Hostname: page-component-77f85d65b8-2tv5m Total loading time: 0 Render date: 2026-03-27T06:08:22.589Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative genomics reveals evolutionary drivers of the dietary shift in Hemiptera

Published online by Cambridge University Press:  15 December 2023

Guangyao Wu ,
Chunyan Wu ,
Youssef Dewer ,
Peiyao Li ,
Baojun Hao ,
Liansheng Zang  and
Fengqi Li Open the ORCID record for Fengqi Li [Opens in a new window]
Guangyao Wu
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China
Chunyan Wu
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China
Youssef Dewer
Affiliation:
Phytotoxicity Research Department, Central Agricultural Pesticide Laboratory, Agricultural Research Center, Dokki 12618, Giza, Egypt
Peiyao Li
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China
Baojun Hao
Affiliation:
School of Life and Health Science, Kaili University, Guizhou 556000, China
Liansheng Zang
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China
Fengqi Li*
Affiliation:
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Center for R&D of Fine Chemicals of Guizhou University, Guiyang 550025, China
*
Corresponding author: Fengqi Li; Email: fqli@gzu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Hemiptera insects exhibit a close relationship to plants and demonstrate a diverse range of dietary preferences, encompassing phytophagy as the predominant feeding habit while a minority engages in carnivorous or haematophagous behaviour. To counteract the challenges posed by phytophagous insects, plants have developed an array of toxic compounds, causing significant evolutionary selection pressure on these insects. In this study, we employed a comparative genomics approach to analyse the expansion and contraction of gene families specific to phytophagous insect lineages, along with their adaptive evolutionary traits, utilising representative species from the Hemiptera order. Our investigation revealed substantial expansions of gene families within the phytophagous lineages, especially in the Pentatomomorpha branch represented by Oncopeltus fasciatus and Riptortus pedestris. Notably, these expansions of gene families encoding enzymes are potentially involved in hemipteran-plant interactions. Moreover, the adaptive evolutionary analysis of these lineages revealed a higher prevalence of adaptively evolved genes in the Pentatomomorpha branch. The observed branch-specific gene expansions and adaptive evolution likely contribute significantly to the diversification of species within Hemiptera. These results help enhance our understanding of the genomic characteristics of the evolution of different feeding habits in hemipteran insects.

Keywords

adaptive evolutioncomparative genomicsHemipteranOncopeltus fasciatusRiptortus pedestris

Information

Type
Research Paper
Information
Bulletin of Entomological Research , Volume 114 , Issue 1 , February 2024 , pp. 41 - 48
Check for updates
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Armisén, D, Rajakumar, R, Friedrich, M, Benoit, JB, Robertson, HM, Panfilio, KA, Ahn, S-J, Poelchau, MF, Chao, H, Dinh, H, Doddapaneni, HV, Dugan, S, Gibbs, RA, Hughes, DST, Han, Y, Lee, SL, Murali, SC, Muzny, DM, Qu, J, Worley, KC, Munoz-Torres, M, Abouheif, E, Bonneton, F, Chen, T, Chiang, L-M, Childers, CP, Cridge, AG, Crumière, AJJ, Decaras, A, Didion, EM, Duncan, EJ, Elpidina, EN, Favé, M-J, Finet, C, Jacobs, CGC, Cheatle Jarvela, AM, Jennings, EC, Jones, JW, Lesoway, MP, Lovegrove, MR, Martynov, A, Oppert, B, Lillico-Ouachour, A, Rajakumar, A, Refki, PN, Rosendale, AJ, Santos, ME, Toubiana, W, van der Zee, M, Vargas Jentzsch, IM, Lowman, AV, Viala, S, Richards, S and Khila, A (2018) The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water. BMC Genomics 19, 832. https://doi.org/10.1186/s12864-018-5163-2.Google Scholar
Bruen, TC, Philippe, H and Bryant, D (2006) A simple and robust statistical test for detecting the presence of recombination. Genetics 172, 2665–2681.CrossRefGoogle ScholarPubMed
Calla, B (2021) Signatures of selection and evolutionary relevance of cytochrome P450s in plant-insect interactions. Current Opinion in Insect Science 43, 92–96.CrossRefGoogle ScholarPubMed
De Bie, T, Cristianini, N, Demuth, JP and Hahn, MW (2006) CAFE: a computational tool for the study of gene family evolution. Bioinformatics (Oxford, England) 22, 1269–1271.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Emms, DM and Kelly, S (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biology 20, 238.CrossRefGoogle ScholarPubMed
Goldman-Huertas, B, Mitchell, RF, Lapoint, RT, Faucher, CP, Hildebrand, JG and Whiteman, NK (2015) Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. Proceedings of the National Academy of Sciences of the United States of America 112, 3026–3031.CrossRefGoogle ScholarPubMed
Heckel, DG (2012) Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pesticide Biochemistry and Physiology 104, 103–110.CrossRefGoogle Scholar
Heidel-Fischer, HM and Vogel, H (2015) Molecular mechanisms of insect adaptation to plant secondary compounds. Current Opinion in insect Science 8, 8–14.CrossRefGoogle ScholarPubMed
Huang, HJ, Ye, YX, Ye, ZX, Yan, XT, Wang, X, Wei, ZY, Chen, JP, Li, JM, Sun, ZT and Zhang, CX (2021) Chromosome-level genome assembly of the bean bug Riptortus pedestris. Molecular Ecology Resources 21, 2423–2436.CrossRefGoogle ScholarPubMed
Hurst, LD (2009) Fundamental concepts in genetics: genetics and the understanding of selection. Nature Reviews Genetics 10, 83–93.CrossRefGoogle ScholarPubMed
Innan, H and Kondrashov, F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nature Reviews Genetics 11, 97–108.CrossRefGoogle ScholarPubMed
Johnson, KP, Dietrich, CH, Friedrich, F, Beutel, RG, Wipfler, B, Peters, RS, Allen, JM, Petersen, M, Donath, A, Walden, KKO, Kozlov, AM, Podsiadlowski, L, Mayer, C, Meusemann, K, Vasilikopoulos, A, Waterhouse, RM, Cameron, SL, Weirauch, C, Swanson, DR, Percy, DM, Hardy, NB, Terry, I, Liu, S, Zhou, X, Misof, B, Robertson, HM and Yoshizawa, K (2018) Phylogenomics and the evolution of hemipteroid insects. Proceedings of the National Academy of Sciences of the United States of America 115, 12775–12780.CrossRefGoogle ScholarPubMed
Jones, P, Binns, D, Chang, HY, Fraser, M, Li, W, McAnulla, C, McWilliam, H, Maslen, J, Mitchell, A, Nuka, G, Pesseat, S, Quinn, AF, Sangrador-Vegas, A, Scheremetjew, M, Yong, SY, Lopez, R and Hunter, S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics (Oxford, England) 30, 1236–1240.Google ScholarPubMed
Kanehisa, M and Goto, S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28, 27–30.CrossRefGoogle ScholarPubMed
Kanehisa, M, Sato, Y and Morishima, K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. Journal of Molecular Biology 428, 726–731.CrossRefGoogle ScholarPubMed
Kondrashov, FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proceedings. Biological Sciences 279, 5048–5057.Google ScholarPubMed
Li, H, Leavengood, JM Jr., Chapman, EG, Burkhardt, D, Song, F, Jiang, P, Liu, J, Zhou, X and Cai, W (2017) Mitochondrial phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs. Proceedings. Biological Sciences 284, 20171223. https://doi.org/10.1098/rspb.2017.1223.Google Scholar
Liu, Q, Guo, Y, Zhang, Y, Hu, W, Li, Y, Zhu, D, Zhou, Z, Wu, J, Chen, N and Zhou, XN (2019) A chromosomal-level genome assembly for the insect vector for Chagas disease, Triatoma rubrofasciata. Gigascience 8, giz089. https://doi.org/10.1093/gigascience/giz089.CrossRefGoogle ScholarPubMed
McKenna, DD, Scully, ED, Pauchet, Y, Hoover, K, Kirsch, R, Geib, SM, Mitchell, RF, Waterhouse, RM, Ahn, SJ, Arsala, D, Benoit, JB, Blackmon, H, Bledsoe, T, Bowsher, JH, Busch, A, Calla, B, Chao, H, Childers, AK, Childers, C, Clarke, DJ, Cohen, L, Demuth, JP, Dinh, H, Doddapaneni, H, Dolan, A, Duan, JJ, Dugan, S, Friedrich, M, Glastad, KM, Goodisman, MA, Haddad, S, Han, Y, Hughes, DS, Ioannidis, P, Johnston, JS, Jones, JW, Kuhn, LA, Lance, DR, Lee, CY, Lee, SL, Lin, H, Lynch, JA, Moczek, AP, Murali, SC, Muzny, DM, Nelson, DR, Palli, SR, Panfilio, KA, Pers, D, Poelchau, MF, Quan, H, Qu, J, Ray, AM, Rinehart, JP, Robertson, HM, Roehrdanz, R, Rosendale, AJ, Shin, S, Silva, C, Torson, AS, Jentzsch, IM, Werren, JH, Worley, KC, Yocum, G, Zdobnov, EM, Gibbs, RA and Richards, S (2016) Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface. Genome Biology 17, 227.CrossRefGoogle ScholarPubMed
Merzendorfer, H (2014) Chapter One - ABC transporters and their role in protecting insects from pesticides and their metabolites. In Cohen, E (ed.), Advances in Insect Physiology. New York: Academic Press, pp. 1–72.Google Scholar
Panfilio, KA, Vargas Jentzsch, IM, Benoit, JB, Erezyilmaz, D, Suzuki, Y, Colella, S, Robertson, HM, Poelchau, MF, Waterhouse, RM, Ioannidis, P, Weirauch, MT, Hughes, DST, Murali, SC, Werren, JH, Jacobs, CGC, Duncan, EJ, Armisén, D, Vreede, BMI, Baa-Puyoulet, P, Berger, CS, Chang, CC, Chao, H, Chen, MM, Chen, YT, Childers, CP, Chipman, AD, Cridge, AG, Crumière, AJJ, Dearden, PK, Didion, EM, Dinh, H, Doddapaneni, HV, Dolan, A, Dugan, S, Extavour, CG, Febvay, G, Friedrich, M, Ginzburg, N, Han, Y, Heger, P, Holmes, CJ, Horn, T, Hsiao, YM, Jennings, EC, Johnston, JS, Jones, TE, Jones, JW, Khila, A, Koelzer, S, Kovacova, V, Leask, M, Lee, SL, Lee, CY, Lovegrove, MR, Lu, HL, Lu, Y, Moore, PJ, Munoz-Torres, MC, Muzny, DM, Palli, SR, Parisot, N, Pick, L, Porter, ML, Qu, J, Refki, PN, Richter, R, Rivera-Pomar, R, Rosendale, AJ, Roth, S, Sachs, L, Santos, ME, Seibert, J, Sghaier, E, Shukla, JN, Stancliffe, RJ, Tidswell, O, Traverso, L, van der Zee, M, Viala, S, Worley, KC, Zdobnov, EM, Gibbs, RA and Richards, S (2019) Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. Genome Biology 20, 64.CrossRefGoogle ScholarPubMed
Pauchet, Y, Wilkinson, P, Chauhan, R and Ffrench-Constant, RH (2010) Diversity of beetle genes encoding novel plant cell wall degrading enzymes. PLoS One 5, e15635.CrossRefGoogle ScholarPubMed
Ranwez, V, Douzery, EJP, Cambon, C, Chantret, N and Delsuc, F (2018) MACSE v2: toolkit for the alignment of coding sequences accounting for frameshifts and stop codons. Molecular Biology and Evolution 35, 2582–2584.CrossRefGoogle ScholarPubMed
Rider, DA (1996) The true bugs of the world (Hemiptera: Heteroptera). classification and natural history. Annals of the Entomological Society of America 89, 609–610.CrossRefGoogle Scholar
Rijal, JP, Joyce, AL and Gyawaly, S (2021) Biology, ecology, and management of Hemipteran pests in almond orchards in the United States. Journal of Integrated Pest Management 12, 1-14. https://doi.org/10.1093/jipm/pmab018.Google Scholar
Rosenfeld, JA, Reeves, D, Brugler, MR, Narechania, A, Simon, S, Durrett, R, Foox, J, Shianna, K, Schatz, MC, Gandara, J, Afshinnekoo, E, Lam, ET, Hastie, AR, Chan, S, Cao, H, Saghbini, M, Kentsis, A, Planet, PJ, Kholodovych, V, Tessler, M, Baker, R, DeSalle, R, Sorkin, LN, Kolokotronis, S-O, Siddall, ME, Amato, G and Mason, CE (2016) Genome assembly and geospatial phylogenomics of the bed bug Cimex lectularius. Nature Communications 7, 10164. https://doi.org/10.1038/ncomms10164.Google Scholar
Santamaria, ME, Martínez, M, Cambra, I, Grbic, V and Diaz, I (2013) Understanding plant defence responses against herbivore attacks: an essential first step towards the development of sustainable resistance against pests. Transgenic Research 22, 697–708.CrossRefGoogle ScholarPubMed
Seppey, M, Ioannidis, P, Emerson, BC, Pitteloud, C, Robinson-Rechavi, M, Roux, J, Escalona, HE, McKenna, DD, Misof, B, Shin, S, Zhou, X, Waterhouse, RM and Alvarez, N (2019) Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles. Genome Biology 20, 98.CrossRefGoogle ScholarPubMed
Simon, JC, d'Alençon, E, Guy, E, Jacquin-Joly, E, Jaquiéry, J, Nouhaud, P, Peccoud, J, Sugio, A and Streiff, R (2015) Genomics of adaptation to host-plants in herbivorous insects. Briefings in Functional Genomics 14, 413–423.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313.Google ScholarPubMed
Suzek, BE, Wang, Y, Huang, H, McGarvey, PB and Wu, CH (2015) UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics (Oxford, England) 31, 926–932.Google ScholarPubMed
Sweet, MH (1979) On the original feeding habits of the Hemiptera (Insecta). Annals of the Entomological Society of America 72, 575–579.CrossRefGoogle Scholar
Thurmond, J, Goodman, JL, Strelets, VB, Attrill, H, Gramates, LS, Marygold, SJ, Matthews, BB, Millburn, G, Antonazzo, G, Trovisco, V, Kaufman, TC and Calvi, BR (2019) FlyBase 2.0: the next generation. Nucleic Acids Research 47, D759–D765.CrossRefGoogle ScholarPubMed
Tian, T, Liu, Y, Yan, H, You, Q, Yi, X, Du, Z, Xu, W and Su, Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research 45, W122–W129.CrossRefGoogle ScholarPubMed
Voelckel, CJG (2014) Insect-plant interactions. Annual Plant Reviews 47.CrossRefGoogle Scholar
Volonté, M, Traverso, L, Estivalis, JML, Almeida, FC and Ons, S (2022) Comparative analysis of detoxification-related gene superfamilies across five Hemipteran species. BMC Genomics 23, 757.CrossRefGoogle ScholarPubMed
Waterhouse, RM, Seppey, M, Simão, FA, Manni, M, Ioannidis, P, Klioutchnikov, G, Kriventseva, EV and Zdobnov, EM (2018) BUSCO applications from quality assessments to gene prediction and phylogenomics. Molecular Biology and Evolution 35, 543–548.CrossRefGoogle ScholarPubMed
Weirauch, C, Schuh, RT, Cassis, G and Wheeler, WC (2019) Revisiting habitat and lifestyle transitions in Heteroptera (Insecta: Hemiptera): insights from a combined morphological and molecular phylogeny. Cladistics 35, 67–105.CrossRefGoogle ScholarPubMed
Xie, C, Mao, X, Huang, J, Ding, Y, Wu, J, Dong, S, Kong, L, Gao, G, Li, CY and Wei, L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research 39, W316–W322.CrossRefGoogle ScholarPubMed
Yang, Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586–1591.CrossRefGoogle ScholarPubMed
Yazaki, K (2006) ABC transporters involved in the transport of plant secondary metabolites. FEBS Letters 580, 1183–1191.CrossRefGoogle ScholarPubMed
Supplementary material: File

Wu et al. supplementary material

Wu et al. supplementary material
Download Wu et al. supplementary material(File)
File 18.3 KB