., Wang, J.-J., and Wei, D. (2022). Expression and role of vitellogenin genes in ovarian development of Zeugodacus cucurbitae. Insects, 13.","DOI":"10.3390\/insects13050452"},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/0012-1606(82)90309-8","article-title":"The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster","volume":"89","author":"Brennan","year":"1982","journal-title":"Dev. Biol."},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"19390","DOI":"10.1073\/pnas.0809723105","article-title":"Molecular and cellular components of the mating machinery in Anopheles gambiae females","volume":"105","author":"Rogers","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_127","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1146\/annurev-ento-112408-085356","article-title":"Insect fat body: Energy, metabolism, and regulation","volume":"55","author":"Arrese","year":"2010","journal-title":"Annu. Rev. Entomol."},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.cois.2015.05.001","article-title":"A comparative analysis of reproductive biology of insect vectors of human disease","volume":"10","author":"Shaw","year":"2015","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1016\/0965-1748(94)90038-8","article-title":"De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito","volume":"24","author":"Borovsky","year":"1994","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_130","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.jinsphys.2014.03.006","article-title":"Male Aedes aegypti mosquitoes use JH III transferred during copulation to influence previtellogenic ovary physiology and affect the reproductive output of female mosquitoes","volume":"64","author":"Clifton","year":"2014","journal-title":"J. Insect Physiol."},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"1366","DOI":"10.1016\/j.jinsphys.2010.02.014","article-title":"Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods","volume":"56","author":"Benoit","year":"2010","journal-title":"J. Insect Physiol."},{"key":"ref_132","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1016\/S0022-1910(99)00085-2","article-title":"Adaptation of Aedes aegypti (Diptera: Culicidae) oviposition behavior in response to humidity and diet","volume":"45","author":"Canyon","year":"1999","journal-title":"J. Insect Physiol."},{"key":"ref_133","first-page":"1","article-title":"Aedes aegypti disregard humidity-related conditions with adequate nutrition","volume":"30","author":"Canyon","year":"2013","journal-title":"Trop. Biomed."},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"1375","DOI":"10.1093\/jme\/tjx077","article-title":"Aedes aegypti (Diptera: Culicidae) abundance model improved with relative humidity and precipitation-driven egg hatching","volume":"54","author":"Lega","year":"2017","journal-title":"J. Med. Entomol."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1111\/ele.14228","article-title":"Humidity\u2014The overlooked variable in the thermal biology of mosquito-borne disease","volume":"26","author":"Brown","year":"2023","journal-title":"Ecol. Lett."}],"container-title":["Insects"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4450\/16\/9\/921\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:37:54Z","timestamp":1760035074000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4450\/16\/9\/921"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,9,2]]},"references-count":135,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2025,9]]}},"alternative-id":["insects16090921"],"URL":"https:\/\/doi.org\/10.3390\/insects16090921","relation":{},"ISSN":["2075-4450"],"issn-type":[{"value":"2075-4450","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,9,2]]}}}