The monarch butterfly genome yields insights into long-distance migration

We present the draft 273 Mb genome of the migratory monarch butterfly (Danaus plexippus) and a set of 16,866 protein-coding genes. Orthology properties suggest that the Lepidoptera are the fastest evolving insect order yet examined. Compared to the silkmoth Bombyx mori, the monarch genome shares prominent similarity in orthology content, microsynteny, and protein family sizes. The monarch genome reveals a vertebrate-like opsin whose existence in insects is widespread; a full repertoire of molecular components for the monarch circadian clockwork; all members of the juvenile hormone biosynthetic pathway whose regulation shows unexpected sexual dimorphism; additional molecular signatures of oriented flight behavior; microRNAs that are differentially expressed between summer and migratory butterflies; monarch-specific expansions of chemoreceptors potentially important for long-distance migration; and a variant of the sodium/potassium pump that underlies a valuable chemical defense mechanism. The monarch genome enhances our ability to better understand the genetic and molecular basis of long-distance migration.     

Tracking climate impacts on the migratory monarch butterfly

Understanding the impacts of climate on migratory species is complicated by the fact that these species travel through several climates that may be changing in diverse ways throughout their complete migratory cycle. Most studies are not designed to tease out the direct and indirect effects of climate at various stages along the migration route. We assess the impacts of spring and summer climate conditions on breeding monarch butterflies, a species that completes its annual migration cycle over several generations. No single, broad‐scale climate metric can explain summer breeding phenology or the substantial year‐to‐year fluctuations observed in population abundances. As such, we built a Poisson regression model to help explain annual arrival times and abundances in the Midwestern United States. We incorporated the climate conditions experienced both during a spring migration/breeding phase in Texas as well as during subsequent arrival and breeding during the main recruitment period in Ohio. Using data from a state‐wide butterfly monitoring network in Ohio, our results suggest that climate acts in conflicting ways during the spring and summer seasons. High spring precipitation in Texas is associated with the largest annual population growth in Ohio and the earliest arrival to the summer breeding ground, as are intermediate spring temperatures in Texas. On the other hand, the timing of monarch arrivals to the summer breeding grounds is not affected by climate conditions within Ohio. Once in Ohio for summer breeding, precipitation has minimal impacts on overall abundances, whereas warmer summer temperatures are generally associated with the highest expected abundances, yet this effect is mitigated by the average seasonal temperature of each location in that the warmest sites receive no benefit of above average summer temperatures. Our results highlight the complex relationship between climate and performance for a migrating species and suggest that attempts to understand how monarchs will be affected by future climate conditions will be challenging.     

The fall migration flyways of monarch butterflies in eastern North America revealed by citizen scientists

The migration of monarch butterflies (Danaus plexippus) from Canada and the United States to overwintering sites in Mexico is one of the world’s most amazing biological phenomena, although recent threats make it imperative that the resources needed by migrating monarchs be conserved. The most important first step in preserving migration resources—determining the migration flyways—is also the most challenging because of the large-scale nature of the migration. Prior attempts to determine the flyways using mark-recapture techniques with wing tags gave some clues, but this important information has never been fully obtainable until now. In 2005 the citizen-science program, Journey North, initiated a project that asked participants to record sightings of overnight roosts of monarchs during their fall migration, and this project now provides an ideal way to illustrate the flyways used by monarchs on their way to Mexico, with the assumption that roost locations indicate migration routes. We used 3 years of this data to elucidate the flyways on a continent-wide scale, that revealed two distinct flyways, but only one appears to lead directly to Mexico. This main, ‘central’ flyway begins in the American Midwest states and southern Ontario, then continues south-southwest through the states of Kansas, Missouri, Oklahoma and Arkansas, and finally passes through Texas and northern Mexico. These data also highlighted a separate, smaller flyway along the eastern and coastal states, but there was a noticeable lack of roost sightings in this flyway at lower latitudes. Since there are few recoveries of marked monarchs in Mexico originating from coastal areas, we compared the timing of roost formation in this ‘eastern’ flyway with the main, central flyway. Roosts in the eastern flyway lagged behind the central roosts in timing, suggesting that monarchs traveling in this flyway have a reduced chance of making it to the Mexico wintering site. Combined, our evidence indicates that locations in the central flyway should be considered priority areas for conserving migration resources.     

Flight-induced compass representation in the monarch butterfly heading network

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Effects of climate on fall migration phenology of monarch butterflies departing the northeastern breeding grounds in Canada

Monarch butterflies (Danaus plexippus) undergo an iconic multi-generational migration, traveling thousands of kilometers from the summer breeding grounds in southern Canada to overwintering sites in central Mexico. This migration phenomena can be affected by climate change, which may have important implications on fitness and ultimately populations status. We investigated the long-term trends in fall migration phenology of monarchs using a 25-year dataset collected along the coast of Lake Erie in Ontario, Canada. We also investigated local long-term trends in weather covariates that have the potential to influence migration phenology at this site. Patterns in standardized daily counts of monarchs were compared with local weather covariates using two methods (i.e., monthly averages and moving windows) to assess difference in outputs between analytical approaches. Our results suggest that monarch migration timing (migration midpoint, average peak, first peak, and late passage) and weather covariates have been consistent over time, in direct contrast to a similar study in Cape May, New Jersey, which showed a significant increase in both fall temperature and a 16- to 19-day shift in monarch migration timing. Furthermore, our results differed between analytical approaches. With respect to annual variability in air temperature, our monthly average analysis suggested that for each degree increase in September air temperature, late season passage would advance 4.71 days (±1.59 SE, p = .01). However, the moving window analysis suggested that this result is likely spurious and found no significant correlations between migration timing and any weather covariates. Importantly, our results caution against extrapolating the effects of climate change on the migration phenology of the monarch across study regions and the need for more long-term monitoring efforts to better understand regional drivers of variability in migration timing.     

Behavioural resistance against a protozoan parasite in the monarch butterfly

1. As parasites can dramatically reduce the fitness of their hosts, there should be strong selection for hosts to evolve and maintain defence mechanisms against their parasites. One way in which hosts may protect themselves against parasitism is through altered behaviours, but such defences have been much less studied than other forms of parasite resistance. 2. We studied whether monarch butterflies (Danaus plexippus L.) use altered behaviours to protect themselves and their offspring against the protozoan parasite Ophryocystis elektroscirrha (McLaughlin & Myers (1970), Journal of Protozoology, 17, p. 300). In particular, we studied whether (i) monarch larvae can avoid contact with infectious parasite spores; (ii) infected larvae preferentially consume therapeutic food plants when given a choice or increase the intake of such plants in the absence of choice; and (iii) infected female butterflies preferentially lay their eggs on medicinal plants that make their offspring less sick. 3. We found that monarch larvae were unable to avoid infectious parasite spores. Larvae were also not able to preferentially feed on therapeutic food plants or increase the ingestion of such plants. However, infected female butterflies preferentially laid their eggs on food plants that reduce parasite growth in their offspring. 4. Our results suggest that animals may use altered behaviours as a protection against parasites and that such behaviours may be limited to a single stage in the host-parasite life cycle. Our results also suggest that animals may use altered behaviours to protect their offspring instead of themselves. Thus, our study indicates that an inclusive fitness approach should be adopted to study behavioural defences against parasites.     

Male monarch butterfly spermatophore mass and mating strategies

Male monarch butterflies, Danaus plexippus, produce a spermatophore which can represent approximately 10% of their body mass. Spermatophore mass increased with age in virgin males, and with the time since last mating in non-virgin males. Male monarchs did not delay re-mating until they were able to produce a large spermatophore. Recently mated males were as likely as virgins to copulate with both virgin and non-virgin females. Monarchs provide an example of Bateman's principle, mating whenever possible, despite the non-trivial cost involved.     

Juvenile hormone regulation of longevity in the migratory monarch butterfly.

Monarch butterflies (Danaus plexippus) of eastern North America are well known for their long-range migration to overwintering roosts in south-central Mexico. An essential feature of this migration involves the exceptional longevity of the migrant adults; individuals persist from August/September to March while their summer counterparts are likely to live less than two months as adults. Migrant adults persist during a state of reproductive diapause in which both male and female reproductive development is arrested as a consequence of suppressed synthesis of juvenile hormone. Here, we describe survival in monarch butterflies as a function of the migrant syndrome. We show that migrant adults are longer lived than summer adults when each are maintained under standard laboratory conditions, that the longevity of migrant adults is curtailed by treatment with juvenile hormone and that the longevity of summer adults is increased by 100% when juvenile hormone synthesis is prevented by surgical removal of its source, the corpora allatum. Thus, monarch butterfly persistence through a long winter season is ensured in part by reduced ageing that is under endocrine regulation, as well as by the unique environmental properties of their winter roost sites. Phenotypic plasticity for ageing is an integral component of the monarch butterflies' migration-diapause syndrome.     

The case of the monarch butterfly: a verdict is returned

A publication reporting the harmful effects on the monarch butterfly of maize genetically modified to express insecticidal delta-endotoxins from the soil bacterium Bacillus thuringiensis (Bt) caused much public interest. A series of ecologically based studies were subsequently carried out to evaluate rigorously the impact of pollen from such crops and to quantify the risks. The results demonstrated that the commercial large-scale cultivation of current Bt-maize hybrids did not pose a significant risk to the monarch population. Further studies also demonstrated that Bt-expressing crops posed little risk to other nontarget insects, including beneficial insects such as pollinators and natural enemies.     

The monarch butterfly controversy: scientific interpretations of a phenomenon

The future development and use of agricultural biotechnology has been challenged by two preliminary studies indicating potential risk to monarch butterfly populations by pollen from corn engineered to express proteins from Bacillus thuringiensis. Likewise, these studies have also challenged the way in which science should be performed, published in scientific journals and communicated to the public at large. Herein, we provide a history of the monarch controversy to date. We believe a retrospective view may be useful for providing insights into the proper roles and responsibilities of scientists, the media and public agencies and the consequences when they go awry.     

Host plant species affects virulence in monarch butterfly parasites

1. Studies have considered how intrinsic host and parasite properties determine parasite virulence, but have largely ignored the role of extrinsic ecological factors in its expression. 2. We studied how parasite genotype and host plant species interact to determine virulence of the protozoan parasite Ophryocystis elektroscirrha (McLaughlin & Myers 1970) in the monarch butterfly Danaus plexippus L. We infected monarch larvae with one of four parasite genotypes and reared them on two milkweed species that differed in their levels of cardenolides: toxic chemicals involved in predator defence. 3. Parasite infection, replication and virulence were affected strongly by host plant species. While uninfected monarchs lived equally long on both plant species, infected monarchs suffered a greater reduction in their life spans (55% vs. 30%) on the low-cardenolide vs. the high-cardenolide host plant. These life span differences resulted from different levels of parasite replication in monarchs reared on the two plant species. 4. The virulence rank order of parasite genotypes was unaffected by host plant species, suggesting that host plant species affected parasite genotypes similarly, rather than through complex plant species-parasite genotype interactions. 5. Our results demonstrate that host ecology importantly affects parasite virulence, with implications for host-parasite dynamics in natural populations.     

Host plant adaptation during contemporary range expansion in the monarch butterfly

Herbivores that have recently expanded their host plant ranges provide opportunities to test hypotheses about the evolution of host plant specialization. Here, we take advantage of the contemporary global range expansion of the monarch butterfly (Danaus plexippus) and conduct a reciprocal rearing experiment involving monarch populations with divergent host plant assemblages. Specifically, we ask the following questions: (1) Do geographically disparate populations of monarch butterflies show evidence for local adaptation to their host plants? If so, what processes contribute to this pattern? (2) How is dietary breadth related to performance across multiple host species in monarch populations? (3) Does the coefficient of variation in performance vary across sympatric versus allopatric hosts? We find evidence for local adaptation in larval growth rate and survival based on sympatric/allopatric contrasts. Migratory North American monarchs, which have comparatively broad host breadth, have higher mean performance than derived nonmigratory populations across all host plant species. Monarchs reared on their sympatric host plants show lower coefficient of variation in performance than monarchs reared on allopatric hosts. We focus our discussion on possible mechanisms contributing to local adaptation to novel host plants and potential explanations for the reduction in performance that we observed in derived monarch populations.     

Migration of the monarch butterfly, Danaus plexippus: energy sources,

The origin and nature of the metabolic reserves of the monarch butterfly during its autumn migration through Missouri were examined. Information was obtained about the butterfly's protein, glycogen, lipid, and lipid-soluble pigment composition. The principal results showed that lipids, which made up ca. 45 per cent of the insect's dry weight, were the major reserve. Analyses of the lipid classes showed that triglycerides were the dominant class in each sex. Separate analyses of the thorax and abdomen showed that >90 per cent of the lipids were present in the massive fat body which is restricted to the abdomen. The adult female rapidly incorporated U-¹⁴C-d-glucose into abdominal glycerides. The rôle of larval reserves and nectar consumption in migration and ovarial maturation was discussed.     

Thoughts of a travelling ecologist 12.The plight of the monarch butterfly

<正>Nature conservation needs people who care about nature,and the efforts to convince people to care about the fate of nature has extensively relied on selected charismatic species,the"conservation icons".One famous example is the great panda,Ailuropoda melanoleuca,well known as the World Wide Fund for Nature(WWF)logo.When it comes to invertebrates,the     

Connecting the navigational clock to sun compass input in monarch butterfly brain

Migratory monarch butterflies (Danaus plexippus) use a time-compensated sun compass to navigate to their overwintering grounds in Mexico. Although polarized light is one of the celestial cues used for orientation, the spectral content (color) of that light has not been fully explored. We cloned the cDNAs of three visual pigment-encoding opsins (ultraviolet [UV], blue, and long wavelength) and found that all three are expressed uniformly in main retina. The photoreceptors of the polarization-specialized dorsal rim area, on the other hand, are monochromatic for the UV opsin. Behavioral studies support the importance of polarized UV light for flight orientation. Next, we used clock protein expression patterns to identify the location of a circadian clock in the dorsolateral protocerebrum of butterfly brain. To provide a link between the clock and the sun compass, we identified a CRYPTOCHROME-staining neural pathway that likely connects the circadian clock to polarized light input entering brain.     

Mazahua ethnobotany and subsistence in the monarch butterfly biosphere reserve, Mexico

This is the first report on Mazahua knowledge and classification of plants and mushrooms and the roles of these resources in the local economy in the Monarch Butterfly Biosphere Reserve, Mexico. A total of 213 useful plant species and 31 species of edible mushrooms were recorded. Fruits ofPrunus serotina, Rubus liebmanii, andCrataegus mexicana were the main wild fruit gathered by people (7.47, 4.40, and 1.82 tons of fruits per year, respectively), whereas their availability in the territory of the village was approximately 302.6, 6.0, and 34.188 tons.Brassica campestris, Rorippa nasturtium-aquaticum, Chenopodium berlandieri, and Amaranthus hybridus were the principal non-cultivated greens consumed by people (4.3, 0.5, 0.7, and 0.9 tons per year, while 23.6, 3.78, traces, and 46.0 tons, respectively, were available). Extraction of medicinal plants is low but gathering ofTernstroemia spp. flowers endangers local populations of these plants. All households of the village used fuelwood (1,767.2 tons per year), mainly of pine and oak species. Strategies for sustainable use of these resources are discussed     

Combining stochastic models with experiments to understand the dynamics of monarch butterfly colonization

Stochastic models are of increasing importance in ecology but are usually only applied to observational data. Here we use a stochastic population model to combine experimental and observational data to understand the colonization of old fields by monarch butterflies Danaus plexippus. We experimentally tested for density dependence in oviposition rates when predators were excluded, and we measured predation rates under natural conditions. Significance tests on the resulting data showed that both oviposition and predation were density dependent but could not show how oviposition and mortality combine to determine egg densities in nature. We therefore used our data to calculate the Akaike Information Criterion to choose between a nested suite of stochastic models that differed in their oviposition and mortality terms. When we simply fit the models to the observational data, the best model assumed density independence in both oviposition and predation. When we instead first estimated the oviposition rate at low density from experimental data, however, the best model included density dependence in oviposition, and a model that included density dependence in both oviposition and predation performed nearly as well. This result is consistent with our experiments and suggests that experiments can enhance the usefulness of stochastic models in ecology.