The genetics of monarch butterfly migration and warning colouration

Zhan, Shuai; Zhang, W.; Niitepõld, Kristjan; Hsu, Jeremy; Haeger, J. Fernández; Zalucki, Myron P.; Altizer, Sonia; Roode, Jacobus C. de; Reppert, Steven M.; Kronforst, Marcus R.

doi:10.1038/nature13812

Cited by 254 publications

(332 citation statements)

References 70 publications

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“…The estimated migration rates represent the number of migrating chromosomes per generation. To obtain the population sizes and the time of population splitting from the estimated relative values, we followed a previous study 88 that assumes the generation time of 0.3 year and uses the standard mutation rate of 8.4 × 10 −9 (per site per generation) from Drosophila 89 . The standard errors were obtained by parametric bootstrap of coalescent simulation 86 .…”

Section: Quantitative Pcr With Reverse Transcription (Rt-qpcr)mentioning

confidence: 99%

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

et al. 2017

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The tobacco cutworm, Spodoptera litura, is among the most widespread and destructive agricultural pests, feeding on over 100 crops throughout tropical and subtropical Asia. By genome sequencing, physical mapping and transcriptome analysis, we found that the gene families encoding receptors for bitter or toxic substances and detoxification enzymes, such as cytochrome P450, carboxylesterase and glutathione-S-transferase, were massively expanded in this polyphagous species, enabling its extraordinary ability to detect and detoxify many plant secondary compounds. Larval exposure to insecticidal toxins induced expression of detoxification genes, and knockdown of representative genes using short interfering RNA (siRNA) reduced larval survival, consistent with their contribution to the insect’s natural pesticide tolerance. A population genetics study indicated that this species expanded throughout southeast Asia by migrating along a South India–South China–Japan axis, adapting to wide-ranging ecological conditions with diverse host plants and insecticides, surviving and adapting with the aid of its expanded detoxification systems. The findings of this study will enable the development of new pest management strategies for the control of major agricultural pests such as S. litura.

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Section: Quantitative Pcr With Reverse Transcription (Rt-qpcr)mentioning

confidence: 99%

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

et al. 2017

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“…Most monarch populations outside of North America are, in fact, non-migratory [29,30], or locally travel only short distances in the form of modest range shifts [31]. Historical records and recent genomic analyses suggest that monarchs colonized other locations throughout the world from North American origins [32].…”

Section: Introductionmentioning

confidence: 99%

“…Records of monarchs outside of the New World are limited to the last 200 years, after suitable milkweed host plants (mostly in the genus Asclepias) were introduced [27]; however, recent genome-wide analyses suggest that these colonizations may have occurred earlier [32]. Monarchs likely colonized locations around the world through serial founder effects (stepwise dispersal) or multiple independent colonization events [27,33], and were aided in reaching new locations through human transportation of both milkweeds and monarchs [34], and extreme weather events [35].…”

Section: Introductionmentioning

confidence: 99%

Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies

et al. 2014

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Range expansions can result in founder effects, increasing genetic differentiation between expanding populations and reducing genetic diversity along the expansion front. However, few studies have addressed these effects in long-distance migratory species, for which high dispersal ability might counter the effects of genetic drift. Monarchs (Danaus plexippus) are best known for undertaking a long-distance annual migration in North America, but have also dispersed around the world to form populations that do not migrate or travel only short distances. Here, we used microsatellite markers to assess genetic differentiation among 18 monarch populations and to determine worldwide colonization routes. Our results indicate that North American monarch populations connected by land show limited differentiation, probably because of the monarch's ability to migrate long distances. Conversely, we found high genetic differentiation between populations separated by large bodies of water. Moreover, we show evidence for serial founder effects across the Pacific, suggesting stepwise dispersal from a North American origin. These findings demonstrate that genetic drift played a major role in shaping allele frequencies and created genetic differentiation among newly formed populations. Thus, range expansion can give rise to genetic differentiation and declines in genetic diversity, even in highly mobile species.

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“…Collagen IV forms the central component of basement membranes essential for muscle structure and function and the downregulation of this gene in migratory monarchs, coupled with decreased metabolic rates during flight, suggested the evolution of greater metabolic efficiency in the migratory forms (Zhan et al . 2014). Collagen II is the main structural component of cartilage in humans (Garofalo et al .…”

Section: Resultsmentioning

confidence: 99%

“…For example, signatures of positive selection acting upon flight muscle genes were detected in migratory populations of the monarch butterfly, Danaus plexippus (Zhan et al . 2014). Few studies have applied next‐generation sequencing to migratory insects from the same population displaying intraspecific variation in a behavioural migratory trait.…”

Section: Introductionmentioning

confidence: 99%

Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest

et al. 2015

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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 nonmigratory 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 km 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 mobilization 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.

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The genetics of monarch butterfly migration and warning colouration

Cited by 254 publications

References 70 publications

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

Genomic adaptation to polyphagy and insecticides in a major East Asian noctuid pest

Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies

Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest

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