The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens

Abstract The insect circadian clock synchronizes daily activities, such as feeding, eclosion, and mating to diurnal light:dark cycles, while the photoperiodic clock synchronizes development and reproduction to the appropriate season. Despite mounting evidence that the circadian and photoperiodic tim...

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Main Authors: Matthew Wolkoff, Mizuki Yoshida, Taylor Lowmiller, Cheolho Sim, Megan E. Meuti
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-06637-y
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author Matthew Wolkoff
Mizuki Yoshida
Taylor Lowmiller
Cheolho Sim
Megan E. Meuti
author_facet Matthew Wolkoff
Mizuki Yoshida
Taylor Lowmiller
Cheolho Sim
Megan E. Meuti
author_sort Matthew Wolkoff
collection DOAJ
description Abstract The insect circadian clock synchronizes daily activities, such as feeding, eclosion, and mating to diurnal light:dark cycles, while the photoperiodic clock synchronizes development and reproduction to the appropriate season. Despite mounting evidence that the circadian and photoperiodic timekeeping systems are linked, it is unclear whether the circadian clock as a whole or individual genes within the circadian clock are responsible for measuring daylength, releasing hormones and/or inducing diapause phenotypes. To interrogate the role of a core circadian transcription factor, cycle, in mediating both seasonal and daily behaviors we used CRISPR/Cas-9 genome editing to introduce a deletion mutation into cycle in the Northern house mosquito, Culex pipiens. Females homozygous for this deletion exhibited high rates of reproductive arrest characteristic of an overwintering diapause even when reared in summer-like conditions, while a minority remained reproductive even when reared in winter-like conditions. Nearly all (79%) homozygotes lacked robust behavioral rhythms in constant darkness, while 52% of heterozygotes carrying one wild-type copy of the cycle gene lacked robust rhythmicity in constant darkness. Heterozygotes and homozygotes were more active in constant darkness than WT mosquitoes, but this difference was abolished under light:dark conditions. Lastly, the daily transcription profiles of various circadian genes, especially timeless and vrille, were disrupted in homozygous females even when they were reared under long and short days with light:dark cycles. These results demonstrate that cycle is essential for coordinating both daily activity and transcript abundance and seasonal diapause in Cx. pipiens.
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spelling doaj-art-dd9e2c17cb1b492a91b6aaefa9f2a8bb2025-08-20T04:02:46ZengNature PortfolioScientific Reports2045-23222025-08-0115111610.1038/s41598-025-06637-yThe cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiensMatthew Wolkoff0Mizuki Yoshida1Taylor Lowmiller2Cheolho Sim3Megan E. Meuti4Department of Entomology, The Ohio State UniversityDepartment of Entomology, The Ohio State UniversityDepartment of Entomology, The Ohio State UniversityDepartment of Biology, Baylor UniversityDepartment of Entomology, The Ohio State UniversityAbstract The insect circadian clock synchronizes daily activities, such as feeding, eclosion, and mating to diurnal light:dark cycles, while the photoperiodic clock synchronizes development and reproduction to the appropriate season. Despite mounting evidence that the circadian and photoperiodic timekeeping systems are linked, it is unclear whether the circadian clock as a whole or individual genes within the circadian clock are responsible for measuring daylength, releasing hormones and/or inducing diapause phenotypes. To interrogate the role of a core circadian transcription factor, cycle, in mediating both seasonal and daily behaviors we used CRISPR/Cas-9 genome editing to introduce a deletion mutation into cycle in the Northern house mosquito, Culex pipiens. Females homozygous for this deletion exhibited high rates of reproductive arrest characteristic of an overwintering diapause even when reared in summer-like conditions, while a minority remained reproductive even when reared in winter-like conditions. Nearly all (79%) homozygotes lacked robust behavioral rhythms in constant darkness, while 52% of heterozygotes carrying one wild-type copy of the cycle gene lacked robust rhythmicity in constant darkness. Heterozygotes and homozygotes were more active in constant darkness than WT mosquitoes, but this difference was abolished under light:dark conditions. Lastly, the daily transcription profiles of various circadian genes, especially timeless and vrille, were disrupted in homozygous females even when they were reared under long and short days with light:dark cycles. These results demonstrate that cycle is essential for coordinating both daily activity and transcript abundance and seasonal diapause in Cx. pipiens.https://doi.org/10.1038/s41598-025-06637-yDiapauseCircadian biologyJuvenile hormone signalingBmalPeriodTimeless
spellingShingle Matthew Wolkoff
Mizuki Yoshida
Taylor Lowmiller
Cheolho Sim
Megan E. Meuti
The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens
Scientific Reports
Diapause
Circadian biology
Juvenile hormone signaling
Bmal
Period
Timeless
title The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens
title_full The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens
title_fullStr The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens
title_full_unstemmed The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens
title_short The cycle gene is essential for both daily responses and seasonal reproduction in the Northern house mosquito, Culex pipiens
title_sort cycle gene is essential for both daily responses and seasonal reproduction in the northern house mosquito culex pipiens
topic Diapause
Circadian biology
Juvenile hormone signaling
Bmal
Period
Timeless
url https://doi.org/10.1038/s41598-025-06637-y
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