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Evolution, behavior, and physiology of locust phase polyphenism

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Background

Nineteen grasshopper species are categorized as true locusts because they display intense density-dependent phase polyphenism and form substantial, densely populated swarms of migrating individuals. [1] [2] [3] [4]

Evolution

Phase polyphenism has arisen independently multiple times within the Acrididae family. [1] [5][4] Each locust species has likely developed its own distinct mechanism for undergoing phase transition driven by diverse environmental influences. In-depth examination of behavioral phase shifts is limited to four locust species (Schistocerca gregaria, Schistocerca piceifrons, Locusta migratoria, and Chortoicetes terminifera [6] [7] [8] [9] [10] ). Nevertheless, available evidence indicates that phase change is triggered by extended exposure to visual, olfactory, and/or tactile signals from individuals of the same species, rather than being a result of any indirect influence from high population density or related stressors.[2] Continued research on lesser-known locust species and their closely related non-swarming counterparts, like the Australian plague locust [10] [11][12] and Schistocerca species [5] [13] [14] [15] [16] [8], will expand our comprehension of how and why phase polyphenism has evolved. Additionally, the introduction of increasingly affordable sequencing technologies has enabled us to better understand the molecular mechanisms that drive density-dependent phase polyphenism in diverse locust species.[17] [15] These technologies have facilitated the revelation of several molecular regulatory mechanisms responsible for governing traits associated with different phases. [18] [19] [20]

Behavior

Phase polyphenism

Read about the history of locust phase change research

References

  1. ↑ 1.0 1.1 Song H (2011) Density-dependent phase polyphenism in non-model locusts. Psyche: A Journal of Entomology 2011: 1–16. https://doi.org/10.1155/2011/741769
  2. ↑ 2.0 2.1 Cullen DA, Cease AJ, Latchininsky AV, Ayali A, Berry K, Buhl J, De Keyser R, Foquet B, Hadrich JC, Matheson T, Ott SR, Poot-Pech MA, Robinson BE, Smith JM, Song H, Sword GA, Vanden Broeck J, Verdonck R, Verlinden H, Rogers SM (2017) From molecules to management: mechanisms and consequences of locust phase polyphenism. Advances in Insect Physiology 53: 167–285. https://doi.org/10.1016/bs.aiip.2017.06.002
  3. ↑ Ayali A (2019) The puzzle of locust density-dependent phase polyphenism. Current Opinion in Insect Science 35: 41–47. https://doi.org/10.1016/j.cois.2019.06.008
  4. ↑ 4.0 4.1 Ries MW, Adriaansen C, Aldobai S, Berry K, Bal AB, Catenaccio MC, Cigliano MM, Cullen DA, Deveson T, Diongue A, Foquet B, Hadrich J, Hunter D, Johnson DL, Pablo Karnatz J, Lange CE, Lawton D, Lazar M, Latchininsky AV, Lecoq M, Le Gall M, Lockwood J, Manneh B, Overson R, Peterson BF, Piou C, Poot-Pech MA, Robinson BE, Rogers SM, Song H, Springate S, Therville C, Trumper E, Waters C, Woller DA, Youngblood JP, Zhang L, Cease A (2024) Global perspectives and transdisciplinary opportunities for locust and grasshopper pest management and research. Journal of Orthoptera Research 33(2): 169–216. doi:10.3897/jor.33.112803.
  5. ↑ 5.0 5.1 Song H, Foquet B, Mariño-Pérez R, Woller DA (2017) Phylogeny of locusts and grasshoppers reveals complex evolution of density-dependent phenotypic plasticity. Scientific Reports 7: 6606. https://doi.org/10.1038/s41598-017-07105-y
  6. ↑ Roessingh P, Simpson SJ (1994) The time course of behavioural phase change in nymphs of the desert locust, Schistocerca gregaria. Physiological Entomology 19: 191–197. https://doi.org/10.1111/j.1365-3032.1994.tb01042.x
  7. ↑ Rogers SM, Cullen DA, Anstey ML, Burrows M, Despland E, Dodgson T, Matheson T, Ott SR, Stettin K, Sword GA, Simpson SJ (2014). Rapid behavioural gregarization in the desert locust, Schistocerca gregaria entails synchronous changes in both activity and attraction to conspecifics. Journal of Insect Physiology 65: 9-26. https://doi.org/10.1016/j.jinsphys.2014.04.004
  8. ↑ 8.0 8.1 Foquet B, Little DW, Medina-Durán JH, Song H (2022) The time course of behavioural phase change in the Central American locust Schistocerca piceifrons. Journal of Experimental Biology 225: jeb244621. https://doi.org/10.1242/jeb.244621
  9. ↑ Guo W, Wang X, Ma Z, Xue L, Han J, Yu D, Kang L (2011) CSP and takeout genes modulate the switch between attraction and repulsion during behavioral phase change in the migratory locust. PLoS Genetics 7: e1001291. https://doi.org/10.1371/journal.pgen.1001291
  10. ↑ 10.0 10.1 Gray LJ, Sword GA, Anstey ML, Clissold FJ, Simpson SJ (2009) Behavioural phase polyphenism in the Australian plague locust (Chortoicetes terminifera). Biology Letters 5: 306–309. https://doi.org/10.1098/rsbl.2008.0764
  11. ↑ 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. Journal of Insect Physiology 56: 937–942. https://doi.org/10.1016/j.jinsphys.2010.04.023
  12. ↑ Cullen DA, Sword GA, Simpson SJ (2012) Optimizing multivariate behavioural syndrome models in locusts using automated video tracking. Animal Behaviour 84: 771–784. https://doi.org/10.1016/j.anbehav.2012.06.031
  13. ↑ Kilpatrick, SK, Foquet, B, Castellanos, AA, Gotham, S, Little, DW, and Song, H (2019) Revealing hidden density-dependent phenotypic plasticity in sedentary grasshoppers in the genus Schistocerca Stål (Orthoptera: Acrididae: Crytacantcridinae). Journal of Insect Physiology 118:103937. https://doi.org/10.1016/j.jinsphys.2019.103937
  14. ↑ Pocco M E, Cigliano MM, Foquet B, Lange CE, Nieves EL, Song H (2019) Density-Dependent Phenotypic Plasticity in the South American locust, Schistocerca cancellata (Orthoptera: Acrididae). Annals of the Entomological Society of America 112: 458–472. https://doi.org/10.1093/aesa/saz032
  15. ↑ 15.0 15.1 Foquet B, Castellanos AA, Song H (2021) Comparative analysis of phenotypic plasticity sheds light on the evolution and molecular underpinnings of locust phase polyphenism. Scientific Reports 1: 1–15. https://doi.org/10.1038/s41598-021-91317-w
  16. ↑ Foquet B and Song H (2021) The role of the neuropeptide [His7]-corazonin on phase-related characteristics in the Central American locust. Journal of Insect Physiology 131: 104244. https://doi.org/10.1016/j.jinsphys.2021.104244
  17. ↑ Yang P, Hou L, Wang X, Kang L (2019) Core transcriptional signatures of phase change in the migratory locust. Protein & Cell 10: 883–901. https://doi.org/10.1007/s13238-019-0648-6
  18. ↑ Zhang X, Xu Yn, Chen B, Kang L (2020) Long noncoding RNA PAHAL modulates locust behavioural plasticity through the feedback regulation of dopamine biosynthesis. PLoS Genetics 16: e1008771. https://doi.org/10.1371/journal.pgen.1008771
  19. ↑ Zhao L, Guo W, Jiang F, He J, Liu H, Song J, Yu D, Kang L (2021) Phase-related differences in egg production of the migratory locust regulated by differential oosorption through microRNA-34 targeting activinβ. PLoS Genetics 17: e1009174. https://doi.org/10.1371/journal.pgen.1009174
  20. ↑ Guo W, Song J, Yang P, Chen X, Chen D, Ren D, Kang L, Wang X (2020a) Juvenile hormone suppresses aggregation behavior through influencing antennal gene expression in locusts. PLoS Genetics 16: e1008762. https://doi.org/10.1371/journal.pgen.1008762
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