Article

Defining behavioral and molecular differences between summer and migratory monarch butterflies

Department of Neurobiology, University of Massachusetts Medical School, Plantation Street, Worcester, MA 01605, USA.
BMC Biology (Impact Factor: 7.98). 04/2009; 7(1):14. DOI: 10.1186/1741-7007-7-14
Source: PubMed

ABSTRACT

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 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.
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.

Download full-text

Full-text

Available from: Sriramana Kanginakudru, Nov 11, 2014
  • Source
    • "The Bombyx mori homologue of the neuropeptide receptor A16 (BNGR-A16), downregulated in long-distance moths from China (FC = 2.67), is the receptor for the hormone allatotropin (AT) which stimulates juvenile hormone (JH) biosynthesis (Yamanaka et al. 2008). The relationship between AT mRNA expression and JH levels is tightly coupled and injection of AT induces resident behaviour in migrant insects (McNeil et al. 2005; Zhu et al. 2009; Jiang et al. 2011). The downregulation of the AT receptor, BNGR-A16, in long fliers from Dafeng suggests that the contrasting flight propensities between Dafeng and Anyang (Fig. 1B) are a reflection of true differences in migratory potential. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Migration is a key life-history strategy for many animals and requires a suite of behavioural, morphological and physiological adaptations which together form the 'migratory syndrome'. Genetic variation has been demonstrated for many traits that make up this syndrome but the underlying genes involved remain elusive. Recent studies investigating migration associated genes have focussed on sampling migratory and non-migratory populations from different geographic locations but have seldom explored phenotypic variation in a migratory trait. Here, we use a novel combination of tethered flight and next-generation sequencing to determine transcriptomic differences associated with flight activity in a globally invasive moth pest, the cotton bollworm Helicoverpa armigera. By developing a state-of-the-art phenotyping platform we show that field-collected H. armigera display continuous variation in flight performance with individuals capable of flying up to 40 kilometres during a single night. Comparative transcriptomics of flight phenotypes drove a gene expression analysis to reveal a suite of expressed candidate genes which are clearly related to physiological adaptations required for long-distance flight. These include genes important to the mobilisation of lipids as flight fuel, the development of flight muscle structure and the regulation of hormones that influence migratory physiology. We conclude that the ability to express this complex set of pathways underlines the remarkable flexibility of facultative insect migrants to respond to deteriorating conditions in the form of migratory flight and, more broadly, the results provide novel insights into the fundamental transcriptional changes required for migration in insects and other taxa. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Full-text · Article · Sep 2015 · Molecular Ecology
  • Source
    • "Genetic mechanisms underpinning various aspects of migratory behavior have been discovered in animals that traverse great distances and display precise homing ability (e.g., timing, sun compass orientation, and propensity to migrate; Zhu et al. 2009; Hecht et al. 2013; O'Malley et al. 2013). Characterization of particular genetic traits may increase our ability to predict the spatial and temporal distribution of migratory species and could thus increase effectiveness of the management of such species, many of which play key cultural and economic roles in our society. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Elucidation of genetic mechanisms underpinning migratory behavior could help predict how changes in genetic diversity may affect future spatiotemporal distribution of a migratory species. This ability would benefit conservation of one such declining species, anadromous Pacific lamprey (Entosphenus tridentatus). Nonphilopatric migration of adult Pacific lamprey has homogenized population-level neutral variation but has maintained adaptive variation that differentiates groups based on geography, run-timing and adult body form. To investigate causes for this adaptive divergence, we examined 647 adult lamprey sampled at a fixed location on the Columbia River and radiotracked during their subsequent upstream migration. We tested whether genetic variation [94 neutral and adaptive single nucleotide polymorphisms (SNPs) previously identified from a genomewide association study] was associated with phenotypes of migration distance, migration timing, or morphology. Three adaptive markers were strongly associated with morphology, and one marker also correlated with upstream migration distance and timing. Genes physically linked with these markers plausibly influence differences in body size, which is also consistently associated with migration distance in Pacific lamprey. Pacific lamprey conservation implications include the potential to predict an individual’s upstream destination based on its genotype. More broadly, the results suggest a genetic basis for intrapopulation variation in migration distance in migratory species.
    Full-text · Article · Sep 2014 · Evolutionary Applications
    • "Genetic mechanisms underpinning various aspects of migratory behavior have been discovered in animals that traverse great distances and display precise homing ability (e.g., timing, sun compass orientation, and propensity to migrate; Zhu et al. 2009; Hecht et al. 2013; O'Malley et al. 2013). Characterization of particular genetic traits may increase our ability to predict the spatial and temporal distribution of migratory species and could thus increase effectiveness of the management of such species, many of which play key cultural and economic roles in our society. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Elucidation of genetic mechanisms underpinning migratory behavior could help predict how changes in genetic diversity may affect the future spatio-temporal distribution of a migratory species. This ability would benefit conservation of one such declining species, anadromous Pacific lamprey (Entosphenus tridentatus). Nonphilopatric migration of adult lamprey has homogenized population-level neutral variation, but has maintained adaptive variation that differentiates groups based on geography, run-timing, and adult body form. To investigate causes for this adaptive divergence, we examined 647 adult lamprey sampled at a fixed location on the Columbia River and radio-tracked during their subsequent upstream migration. We tested whether genetic variation (96 neutral and adaptive single nucleotide polymorphism markers previously identified from a genome-wide association study) was associated with migration distance, migration timing, or morphology. Three adaptive markers were strongly associated with morphology, and one marker was also significantly correlated with upstream migration distance. Genes physically linked with these markers plausibly influence differences in body size, which is also consistently associated with migration distance in Pacific lamprey. Lamprey conservation implications include the potential to predict an individual’s upstream fate based on its genotype. More broadly, the results suggest a genetic basis for intrapopulation variation in migration distance in other migratory species.
    No preview · Conference Paper · Aug 2014
Show more