Dataset Information

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics.

ABSTRACT: The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically-determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally-controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause-inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin-like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.

SUBMITTER: Green DA

PROVIDER: S-EPMC6834359 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

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Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics.

Green Delbert A DA Kronforst Marcus R MR

Molecular ecology 20190801 16

The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically-determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different ...[more]

PMID: 31338928

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Project description:In the fall, Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration. In contrast to spring and summer butterflies, fall migrants are juvenile hormone deficient, which leads to reproductive arrest and increased longevity. Migrants also use a time-compensated sun compass to help them navigate in the south/southwesterly direction en route for Mexico. Central issues in this area are defining the relationship between juvenile hormone status and oriented flight, critical features that differentiate summer monarchs from fall migrants, and identifying molecular correlates of behavioral state. Here we show that increasing juvenile hormone activity to induce summer-like reproductive development in fall migrants does not alter directional flight behavior or its time-compensated orientation, as monitored in a flight simulator. Reproductive summer butterflies, in contrast, uniformly fail to exhibit directional, oriented flight. To define molecular correlates of behavioral state, we used microarray analysis of 9417 unique cDNA sequences. Gene expression profiles reveal a suite of 40 genes whose differential expression in brain correlates with oriented flight behavior in individual migrants, independent of juvenile hormone activity, thereby separating molecularly fall migrants from summer butterflies. Intriguing genes that are differentially regulated include the clock gene vrille and the locomotion-relevant tyramine beta hydroxylase gene. In addition, several differentially regulated genes (37.5% of total) are not annotated, suggesting unique functions associated with oriented flight behavior. We also identified 23 juvenile hormone-dependent genes in brain, which separate reproductive from non-reproductive monarchs; genes involved in longevity, fatty acid metabolism, and innate immunity are upregulated in non-reproductive (juvenile-hormone deficient) migrants. The results link key behavioral traits with gene expression profiles in brain that differentiate migratory from summer butterflies and thus show that seasonal changes in genomic function help define the migratory state. A total of 40 monarch butterflies were used for the microarray analysis. Of the 40, 10 (5 male/5 female) were summer butterflies (Designated as S) and 30 were fall butterflies. The fall butterflies were further divided into three groups: 10 (5 male/5 female) were untreated (F); 10 (5 male/5 female) were treated with methoprene (M), which is a juvenile hormone analog and induces the development of reproductive organs in migrant butterflies; and 10 (5 male/5 female) were treated with vehicle only (V). We collected total brain RNA from each of the 40 butterflies. The brain RNAs were amplified and then used to probe a custom Nimblegen array that was designed to analyze the 9,417 unique cDNA sequences established in our published EST library (http://titan.biotec.uiuc.edu/cgi-bin/ESTWebsite/estima_start?seqSet=butterfly). Our main interest is to find genes involved in migration. This includes genes regulating oriented flight behavior of the butterfly and genes that regulate reproductive status. To identify these genes, we approached the microarray data in two ways. First, we identified the potential genes involved in oriented flight behavior using the following strategy. We compared the summer group to each of the three fall groups (untreated, methoprene-treated, and vehicle-treated) for males and for females, and looked for gene regulation patterns common among the three comparisons for each sex. Because the comparisons were done separately for males and females, and our behavioral data did not show significant sex differences in flight orientation, we focused on the common differentially regulated genes that were shared between males and females. Accordingly, we identified 40 cDNAs that were differentially regulated between summer butterflies and fall migrants, irrespective of sex. Second, we looked for the juvenile hormone-response genes. Again, we performed sex-specific statistical analyses, and compared the summer and the fall groups, and the methoprene-treated and vehicle-treated migrants. We then screened for shared genes between the two groups for each sex. We next examined cDNAs that were differentially regulated in both males and females, to determine juvenile hormone-regulated genes involved in more global processes (e.g., longevity and fatty acid metabolism) that would not be expected to be sex-specific. We identified 23 putative juvenile hormone-response genes that were common between males and females.

Dataset Information

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics.

Publications

Monarch butterflies use an environmentally sensitive, internal timer to control overwintering dynamics.

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