Functional polymorphism of CYCLE underlies the diapause variation in moths

Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been identified. By leveraging cross-mapping and genome-wide association analysis, we identified the N terminus of the clock protein CYCLE as a major c...

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Published inScience (American Association for the Advancement of Science) Vol. 388; no. 6750; p. eado2129
Main Authors Zheng, Shirui, Wang, Yaohui, Li, Guiyun, Qin, Sheng, Dong, Zhi, Yang, Xu, Xu, Xiaomiao, Fang, Gangqi, Li, Muwang, Zhan, Shuai
Format Journal Article
LanguageEnglish
Published United States The American Association for the Advancement of Science 29.05.2025
Subjects
Adaptation
Alleles
Animals
BMAL1 protein
Bombyx - embryology
Bombyx - genetics
Bombyx - physiology
Bombyx mori
Butterflies & moths
Changing environments
Circadian rhythm
Circadian Rhythm - genetics
Circadian rhythms
Climate change
Clock gene
CLOCK Proteins - chemistry
CLOCK Proteins - genetics
Diapause
Diapause, Insect - genetics
Domestication
Dormancy
Environmental changes
Environmental conditions
Frameshift mutation
Gene deletion
Gene loci
Genetic crosses
Genetic diversity
Genome-Wide Association Study
Genomes
Global climate
Hibernation
Insect Proteins - chemistry
Insect Proteins - genetics
Insects
Isoforms
Lepidoptera
Life history
Loci
Molecular modelling
Mutagenesis
Mutation
Phenotype
Phenotypes
Polymorphism
Polymorphism, Genetic
Protein Isoforms - genetics
Range extension
Silk
Speciation
Species
Tropical environment
Tropical environments
Vertebrates
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Abstract Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been identified. By leveraging cross-mapping and genome-wide association analysis, we identified the N terminus of the clock protein CYCLE as a major causal effector underlying embryonic diapause differences in the silk moth. We found that the nondiapause phenotype in polyvoltine strains results from a specific deletion that disrupts an alternative isoform of CYCLE. We further demonstrated that different CYCLE isoforms contribute to a functional diversity in modulating circadian rhythms and diapause, which has been preserved in Lepidoptera for at least 110 million years. Our study proposes a model that explains how adaptive phenotypes can evolve rapidly without affecting related essential functions. Akin to hibernation in other species, diapause allows insects to remain dormant through harsh seasons. Zheng et al . examined the genetic basis of this trait in silk moths ( Bombyx mori ), the strains of which vary in their diapause timing and expression. Several genomic loci associated with this variation, including a peak encompassing the gene Cycle . This transcription factor is well known for its importance in circadian rhythms across species. Strains lacking the diapause phenotype altogether were homozygous for a frameshift mutation that completely disrupted a single isoform of Cycle . Given the conservation of Cycle across Lepidoptera (moths and butterflies), this gene may control diapause more broadly. —Corinne Simonti
AbstractList Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been identified. By leveraging cross-mapping and genome-wide association analysis, we identified the N terminus of the clock protein CYCLE as a major causal effector underlying embryonic diapause differences in the silk moth. We found that the nondiapause phenotype in polyvoltine strains results from a specific deletion that disrupts an alternative isoform of CYCLE. We further demonstrated that different CYCLE isoforms contribute to a functional diversity in modulating circadian rhythms and diapause, which has been preserved in Lepidoptera for at least 110 million years. Our study proposes a model that explains how adaptive phenotypes can evolve rapidly without affecting related essential functions.
Editor’s summaryAkin to hibernation in other species, diapause allows insects to remain dormant through harsh seasons. Zheng et al. examined the genetic basis of this trait in silk moths (Bombyx mori), the strains of which vary in their diapause timing and expression. Several genomic loci associated with this variation, including a peak encompassing the gene Cycle. This transcription factor is well known for its importance in circadian rhythms across species. Strains lacking the diapause phenotype altogether were homozygous for a frameshift mutation that completely disrupted a single isoform of Cycle. Given the conservation of Cycle across Lepidoptera (moths and butterflies), this gene may control diapause more broadly. —Corinne SimontiINTRODUCTIONSeasonal adaptation is crucial for the survival of natural animals. As a specific form of dormancy, diapause halts development to endure unfavorable seasons and commonly serves as a seasonal adaptative strategy in insects. Diapause traits vary pronouncedly within and among species, contributing to life history diversification in response to latitude and climate changes. Elucidating the genetic basis of diapause variation enhances our understanding of how insects rapidly adapt to changing environments for speciation and range expansion and allows for prediction of their further adaptation under global climate change. Despite broad interest, the molecular bases underlying the diversity of diapause traits and annual timing remain largely unexplored in insects, particularly for specified causal alleles in nonmodel species.RATIONALEThe domestic silk moth (Bombyx mori) exhibits characteristic diapause phenotypes across strains. To synchronize their life cycles with human activities, most domestic strains produce one or two generations a year through embryonic diapause (univoltinism or bivoltinism), depending on the perception of environmental cues in the maternal generation. By contrast, local strains originating from the tropics do not enter diapause regardless of environmental conditions (polyvoltinism). The rich variety of resources and well-documented phenotypes enable in-depth studies in this species to characterize the molecular mechanisms underlying diapause traits in Lepidoptera (moths and butterflies). We aimed to combine canonical genetic approaches and high-throughput genome-wide investigations to (i) identify causal loci responsible for the diapause variation in B. mori and (ii) test whether these identified loci have analogous effects in other species of Lepidoptera.RESULTSWe generated cross-mapping progeny between a facultative diapause bivoltine strain and a nondiapause polyvoltine strain of silk moths that mapped the major locus responsible for diapause variation on chromosome Z. By integrating with genome-wide association of 255 parental strains exhibiting diapause polymorphism, we localized the most effecting locus to the 5′ region of a central clock gene, Cycle (an insect homolog of BMAL1 in vertebrates). We identified a 1–base pair deletion exclusive to nondiapause strains as the key causal allele that disrupts one specific isoform of CYC (CYC-C), while preserving the complete copies of alternative isoforms (CYC-A/B). Multidimensional lines of evidence supported the involvement of CYC-C in controlling diapause in the silk moth, linking it with multiple functional modules potentially related to diapause modulation, and showed that CYC-A/B may play the native role of CYC as a fundamental component of circadian regulation. We further showed that the expression of alternative CYC transcripts is subject to independent regulation and that this functional diversity has been reserved across a wide range of Lepidoptera taxa. On the basis of isoform-specific mutagenesis, we validated the effect of CYC-C in initiating larval diapause in the Asian corn borer (Ostrinia furnacalis) that diverged with the silk moth approximately 100 million years ago.CONCLUSIONIn this study, we defined the additional function of the circadian protein CYC, through one of its alternative isoforms, in controlling the entry into diapause in Lepidoptera, and identified a newly derived mutation in this isoform, arising along with the domestication in tropical regions, which is responsible for the diapause variation in silk moths. The potential functional diversity of CYC is widespread in Lepidoptera, which may reconcile the flexibility of seasonal adaptation with the functional constraint on fundamental circadian regulation. Combined with previously documented examples in TIMELESS (TIM) and PERIOD (PER) in Drosophila, the diverse isoforms of central clock genes may serve as common targets of selection for seasonal adaptation in insects.
Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been identified. By leveraging cross-mapping and genome-wide association analysis, we identified the N terminus of the clock protein CYCLE as a major causal effector underlying embryonic diapause differences in the silk moth. We found that the nondiapause phenotype in polyvoltine strains results from a specific deletion that disrupts an alternative isoform of CYCLE. We further demonstrated that different CYCLE isoforms contribute to a functional diversity in modulating circadian rhythms and diapause, which has been preserved in Lepidoptera for at least 110 million years. Our study proposes a model that explains how adaptive phenotypes can evolve rapidly without affecting related essential functions. Akin to hibernation in other species, diapause allows insects to remain dormant through harsh seasons. Zheng et al . examined the genetic basis of this trait in silk moths ( Bombyx mori ), the strains of which vary in their diapause timing and expression. Several genomic loci associated with this variation, including a peak encompassing the gene Cycle . This transcription factor is well known for its importance in circadian rhythms across species. Strains lacking the diapause phenotype altogether were homozygous for a frameshift mutation that completely disrupted a single isoform of Cycle . Given the conservation of Cycle across Lepidoptera (moths and butterflies), this gene may control diapause more broadly. —Corinne Simonti
Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been identified. By leveraging cross-mapping and genome-wide association analysis, we identified the N terminus of the clock protein CYCLE as a major causal effector underlying embryonic diapause differences in the silk moth. We found that the nondiapause phenotype in polyvoltine strains results from a specific deletion that disrupts an alternative isoform of CYCLE. We further demonstrated that different CYCLE isoforms contribute to a functional diversity in modulating circadian rhythms and diapause, which has been preserved in Lepidoptera for at least 110 million years. Our study proposes a model that explains how adaptive phenotypes can evolve rapidly without affecting related essential functions.Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been identified. By leveraging cross-mapping and genome-wide association analysis, we identified the N terminus of the clock protein CYCLE as a major causal effector underlying embryonic diapause differences in the silk moth. We found that the nondiapause phenotype in polyvoltine strains results from a specific deletion that disrupts an alternative isoform of CYCLE. We further demonstrated that different CYCLE isoforms contribute to a functional diversity in modulating circadian rhythms and diapause, which has been preserved in Lepidoptera for at least 110 million years. Our study proposes a model that explains how adaptive phenotypes can evolve rapidly without affecting related essential functions.
Author Qin, Sheng
Zheng, Shirui
Xu, Xiaomiao
Zhan, Shuai
Yang, Xu
Li, Muwang
Li, Guiyun
Fang, Gangqi
Wang, Yaohui
Dong, Zhi
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SSID ssj0009593
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Snippet Diapause is a common seasonal adaptive strategy that regulates annual timing in insects. Very few causal loci underlying diapause variation have yet been...
Editor’s summaryAkin to hibernation in other species, diapause allows insects to remain dormant through harsh seasons. Zheng et al. examined the genetic basis...
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StartPage eado2129
SubjectTerms Adaptation
Alleles
Animals
BMAL1 protein
Bombyx - embryology
Bombyx - genetics
Bombyx - physiology
Bombyx mori
Butterflies & moths
Changing environments
Circadian rhythm
Circadian Rhythm - genetics
Circadian rhythms
Climate change
Clock gene
CLOCK Proteins - chemistry
CLOCK Proteins - genetics
Diapause
Diapause, Insect - genetics
Domestication
Dormancy
Environmental changes
Environmental conditions
Frameshift mutation
Gene deletion
Gene loci
Genetic crosses
Genetic diversity
Genome-Wide Association Study
Genomes
Global climate
Hibernation
Insect Proteins - chemistry
Insect Proteins - genetics
Insects
Isoforms
Lepidoptera
Life history
Loci
Molecular modelling
Mutagenesis
Mutation
Phenotype
Phenotypes
Polymorphism
Polymorphism, Genetic
Protein Isoforms - genetics
Range extension
Silk
Speciation
Species
Tropical environment
Tropical environments
Vertebrates
Title Functional polymorphism of CYCLE underlies the diapause variation in moths
URI https://www.ncbi.nlm.nih.gov/pubmed/40440392
https://www.proquest.com/docview/3213406926
https://www.proquest.com/docview/3214300462
Volume 388
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