Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor
Abstract Background The Disposable Soma Theory of aging suggests a trade-off between energy allocation for growth, reproduction and somatic maintenance, including immunity. While trade-offs between reproduction and immunity are well documented, those involving growth remain under-explored. Rapid gro...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2024-01-01
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| Series: | Immunity & Ageing |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12979-023-00409-w |
| _version_ | 1797355486942593024 |
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| author | Agathe Crosland Thierry Rigaud Charlène Develay Yannick Moret |
| author_facet | Agathe Crosland Thierry Rigaud Charlène Develay Yannick Moret |
| author_sort | Agathe Crosland |
| collection | DOAJ |
| description | Abstract Background The Disposable Soma Theory of aging suggests a trade-off between energy allocation for growth, reproduction and somatic maintenance, including immunity. While trade-offs between reproduction and immunity are well documented, those involving growth remain under-explored. Rapid growth might deplete resources, reducing investment in maintenance, potentially leading to earlier or faster senescence and a shorter lifespan. However, rapid growth could limit exposure to parasitism before reaching adulthood, decreasing immunity needs. The insect immunity’s components (cellular, enzymatic, and antibacterial) vary in cost, effectiveness, and duration. Despite overall immunity decline (immunosenescence), its components seem to age differently. We hypothesize that investment in these immune components is adjusted based on the resource cost of growth, longevity, and the associated risk of parasitism. Results We tested this hypothesis using the mealworm beetle, Tenebrio molitor as our experimental subject. By manipulating the larval environment, including three different temperatures and three relative humidity levels, we achieved a wide range of growth durations and longevities. Our main focus was on the relationship between growth duration, longevity, and specific immune components: hemocyte count, phenoloxidase activity, and antibacterial activity. We measured these immune parameters both before and after exposing the individuals to a standard bacterial immune challenge, enabling us to assess immune responses. These measurements were taken in both young and older adult beetles. Upon altering growth duration and longevity by modifying larval temperature, we observed a more pronounced investment in cellular and antibacterial defenses among individuals with slow growth and extended lifespans. Intriguingly, slower-growing and long-lived beetles exhibited reduced enzymatic activity. Similar results were found when manipulating larval growth duration and adult longevity through variations in relative humidity, with a particular focus on antibacterial activity. Conclusion The impact of growth manipulation on immune senescence varies by the specific immune parameter under consideration. Yet, in slow-growing T. molitor, a clear decline in cellular and antibacterial immune responses with age was observed. This decline can be linked to their initially stronger immune response in early life. Furthermore, our study suggests an immune strategy favoring enhanced antibacterial activity among slow-growing and long-lived T. molitor individuals. |
| first_indexed | 2024-03-08T14:11:52Z |
| format | Article |
| id | doaj.art-1d5e7c8bcd874035af7f9feb9d211a56 |
| institution | Directory Open Access Journal |
| issn | 1742-4933 |
| language | English |
| last_indexed | 2024-03-08T14:11:52Z |
| publishDate | 2024-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Immunity & Ageing |
| spelling | doaj.art-1d5e7c8bcd874035af7f9feb9d211a562024-01-14T12:36:31ZengBMCImmunity & Ageing1742-49332024-01-0121111810.1186/s12979-023-00409-wGrowth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitorAgathe Crosland0Thierry Rigaud1Charlène Develay2Yannick Moret3Biogéosciences (UMR-CNRS 6282), Université de BourgogneBiogéosciences (UMR-CNRS 6282), Université de BourgogneBiogéosciences (UMR-CNRS 6282), Université de BourgogneBiogéosciences (UMR-CNRS 6282), Université de BourgogneAbstract Background The Disposable Soma Theory of aging suggests a trade-off between energy allocation for growth, reproduction and somatic maintenance, including immunity. While trade-offs between reproduction and immunity are well documented, those involving growth remain under-explored. Rapid growth might deplete resources, reducing investment in maintenance, potentially leading to earlier or faster senescence and a shorter lifespan. However, rapid growth could limit exposure to parasitism before reaching adulthood, decreasing immunity needs. The insect immunity’s components (cellular, enzymatic, and antibacterial) vary in cost, effectiveness, and duration. Despite overall immunity decline (immunosenescence), its components seem to age differently. We hypothesize that investment in these immune components is adjusted based on the resource cost of growth, longevity, and the associated risk of parasitism. Results We tested this hypothesis using the mealworm beetle, Tenebrio molitor as our experimental subject. By manipulating the larval environment, including three different temperatures and three relative humidity levels, we achieved a wide range of growth durations and longevities. Our main focus was on the relationship between growth duration, longevity, and specific immune components: hemocyte count, phenoloxidase activity, and antibacterial activity. We measured these immune parameters both before and after exposing the individuals to a standard bacterial immune challenge, enabling us to assess immune responses. These measurements were taken in both young and older adult beetles. Upon altering growth duration and longevity by modifying larval temperature, we observed a more pronounced investment in cellular and antibacterial defenses among individuals with slow growth and extended lifespans. Intriguingly, slower-growing and long-lived beetles exhibited reduced enzymatic activity. Similar results were found when manipulating larval growth duration and adult longevity through variations in relative humidity, with a particular focus on antibacterial activity. Conclusion The impact of growth manipulation on immune senescence varies by the specific immune parameter under consideration. Yet, in slow-growing T. molitor, a clear decline in cellular and antibacterial immune responses with age was observed. This decline can be linked to their initially stronger immune response in early life. Furthermore, our study suggests an immune strategy favoring enhanced antibacterial activity among slow-growing and long-lived T. molitor individuals.https://doi.org/10.1186/s12979-023-00409-wAged immune responseInvertebrate immunityDisposable soma theoryConstitutive and inducible immunityMealworm beetle |
| spellingShingle | Agathe Crosland Thierry Rigaud Charlène Develay Yannick Moret Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor Immunity & Ageing Aged immune response Invertebrate immunity Disposable soma theory Constitutive and inducible immunity Mealworm beetle |
| title | Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor |
| title_full | Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor |
| title_fullStr | Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor |
| title_full_unstemmed | Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor |
| title_short | Growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of Tenebrio molitor |
| title_sort | growth and longevity modulation through larval environment mediate immunosenescence and immune strategy of tenebrio molitor |
| topic | Aged immune response Invertebrate immunity Disposable soma theory Constitutive and inducible immunity Mealworm beetle |
| url | https://doi.org/10.1186/s12979-023-00409-w |
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