The Circadian Clock in Lepidoptera

Abstract

With approximately 160,000 identified species of butterflies and moths, Lepidoptera are among the most species-rich and diverse insect orders. Lepidopteran insects have fundamental ecosystem functions as pollinators and valuable food sources for countless animals. Furthermore, Lepidoptera have a significant impact on the economy and global food security because many species in their larval stage are harmful pests of staple food crops. Moreover, domesticated species such as the silkworm Bombyx mori produce silk and silk byproducts that are utilized by the luxury textile, biomedical, and cosmetics sectors. Several Lepidoptera have been fundamental as model organisms for basic biological research, from formal genetics to evolutionary studies. Regarding chronobiology, in the 1970s, Truman’s seminal transplantation experiments on different lepidopteran species were the first to show that the circadian clock resides in the brain. With the implementation of molecular genetics, subsequent studies identified key differences in core components of the molecular circadian clock of Lepidoptera compared to the dipteran Drosophila melanogaster, the dominant insect species in chronobiological research. More recently, studies on the butterfly Danaus plexippus have been fundamental in characterizing the interplay between the circadian clock and navigation during the seasonal migration of this species. Moreover, the advent of Next Generation Omic technologies has resulted in the production of many publicly available datasets regarding circadian clocks in pest and beneficial Lepidoptera. This review presents an updated overview of the molecular and anatomical organization of the circadian clock in Lepidoptera. We report different behavioral circadian rhythms currently identified, focusing on the importance of the circadian clock in controlling developmental, mating and migration phenotypes. We then describe the ecological importance of circadian clocks detailing the complex interplay between the feeding behavior of these organisms and plants. Finally, we discuss how the characterization of these features could be useful in both pest control, and in optimizing rearing of beneficial Lepidoptera.

Circadian Clock Genes Regulate Temperature-Dependent Diapause Induction in Silkworm Bombyx mori

“…Over the years, studies have indicated the oscillating expression of core clock genes in lepidopterans, including various strains of B. mori , and in the monarch butterfly cell line, DpN1 ( Zhu et al, 2008 ; Brady et al, 2021 ). The findings of the present study show that knocking out clock genes of per , tim , Clk , cyc , and cry2 disrupts temperature-dependent diapause induction in silkworms.…”

“…CRY2, a clock factor that forms the core feedback loop, is the major transcriptional repressor of CLK/CYC-mediated transcription, whereas PER is associated with CRY2 stabilization rather than with active transcriptional repression ( Reppert, 2007 ; Zhu et al, 2008 ; Zhan et al, 2011 ). These findings suggest that extensive functional diversity exists among species with regard to cry genes and that clock genes participating in the core feedback loop have been evolutionally selected in insects ( Reppert, 2007 ; Tomioka and Matsumoto, 2015 ; Beer and Helfrich-Forster, 2020 ; Brady et al, 2021 ).…”

“…The circadian clock is involved not only in the daily regulation of several physiological, metabolic, and behavioral activities, including egg hatching and adult eclosion, but also in time-compensated Sun compass navigation, photoperiodism, and dormancy in insects ( Patke et al, 2020 ; Saunders, 2020 ; Ahmad et al, 2021 ; Brady et al, 2021 ). Certain clock gene members drive the core functioning of the circadian clock, forming a transcriptional feedback loop module referred to as the “core feedback loop” ( Hardin, 2011 ).…”

Local adaptation of life cycles in a butterfly is associated with variation in several circadian clock genes

“…It is difficult to say what the effect the deletion may have. The lepidopteran circadian clock is relatively well described at the level of whole protein interactions (Brady et al, 2021; Zhu et al, 2008), and experimental data exist on the function of specific parts of a few circadian proteins (Zhang et al, 2017), but to our knowledge the lepidopteran TIM protein has not yet been studied at this level of mechanistic detail. Results from silk moths show that, at least on an amino acid sequence level, both TIM and PER contain many of the functional domains described in Drosophila (Iwai et al, 2006).…”

“…In Drosophila, the CWO protein acts synergistically with the main period/timeless loop by binding to and repressing several circadian oscillator genes (including tim, per and cwo itself) in the late night, thus forming an essential subloop that helps keep circadian rhytmicity at high amplitude (Kadener et al, 2007;Tomioka & Matsumoto, 2015). While this function has also been inferred in lepidopterans, it has not yet been experimentally confirmed (Brady et al, 2021). Less is known about the function of timeless2 (also known as "mammalian timeless" or timeout), although it appears to help entrain the insect circadian clock to light (Benna et al, 2010), and has been tied to population variation in circadian activity rhythms in rice borer moths (Zhu et al, 2019).…”