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Mosquitoes cannot use metabolism to regulate their body temperature and therefore climate warming is altering their physiology. Mosquitoes also experience a physiological decline with aging, a phenomenon called senescence. Because both high temperature and aging are detrimental to mosquitoes, we hypothesized that high temperatures accelerate senescence. Here, we investigated how temperature and aging, independently and interactively, shape the antimicrobial immune response of the mosquito Anopheles gambiae. Using a zone-of-inhibition assay that measures the antimicrobial activity of hemolymph, we found that antimicrobial activity increases following infection. Moreover, in infected mosquitoes, antimicrobial activity weakens as the temperature rises to 32°C, and antimicrobial activity increases from 1 to 5 days of age and stabilizes with further aging. Importantly, in E. coli-infected mosquitoes, higher temperature causes an aging-dependent decline in antimicrobial activity. Altogether, this study demonstrates that higher temperature can accelerate immune senescence in infected mosquitoes, thereby interactively shaping their ability to fight an infection.
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Higher temperature accelerates the aging-dependent weakening of the melanization immune response in mosquitoes
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.
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- Award ID(s):
- 1936843
- PAR ID:
- 10492971
- Editor(s):
- McGraw, Elizabeth A.
- Publisher / Repository:
- PLOS
- Date Published:
- Journal Name:
- PLOS Pathogens
- Volume:
- 20
- Issue:
- 1
- ISSN:
- 1553-7374
- Page Range / eLocation ID:
- e1011935
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract BackgroundMost insects are poikilotherms and ectotherms, so their body temperature is predicated by environmental temperature. With climate change, insect body temperature is rising, which affects how insects develop, survive, and respond to infection. Aging also affects insect physiology by deteriorating body condition and weakening immune proficiency via senescence. Aging is usually considered in terms of time, or chronological age, but it can also be conceptualized in terms of body function, or physiological age. We hypothesized that warmer temperature decouples chronological and physiological age in insects by accelerating senescence. To investigate this, we reared the African malaria mosquito,Anopheles gambiae, at 27 °C, 30 °C and 32 °C, and measured survival starting at 1-, 5-, 10- and 15-days of adulthood after no manipulation, injury, or a hemocoelic infection withEscherichia coliorMicrococcus luteus. Then, we measured the intensity of anE. coliinfection to determine how the interaction between environmental temperature and aging shapes a mosquito’s response to infection. ResultsWe demonstrate that longevity declines when a mosquito is infected with bacteria, mosquitoes have shorter lifespans when the temperature is warmer, older mosquitoes are more likely to die, and warmer temperature marginally accelerates the aging-dependent decline in survival. Furthermore, we discovered thatE. coliinfection intensity increases when the temperature is warmer and with aging, and that warmer temperature accelerates the aging-dependent increase in infection intensity. Finally, we uncovered that warmer temperature affects both bacterial and mosquito physiology. ConclusionsWarmer environmental temperature accelerates aging in mosquitoes, negatively affecting both longevity and infection outcomes. These findings have implications for how insects will serve as pollinators, agricultural pests, and disease vectors in our warming world.more » « less
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Most insects are poikilotherms and ectotherms, so their body temperature fluctuates and closely aligns with the temperature of their environment. The rise in global temperatures is affecting the physiology of insects by altering their ability to survive, reproduce, and transmit disease. Aging also impacts insect physiology because the body deteriorates via senescence as the insect ages. Although temperature and age both impact insect biology, these factors have historically been studied in isolation. So, it is unknown whether or how temperature and age interact to shape insect physiology. Here, we investigated the effects of warmer temperature (27 °C, 30 °C and 32 °C), aging (1, 5, 10, and 15 days post-eclosion), and their interaction on the size and body composition of the mosquito, Anopheles gambiae. We found that warmer temperatures result in slightly smaller adult mosquitoes, as measured by abdomen and tibia length. Aging alters both abdominal length and dry weight in a manner that correlates with the increase in energetic resources and tissue remodeling that occurs after metamorphosis and the senescence-based decline that ensues later. Moreover, the carbohydrate and lipid contents of adult mosquitoes are not meaningfully affected by temperature but are altered by aging: carbohydrate content increases with age whereas lipid content increases over the first few days of adulthood and then decreases. Protein content decreases with both rising temperature and aging, and the aging-associated decrease accelerates at warmer temperatures. Altogether, temperature and age, individually and to a lesser extent interactively, shape the size and composition of adult mosquitoes.more » « less
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Abstract The immune and circulatory systems of insects are functionally integrated. Following infection, immune cells called hemocytes aggregate around the ostia (valves) of the heart. An earlier RNA sequencing project in the African malaria mosquito,Anopheles gambiae, revealed that the heart-associated hemocytes, called periostial hemocytes, express transglutaminases more highly than hemocytes elsewhere in the body. Here, we further queried the expression of these transglutaminase genes and examined whether they play a role in heart-associated immune responses. We found that, in the whole body, injury upregulates the expression ofTGase2, whereas infection upregulatesTGase1,TGase2andTGase3. RNAi-based knockdown ofTGase1andTGase2did not alter periostial hemocyte aggregation, but knockdown ofTGase3increased the number of periostial hemocytes during the early stages of infection and the sequestration of melanin by periostial hemocytes during the later stages of infection. In uninfected mosquitoes, knockdown ofTGase3also slightly reduced the number of sessile hemocytes outside of the periostial regions. Taken altogether, these data show thatTGase3negatively regulates periostial hemocyte aggregation, and we hypothesize that this occurs by negatively regulating the immune deficiency pathway and by altering hemocyte adhesion. In conclusion,TGase3is involved in the functional integration between the immune and circulatory systems of mosquitoes.more » « less
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null (Ed.)The immune and circulatory systems of mammals are functionally integrated, as exemplified by the immune function of the spleen and lymph nodes. Similar functional integration exists in the malaria mosquito, Anopheles gambiae , as exemplified by the infection-induced aggregation of hemocytes around the heart valves. Whether this is specific to mosquitoes or a general characteristic of insects remained unknown. We analyzed 68 species from 51 families representing 16 orders and found that infection induces the aggregation of hemocytes and pathogens on the heart of insects from all major branches of the class Insecta. An expanded analysis in the holometabolous mosquito, Aedes aegypti , and the hemimetabolous bed bug, Cimex lectularius , showed that infection induces the aggregation of phagocytic hemocytes on the hearts of distantly related insects, with aggregations mirroring the patterns of hemolymph flow. Therefore, the functional integration of the immune and circulatory systems is conserved across the insect tree of life.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.ppat.1011935
