1932
0

Annual Review of Entomology

Volume 70, 2025

Phenotypic Plasticity in Locusts: Trade-Off Between Migration and Reproduction

  • Xiaojiao Guo1 and Le Kang1,2
  • 1State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China; email: [email protected], [email protected] 2Institute of Life Science and Green Development/College of Life Science, Hebei University, Baoding, China
  • Vol. 70:23-44 (Volume publication date January 2025)
  • First published as a Review in Advance on September 03, 2024
  • Copyright © 2025 by the author(s).
    This work is licensed under a Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See credit lines of images or other third-party material in this article for license information.

Abstract

Locusts exhibit phenotypic plasticity in response to population density changes, with distinct phenotypes in the solitary and gregarious phases. In the past decade, many studies have revealed the molecular mechanisms underlying phase changes, which include the change of body coloration, pheromones, behavior, flight, fecundity, immunity, and aging. Our understanding of the molecular mechanisms related to these phenotypic differences has expanded in breadth and depth with the decoding of the locust genome, involving transcriptional, post-transcriptional, translational, and epigenetic regulation. Large-scale regulation networks composed of genes and noncoding RNAs reflect the systematic modifications of the locust phase transition in response to environmental changes. Gene manipulation techniques have verified the functions of specific genes and related pathways in phase changes. This review highlights the latest advances in studies of locust phase changes and suggests that the divergence of energy and metabolism allocation in gregarious and solitary locusts is an adaptive strategy for long-distance migration and local reproduction, respectively. Finally, we propose future research directions and discuss emerging questions in the area of phenotypic plasticity of locusts.

Keyword(s): behavior, dopamine, noncoding RNAs, phase change, phenylalanine, pheromone
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-013124-124333
2025-01-28
2025-06-21
Loading full text...

Full text loading...

/deliver/fulltext/ento/70/1/annurev-ento-013124-124333.html?itemId=/content/journals/10.1146/annurev-ento-013124-124333&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alessi AM, O'Connor V, Aonuma H, Newland PL. 2014.. Dopaminergic modulation of phase reversal in desert locusts. . Front. Behav. Neurosci. 8::371
     [Crossref] [Google Scholar]
  2. 2.
    Boerjan B, Sas F, Ernst UR, Tobback J, Lemière F, et al. 2011.. Locust phase polyphenism: Does epigenetic precede endocrine regulation?. Gen. Comp. Endocr. 173::120–28
     [Crossref] [Google Scholar]
  3. 3.
    Boerjan W, Ralph J, Baucher M. 2003.. Lignin biosynthesis. . Annu. Rev. Plant Biol. 54::519–46
     [Crossref] [Google Scholar]
  4. 4.
    Burrows M. 2016.. Development and deposition of resilin in energy stores for locust jumping. . J. Exp. Biol. 219::2449–57
     [Google Scholar]
  5. 5.
    Cassau S, Sander D, Karcher T, Laue M, Hause G, et al. 2022.. The sensilla-specific expression and subcellular localization of SNMP1 and SNMP2 reveal novel insights into their roles in the antenna of the desert locust Schistocerca gregaria. . Insects 13::579
     [Crossref] [Google Scholar]
  6. 6.
    Chang H, Cassau S, Krieger J, Guo X, Knaden M, et al. 2023.. A chemical defense deters cannibalism in migratory locusts. . Science 380::537–43 6. Found that a density-dependent pheromone plays pivotal roles in deterring conspecific cannibalism during locust aggregation.
     [Crossref] [Google Scholar]
  7. 7.
    Chang HT, Unni AP, Tom MT, Cao Q, Liu Y, et al. 2023.. Odorant detection in a locust exhibits unusually low redundancy. . Curr. Biol. 33::5427–38.e5
     [Crossref] [Google Scholar]
  8. 8.
    Chen B, Li SQ, Ren Q, Tong XW, Zhang X, Kang L. 2015.. Paternal epigenetic effects of population density on locust phase-related characteristics associated with heat-shock protein expression. . Mol. Ecol. 24::851–62
     [Crossref] [Google Scholar]
  9. 9.
    Chen B, Tong X, Zhang X, Gui W, Ai G, et al. 2022.. Sulfation modification of dopamine in brain regulates aggregative behavior of animals. . Natl. Sci. Rev. 9::nwab163
     [Crossref] [Google Scholar]
  10. 10.
    Chen D, Hou L, Wei J, Guo S, Cui W, et al. 2022.. Aggregation pheromone 4-vinylanisole promotes the synchrony of sexual maturation in female locusts. . eLife 11::e74581
     [Crossref] [Google Scholar]
  11. 11.
    Chen Q, He J, Ma C, Yu D, Kang L. 2015.. Syntaxin 1A modulates the sexual maturity rate and progeny egg size related to phase changes in locusts. . Insect Biochem. Mol. Biol. 56::1–8
     [Crossref] [Google Scholar]
  12. 12.
    Chen S, Yang P, Jiang F, Wei Y, Ma Z, Kang L. 2010.. De novo analysis of transcriptome dynamics in the migratory locust during the development of phase traits. . PLOS ONE 5::e15633
     [Crossref] [Google Scholar]
  13. 13.
    Clynen E, Huybrechts J, Verleyen P, De Loof A, Schoofs L. 2006.. Annotation of novel neuropeptide precursors in the migratory locust based on transcript screening of a public EST database and mass spectrometry. . BMC Genom. 7::201
     [Crossref] [Google Scholar]
  14. 14.
    Cui W, Ge J, Chen D, Nie X, Dong L, et al. 2024.. Dibutyl phthalate released by solitary female locusts mediates sexual communication at low density. . PNAS 121:(30):e2401926121
     [Crossref] [Google Scholar]
  15. 15.
    Cullen DA, Cease AJ, Latchininsky AV, Ayali A, Berry K, et al. 2017.. From molecules to management: mechanisms and consequences of locust phase polyphenism. . Adv. Insect Physiol. 53::167–285
     [Crossref] [Google Scholar]
  16. 16.
    Cullen DA, Sword GA, Dodgson T, Simpson SJ. 2010.. Behavioural phase change in the Australian plague locust, Chortoicetes terminifera, is triggered by tactile stimulation of the antennae. . J. Insect Physiol. 56::937–42
     [Crossref] [Google Scholar]
  17. 17.
    Cullen DA, Sword GA, Rosenthal GG, Simpson SJ, Dekempeneer E, et al. 2022.. Sexual repurposing of juvenile aposematism in locusts. . PNAS 119::e2200759119
     [Crossref] [Google Scholar]
  18. 18.
    Daubner SC, Le T, Wang S. 2011.. Tyrosine hydroxylase and regulation of dopamine synthesis. . Arch. Biochem. Biophys. 508::1–12
     [Crossref] [Google Scholar]
  19. 19.
    Despland E, Simpson SJ. 2005.. Food choices of solitarious and gregarious locusts reflect cryptic and aposematic antipredator strategies. . Anim. Behav. 69::471–79
     [Crossref] [Google Scholar]
  20. 20.
    Despland E, Simpson SJ. 2006.. Resource distribution mediates synchronization of physiological rhythms in locust groups. . Proc. R. Soc. B 273::1517–22
     [Crossref] [Google Scholar]
  21. 21.
    Dillen S, Verdonck R, Zels S, Van Wielendaele P, Vanden Broeck J. 2014.. Identification of the short neuropeptide F precursor in the desert locust: evidence for an inhibitory role of sNPF in the control of feeding. . Peptides 53::134–39
     [Crossref] [Google Scholar]
  22. 22.
    Dillon RJ, Webster G, Weightman AJ, Charnley AK. 2010.. Diversity of gut microbiota increases with aging and starvation in the desert locust. . Antonie Van Leeuwenhoek 97::69–77
     [Crossref] [Google Scholar]
  23. 23.
    Ding D, Zhang J, Du BZ, Wang XZ, Hou L, et al. 2022.. Non-canonical function of an Hif-1α splice variant contributes to the sustained flight of locusts. . eLife 11::e74554
     [Crossref] [Google Scholar]
  24. 24.
    Du B, Ding D, Ma C, Guo W, Kang L. 2022.. Locust density shapes energy metabolism and oxidative stress resulting in divergence of flight traits. . PNAS 119::e2115753118 24. Provides direct evidence for the divergence of locust flight traits.
     [Crossref] [Google Scholar]
  25. 25.
    Falckenhayn C, Boerjan B, Raddatz G, Frohme M, Schoofs L, Lyko F. 2013.. Characterization of genome methylation patterns in the desert locust Schistocerca gregaria. . J. Exp. Biol. 216::1423–29
     [Google Scholar]
  26. 26.
    Feng YJ, Ge Y, Tan SQ, Zhang KQ, Ji R, Shi WP. 2015.. Effect of Paranosema locustae (Microsporidia) on the behavioural phases of Locusta migratoria (Orthoptera: Acrididae) in the laboratory. . Biocontrol Sci. Technol. 25::48–55
     [Crossref] [Google Scholar]
  27. 27.
    Foquet B, Song H. 2021.. The role of the neuropeptide [His7]-corazonin on phase-related characteristics in the Central American locust. . J. Insect Physiol. 131::104244
     [Crossref] [Google Scholar]
  28. 28.
    Galili G, Amir R, Fernie AR. 2016.. The regulation of essential amino acid synthesis and accumulation in plants. . Annu. Rev. Plant Biol. 67::153–78
     [Crossref] [Google Scholar]
  29. 29.
    Golov Y, Rillich J, Douek M, Harari AR, Ayali A. 2018.. Sexual behavior of the desert locust during intra- and inter-phase interactions. . J. Insect Behav. 31::629–41
     [Crossref] [Google Scholar]
  30. 30.
    Golov Y, Rillich J, Harari A, Ayali A. 2018.. Precopulatory behavior and sexual conflict in the desert locust. . PeerJ 6::e4356
     [Crossref] [Google Scholar]
  31. 31.
    Gordon SD, Windmill JF. 2015.. Hearing ability decreases in ageing locusts. . J. Exp. Biol. 218::1990–94
     [Google Scholar]
  32. 32.
    Gospocic J, Shields EJ, Glastad KM, Lin Y, Penick CA, et al. 2017.. The neuropeptide corazonin controls social behavior and caste identity in ants. . Cell 170::748–59.e12
     [Crossref] [Google Scholar]
  33. 33.
    Gray LJ, Sword GA, Anstey ML, Clissold FJ, Simpson SJ. 2009.. Behavioural phase polyphenism in the Australian plague locust (Chortoicetes terminifera). . Biol. Lett. 5::306–9
     [Crossref] [Google Scholar]
  34. 34.
    Guo M, Krieger J, Grosse-Wilde E, Missbach C, Zhang L, Breer H. 2014.. Variant ionotropic receptors are expressed in olfactory sensory neurons of coeloconic sensilla on the antenna of the desert locust (Schistocerca gregaria). . Int. J. Biol. Sci. 10::1–14
     [Crossref] [Google Scholar]
  35. 35.
    Guo S, Hou L, Dong L, Nie X, Kang L, Wang X. 2023.. PLIN2-induced ectopic lipid accumulation promotes muscle ageing in gregarious locusts. . Nat. Ecol. Evol. 7::914–26
     [Crossref] [Google Scholar]
  36. 36.
    Guo S, Jiang F, Yang P, Liu Q, Wang X, Kang L. 2016.. Characteristics and expression patterns of histone-modifying enzyme systems in the migratory locust. . Insect Biochem. Mol. Biol. 76::18–28
     [Crossref] [Google Scholar]
  37. 37.
    Guo SY, Yang PC, Liang B, Zhou F, Hou L, et al. 2021.. Aging features of the migratory locust at physiological and transcriptional levels. . BMC Genom. 22::257
     [Crossref] [Google Scholar]
  38. 38.
    Guo W, Ren D, Zhao LF, Jiang F, Song J, et al. 2018.. Identification of odorant-binding proteins (OBPs) and functional analysis of phase-related OBPs in the migratory locust. . Front. Physiol. 9::984
     [Crossref] [Google Scholar]
  39. 39.
    Guo W, Song J, Yang PC, Chen XY, Chen DF, et al. 2020.. Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts. . PLOS Genet. 16::e1008762
     [Crossref] [Google Scholar]
  40. 40.
    Guo W, Wang X, Ma Z, Xue L, Han J, et al. 2011.. CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. . PLOS Genet. 7::5657–63
     [Google Scholar]
  41. 41.
    Guo X, Ma Z, Du B, Li T, Li W, et al. 2018.. Dop1 enhances conspecific olfactory attraction by inhibiting miR-9a maturation in locusts. . Nat. Commun. 9::1193 41. Found that miRNAs act as key messengers in GPCR signaling during the locust behavioral phase change.
     [Crossref] [Google Scholar]
  42. 42.
    Guo X, Ma Z, Kang L. 2015.. Two dopamine receptors play different roles in phase change of the migratory locust. . Front. Behav. Neurosci. 9::80
     [Crossref] [Google Scholar]
  43. 43.
    Guo X, Yu Q, Chen D, Wei J, Yang P, et al. 2020.. 4-Vinylanisole is an aggregation pheromone in locusts. . Nature 584::584–88 43. Identifies the true aggregation pheromone in the migratory locust through multilevel assays.
     [Crossref] [Google Scholar]
  44. 44.
    Hassanali A, Njagi PG, Bashir MO. 2005.. Chemical ecology of locusts and related acridids. . Annu. Rev. Entomol. 50::223–45
     [Crossref] [Google Scholar]
  45. 45.
    He J, Chen Q, Wei Y, Jiang F, Yang M, et al. 2016.. MicroRNA-276 promotes egg-hatching synchrony by up-regulating brm in locusts. . PNAS 113::584–89 45. Found that miRNA-mediated upregulation of genes regulates egg-hatching synchrony to guarantee the high density of offspring.
     [Crossref] [Google Scholar]
  46. 46.
    He J, Kang L. 2024.. Regulation of insect behavior by non-coding RNAs. . Sci. China Life Sci. 67::110618
     [Crossref] [Google Scholar]
  47. 47.
    He J, Zhu YN, Wang B, Yang P, Guo W, et al. 2022.. piRNA-guided intron removal from pre-mRNAs regulates density-dependent reproductive strategy. . Cell Rep. 39::110593
     [Crossref] [Google Scholar]
  48. 48.
    Hiroyoshi S, Mitsunaga T, Ganaha-Kikumura T, Reddy GVP. 2021.. Effects of age, phase variation and pheromones on male sperm storage in the desert locust, Schistocerca gregaria. . Insects 12::642
     [Crossref] [Google Scholar]
  49. 49.
    Hiroyoshi S, Mitsunaga T, Reddy GVP. 2022.. The association of the development of the internal reproductive organs of male desert locusts, Schistocerca gregaria (Orthoptera: Acrididae), with age, phase and the effect of exposure to pheromones. . Eur. J. Entomol. 119::300–8
     [Crossref] [Google Scholar]
  50. 50.
    Hou L, Guo S, Wang Y, Nie X, Yang P, et al. 2021.. Neuropeptide ACP facilitates lipid oxidation and utilization during long-term flight in locusts. . eLife 10::e65279
     [Crossref] [Google Scholar]
  51. 51.
    Hou L, Guo SY, Wang YY, Liu SY, Wang XH. 2024.. Neuropeptide ACP is required for fat body lipid metabolism homeostasis in locusts. . Insect Sci. In press
    [Google Scholar]
  52. 52.
    Hou L, Jiang F, Yang PC, Wang XH, Kang L. 2015.. Molecular characterization and expression profiles of neuropeptide precursors in the migratory locust. . Insect Biochem. Mol. Biol. 63::63–71
     [Crossref] [Google Scholar]
  53. 53.
    Hou L, Li BB, Ding D, Kang L, Wang XH. 2019.. CREB-B acts as a key mediator of NPF/NO pathway involved in phase-related locomotor plasticity in locusts. . PLOS Genet. 15::e1008176
     [Crossref] [Google Scholar]
  54. 54.
    Hou L, Wang XS, Yang PC, Li BB, Lin Z, et al. 2020.. DNA methyltransferase 3 participates in behavioral phase change in the migratory locust. . Insect Biochem. Mol. Biol. 121::103374
     [Crossref] [Google Scholar]
  55. 55.
    Hou L, Yang P, Jiang F, Liu Q, Wang X, Kang L. 2017.. The neuropeptide F/nitric oxide pathway is essential for shaping locomotor plasticity underlying locust phase transition. . eLife 6::e22526
     [Crossref] [Google Scholar]
  56. 56.
    Huang X, Li Q, Xu Y, Li A, Wang S, et al. 2024.. A neural m6A pathway regulates behavioral aggregation in migratory locusts. . Sci. China Life Sci. 67::124254
     [Crossref] [Google Scholar]
  57. 57.
    Jiang F, Liu Q, Wang Y, Zhang J, Wang H, et al. 2017.. Comparative genomic analysis of SET domain family reveals the origin, expansion, and putative function of the arthropod-specific SmydA genes as histone modifiers in insects. . Gigascience 6::1–16
     [Crossref] [Google Scholar]
  58. 58.
    Jiang XC, Krieger J, Breer H, Pregitzer P. 2017.. Distinct subfamilies of odorant binding proteins in locust (Orthoptera, Acrididae): molecular evolution, structural variation, and sensilla-specific expression. . Front. Physiol. 8::734
     [Crossref] [Google Scholar]
  59. 59.
    Kang XL, Yang ML, Cui XS, Wang HM, Kang L. 2023.. Spatially differential regulation of ATF2 phosphorylation contributes to warning coloration of gregarious locusts. . Sci. Adv. 9:. https://doi.org/10.1126/sciadv.adi5168
    [Google Scholar]
  60. 60.
    Kelly SA, Panhuis TM, Stoehr AM. 2012.. Phenotypic plasticity: molecular mechanisms and adaptive significance. . Compr. Physiol. 2::1417–39
     [Crossref] [Google Scholar]
  61. 61.
    Lavy O, Gophna U, Gefen E, Ayali A. 2019.. The effect of density-dependent phase on the locust gut bacteria composition. . Front. Microbiol. 9::3020
     [Crossref] [Google Scholar]
  62. 62.
    Lavy O, Lewin-Epstein O, Bendett Y, Gophna U, Gefen E, et al. 2022.. Microbiome-related aspects of locust density-dependent phase transition. . Environ. Microbiol. 24::507–16
     [Crossref] [Google Scholar]
  63. 63.
    Leal WS. 2013.. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. . Annu. Rev. Entomol. 58::373–91
     [Crossref] [Google Scholar]
  64. 64.
    Li AM, Yin Y, Zhang YX, Zhang L, Zhang KQ, et al. 2020.. Effects of Paranosema iocustae (Microsporidia) on the development and morphological phase transformation of Locusta migratoria (Orthoptera: Acrididae) through modulation of the neurotransmitter taurine. . J. Integr. Agric. 19::204–10
     [Crossref] [Google Scholar]
  65. 65.
    Li J, Wei L, Wang Y, Zhang H, Yang P, et al. 2023.. Cytosolic and mitochondrial ribosomal proteins mediate the locust phase transition via divergence of translational profiles. . PNAS 120::e2216851120 65. Sheds light on the molecular mechanisms underlying locust phase transition to translational levels.
     [Crossref] [Google Scholar]
  66. 66.
    Li T, Chen B, Yang P, Wang D, Du B, Kang L. 2020.. Long non-coding RNA derived from lncRNA-mRNA co-expression networks modulates the locust phase change. . Genom. Proteom. Bioinform. 18::664–78
     [Crossref] [Google Scholar]
  67. 67.
    Li Y, Zhang J, Chen DF, Yang PC, Jiang F, et al. 2016.. CRISPR/Cas9 in locusts: successful establishment of an olfactory deficiency line by targeting the mutagenesis of an odorant receptor co-receptor (Orco). . Insect Biochem. Mol. Biol. 79::27–35
     [Crossref] [Google Scholar]
  68. 68.
    Livingstone MS, Tempel BL. 1983.. Genetic dissection of monoamine neurotransmitter synthesis in Drosophila. . Nature 303::67–70
     [Crossref] [Google Scholar]
  69. 69.
    Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M. 2001.. Biological control of locusts and grasshoppers. . Annu. Rev. Entomol. 46::667–702
     [Crossref] [Google Scholar]
  70. 70.
    Ma Z, Guo W, Guo X, Wang X, Kang L. 2011.. Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. . PNAS 108::3882–87
     [Crossref] [Google Scholar]
  71. 71.
    Ma Z, Guo X, Lei H, Li T, Hao S, Kang L. 2015.. Octopamine and tyramine respectively regulate attractive and repulsive behavior in locust phase changes. . Sci. Rep. 5::8036
     [Crossref] [Google Scholar]
  72. 72.
    Ma Z, Guo X, Liu J. 2020.. Translocator protein mediates olfactory repulsion. . FASEB J. 34::513–24
     [Crossref] [Google Scholar]
  73. 73.
    Ma Z, Liu J, Guo X. 2019.. A retinal-binding protein mediates olfactory attraction in the migratory locusts. . Insect Biochem. Mol. Biol. 114::103214
     [Crossref] [Google Scholar]
  74. 74.
    Maeno K, Tanaka S. 2008.. Maternal effects on progeny size, number and body color in the desert locust, Schistocerca gregaria: density- and reproductive cycle-dependent variation. . J. Insect Physiol. 54::1072–80
     [Crossref] [Google Scholar]
  75. 75.
    Maeno KO, Piou C, Ghaout S. 2020.. The desert locust, Schistocerca gregaria, plastically manipulates egg size by regulating both egg numbers and production rate according to population density. . J. Insect Physiol. 122::104020
     [Crossref] [Google Scholar]
  76. 76.
    Maeno KO, Piou C, Ghaout S. 2022.. Allocation of more reproductive resource to egg size rather than clutch size of gregarious desert locust (Schistocerca gregaria) through increasing oogenesis period and oosorption rate. . J. Insect Physiol. 136::104331
     [Crossref] [Google Scholar]
  77. 77.
    Maeno KO, Piou C, Lemenager N. 2023.. Egg size-dependent embryonic development in the desert locust, Schistocerca gregaria. . J. Insect Physiol. 145::104467
     [Crossref] [Google Scholar]
  78. 78.
    Maeno KO, Piou C, Ould Ely S, Ould Mohamed S, Jaavar MEH, et al. 2021.. Density-dependent mating behaviors reduce male mating harassment in locusts. . PNAS 118::e2104673118 78. Provides field evidence on differential mating behaviors between gregarious and solitary locusts.
     [Crossref] [Google Scholar]
  79. 79.
    Mallon EB, Amarasinghe HE, Ott SR. 2016.. Acute and chronic gregarisation are associated with distinct DNA methylation fingerprints in desert locusts. . Sci. Rep. 6::35608
     [Crossref] [Google Scholar]
  80. 80.
    Monastirioti M, Linn CE, White K. 1996.. Characterization of Drosophila tyramine β-hydroxylase gene and isolation of mutant flies lacking octopamine. . J. Neurosci. 16::3900–11
     [Crossref] [Google Scholar]
  81. 81.
    Neve KA. 2010.. The Dopamine Receptors. Berlin:: Springer
     [Google Scholar]
  82. 82.
    Niassy A, Torto B, Njagi PGN, Hassanali A, Obeng-Ofori D, Ayertey JN. 1999.. Intra- and interspecific aggregation responses of Locusta migratoria migratorioides and Schistocerca gregaria and a comparison of their pheromone emissions. . J. Chem. Ecol. 25::1029–42
     [Crossref] [Google Scholar]
  83. 83.
    Nishide Y, Tanaka S. 2016.. Desert locust, Schistocerca gregaria, eggs hatch in synchrony in a mass but not when separated. . Behav. Ecol. Sociobiol. 70::1507–15
     [Crossref] [Google Scholar]
  84. 84.
    Njagi PGN, Torto B, Obeng-Ofori D, Hassanali A. 1996.. Phase-independent responses to phase-specific aggregation pheromone in adult desert locusts, Schistocerca gregaria (Orthoptera: Acrididae). . Physiol. Entomol. 21::131–37
     [Crossref] [Google Scholar]
  85. 85.
    Parle E, Taylor D. 2017.. The effect of aging on the mechanical behaviour of cuticle in the locust Schistocerca gregaria. . J. Mech. Behav. Biomed. Mater. 68::247–51
     [Crossref] [Google Scholar]
  86. 86.
    Pelosi P, Calvello M, Ban LP. 2005.. Diversity of odorant-binding proteins and chemosensory proteins in insects. . Chem. Senses 30::i291–92
     [Crossref] [Google Scholar]
  87. 87.
    Pelosi P, Iovinella I, Zhu J, Wang G, Dani FR. 2018.. Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. . Biol. Rev. Camb. Philos. Soc. 93::184–200
     [Crossref] [Google Scholar]
  88. 88.
    Pener MP. 1991.. Locust phase polymorphism and its endocrine relations. . Adv. Insect Physiol. 23::1–79
     [Crossref] [Google Scholar]
  89. 89.
    Pener MP, Simpson SJ. 2009.. Locust phase polyphenism: an update. . Adv. Insect Physiol. 36::1–272
     [Crossref] [Google Scholar]
  90. 90.
    Pregitzer P, Jiang X, Lemke RS, Krieger J, Fleischer J, Breer H. 2019.. A subset of odorant receptors from the desert locust Schistocerca gregaria is co-expressed with the sensory neuron membrane protein 1. . Insects 10::350
     [Crossref] [Google Scholar]
  91. 91.
    Pregitzer P, Jiang XC, Grosse-Wilde E, Breer H, Krieger J, Fleischer J. 2017.. In search for pheromone receptors: Certain members of the odorant receptor family in the desert locust Schistocerca gregaria (Orthoptera: Acrididae) are co-expressed with SNMP1. . Int. J. Biol. Sci. 13::911–22
     [Crossref] [Google Scholar]
  92. 92.
    Rajapakse S, Qu D, Ahmed AS, Rickers-Haunerland J, Haunerland NH. 2019.. Effects of FABP knockdown on flight performance of the desert locust, Schistocerca gregaria. . J. Exp. Biol. 222::jeb203455
     [Crossref] [Google Scholar]
  93. 93.
    Richard G, Le Trionnaire G, Danchin E, Sentis A. 2019.. Epigenetics and insect polyphenism: mechanisms and climate change impacts. . Curr. Opin. Insect Sci. 35::138–45
     [Crossref] [Google Scholar]
  94. 94.
    Robinson KL, Tohidi-Esfahani D, Lo N, Simpson SJ, Sword GA. 2011.. Evidence for widespread genomic methylation in the migratory locust, Locusta migratoria (Orthoptera: Acrididae). . PLOS ONE 6::e28167
     [Crossref] [Google Scholar]
  95. 95.
    Robinson KL, Tohidi-Esfahani D, Ponton F, Simpson SJ, Sword GA, Lo N. 2016.. Alternative migratory locust phenotypes are associated with differences in the expression of genes encoding the methylation machinery. . Insect Mol. Biol. 25::105–15
     [Crossref] [Google Scholar]
  96. 96.
    Roessingh P, Bouaichi A, Simpson SJ. 1998.. Effects of sensory stimuli on the behavioural phase state of the desert locust, Schistocerca gregaria. . J. Insect Physiol. 44::883–93
     [Crossref] [Google Scholar]
  97. 97.
    Roessingh P, Simpson SJ. 1994.. The time-course of behavioral phase change in nymphs of the desert locust, Schistocerca gregaria. . Physiol. Entomol. 19::191–97
     [Crossref] [Google Scholar]
  98. 98.
    Rogers SM, Cullen DA, Anstey ML, Burrows M, Despland E, et al. 2014.. Rapid behavioural gregarization in the desert locust, Schistocerca gregaria entails synchronous changes in both activity and attraction to conspecifics. . J. Insect Physiol. 65::9–26
     [Crossref] [Google Scholar]
  99. 99.
    Rogers SM, Ott SR. 2015.. Differential activation of serotonergic neurons during short- and long-term gregarization of desert locusts. . Proc. Biol. Sci. 282::20142062
     [Google Scholar]
  100. 100.
    Rogers SM, Riley J, Brighton C, Sutton GP, Cullen DA, Burrows M. 2016.. Increased muscular volume and cuticular specialisations enhance jump velocity in solitarious compared with gregarious desert locusts, Schistocerca gregaria. . J. Exp. Biol. 219::635–48
     [Crossref] [Google Scholar]
  101. 101.
    Rytkönen KT, Storz JF. 2011.. Evolutionary origins of oxygen sensing in animals. . EMBO Rep. 12::3–4
     [Crossref] [Google Scholar]
  102. 102.
    Sakamoto H, Tanaka S, Hata T. 2019.. Identification of vibrational signals emitted by embryos of the migratory locust Locusta migratoria (Orthoptera: Acrididae) that induce synchronous hatching. . Eur. J. Entomol. 116::258–68
     [Crossref] [Google Scholar]
  103. 103.
    Shi WP, Guo Y, Xu C, Tan SQ, Miao J, et al. 2014.. Unveiling the mechanism by which microsporidian parasites prevent locust swarm behavior. . PNAS 111::1343–48
     [Crossref] [Google Scholar]
  104. 104.
    Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C, et al. 2016.. Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. . Science 351::aac6633
     [Crossref] [Google Scholar]
  105. 105.
    Simpson SJ, Despland E, Hagele BF, Dodgson T. 2001.. Gregarious behavior in desert locusts is evoked by touching their back legs. . PNAS 98::3895–97
     [Crossref] [Google Scholar]
  106. 106.
    Song H. 2005.. Phylogenetic perspectives on the evolution of locust phase polyphenism. . J. Orthoptera Res. 14::235–45
     [Crossref] [Google Scholar]
  107. 107.
    Song H. 2011.. Density-dependent phase polyphenism in nonmodel locusts: a minireview. . Psyche 2011::741769
     [Google Scholar]
  108. 108.
    Song H, Wenzel JW. 2008.. Phylogeny of bird-grasshopper subfamily Cyrtacanthacridinae (Orthoptera: Acrididae) and the evolution of locust phase polyphenism. . Cladistics 24::515–42
     [Crossref] [Google Scholar]
  109. 109.
    Su CY, Menuz K, Carlson JR. 2009.. Olfactory perception: receptors, cells, and circuits. . Cell 139::45–59
     [Crossref] [Google Scholar]
  110. 110.
    Sugahara R, Tanaka S. 2018.. Environmental and hormonal control of body color polyphenism in late-instar desert locust nymphs: role of the yellow protein. . Insect Biochem. Mol. 93::27–36
     [Crossref] [Google Scholar]
  111. 111.
    Sultan SE, Stearns SC. 2005.. Environmentally contingent variation: phenotypic plasticity and norms of reaction. . Variation 2005::303–32
     [Crossref] [Google Scholar]
  112. 112.
    Sword GA, Simpson SJ, El Hadi OTM, Wilps H. 2000.. Density-dependent aposematism in the desert locust. . Proc. R. Soc. B 267::63–68
     [Crossref] [Google Scholar]
  113. 113.
    Tanaka S. 2000.. The role of [His7]-corazonin in the control of body-color polymorphism in the migratory locust, Locusta migratoria (Orthoptera: Acrididae). . J. Insect Physiol. 46::1169–76
     [Crossref] [Google Scholar]
  114. 114.
    Tanaka S. 2001.. Endocrine mechanisms controlling body-color polymorphism in locusts. . Arch. Insect Biochem. 47::139–49
     [Crossref] [Google Scholar]
  115. 115.
    Tanaka S. 2006.. Corazonin and locust phase polyphenism. . Appl. Entomol. Zool. 41::179–93
     [Crossref] [Google Scholar]
  116. 116.
    Tanaka S, Harano K, Nishide Y. 2012.. Re-examination of the roles of environmental factors in the control of body-color polyphenism in solitarious nymphs of the desert locust Schistocerca gregaria with special reference to substrate color and humidity. . J. Insect Physiol. 58::89–101
     [Crossref] [Google Scholar]
  117. 117.
    Tanaka S, Nishide Y. 2013.. Behavioral phase shift in nymphs of the desert locust, Schistocerca gregaria: special attention to attraction/avoidance behaviors and the role of serotonin. . J. Insect Physiol. 59::101–12
     [Crossref] [Google Scholar]
  118. 118.
    Toga K, Yokoi K, Bono H. 2022.. Meta-analysis of transcriptomes in insects showing density-dependent polyphenism. . Insects 13::864
     [Crossref] [Google Scholar]
  119. 119.
    Tong X, Wang Y, Yang P, Wang C, Kang L. 2020.. Tryptamine accumulation caused by deletion of MrMao-1 in Metarhizium genome significantly enhances insecticidal virulence. . PLOS Genet. 16::e1008675
     [Crossref] [Google Scholar]
  120. 120.
    Tong XW, Wang YD, Li J, Hu S, Yang PC, Kang L. 2021.. Transformation of glycerate kinase (GLYK) into Metarhizium acridum increases virulence to locust. . Pest Manag. Sci. 77::1465–75
     [Crossref] [Google Scholar]
  121. 121.
    Torto B, Obeng-Ofori D, Njagi PGN, Hassanali A, Amiani H. 1994.. Aggregation pheromone system of adult gregarious desert locust Schistocerca gregaria (Forskal). . J. Chem. Ecol. 20::1749–62
     [Crossref] [Google Scholar]
  122. 122.
    Uvarov BP. 1921.. A revision of the genus Locusta L. (= Pachytylus Fieb.), with a new theory as to the periodicity and migrations of locusts. . Bull. Entomol. Res. Lond. 12::135–63
     [Crossref] [Google Scholar]
  123. 123.
    Uvarov SB. 1966.. Grasshoppers and Locusts: A Handbook of General Acridology, Vol. I: Anatomy, Physiology, Development, Phase Polymorphism, Introduction to Taxonomy. London:: Cent. Overseas Pest Res.
     [Google Scholar]
  124. 124.
    Uvarov BP. 1977.. Grasshoppers and Locusts. A Handbook of General Acridology, Vol. 2: Behaviour, Ecology, Biogeography, Population Dynamics. London:: Cent. Overseas Pest Res.
     [Google Scholar]
  125. 125.
    Van Wielendaele P, Dillen S, Zels S, Badisco L, Vanden Broeck J. 2013.. Regulation of feeding by Neuropeptide F in the desert locust. . Insect Biochem. Mol. 43::102–14
     [Crossref] [Google Scholar]
  126. 126.
    Veenstra JA. 2014.. The contribution of the genomes of a termite and a locust to our understanding of insect neuropeptides and neurohormones. . Front. Physiol. 5::454
     [Crossref] [Google Scholar]
  127. 127.
    Verlinden H. 2018.. Dopamine signalling in locusts and other insects. . Insect Biochem. Mol. Biol. 97::40–52
     [Crossref] [Google Scholar]
  128. 128.
    Verlinden H, Sterck L, Li J, Li Z, Yssel A, et al. 2020.. First draft genome assembly of the desert locust, Schistocerca gregaria. . F1000Research 9::775
     [Crossref] [Google Scholar]
  129. 129.
    Verlinden H, Vleugels R, Marchal E, Badisco L, Pflüger HJ, et al. 2010.. The role of octopamine in locusts and other arthropods. . J. Insect Physiol. 56::854–67
     [Crossref] [Google Scholar]
  130. 130.
    Wang HM, Jiang F, Liu X, Liu Q, Fu YY, et al. 2022.. Piwi/piRNAs control food intake by promoting neuropeptide F expression in locusts. . EMBO Rep. 23::e50851
     [Crossref] [Google Scholar]
  131. 131.
    Wang X, Fang X, Yang P, Jiang X, Jiang F, et al. 2014.. The locust genome provides insight into swarm formation and long-distance flight. . Nat. Commun. 5::2957
     [Crossref] [Google Scholar]
  132. 132.
    Wang X, Kang L. 2014.. Molecular mechanisms of phase change in locusts. . Annu. Rev. Entomol. 59::225–44
     [Crossref] [Google Scholar]
  133. 133.
    Wang Y, Jiang F, Wang H, Song T, Wei Y, et al. 2015.. Evidence for the expression of abundant microRNAs in the locust genome. . Sci. Rep. 5::13608
     [Crossref] [Google Scholar]
  134. 134.
    Wang YD, Tong XW, Yuan SL, Yang PC, Li L, et al. 2022.. Variation of TNF modulates cellular immunity of gregarious and solitary locusts against fungal pathogen Metarhizium anisopliae. . PNAS 119::e2120835119
     [Crossref] [Google Scholar]
  135. 135.
    Wang YD, Yang PC, Cui F, Kang L. 2013.. Altered immunity in crowded locust reduced fungal (Metarhizium anisopliae) pathogenesis. . PLOS Pathog. 9::e1003102
     [Crossref] [Google Scholar]
  136. 136.
    Wang YL, Yang ML, Jiang F, Zhang JZ, Kang L. 2013.. MicroRNA-dependent development revealed by RNA interference-mediated gene silencing of LmDicer1 in the migratory locust. . Insect. Sci. 20::53–60
     [Crossref] [Google Scholar]
  137. 137.
    Wang ZF, Yang PC, Chen DF, Jiang F, Li Y, et al. 2015.. Identification and functional analysis of olfactory receptor family reveal unusual characteristics of the olfactory system in the migratory locust. . Cell Mol. Life Sci. 72::4429–43
     [Crossref] [Google Scholar]
  138. 138.
    Wei JN, Shao WB, Cao MM, Ge J, Yang PC, et al. 2019.. Phenylacetonitrile in locusts facilitates an antipredator defense by acting as an olfactory aposematic signal and cyanide precursor. . Sci. Adv. 5::eaav5495 138. Provides new insights into the crucial roles of PAN in antipredator defense during locust aggregation.
     [Crossref] [Google Scholar]
  139. 139.
    Wei JN, Shao WB, Wang XH, Ge J, Chen XY, et al. 2017.. Composition and emission dynamics of migratory locust volatiles in response to changes in developmental stages and population density. . Insect. Sci. 24::60–72
     [Crossref] [Google Scholar]
  140. 140.
    Wei YY, Chen S, Yang PC, Ma ZY, Kang L. 2009.. Characterization and comparative profiling of the small RNA transcriptomes in two phases of locust. . Genome Biol. 10::R6
     [Crossref] [Google Scholar]
  141. 141.
    Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL. 2002.. Coping with crowds: density-dependent disease resistance in desert locusts. . PNAS 99::5471–75
     [Crossref] [Google Scholar]
  142. 142.
    Yang J, Yu Q, Yu J, Kang L, Guo X. 2023.. 4-Vinylanisole promotes conspecific interaction and acquisition of gregarious behavior in the migratory locust. . PNAS 120::e2306659120
     [Crossref] [Google Scholar]
  143. 143.
    Yang M, Du B, Xu L, Wang H, Wang Y, et al. 2023.. Glutamate-GABA imbalance mediated by miR-8-5p and its STTM regulates phase-related behavior of locusts. . PNAS 120::e2215660120
     [Crossref] [Google Scholar]
  144. 144.
    Yang M, Wang Y, Liu Q, Liu Z, Jiang F, et al. 2019.. A β-carotene-binding protein carrying a red pigment regulates body-color transition between green and black in locusts. . eLife 8::e41362 144. Shows that a density-dependent color scheme perfectly fits the principle of three primary colors.
     [Crossref] [Google Scholar]
  145. 145.
    Yang ML, Wang YL, Jiang F, Song TQ, Wang HM, et al. 2016.. miR-71 and miR-263 jointly regulate target genes chitin synthase and chitinase to control locust molting. . PLOS Genet. 12::e1006257
     [Crossref] [Google Scholar]
  146. 146.
    Yang ML, Wei YY, Jiang F, Wang YL, Guo XJ, et al. 2014.. MicroRNA-133 inhibits behavioral aggregation by controlling dopamine synthesis in locusts. . PLOS Genet. 10::e1004206 146. The first study on miRNA function in locust behavioral phase change.
     [Crossref] [Google Scholar]
  147. 147.
    Yang P, Hou L, Wang X, Kang L. 2019.. Core transcriptional signatures of phase change in the migratory locust. . Protein Cell 10::883–901
     [Crossref] [Google Scholar]
  148. 148.
    Zhang L, Lecoq M, Latchininsky A, Hunter D. 2019.. Locust and grasshopper management. . Annu. Rev. Entomol. 64::15–34
     [Crossref] [Google Scholar]
  149. 149.
    Zhang S, Li J, Zhang D, Zhang Z, Meng S, et al. 2023.. miR-252 targeting temperature receptor CcTRPM to mediate the transition from summer-form to winter-form of Cacopsylla chinensis. . eLife 12::RP88744
     [Crossref] [Google Scholar]
  150. 150.
    Zhang X, Xu Y, Chen B, Kang L. 2020.. Long noncoding RNA PAHAL modulates locust behavioural plasticity through the feedback regulation of dopamine biosynthesis. . PLOS Genet. 16::e1008771
     [Crossref] [Google Scholar]
  151. 151.
    Zhang X, Zhu YN, Chen B, Kang L. 2022.. A Gypsy element contributes to the nuclear retention and transcriptional regulation of the resident lncRNA in locusts. . RNA Biol. 19::206–20
     [Crossref] [Google Scholar]
  152. 152.
    Zhang Y, Wang XH, Kang L. 2011.. A k-mer scheme to predict piRNAs and characterize locust piRNAs. . Bioinformatics 27::771–76
     [Crossref] [Google Scholar]
  153. 153.
    Zhang ZQ, Yang Q, Zhao J, Chang B, Liu XK. 2019.. Kinematic synthesis method for the one-degree-of-freedom jumping leg mechanism of a locust-inspired robot. . Sci. China Technol. Sci. 63::472–87
     [Crossref] [Google Scholar]
  154. 154.
    Zhao LF, Guo W, Jiang F, He J, Liu HR, et al. 2021.. Phase-related differences in egg production of the migratory locust regulated by differential oosorption through microRNA-34 targeting activinβ. . PLOS Genet. 17::e1009174
     [Crossref] [Google Scholar]
  155. 155.
    Zhou F, Kang L, Wang XH. 2020.. JumpDetector: an automated monitoring equipment for the locomotion of jumping insects. . Insect. Sci. 27::613–24
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-ento-013124-124333
Loading
Phenotypic Plasticity in Locusts: Trade-Off Between Migration and Reproduction
Annual Review of Entomology 70, 23 (2025); https://doi.org/10.1146/annurev-ento-013124-124333
/content/journals/10.1146/annurev-ento-013124-124333
/content/journals/10.1146/annurev-ento-013124-124333
Loading

Data & Media loading...

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error