Geomagnetic field absence reduces adult body weight of a migratory insect by disrupting feeding behavior and appetite regulation

Abstract

The geomagnetic field (GMF) is well documented for its essential role as a cue used in animal orientation or navigation. Recent evidence indicates that the absence of GMF (mimicked by the near-zero magnetic field, NZMF) can trigger stress-like responses such as reduced body weight, as we have previously shown in the brown planthopper, Nilaparvata lugens. In this study, we found that consistent with the significantly decreased body weight of newly emerged female (−14.67%) and male (−13.17%) adult N. lugens, the duration of the phloem ingestion feeding waveform was significantly reduced by 32.02% in 5th instar nymphs reared under the NZMF versus GMF. Interestingly, 5th instar nymphs that exhibited reduced feeding had significantly higher glucose levels (+16.98% and +20.05%; 24 h and 48 h after molting), which are associated with food aversion, and expression patterns of their appetite-related neuropeptide genes (neuropeptide F, downregulated overall; short neuropeptide F, down-regulated overall; adipokinetic hormone, up-regulated overall; and adipokinetic hormone receptor, down-regulated overall) were also altered under the absence of GMF in a manner consistent with diminishing appetite. Moreover, the expressions of the potential magnetosensor cryptochromes (Crys) were found significantly altered under the absence of GMF, indicating the likely upstream signaling of the Cry-mediated magnetoreception mechanisms. These findings support the hypothesis that strong changes in GMF intensity can reduce adult body weight through affecting insect feeding behavior and underlying regulatory processes including appetite regulation. Our results highlight that GMF could be necessary for the maintenance of energy homeostasis in insects.

Change in geomagnetic field intensity alters migration-associated traits in a migratory insect

“…It is well established that multifunctional Cry are involved in magnetoreception, phototaxis, and the circadian clock [42,43], and developmental changes in Cry1 and Cry2 gene expression associated with extreme variation in the GMF have been observed in N. lugens adults [17,35]. Here, except for Cry1 in males, the expression levels of Crys in both females and males on the first to third days after emergence all varied significantly over time.…”

“…In addition to using GMF for orientation and navigation, animals can also exhibit other physiological and behavioural responses to changes in magnetic field intensity [10][11][12][13][14][15][16][17]. However, few studies have focused on responses of animals to changes in GMF intensity at levels that naturally vary in their environment [13,18].…”

“…However, few studies have focused on responses of animals to changes in GMF intensity at levels that naturally vary in their environment [13,18]. Most studies of the bioeffects of GMF intensity on organisms have been conducted by either shielding or enhancing the GMF intensity, and have highlighted its importance in maintaining homeostasis [14,16,17,19]. Our work with migratory white-backed planthopper, Sogatella furcifera, showed that the absence of GMF could affect the critical migration-related behaviours, including positive phototaxis and flight capacity [10,20].…”

“…Physiological responses to variation in GMF intensity have been demonstrated in N. lugens [17,33]. Notably, the candidate magnetite crystals [34], possible magnetic field targets including Cry1 and Cry2 [35], and the iron-sulfur cluster assembly 1 [36] have all been investigated.…”

Transcriptomic analysis reveals the inhibition of reproduction in rice brown planthopper, Nilaparvata lugens, after silencing the gene of MagR (IscA1)

“…In this study, in order to explore the physiological functions of MagR (IscA1) in insects, the rice brown planthopper (Nilaparvata lugens) was selected as a model insect because of its special feeding habit and magnetic response ability due to the magnetic particles in its abdomen (Chapman et al, 2011;Xie et al, 2011;Yan et al, 2015;Pan et al, 2016;Wan et al, 2020Wan et al, , 2021. The target gene, MagR (NlMagR), was silenced by using RNAi in the brachypterous female adults of N. lugens to investigate the effect of NlMagR on insect reproduction via measuring their fecundity and hatchability.…”