The importance of fat accumulation and reserves for insect overwintering.

[en] Winter is a challenging season for ectothermic species such as insects. In addition to thermal stress imposed by cold temperatures, food scarcity during winter can lead to starvation and energy drain. In preparation for winter, most insects accumulate lipid (fat) reserves, which are the principal source of energetic fuel during overwintering. In this review, we highlight the most recent literature on lipid metabolism in response to cold. We first discuss how lipid metabolism is affected by biotic and abiotic environmental changes in preparation for winter. We then highlight how lipid dynamics are affected during winter, including physiological and (epi)genetic mechanisms. We end our review emphasizing the importance of remaining fat reserves in spring and how climate change can negatively impact lipid metabolism and fitness.

Disciplines :

Zoology

Author, co-author :

Enriquez, Thomas ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Visser, Bertanne ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs

Language :

English

Title :

The importance of fat accumulation and reserves for insect overwintering.

Publication date :

December 2023

Journal title :

Current Opinion in Insect Science

ISSN :

2214-5745

eISSN :

2214-5753

Publisher :

Elsevier Inc.

Volume :

Pages :

101118

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Fondation Fyssen [FR]
ULiège - Université de Liège [BE]

Funding text :

This work was supported by the Fyssen Foundation , the University of Liège , and the Fonds National de la Recherche Scientifique (F.R.S.-FNRS).

Available on ORBi :

since 29 January 2024

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Bibliography

Rozsypal, J., Cold and freezing injury in insects: an overview of molecular mechanisms. Eur J Entomol 119 (2022), 43–57.
Overgaard, J., MacMillan, H.A., The integrative physiology of insect chill tolerance. Annu Rev Physiol 79 (2017), 187–208.
Enriquez, T., Teets, N., Lipid metabolism in response to cold. Musselman, L.P., Toprak, U., (eds.) Under Revision for Publication in “Insect Lipid Metabolism”, 2023, Springer, 10.32942/X2VS3F.
Short, C.A., Hahn, D.A., Fat enough for the winter? Does nutritional status affect diapause?. J Insect Physiol, 145, 2023, 10.1016/j.jinsphys.2023.104488.
Denlinger, D.L., Insect diapause: from a rich history to an exciting future. J Exp Biol, 226, 2023, jeb245329.
Teets, N.M., Marshall, K.E., Reynolds, J.A., Molecular mechanisms of winter survival. Annu Rev Entomol 68 (2023), 319–339.
Sinclair, B.J., Marshall, K.E., The many roles of fats in overwintering insects. J Exp Biol, 221, 2018, jeb161836.
Isobe, K., Takahashi, A., Tamura, K., Cold tolerance and metabolic rate increased by cold acclimation in Drosophila albomicans from natural populations. Genes Genet Syst 88 (2013), 289–300.
Sinclair, B.J., Linking energetics and overwintering in temperate insects. J Therm Biol 54 (2015), 5–11.
Visser, B., Le Lann, C., Nieberding, C., Lammers, M., Hahn, D., Alborn, H., Enriquez, T., Scheifler, M., Harvey, J., Ellers, J., Many parasitoids lack adult triglyceride accumulation, despite functioning fatty acid biosynthesis: a discussion of concepts and considerations for future research. Curr Res Insect Sci, 3, 2023, 100055.
Zhao, L., Wang, W., Qiu, Y., Torson, A.S., Physiological Mechanisms of Variable Nutrient Accumulation Patterns Between Diapausing and Non-Diapausing Fall Webworm (Lepidoptera: Arctiidae) Pupae. Environmental Entomology 50 (2021), 1158–1165.
Chen, J., Guo, P., Li, Y., He, W., Chen, W., Shen, Z., Zhang, M., Mao, J., Zhang, L., Cathepsin L contributes to reproductive diapause by regulating lipid storage and survival of Coccinella septempunctata (Linnaeus). Int J Mol Sci, 24, 2023, 611.
Kivelä, S.M., Gotthard, K., Lehmann, P., Developmental plasticity in metabolism but not in energy reserve accumulation in a seasonally polyphenic butterfly. Journal of Experimental Biology, 2019, 10.1242/jeb.202150.
Mensch, J., Di Battista, C., De Majo, M.S., Campos, R.E., Fischer, S., Increased size and energy reserves in diapausing eggs of temperate Aedes aegypti populations. Journal of Insect Physiology, 131, 2021, 104232.
Batz, Z.A., Armbruster, P.A., Diapause-associated changes in the lipid and metabolite profiles of the Asian tiger mosquito, Aedes albopictus. J Exp Biol, 221, 2018, 189480.
Chang, V., Meuti, M.E., Circadian transcription factors differentially regulate features of the adult overwintering diapause in the Northern house mosquito, Culex pipiens. Insect Biochemistry and Molecular Biology, 121, 2020, 103365.
Verheyen, J, Temmerman, K, De Block, M, Stoks, R, Voltinism-associated differences in winter survival across latitudes: integrating growth, physiology, and food intake. Oecologia 186 (2018), 919–929.
Neven, L.G., Yee, W.L., Metabolic reserves of diapausing western cherry fruit fly (Diptera: Tephritidae) pupae in relation to chill duration and post-chill rearing conditions. Frontiers in Insect Science, 2, 2022.
Song, Y, Huang, W, Zhou, Y, Li, Z, Ji, R, Ye, X, Physiological characteristics and cold tolerance of overwintering eggs in Gomphocerus sibiricus L. (Orthoptera: Acrididae). Archives of Insect Biochemistry and Physiology, 108, 2021, e21846.
Mohammadzadeh, M., Borzoui, E., Izadi, H., Physiological and Biochemical Differences in Diapausing and Nondiapausing Larvae of Eurytoma plotnikovi (Hymenoptera: Eurytomidae). Environmental Entomology 46 (2017), 1424–1431.
Xu, R., Chen, Y.-H., Xia, J.-F., Zeng, T.-X., Li, Y.-H., Zhu, J.-Y., Metabolic dynamics across prolonged diapause development in larvae of the sawfly, Cephalcia chuxiongica (Hymenoptera: Pamphiliidae). Journal of Asia-Pacific Entomology 24 (2021), 1–6.
Rozsypal, J., Moos, M., Rudolf, I., Košťál, V., Do energy reserves and cold hardiness limit winter survival of Culex pipiens?. Comp Biochem Physiol Part A: Mol Integr Physiol, 255, 2021, 110912 A population of overwintering mosquitoes was monitored in a shelter microhabitat during winter. Females had a low metabolic rate with fat reserves gradually decreasing during winter in diapausing females. This suggests that lipids are the main fuel to meet the metabolic requirements of diapause. Females leave the shelter at the onset of spring with large fat reserves (compared with summer mosquitoes), which are probably required to resume reproduction and disperse in spring.
Shao, Y., Feng, Y., Tian, B., Wang, T., He, Y., Zong, S., Cold hardiness of larvae of Dendrolimus tabulaeformis (Lepidoptera: Lasiocampidae) at different stages during the overwintering period. EJE 115 (2018), 198–207.
Lehmann, P., Westberg, M., Tang, P., Lindström, L., Käkelä, R., The Diapause Lipidomes of Three Closely Related Beetle Species Reveal Mechanisms for Tolerating Energetic and Cold Stress in High-Latitude Seasonal Environments. Frontiers in Physiology, 11, 2020.
Ciancio, J.J., Turnbull, K.F., Gariepy, T.D., Sinclair, B.J., Cold tolerance, water balance, energetics, gas exchange, and diapause in overwintering brown marmorated stink bugs. J Insect Physiol, 128, 2021, 104171.
Su, M., Tan, X., Yang, Q., Wan, F., Zhou, H., Temperature adaptability of two clades of Aphelinus mali (Hymenoptera: Aphelinidae) in China. Egyptian Journal of Biological Pest Control, 28, 2018, 16.
Alcântara, C.O.de, Silva, P.G. da, Hernández, M.I.M., Body size and body conditions of two dung beetles species (Coleoptera: Scarabaeidae) related to environmental temperatures. Rev Bras entomol, 67, 2023, e20220099.
Spacht, D.E., Gantz, J.D., Devlin, J.J., McCabe, E.A., Lee, R.E., Denlinger, D.L., Teets, N.M., Fine-scale variation in microhabitat conditions influences physiology and metabolism in an Antarctic insect. Oecologia 197 (2021), 373–385 Studying different populations of the midge Belgica antarctica during preparation for winter revealed that fat content was not changing during the season in larvae, but changed depending on microhabitat type. Food abundance, rather than microclimatic conditions, influences fat reserve levels. Temperature is thus not the only factor that can lead to considerable changes in fat reserves.
Pei, J., Li, C., Ren, L., Zong, S., Factors influencing cold hardiness during overwintering of Streltzoviella insularis (Lepidoptera: Cossidae). J Econ Entomol 113 (2020), 1254–1261.
Lai, Y.-P., Tao, K., Hou, T.-P., Preliminary analysis of geographical distribution based on cold hardiness for Evergestis extimalis (Scopoli) (Lepidoptera: Pyralidae) on Qinghai–Tibet Plateau. Entomological Research 49 (2019), 13–20.
Wang, Z., Chen, Y., Diaz, R., Laine, R.A., Physiology of crapemyrtle bark scale, Acanthococcus lagerstroemiae (Kuwana), associated with seasonally altered cold tolerance. Journal of Insect Physiology 112 (2019), 1–8.
Jensen, K., Michaelsen, J.V., Larsen, M.T., Kristensen, T.N., Holmstrup, M., Overgaard, J., Increased lipid accumulation but not reduced metabolism explains improved starvation tolerance in cold-acclimated arthropod predators. Sci Nat, 105, 2018, 65.
Rendon, D., Walton, V., Tait, G., Buser, J., Lemos Souza, I., Wallingford, A., Loeb, G., Lee, J., Interactions among morphotype, nutrition, and temperature impact fitness of an invasive fly. Ecology and Evolution 9 (2019), 2615–2628.
Saeed, M.M., Tougeron, K., Raza, A.B.M., Afzal, M., Aqueel, A., Le Goff, G.J., Renoz, F., Pirotte, J., Hance, T., Transgenerational phenotypic plasticity of diapause induction and related fitness cost in a commercial strain of the parasitoid Aphidius ervi Haliday. Insect Sci 28 (2021), 780–792.
Hubhachen, Z., Madden, R.D., Dillwith, J.W., Influence of rearing temperature on triacylglycerol storage in the pea aphid, Acyrthosiphon pisum. Arch Insect Biochem Physiol, 99, 2018, e21495.
Alfaro-Tapia, A., Alvarez-Baca, J.K., Tougeron, K., Lavandero, B., Le Lann, C., Van Baaren, J., Overwintering strategies and life-history traits of different populations of Aphidius platensis along a latitudinal gradient in Chile. Entomol Gen 42 (2021), 127–145.
Xiang, M., Zhang, H.-Z., Jing, X.-Y., Wang, M.-Q., Mao, J.-J., Li, Y.-Y., Zang, L.-S., Zhang, L.-S., Sequencing, expression, and functional analyses of four genes related to fatty acid biosynthesis during the diapause process in the female ladybird, Coccinella septempunctata L. Front Physiol, 12, 2021, 1249.
Tan, Q.-Q., Liu, W., Zhu, F., Lei, C.-L., Hahn, D.A., Wang, X.-P., Describing the diapause-preparatory proteome of the beetle Colaphellus bowringi and identifying candidates affecting lipid accumulation using isobaric tags for Mass Spectrometry-Based Proteome Quantification (iTRAQ). Front Physiol, 8, 2017, 251.
Zhang, X., Du, W., Zhang, J., Zou, Z., Ruan, C., High-throughput profiling of diapause regulated genes from Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae). BMC Genomics, 21, 2020, 864.
Güney, G., Toprak, U., Hegedus, D.D., Bayram, Ş., Coutu, C., Bekkaoui, D., Baldwin, D., Heckel, D.G., Hänniger, S., Cedden, D., et al. A look into Colorado potato beetle lipid metabolism through the lens of lipid storage droplet proteins. Insect Biochemistry and Molecular Biology, 133, 2021, 103473.
Chen, Z.-Z., Wang, X., Kong, X., Zhao, Y.-M., Xu, M.-H., Gao, Y.-Q., Huang, H.-Y., Liu, F.-H., Wang, S., Xu, Y.-Y., et al. Quantitative transcriptomic and proteomic analyses reveal the potential maintenance mechanism of female adult reproductive diapause in Chrysoperla nipponensis. Pest Management Science 79 (2023), 1897–1911.
King, B., Li, S., Liu, C., Kim, S.J., Sim, C., Suppression of glycogen synthase expression reduces glycogen and lipid storage during mosquito overwintering diapause. Journal of Insect Physiology, 120, 2020, 103971.
Didion, E.M., Sabree, Z.L., Kenyon, L., Nine, G., Hagan, R.W., Osman, S., Benoit, J.B., Microbiome reduction prevents lipid accumulation during early diapause in the northern house mosquito, Culex pipiens pipiens. J Insect Physiol, 134, 2021, 104295 By artificially disrupting microbiota diversity in female C. pipiens, fat reserves failed to be accumulated during diapause (but not linked gene expression within lipid synthesis pathways). This study highlights that symbiotic interactions and endosymbionts can have a large effect on fat accumulation during diapause.
Le Lann, C., Visser, B., Mériaux, M., Moiroux, J., van Baaren, J., van Alphen, J.J.M., Ellers, J., Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species. Oecologia 174 (2014), 967–977.
Visser, B., Alborn, H.T., Rondeaux, S., Haillot, M., Hance, T., Rebar, D., Riederer, J.M., Tiso, S., van Eldijk, T.J.B., Weissing, F.J., et al. Phenotypic plasticity explains apparent reverse evolution of fat synthesis in parasitic wasps. Sci Rep, 11, 2021, 7751.
Kimura, M.T., Overwintering of reproductively mature females of a pro‐ovigenic parasitic wasp, Leptopilina heterotoma (Hymenoptera: Figitidae). Èntomol Sci 22 (2019), 264–269.
Chen, C., Mahar, R., Merritt, M.E., Denlinger, D.L., Hahn, D.A., ROS and hypoxia signaling regulate periodic metabolic arousal during insect dormancy to coordinate glucose, amino acid, and lipid metabolism. Proc Natl Acad Sci, 118, 2021, e2017603118 The flesh fly Sarcophaga crassipalpis shows sporadic periods of high metabolic activity during its long pupal diapause. Using metabolic screening combined with isotope tracing and artificial manipulation of ROS levels, Chen et al. showed that metabolic bursts were regulated by ROS levels (a decrease in ROS triggers metabolic bursts), relying on the aerobic metabolism of lipids.
Goto, S.G., Yoshida, T., Beppu, K., Kimura, M., Evolution of overwintering strategies in Eurasian species of the Drosophila obscura species group. Biol J Linn Soc 68 (1999), 429–441.
Batz, Z.A., Goff, A.C., Armbruster, P.A., MicroRNAs are differentially abundant during Aedes albopictus diapause maintenance but not diapause induction. Insect Mol Biol 26 (2017), 721–733.
Meuti, M.E., Bautista-Jimenez, R., Reynolds, J.A., Evidence that microRNAs are part of the molecular toolkit regulating adult reproductive diapause in the mosquito, Culex pipiens. PLoS One, 13, 2018, e0203015.
Zhu, W., Zhang, H., Meng, Q., Wang, M., Zhou, G., Li, X., Wang, H., Miao, L., Qin, Q., Zhang, J., Metabolic insights into the cold survival strategy and overwintering of the common cutworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). J Insect Physiol 100 (2017), 53–64.
Pei, J., Xu, Y., Zong, S., Ren, L., Transcriptomic and metabolomic data reveal the key metabolic pathways affecting Streltzoviella insularis (Staudinger) (Lepidoptera: Cossidae) larvae during overwintering. Front Physiol, 12, 2021, 655059.
Begon, M., Temporal variations in the reproductive condition of Drosophila obscura fallén and D. subobscura collin. Oecologia 23 (1976), 31–47.
Enriquez, T., Colinet, H., Cold acclimation triggers lipidomic and metabolic adjustments in the spotted wing drosophila Drosophila suzukii (Matsumara). Am J Physiol-Regul Integr Comp Physiol 316 (2019), R751–R763.
Vukašinović, E.L., Pond, D.W., Grubor-Lajšić, G., Worland, M.R., Kojić, D., Purać, J., Popović, Ž.D., Blagojević, D.P., Temperature adaptation of lipids in diapausing Ostrinia nubilalis: an experimental study to distinguish environmental versus endogenous controls. J Comp Physiol B 188 (2018), 27–36.
Ellers, J., Alphen, J.J.M.V., Sevenster, J.G., A field study of size–fitness relationships in the parasitoid Asobara tabida. J Anim Ecol 67 (1998), 318–324.
Irwin, J.T., Lee, R.E. Jr, Cold winter microenvironments conserve energy and improve overwintering survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis. Oikos 100 (2003), 71–78.
CaraDonna, P.J., Cunningham, J.L., Iler, A.M., Experimental warming in the field delays phenology and reduces body mass, fat content and survival: implications for the persistence of a pollinator under climate change. Funct Ecol 32 (2018), 2345–2356 In a field experiment with a solitary bee (Osmia lignaria), nest temperature was artificially increased (using black boxes), decreased (using white boxes), or unchanged to represent future, past, or current climatic conditions. They found that compared with present temperatures, future climatic conditions decreased fat content and survival of overwintering bees. This exceptional field study shows that there is a major fitness cost for overwintering insect species under a climate change scenario.
Zhao, L., Wang, W., Effects of autumn warming on energy consumption of Diapausing Fall Webworm (Lepidoptera: Arctiidae) Pupae. J Insect Sci, 21, 2021, 8.
Devlin, J.J., Unfried, L., Lecheta, M.C., McCabe, E.A., Gantz, J.D., Kawarasaki, Y., Elnitsky, M.A., Hotaling, S., Michel, A.P., Convey, P., et al. Simulated winter warming negatively impacts survival of Antarctica's only endemic insect. Funct Ecol 36 (2022), 1949–1960 Simulated winter warming decreased survival, carbohydrate, protein, and lipid reserves in the midge Belgica antarctica. This work highlights that an increase in temperature within the range of actual climate warming in Antarctica affects insect physiology. This could have consequences for fitness and population stability of the only endemic insect species in Antarctica.