Abstract
BackgroundIn 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.ResultsHere 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 molecularly separating 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. 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.ConclusionThe 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.
Highlights
In the fall, Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration
The precise type of flight behavior that the summer monarchs manifest has not been rigorously examined. It is unclear whether juvenile hormone (JH) deficiency and the accompanying reproductive quiescence are required for ongoing time-compensated sun compass orientation in fall migrants
Increased juvenile hormone activity in migrants does not disrupt directed flight or time-compensated orientation Because several aspects of migratory behavior are a consequence of continued JH deficiency, for example, reproductive quiescence and increased longevity [2,3], we examined whether the oriented flight behavior characteristic of fall migrants depends on persistent JH insufficiency
Summary
Eastern North American monarch butterflies (Danaus plexippus) undergo a magnificent long-range migration. Migrants 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. The migrant offspring give rise to three to four successive generations of reproductively active butterflies that repopulate the northern range of their habitat It is unclear whether the successive generations of spring and summer butterflies have oriented flight activity to the north and/or whether they are following the progressive northerly increase in milkweed abundance, while avoiding undue heat stress that would occur if they remained in the southern United States throughout the summer [7]. The precise type of flight behavior that the summer monarchs manifest has not been rigorously examined It is unclear whether JH deficiency and the accompanying reproductive quiescence are required for ongoing time-compensated sun compass orientation in fall migrants
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