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Evolutionary Applications Volume 12 ,Issue 6 ,2019-04-10
A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta
Xinyue Gu 1 Yan Zhao 1 Yun Su 1 Jiajiao Wu 2 Ziya Wang 1 Juntao Hu 3 , 4 Lijun Liu 1 Zihua Zhao 1 Ary A. Hoffmann 5 Bing Chen 6 Zhihong Li 1
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Received 2018-09-26, accepted for publication 2019-03-07, Published 2019-03-07

Abstract Many insects have the capacity to increase their resistance to high temperatures by undergoing heat hardening at nonlethal temperatures. Although this response is well established, its molecular underpinnings have only been investigated in a few species where it seems to relate at least partly to the expression of heat shock protein (Hsp) genes. Here, we studied the mechanism of hardening and associated transcription responses in larvae of two invasive fruit fly species in China, Bactrocera dorsalis and Bactrocera correcta. Both species showed hardening which increased resistance to 45°C, although the more widespread B. dorsalis hardened better at higher temperatures compared to B. correcta which hardened better at lower temperatures. Transcriptional analyses highlighted expression changes in a number of genes representing different biochemical pathways, but these changes and pathways were inconsistent between the two species. Overall B. dorsalis showed expression changes in more genes than B. correcta. Hsp genes tended to be upregulated at a hardening temperature of 38°C in both species, while at 35°C many Hsp genes tended to be upregulated in B. correcta but not B. dorsalis. One candidate gene (the small heat shock protein gene, Hsp23) with a particularly high level of upregulation was investigated functionally using RNA interference (RNAi). We found that RNAi may be more efficient in B. dorsalis, in which suppression of the expression of this gene removed the hardening response, whereas in B. correcta RNAi did not decrease the hardening response. The different patterns of gene expression in these two species at the two hardening temperatures highlight the diverse mechanisms underlying hardening even in closely related species. These results may provide target genes for future control efforts against such pest species.


thermal adaptation;invasive species;Hsp23;hardening response;expression plasticity


© 2019 John Wiley & Sons Ltd


1. Ary A. Hoffmann.School of BioSciences, Bio21 Institute, University of Melbourne, Parkville, Victoria, Australia.ary@unimelb.edu.au
2. Bing Chen.State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.ary@unimelb.edu.au
3. Zhihong Li.Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China.ary@unimelb.edu.au


Xinyue Gu,Yan Zhao,Yun Su,Jiajiao Wu,Ziya Wang,Juntao Hu,Lijun Liu,Zihua Zhao,Ary A. Hoffmann,Bing Chen,Zhihong Li. A transcriptional and functional analysis of heat hardening in two invasive fruit fly species, Bactrocera dorsalis and Bactrocera correcta. Evolutionary Applications ,Vol.12, Issue 6(2019)



[1] Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., … Wei, L. (2011). KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research, 39(Suppl 2), W316–W322.
[2] Wos, G., & Willi, Y. (2018). Thermal acclimation in Arabidopsis lyrata: Genotypic costs and transcriptional changes. Journal of Evolutionary Biology, 31(1), 123–135.
[3] Myers, S. W., Cancio‐Martinez, E., Hallman, G. J., Fontenot, E. A., & Vreysen, M. J. (2016). Relative tolerance of six Bactrocera (Diptera: Tephritidae) species to phytosanitary cold treatment. Journal of Economic Entomology, 109(6), 2341–2347.
[4] Matsumura, T., Matsumoto, H., & Hayakawa, Y. (2017). Heat stress hardening of oriental armyworms is induced by a transient elevation of reactive oxygen species during sublethal stress. Archives of Insect Biochemistry and Physiology, 96(3). https://doi.org/10.1002/arch.21421
[5] DiDomenico, B. J., Bugaisky, G. E., & Lindquist, S. (1982). Heat shock and recovery are mediated by different translational mechanisms. Proceedings of the National Academy of Sciences, 79(20), 6181–6185. https://doi.org/10.1073/pnas.79.20.6181
[6] Díaz, F., Orobio, R. F., Chavarriaga, P., & Toro‐Perea, N. (2015). Differential expression patterns among heat‐shock protein genes and thermal responses in the whitefly Bemisia tabaci (MEAM 1). Journal of Thermal Biology, 52, 199–207. https://doi.org/10.1016/j.jtherbio.2015.07.004
[7] Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009). Ultrafast and memory‐efficient alignment of short DNA sequences to the human genome. Genome Biology, 10(3), R25. https://doi.org/10.1186/gb-2009-10-3-r25
[8] Malmendal, A., Overgaard, J., Bundy, J. G., Sørensen, J. G., Nielsen, N. C., Loeschcke, V., & Holmstrup, M. (2006). Metabolomic profiling of heat stress: Hardening and recovery of homeostasis in Drosophila. American Journal of Physiology‐Regulatory, Integrative and Comparative Physiology, 291(1), R205–R212.
[9] Diamond, S. E., Chick, L., Perez, A., Strickler, S. A., & Martin, R. A. (2017). Rapid evolution of ant thermal tolerance across an urban‐rural temperature cline. Biological Journal of the Linnean Society, 121(2), 248–257. https://doi.org/10.1093/biolinnean/blw047
[10] Sisodia, S., & Singh, B. N. (2006). Effect of exposure to short‐term heat stress on survival and fecundity in Drosophila ananassae. Canadian Journal of Zoology, 84(6), 895–899.
[11] Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped BLAST and PSI‐BLAST: A new generation of protein database search programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389
[12] Klepsatel, P., Gáliková, M., Maio, N., Huber, C. D., Schlötterer, C., & Flatt, T. (2013). Variation in thermal performance and reaction norms among populations of Drosophila melanogaster. Evolution, 67(12), 3573–3587.
[13] Deng, Y., Li, J., Wu, S., Zhu, Y., Chen, Y., & He, F. (2006). Integrated nr database in protein annotation system and its localization. Computer Engineering, 32(5), 71–74.
[14] Sørensen, J., & Loeschcke, V. (2001). Larval crowding in Drosophila melanogaster induces Hsp70 expression, and leads to increased adult longevity and adult thermal stress resistance. Journal of Insect Physiology, 47(11), 1301–1307. https://doi.org/10.1016/S0022-1910(01)00119-6
[15] Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., … Sherlock, G. (2000). Gene ontology: Tool for the unification of biology. Nature Genetics, 25(1), 25. https://doi.org/10.1038/75556
[16] Sørensen, J. G., Kristensen, T. N., & Loeschcke, V. (2003). The evolutionary and ecological role of heat shock proteins. Ecology Letters, 6(11), 1025–1037. https://doi.org/10.1046/j.1461-0248.2003.00528.x
[17] Manjunatha, H., Rajesh, R., & Aparna, H. (2010). Silkworm thermal biology: A review of heat shock response, heat shock proteins and heat acclimation in the domesticated silkworm, Bombyx mori. Journal of Insect Science, 10(1), 204.
[18] Anders, S., & Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biology, 11(10), R106. https://doi.org/10.1186/gb-2010-11-10-r106
[19] King, A. M., & MacRae, T. H. (2015). Insect heat shock proteins during stress and diapause. Annual Review of Entomology, 60, 59–75. https://doi.org/10.1146/annurev-ento-011613-162107
[20] Yang, Y., & Smith, S. A. (2013). Optimizing de novo assembly of short‐read RNA‐seq data for phylogenomics. BMC Genomics, 14(1), 328. https://doi.org/10.1186/1471-2164-14-328
[21] Schulze, S. K., Kanwar, R., Gölzenleuchter, M., Therneau, T. M., & Beutler, A. S. (2012). SERE: Single‐parameter quality control and sample comparison for RNA‐Seq. BMC Genomics, 13(1), 524. https://doi.org/10.1186/1471-2164-13-524
[22] Hombach, A., Ommen, G., MacDonald, A., & Clos, J. (2014). A small heat shock protein is essential for thermotolerance and intracellular survival of Leishmania donovani. Journal of Cell Science, 127, 4762–4773. https://doi.org/10.1242/jcs.157297
[23] Ron, D., & Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews Molecular Cell Biology, 8(7), 519. https://doi.org/10.1038/nrm2199
[24] Hoffmann, A. A., Sørensen, J. G., & Loeschcke, V. (2003). Adaptation of Drosophila to temperature extremes: Bringing together quantitative and molecular approaches. Journal of Thermal Biology, 28(3), 175–216. https://doi.org/10.1016/S0306-4565(02)00057-8
[25] Shen, G. M., Huang, Y., Jiang, X. Z., Dou, W., & Wang, J. J. (2013). Effect of β‐cypermetherin exposure on the stability of nine housekeeping genes in Bactrocera dorsalis (Diptera: Tephritidae). Florida Entomologist, 442–450.
[26] Alexa, A., & Rahnenfuhrer, J. (2010). topGO: Enrichment analysis for gene ontology. R package version 2.22. Vienna, Austria: R Foundation for Statistical Computing Vienna.
[27] Yuan, S., Kong, Q., Xiao, C., Yang, S., Sun, W., Zhang, J., & Li, Z. (2006). Introduction to two kinds of artificial diets for mass rearing of adult Bactrocera dorsalis (Hendel). Journal of Huazhong Agricultural University, 25, 371–374.
[28] Hoffmann, A. A., & Ross, P. A. (2018). Rates and patterns of laboratory adaptation in (mostly) insects. Journal of Economic Entomology, 111(2), 501–509. https://doi.org/10.1093/jee/toy024
[29] Reitz, S. R., & Trumble, J. T. (2002). Competitive displacement among insects and arachnids. Annual Review of Entomology, 47(1), 435–465. https://doi.org/10.1146/annurev.ento.47.091201.145227
[30] Hallman, G. J., Myers, S. W., El‐Wakkad, M. F., Tadrous, M. D., & Jessup, A. J. (2013). Development of phytosanitary cold treatments for oranges infested with Bactrocera invadens and Bactrocera zonata (Diptera: Tephritidae) by comparison with existing cold treatment schedules for Ceratitis capitata (Diptera: Tephritidae). Journal of Economic Entomology, 106(4), 1608–1612.
[31] Zizzari, Z. V., & Ellers, J. (2011). Effects of exposure to short‐term heat stress on male reproductive fitness in a soil arthropod. Journal of Insect Physiology, 57(3), 421–426. https://doi.org/10.1016/j.jinsphys.2011.01.002
[32] Malewski, T., Bogdanowicz, W., Durska, E., Łoś, M., Kamiński, M., & Kowalewska, K. (2015). Expression profiling of heat shock genes in a scuttle fly Megaselia scalaris (Diptera, Phoridae). Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 323(10), 704–713.
[33] Li, B., & Dewey, C. N. (2011). RSEM: Accurate transcript quantification from RNA‐Seq data with or without a reference genome. BMC Bioinformatics, 12(1), 323. https://doi.org/10.1186/1471-2105-12-323
[34] De Meyer, M., Robertson, M. P., Mansell, M. W., Ekesi, S., Tsuruta, K., Mwaiko, W., … Peterson, A. T. (2010). Ecological niche and potential geographic distribution of the invasive fruit fly Bactrocera invadens (Diptera, Tephritidae). Bulletin of Entomological Research, 100(1), 35–48. https://doi.org/10.1017/S0007485309006713
[35] Sørensen, J. G., Nielsen, M. M., Kruhøffer, M., Justesen, J., & Loeschcke, V. (2005). Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress & Chaperones, 10(4), 312–328. https://doi.org/10.1379/CSC-128R1.1
[36] Delpuech, J. M., Moreteau, B., Chiche, J., Pla, E., Vouidibio, J., & David, J. R. (1995). Phenotypic plasticity and reaction norms in temperate and tropical populations of Drosophila melanogaster: Ovarian size and developmental temperature. Evolution, 49(4), 670–675.
[37] Li, Y., Wu, Y., Chen, H., Wu, J., & Li, Z. (2012). Population structure and colonization of Bactrocera dorsalis (Diptera: Tephritidae) in China, inferred from mtDNA COI sequences. Journal of Applied Entomology, 136(4), 241–251. https://doi.org/10.1111/j.1439-0418.2011.01636.x
[38] David, J. R., Gibert, P., Gravot, E., Petavy, G., Morin, J. P., Karan, D., & Moreteau, B. (1997). Phenotypic plasticity and developmental temperature in Drosophila: Analysis and significance of reaction norms of morphometrical traits. Journal of Thermal Biology, 22(6), 441–451. https://doi.org/10.1016/S0306-4565(97)00063-6
[39] Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739. https://doi.org/10.1093/molbev/msr121
[40] Tatusov, R. L., Galperin, M. Y., Natale, D. A., & Koonin, E. V. (2000). The COG database: A tool for genome‐scale analysis of protein functions and evolution. Nucleic Acids Research, 28(1), 33–36. https://doi.org/10.1093/nar/28.1.33
[41] Lux, S. A., Copeland, R. S., White, I. M., Manrakhan, A., & Billah, M. K. (2003). A new invasive fruit fly species from the Bactrocera dorsalis (Hendel) group detected in East Africa. International Journal of Tropical Insect Science, 23(4), 355–361. https://doi.org/10.1017/S174275840001242X
[42] Malacrida, A., Gomulski, L., Bonizzoni, M., Bertin, S., Gasperi, G., & Guglielmino, C. (2007). Globalization and fruitfly invasion and expansion: The medfly paradigm. Genetica, 131(1), 1147. https://doi.org/10.1007/s10709-006-9117-2
[43] Pieterse, W., Terblanche, J. S., & Addison, P. (2017). Do thermal tolerances and rapid thermal responses contribute to the invasion potential of Bactrocera dorsalis (Diptera: Tephritidae)? Journal of Insect Physiology, 98, 1147–6.
[44] Li, R., Li, Y., Kristiansen, K., & Wang, J. (2008). SOAP: Short oligonucleotide alignment program. Bioinformatics, 24(5), 713–714. https://doi.org/10.1093/bioinformatics/btn025
[45] Vayssières, J. F., Carel, Y., Coubes, M., & Duyck, P. F. (2008). Development of immature stages and comparative demography of two cucurbit‐attacking fruit flies in Reunion Island: Bactrocera cucurbitae and Dacus ciliatus (Diptera Tephritidae). Environmental Entomology, 37(2), 307–314.
[46] Żwirowski, S., Kłosowska, A., Obuchowski, I., Nillegoda, N. B., Piróg, A., Ziętkiewicz, S., … Liberek, K. (2017). Hsp70 displaces small heat shock proteins from aggregates to initiate protein refolding. EMBO Journal, 36(6), 783–796. https://doi.org/10.15252/embj.201593378
[47] Qin, Y., Ni, W., Wu, J., Zhao, Z., Chen, H., & Li, Z. (2015). The potential geographic distribution of Bactrocera correcta (Diptera: Tephrididae) in China based on eclosion rate model. Applied Entomology and Zoology, 50(3), 371–381.
[48] Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., … Regev, A. (2013). De novo transcript sequence reconstruction from RNA‐seq using the Trinity platform for reference generation and analysis. Nature Protocols, 8(8), 1494. https://doi.org/10.1038/nprot.2013.084
[49] Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., … Regev, A. (2011). Full‐length transcriptome assembly from RNA‐Seq data without a reference genome. Nature Biotechnology, 29(7), 644–652. https://doi.org/10.1038/nbt.1883
[50] Qin, Y., Paini, D. R., Wang, C., Fang, Y., & Li, Z. (2015). Global establishment risk of economically important fruit fly species (Tephritidae). PLoS ONE, 10(1), e0116424.
[51] Guo, S., Zhao, Z., Liu, L., Li, Z., & Shen, J. (2018). Comparative transcriptome analyses uncover key candidate genes mediating flight capacity in Bactrocera dorsalis (Hendel) and Bactrocera correcta (Bezzi) (Diptera: Tephritidae). International Journal of Molecular Sciences, 19(2), 396.
[52] Barshis, D. J., Ladner, J. T., Oliver, T. A., Seneca, F. O., Traylor‐Knowles, N., & Palumbi, S. R. (2013). Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences, 110(4), 1387–1392. https://doi.org/10.1073/pnas.1210224110
[53] Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
[54] Gibert, P., Hill, M., Pascual, M., Plantamp, C., Terblanche, J. S., Yassin, A., & Sgrò, C. M. (2016). Drosophila as models to understand the adaptive process during invasion. Biological Invasions, 18(4), 1089–1103. https://doi.org/10.1007/s10530-016-1087-4
[55] Bennett, A. F., & Lenski, R. E. (2007). An experimental test of evolutionary trade‐offs during temperature adaptation. Proceedings of the National Academy of Sciences, 104(suppl 1), 8649–8654. https://doi.org/10.1073/pnas.0702117104
[56] Bettencourt, B. R., Hogan, C. C., Nimali, M., & Drohan, B. W. (2008). Inducible and constitutive heat shock gene expression responds to modification of Hsp70 copy number in Drosophila melanogaster but does not compensate for loss of thermotolerance in Hsp70 null flies. BMC Biology, 6(1), 5. https://doi.org/10.1186/1741-7007-6-5
[57] Li, Z. W., Li, X., Yu, Q. Y., Xiang, Z. H., Kishino, H., & Zhang, Z. (2009). The small heat shock protein (sHSP) genes in the silkworm, Bombyx mori, and comparative analysis with other insect sHSP genes. BMC Evolutionary Biology, 9(1), 215. https://doi.org/10.1186/1471-2148-9-215
[58] Permpoon, R., Aketarawong, N., & Thanaphum, S. (2011). Isolation and characterization of Doublesex homologues in the Bactrocera species: B. dorsalis (Hendel) and B. correcta (Bezzi) and their putative promoter regulatory regions. Genetica, 139(1), 113–127.
[59] Liu, H., Zhang, C., Hou, B. H., Ou‐Yang, G. C., & Ma, J. (2017). Interspecific competition between Ceratitis capitata and two Bactrocera spp. (Diptera: Tephritidae) evaluated via adult behavioral interference under laboratory conditions. Journal of Economic Entomology, 110(3), 1145–1155.
[60] Chen, B., & Wagner, A. (2012). Hsp90 is important for fecundity, longevity, and buffering of cryptic deleterious variation in wild fly populations. BMC Evolutionary Biology, 12(1), 25. https://doi.org/10.1186/1471-2148-12-25
[61] Fu, L., Niu, B., Zhu, Z., Wu, S., & Li, W. (2012). CD‐HIT: Accelerated for clustering the next‐generation sequencing data. Bioinformatics, 28(23), 3150–3152. https://doi.org/10.1093/bioinformatics/bts565
[62] Papadopoulos, N. T. (2008). Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). In (Ed.), Encyclopedia of Entomology (pp. 2318–2322). Dordrecht, The Netherlands: Springer.
[63] Liu, H., Hou, B., Zhang, C., He, R., Liang, F., Gu, M., … Ma, J. (2014). Oviposition preference and offspring performance of the oriental fruit fly Bactrocera dorsalis and guava fruit fly B. correcta (Diptera: Tephritidae) on six host fruits. Acta Ecologica Sinica, 9, 2274–2281.
[64] Chen, B., Feder, M. E., & Kang, L. (2018). Evolution of heat‐shock protein expression underlying adaptive responses to environmental stress. Molecular Ecology, 27(15), 3040–3054. https://doi.org/10.1111/mec.14769
[65] Liu, X., Jin, Y., & Ye, H. (2013). Recent spread and climatic ecological niche of the invasive guava fruit fly, Bactrocera correcta, in mainland China. Journal of Pest Science, 86(3), 449–458. https://doi.org/10.1007/s10340-013-0488-8
[66] Overgaard, J., Sørensen, J. G., Com, E., & Colinet, H. (2014). The rapid cold hardening response of Drosophila melanogaster: Complex regulation across different levels of biological organization. Journal of Insect Physiology, 62, 46–53. https://doi.org/10.1016/j.jinsphys.2014.01.009
[67] Borchel, A., Komisarczuk, A. Z., Rebl, A., Goldammer, T., & Nilsen, F. (2018). Systematic identification and characterization of stress‐inducible heat shock proteins (HSPs) in the salmon louse (Lepeophtheirus salmonis). Cell Stress and Chaperones, 23(1), 127–139. https://doi.org/10.1007/s12192-017-0830-9
[68] Ghalambor, C. K., McKay, J. K., Carroll, S. P., & Reznick, D. N. (2007). Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21(3), 394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x
[69] Huerta‐Cepas, J., Szklarczyk, D., Forslund, K., Cook, H., Heller, D., Walter, M. C., … Kuhn, M. (2015). eggNOG 4.5: A hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Research, 44(D1), D286–D293.
[70] Wang, L., Feng, Z., Wang, X., Wang, X., & Zhang, X. (2009). DEGseq: An R package for identifying differentially expressed genes from RNA‐seq data. Bioinformatics, 26(1), 136–138. https://doi.org/10.1093/bioinformatics/btp612
[71] Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., & Hattori, M. (2004). The KEGG resource for deciphering the genome. Nucleic Acids Research, 32(suppl_1), D277–D280. https://doi.org/10.1093/nar/gkh063
[72] Jang, E. B. (1991). Thermal death kinetics and heat tolerance in early and late third instars of the oriental fruit fly (Diptera: Tephritidae). Journal of Economic Entomology, 84(4), 1298–1303. https://doi.org/10.1093/jee/84.4.1298
[73] Wang, H.‐J., Shi, Z.‐K., Shen, Q.‐D., Xu, C.‐D., Wang, B., Meng, Z.‐J., … Wang, S. U. (2017). Molecular cloning and induced expression of six small heat shock proteins mediating cold‐hardiness in Harmonia axyridis (Coleoptera: Coccinellidae). Frontiers in Physiology, 8, 60. https://doi.org/10.3389/fphys.2017.00060
[74] Kawasaki, F., Koonce, N. L., Guo, L., Fatima, S., Qiu, C., Moon, M. T., … Ordway, R. W. (2016). Small heat shock proteins mediate cell‐autonomous and‐nonautonomous protection in a Drosophila model for environmental‐stress‐induced degeneration. Disease Models & Mechanisms, 9(9), 953–964.
[75] Vázquez, D. P., Gianoli, E., Morris, W. F., & Bozinovic, F. (2017). Ecological and evolutionary impacts of changing climatic variability. Biological Reviews, 92(1), 22–42. https://doi.org/10.1111/brv.12216
[76] Bahrndorff, S., Loeschcke, V., Pertoldi, C., Beier, C., & Holmstrup, M. (2009). The rapid cold hardening response of Collembola is influenced by thermal variability of the habitat. Functional Ecology, 23(2), 340–347.
[77] Weldon, C. W., Nyamukondiwa, C., Karsten, M., Chown, S. L., & Terblanche, J. S. (2018). Geographic variation and plasticity in climate stress resistance among southern African populations of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Scientific Reports, 8(1), 9849. https://doi.org/10.1038/s41598-018-28259-3
[78] Bairoch, A., Apweiler, R., Wu, C. H., Barker, W. C., Boeckmann, B., Ferro, S., … Martin, M. J. (2005). The universal protein resource (UniProt). Nucleic Acids Research, 33(suppl_1), D154–D159.
[79] Finn, R. D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R. Y., Eddy, S. R., … Mistry, J. (2013). Pfam: The protein families database. Nucleic Acids Research, 42(D1), D222–D230.
[80] Clarke, A. (2003). Costs and consequences of evolutionary temperature adaptation. Trends in Ecology & Evolution, 18(11), 573–581. https://doi.org/10.1016/j.tree.2003.08.007
[81] Overgaard, J., Kristensen, T. N., Mitchell, K. A., & Hoffmann, A. A. (2011). Thermal tolerance in widespread and tropical Drosophila species: Does phenotypic plasticity increase with latitude? American Naturalist, 178(S1), S80–S96.
[82] Bahrndorff, S., Mariën, J., Loeschcke, V., & Ellers, J. (2009). Dynamics of heat‐induced thermal stress resistance and hsp70 expression in the springtail, Orchesella cincta. Functional Ecology, 23(2), 233–239.
[83] Liu, X., & Ye, H. (2009). Effect of temperature on development and survival of Bactrocera correcta (Diptera: Tephritidae). Scientific Research and Essay, 4(5), 467–472.
[84] Lockwood, B. L., Julick, C. R., & Montooth, K. L. (2017). Maternal loading of a small heat shock protein increases embryo thermal tolerance in Drosophila melanogaster. Journal of Experimental Biology, 220(23), 4492–4501.
[85] Dahlgaard, J., Loeschcke, V., Michalak, P., & Justesen, J. (1998). Induced thermotolerance and associated expression of the heat‐shock protein Hsp70 in adult Drosophila melanogaster. Functional Ecology, 12(5), 786–793. https://doi.org/10.1046/j.1365-2435.1998.00246.x
[86] Nyamukondiwa, C., Terblanche, J. S., Marshall, K. E., & Sinclair, B. J. (2011). Basal cold but not heat tolerance constrains plasticity among Drosophila species (Diptera: Drosophilidae). Journal of Evolutionary Biology, 24(9), 1927–1938. https://doi.org/10.1111/j.1420-9101.2011.02324.x
[87] Lu, Y., Bai, Q., Zheng, X., & Lu, Z. (2017). Expression and enzyme activity of catalase in Chilo suppressalis (Lepidoptera: Crambidae) is responsive to environmental stresses. Journal of Economic Entomology, 110(4), 1803–1812. https://doi.org/10.1093/jee/tox117
[88] Dou, W., Tian, Y., Liu, H., Shi, Y., Smagghe, G., & Wang, J. J. (2017). Characteristics of six small heat shock protein genes from Bactrocera dorsalis: Diverse expression under conditions of thermal stress and normal growth. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 213, 8–16. https://doi.org/10.1016/j.cbpb.2017.07.005
[89] Nyamukondiwa, C., Kleynhans, E., & Terblanche, J. S. (2010). Phenotypic plasticity of thermal tolerance contributes to the invasion potential of Mediterranean fruit flies (Ceratitis capitata). Ecological Entomology, 35(5), 565–575. https://doi.org/10.1111/j.1365-2311.2010.01215.x
[90] Ferreira, J., & Zwinderman, A. (2006). On the Benjamini‐Hochberg method. Annals of Statistics, 34(4), 1827–1849. https://doi.org/10.1214/009053606000000425
[91] Colinet, H., Lee, S. F., & Hoffmann, A. (2010). Functional characterization of the Frost gene in Drosophila melanogaster: Importance for recovery from chill coma. PLoS ONE, 5(6), e10925. https://doi.org/10.1371/journal.pone.0010925
[92] Hu, J. T., Chen, B., & Li, Z. H. (2014). Thermal plasticity is related to the hardening response of heat shock protein expression in two Bactrocera fruit flies. Journal of Insect Physiology, 67, 105–113. https://doi.org/10.1016/j.jinsphys.2014.06.009
[93] Willot, Q., Gueydan, C., & Aron, S. (2017). Proteome stability, heat hardening and heat‐shock protein expression profiles in Cataglyphis desert ants. Journal of Experimental Biology, 220(9), 1721–1728.
[94] Huang, H. J., Xue, J., Zhuo, J. C., Cheng, R. L., Xu, H. J., & Zhang, C. X. (2017). Comparative analysis of the transcriptional responses to low and high temperatures in three rice planthopper species. Molecular Ecology, 26(10), 2726–2737. https://doi.org/10.1111/mec.14067
[95] Wellband, K. W., & Heath, D. D. (2017). Plasticity in gene transcription explains the differential performance of two invasive fish species. Evolutionary Applications, 10(6), 563–576. https://doi.org/10.1111/eva.12463
[96] Huang, L. H., & Kang, L. (2007). Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Molecular Biology, 16(4), 491–500. https://doi.org/10.1111/j.1365-2583.2007.00744.x
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