Dataset Information

An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators.

ABSTRACT: Monarch butterflies (Danaus plexippus) breeding in eastern North America are famous for their annual fall migration to their overwintering grounds in Mexico. However, the mechanisms they use to successfully reach these sites remain poorly understood. Here, we test whether monarchs are true navigators who can determine their location relative to their final destination using both a "compass" and a "map". Using flight simulators, we recorded the orientation of wild-caught monarchs in southwestern Ontario and found that individuals generally flew in a southwest direction toward the wintering grounds. When displaced 2,500 km to the west, the same individuals continued to fly in a general southwest direction, suggesting that monarchs use a simple vector-navigation strategy (i.e., use a specific compass bearing without compensating for displacement). Using over 5 decades of field data, we also show that the directional concentration and the angular SD of recoveries from tagged monarchs largely conformed to two mathematical models describing the directional distribution of migrants expected under a vector-navigation strategy. A third analysis of tagged recoveries shows that the increasing directionality of migration from north to south is largely because of the presence of geographic barriers that guide individuals toward overwintering sites. Our work suggests that monarchs breeding in eastern North America likely combine simple orientation mechanisms with geographic features that funnel them toward Mexican overwintering sites, a remarkable achievement considering that these butterflies weigh less than a gram and travel thousands of kilometers to a site they have never seen.

SUBMITTER: Mouritsen H

PROVIDER: S-EPMC3645515 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators.

Mouritsen Henrik H Derbyshire Rachael R Stalleicken Julia J Mouritsen Ole Ø OØ Frost Barrie J BJ Norris D Ryan DR

Proceedings of the National Academy of Sciences of the United States of America 20130408 18

Monarch butterflies (Danaus plexippus) breeding in eastern North America are famous for their annual fall migration to their overwintering grounds in Mexico. However, the mechanisms they use to successfully reach these sites remain poorly understood. Here, we test whether monarchs are true navigators who can determine their location relative to their final destination using both a "compass" and a "map". Using flight simulators, we recorded the orientation of wild-caught monarchs in southwestern ...[more]

PMID: 23569228

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Project description:North American monarch butterflies (Danaus plexippus) undergo a spectacular fall migration. In contrast to summer butterflies, migrants are juvenile hormone (JH) deficient, which leads to reproductive diapause and increased longevity. Migrants also utilize time-compensated sun compass orientation to help them navigate to their overwintering grounds. Here, we describe a brain expressed sequence tag (EST) resource to identify genes involved in migratory behaviors. A brain EST library was constructed from summer and migrating butterflies. Of 9,484 unique sequences, 6068 had positive hits with the non-redundant protein database; the EST database likely represents approximately 52% of the gene-encoding potential of the monarch genome. The brain transcriptome was cataloged using Gene Ontology and compared to Drosophila. Monarch genes were well represented, including those implicated in behavior. Three genes involved in increased JH activity (allatotropin, juvenile hormone acid methyltransfersase, and takeout) were upregulated in summer butterflies, compared to migrants. The locomotion-relevant turtle gene was marginally upregulated in migrants, while the foraging and single-minded genes were not differentially regulated. Many of the genes important for the monarch circadian clock mechanism (involved in sun compass orientation) were in the EST resource, including the newly identified cryptochrome 2. The EST database also revealed a novel Na+/K+ ATPase allele predicted to be more resistant to the toxic effects of milkweed than that reported previously. Potential genetic markers were identified from 3,486 EST contigs and included 1599 double-hit single nucleotide polymorphisms (SNPs) and 98 microsatellite polymorphisms. These data provide a template of the brain transcriptome for the monarch butterfly. Our "snap-shot" analysis of the differential regulation of candidate genes between summer and migratory butterflies suggests that unbiased, comprehensive transcriptional profiling will inform the molecular basis of migration. The identified SNPs and microsatellite polymorphisms can be used as genetic markers to address questions of population and subspecies structure.

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.

Project description: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.

Dataset Information

An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators.

Publications

An experimental displacement and over 50 years of tag-recoveries show that monarch butterflies are not true navigators.

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