Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2019 Feb 26;13:36.
doi: 10.3389/fnbeh.2019.00036. eCollection 2019.

Prolonged Bat Call Exposure Induces a Broad Transcriptional Response in the Male Fall Armyworm ( Spodoptera frugiperda; Lepidoptera: Noctuidae) Brain

Affiliations
Free PMC article

Prolonged Bat Call Exposure Induces a Broad Transcriptional Response in the Male Fall Armyworm ( Spodoptera frugiperda; Lepidoptera: Noctuidae) Brain

Scott D Cinel et al. Front Behav Neurosci. .
Free PMC article

Abstract

Predation risk induces broad behavioral and physiological responses that have traditionally been considered acute and transitory. However, prolonged or frequent exposure to predators and the sensory cues of their presence they broadcast to the environment impact long-term prey physiology and demographics. Though several studies have assessed acute and chronic stress responses in varied taxa, these attempts have often involved a priori expectations of the molecular pathways involved in physiological responses, such as glucocorticoid pathways and neurohormone production in vertebrates. While relatively little is known about physiological and molecular predator-induced stress in insects, many dramatic insect defensive behaviors have evolved to combat selection by predators. For instance, several moth families, such as Noctuidae, include members equipped with tympanic organs that allow the perception of ultrasonic bat calls and facilitate predation avoidance by eliciting evasive aerial flight maneuvers. In this study, we exposed adult male fall armyworm (Spodoptera frugiperda) moths to recorded ultrasonic bat foraging and attack calls for a prolonged period and constructed a de novo transcriptome based on brain tissue from predator cue-exposed relative to control moths kept in silence. Differential expression analysis revealed that 290 transcripts were highly up- or down-regulated among treatment tissues, with many annotating to noteworthy proteins, including a heat shock protein and an antioxidant enzyme involved in cellular stress. Though nearly 50% of differentially expressed transcripts were unannotated, those that were are implied in a broad range of cellular functions within the insect brain, including neurotransmitter metabolism, ionotropic receptor expression, mitochondrial metabolism, heat shock protein activity, antioxidant enzyme activity, actin cytoskeleton dynamics, chromatin binding, methylation, axonal guidance, cilia development, and several signaling pathways. The five most significantly overrepresented Gene Ontology terms included chromatin binding, macromolecular complex binding, glutamate synthase activity, glutamate metabolic process, and glutamate biosynthetic process. As a first assessment of transcriptional responses to ecologically relevant auditory predator cues in the brain of moth prey, this study lays the foundation for examining the influence of these differentially expressed transcripts on insect behavior, physiology, and life history within the framework of predation risk, as observed in ultrasound-sensitive Lepidoptera and other 'eared' insects.

Keywords: Spodoptera frugiperda; bat; moth; neurophysiology; predation; stress; transcriptomics; ultrasound.

Figures

FIGURE 1
FIGURE 1
(A) Principal components plot showing sample clustering based on the first two principal components of variation in log-based counts per million read estimates for both control (C; black circle) and bat-ultrasound exposed (E; gray triangle) Spodoptera frugiperda moths; numbers (1–4) represent replicate samples from each of the control and exposure groups. (B) Principal components plot after surrogate variable analysis was performed to account for unexpected batch effects showing sample clustering based on the first two principal components of variation in log-based counts per million read estimates for both control (C; black circle) and bat-ultrasound exposed (E; gray triangle) adult male Spodoptera frugiperda moths; numbers (1–4) represent replicate samples from each of the control and exposure groups. (C) Transcript expression heatmap detailing the up- (red) and down- (blue) regulation (log2FC) of each transcript relative to the mean expression of the control group across bat-ultrasound exposed (E) adult male Spodoptera frugiperda moths; samples (horizontal axis) and transcripts (vertical axis) are clustered according to expression similarity (stacked multicolored bars).
FIGURE 2
FIGURE 2
(A) The number of differentially expressed transcripts annotated with Gene Ontology terms corresponding to either a molecular function (MF; green bars), biological process (BP; blue bars), or cellular component (CC; yellow bars) in the brains of four adult male fall armyworm (Spodoptera frugiperda) moths exposed to recorded bat foraging and attack calls for 8 h. (B) Pie graph detailing the Kyoto Encyclopedia of Genes and Genomes (KEGG) Orthology annotations associated with differentially expressed transcripts in the male brains of adult fall armyworm moths exposed for 8 h to recorded bat foraging and attack calls.

Similar articles

See all similar articles

References

    1. Abramsky A. Z., Strauss E., Subach A., Kotler B. P., Riechman A., Url S., et al. (2014). International association for ecology the effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus. Oecologia 105 313–319. 10.1007/BF00328733 - DOI - PubMed
    1. Acharya L., McNeil J. N. (1998). Predation risk and mating behavior: the responses of moths to bat-like ultrasound. Behav. Ecol. 9 552–558. 10.1093/beheco/9.6.552 - DOI
    1. Adamo S. A. (2010). Why should an immune response activate the stress response? Insights from the insects (the cricket Gryllus texensis). Brain Behav. Immun. 24 194–200. 10.1016/j.bbi.2009.08.003 - DOI - PubMed
    1. Adamo S. A. (2017a). Stress responses sculpt the insect immune system, optimizing defense in an ever-changing world. Dev. Comp. Immunol. 66 24–32. 10.1016/j.dci.2016.06.005 - DOI - PubMed
    1. Adamo S. A. (2017b). The stress response and immune system share, borrow, and reconfigure their physiological network elements: evidence from the insects. Horm. Behav. 88 25–30. 10.1016/j.yhbeh.2016.10.003 - DOI - PubMed
Feedback