Dataset Information

Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies.

ABSTRACT:

Background

North American monarchs (Danaus plexippus) are well-known for their long-distance migrations; however, some monarchs within the migratory range have adopted a resident lifestyle and breed year-round at sites where tropical milkweed (Asclepias curassavica) is planted in the southern coastal United States. An important question is whether exposure to exotic milkweed alters monarch migratory physiology, particularly the ability to enter and remain in the hormonally-induced state of reproductive diapause, whereby adults delay reproductive maturity. Cued by cooler temperatures and shorter photoperiods, diapause is a component of the monarch's migratory syndrome that includes directional flight behavior, lipid accumulation, and the exceptional longevity of the migratory generation.

Methods

Here, we experimentally test how exposure to tropical milkweed during the larval and adult stages influences monarch reproductive status during fall migration. Caterpillars reared under fall-like conditions were fed tropical versus native milkweed diets, and wild adult migrants were placed in outdoor flight cages with tropical milkweed, native milkweed, or no milkweed.

Results

We found that monarchs exposed to tropical milkweed as larvae were more likely to be reproductively active (exhibit mating behavior in males and develop mature eggs in females) compared to monarchs exposed to native milkweed. Among wild-caught fall migrants, females exposed to tropical milkweed showed greater egg development than females exposed to native or no milkweed, although a similar response was not observed for males.

Conclusions

Our study provides evidence that exposure to tropical milkweed can increase monarch reproductive activity, which could promote continued residency at year-round breeding sites and decrease monarch migratory propensity.

SUBMITTER: Majewska AA

PROVIDER: S-EPMC6724006 | biostudies-literature | 2019 Aug

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies.

Majewska Ania A AA Altizer Sonia S

Insects 20190816 8

<h4>Background</h4>North American monarchs (<i>Danaus plexippus</i>) are well-known for their long-distance migrations; however, some monarchs within the migratory range have adopted a resident lifestyle and breed year-round at sites where tropical milkweed (<i>Asclepias curassavica</i>) is planted in the southern coastal United States. An important question is whether exposure to exotic milkweed alters monarch migratory physiology, particularly the ability to enter and remain in the hormonally- ...[more]

PMID: 31426310

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Project description:Public interest in ecological landscaping and gardening is fueling a robust market for native plants. Most plants available to consumers through the horticulture trade are cultivated forms that have been selected for modified flowers or foliage, compactness, or other ornamental characteristics. Depending on their traits, some native plant cultivars seem to support pollinators, specialist insect folivores, and insect-based vertebrate food webs as effectively as native plant species, whereas others do not. There is particular need for information on whether native cultivars can be as effective as true or "wild-type" native species for supporting specialist native insects of conservation concern. Herein we compared the suitability of native milkweed species and their cultivars for attracting and supporting one such insect, the iconic monarch butterfly (Danaus plexippus L.), as well as native bees in urban pollinator gardens. Wild-type Asclepias incarnata L. (swamp milkweed) and Asclepias tuberosa L. (butterfly milkweed) and three additional cultivars of each that vary in stature, floral display, and foliage color were grown in a replicated common garden experiment at a public arboretum. We monitored the plants for colonization by wild monarchs, assessed their suitability for supporting monarch larvae in greenhouse trials, measured their defensive characteristics (leaf trichome density, latex, and cardenolide levels), and compared the proportionate abundance and diversity of bee families and genera visiting their blooms. Significantly more monarch eggs and larvae were found on A. incarnata than A. tuberosa in both years, but within each milkweed group, cultivars were colonized to the same extent as wild types. Despite some differences in defense allocation, all cultivars were as suitable as wild-type milkweeds in supporting monarch larval growth. Five bee families and 17 genera were represented amongst the 2,436 total bees sampled from blooms of wild-type milkweeds and their cultivars in the replicated gardens. Bee assemblages of A. incarnata were dominated by Apidae (Bombus, Xylocopa spp., and Apis mellifera), whereas A. tuberosa attracted relatively more Halictidae (especially Lasioglossum spp.) and Megachilidae. Proportionate abundance of bee families and genera was generally similar for cultivars and their respective wild types. This study suggests that, at least in small urban gardens, milkweed cultivars can be as suitable as their parental species for supporting monarch butterflies and native bees.

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

Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies.

Background

Methods

Results

Conclusions

Publications

Exposure to Non-Native Tropical Milkweed Promotes Reproductive Development in Migratory Monarch Butterflies.

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