Higher temperature accelerates the aging-dependent weakening of the melanization immune response in mosquitoes

• Published in: PLoS pathogens Vol. 20; no. 1; p. e1011935
• Main Authors: Martin, Lindsay E, Hillyer, Julián F
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.01.2024; Public Library of Science (PLoS)
• Subjects: Abdominal wall; Age; Aging; Analysis; Animals; Anopheles; Anopheles gambiae; Aquatic insects; Biology and Life Sciences; Body temperature; Climate change; Culicidae; Deposition; Development and progression; Disease control; Disease susceptibility; Disease transmission; Female; Free radicals (Chemistry); Global temperature changes; Health aspects; Hemolymph; High temperature; Hot Temperature; Immune response; Immune system; Immunity; Infections; Insects; Malaria; Medicine and Health Sciences; Melanin; Melanins; Melanization; Mosquitoes; Nitric oxide; Oxidation; Pathogens; Phenoloxidase; Physical Sciences; Physiological aspects; Physiology; Prevention; Senescence; Spectrophotometry; Temperature; Temperature dependence; Temperature effects; Tropical diseases; United States
• ISSN: 1553-7374; 1553-7366; 1553-7374
• DOI: 10.1371/journal.ppat.1011935

The body temperature of mosquitoes, like most insects, is dictated by the environmental temperature. Climate change is increasing the body temperature of insects and thereby altering physiological processes such as immune proficiency. Aging also alters insect physiology, resulting in the weakening of the immune system in a process called senescence. Although both temperature and aging independently affect the immune system, it is unknown whether temperature alters the rate of immune senescence. Here, we evaluated the independent and combined effects of temperature (27°C, 30°C and 32°C) and aging (1, 5, 10 and 15 days old) on the melanization immune response of the adult female mosquito, Anopheles gambiae. Using a spectrophotometric assay that measures phenoloxidase activity (a rate limiting enzyme) in hemolymph, and therefore, the melanization potential of the mosquito, we discovered that the strength of melanization decreases with higher temperature, aging, and infection. Moreover, when the temperature is higher, the aging-dependent decline in melanization begins at a younger age. Using an optical assay that measures melanin deposition on the abdominal wall and in the periostial regions of the heart, we found that melanin is deposited after infection, that this deposition decreases with aging, and that this aging-dependent decline is accelerated by higher temperature. This study demonstrates that higher temperature accelerates immune senescence in mosquitoes, with higher temperature uncoupling physiological age from chronological age. These findings highlight the importance of investigating the consequences of climate change on how disease transmission by mosquitoes is affected by aging.