Ophryocystis elektroscirrha sp. n., a Neogregarine Pathogen of the Monarch Butterfly Danaus plexippus (L.) and the Florida Queen Butterfly D. gilippus berenice Cramer1
01 May 1970-Journal of Eukaryotic Microbiology (Blackwell Publishing Ltd)-Vol. 17, Iss: 2, pp 300-305
TL;DR: This neogregarine pathogen infects the hypodermal tissue, remains in micronclear schizogony until after pupation of the host, and then rapidly completes morphogenesis in the tissue that becomes the scales of the adult butterfly.
Abstract: SYNOPSIS. Naturally occurring populations of the monarch butterfly, Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer were found infected with Ophryocystis elektroscirrha sp. n. This neogregarine pathogen infects the hypodermal tissue, remains in micronclear schizogony until after pupation of the host, and then rapidly completes morphogenesis in the tissue that becomes the scales of the adult butterfly. The adult thus carries the spores externally; no internal infection was detected. The pathogen is unique in the genus Ophryocystis because: other species have all been reported from the Malphigian tubules of Coleoptera; no pseudopodial attachments of schizonts to host tissue were seen; the merozoites were motile; the cystic membrane surrounding the zygote was tenuous, and the sporont developed with no apparent membrane other than the spore wall: and the spore wall appeared amber in transmitted light when morphogenesis was completed.
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TL;DR: From this expos it is clear that research on migration warrants a multitude of techniques and approaches for a complete as possible understanding of a very complex evolutionary syndrome.
Abstract: Long distance migration has evolved in many organisms moving through different media and using various modes of locomotion and transport. Migration continues to evolve or become suppressed as shown by ongoing dynamic and rapid changes of migration patterns. This great evolutionary flexibility may seem surprising for such a complex attribute as migration. Even if migration in most cases has evolved basically as a strategy to maximise fitness in a seasonal environment, its occurrence and extent depend on a multitude of factors. We give a brief overview of different factors (e.g. physical, geographical, historical, ecological) likely to facilitate and/or constrain the evolution of long distance migration and discuss how they are likely to affect migration. The basic driving forces for migration are ecological and biogeographic factors like seasonality, spatiotemporal distributions of resources, habitats, predation and competition. The benefit of increased resource availability will be balanced by costs associated with the migratory process in terms of time (incl. losses of prior occupancy advantages), energy and mortality (incl. increased exposure to parasites). Furthermore, migration requires genetic instructions (allowing substantial room for learning in some of the traits) about timing, duration and distance of migration as well as about behavioural and physiological adaptations (fuelling, organ flexibility, locomotion, use of environmental transport etc) and control of orientation and navigation. To what degree these costs and requirements put constraints on migration often depends on body size according to different scaling relationships. From this expos it is clear that research on migration warrants a multitude of techniques and approaches for a complete as possible understanding of a very complex evolutionary syndrome. In addition, we also present examples of migratory distances in a variety of taxons. In recent years new techniques, especially satellite radio telemetry, provide new information of unprecedented accuracy about journeys of individual animals, allowing re-evaluation of migration, locomotion and navigation theories. (Less)
1,037 citations
Cites background from "Ophryocystis elektroscirrha sp. n.,..."
...Altizer et al. (2000) examined how variation in parasite prevalence relates to host movement patterns, by studying the obligate parasite Ophryocystis elektroscirrha (McLaughlin and Myers 1970) and its host, the Monarch butterfly Danaus plexippus (L.) (Lepidoptera: Nymphalidae)....
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TL;DR: Study of a protozoan parasite of monarch butterflies found that higher levels of within-host replication resulted in both higher virulence and greater transmission, thus lending support to the idea that selection for parasite transmission can favor parasite genotypes that cause substantial harm.
Abstract: Why do parasites harm their hosts? Conventional wisdom holds that because parasites depend on their hosts for survival and transmission, they should evolve to become benign, yet many parasites cause harm. Theory predicts that parasites could evolve virulence (i.e., parasite-induced reductions in host fitness) by balancing the transmission benefits of parasite replication with the costs of host death. This idea has led researchers to predict how human interventions—such as vaccines—may alter virulence evolution, yet empirical support is critically lacking. We studied a protozoan parasite of monarch butterflies and found that higher levels of within-host replication resulted in both higher virulence and greater transmission, thus lending support to the idea that selection for parasite transmission can favor parasite genotypes that cause substantial harm. Parasite fitness was maximized at an intermediate level of parasite replication, beyond which the cost of increased host mortality outweighed the benefit of increased transmission. A separate experiment confirmed genetic relationships between parasite replication and virulence, and showed that parasite genotypes from two monarch populations caused different virulence. These results show that selection on parasite transmission can explain why parasites harm their hosts, and suggest that constraints imposed by host ecology can lead to population divergence in parasite virulence.
286 citations
Cites background from "Ophryocystis elektroscirrha sp. n.,..."
...We studied the protozoan parasite Ophryocystis elektroscirrha (28), which commonly infects wild populations of the monarch butterfly (Danaus plexippus) (29, 30)....
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Journal Article•
TL;DR: The present paper reconstructs the history of understanding the migration of the monarch butterfly in North America and reflects the spirit in which Charles Remington, then a graduate student at Harvard, and his friend and colleague Harry Clench founded The Lepidopterists' Society are reflected.
Abstract: Since 1857, amateurs and professionals have woven a rich tapestry of biological information about the monarch butterfly's migration in North America. Huge fall migrations were first noted in the midwestern states, and then eastward to the Atlantic coast. Plowing of the prairies together with clearing of the eastern forests promoted the growth of the milkweed, Asclepias syriaca, and probably extended the center of breeding from the prairie states into the Great Lakes region. Discovery of overwintering sites along the California coast in 1881 and the failure to find consistent overwintering areas in the east confused everyone for nearly a century. Where did the millions of monarchs migrating southward east of the Rocky Mountains spend the winter before their spring remigration back in to the eastern United States and southern Canada? Through most of the 20th century, the Gulf coast was assumed to be the wintering area, but recent studies rule this out because adults lack sufficient freezing resistance to survive the recurrent severe frosts. Seizing the initiative after C. B. Williams' (1930) review of monarch migration, Fred and Norah Urquhart developed a program that gained the interest of legions of naturalists who tagged and released thousands of monarchs to trace their migration. Just as doubts in the early 1970s over whether there really were overwintering aggregations of the eastern population, on 2 January 1975 two Urquhart collaborators, Kenneth and Cathy Brugger, discovered millions of monarchs overwintering high in the volcanic mountains of central Mexico. This allowed a synthesis of the biology of this remarkable insect, including its migration and overwintering behaviors, its spread across the Pacific Ocean to Australia, its coevolution with milkweeds, and its elaborate milkweed-derived chemical defense which probably makes possible the dense aggregations during the fall migration and at the overwintering sites. Many important questions remain. Can monarchs migrate across the Gulf of Mexico? Can they migrate at night? Do they exploit strong tailwinds? Do they migrate to Central America? Do they overwinter elsewhere in Mexico or Central America? How much interchange is there between the eastern and western North American populations? How important is the fall migration along the Atlantic coast compared to the migration west of the Appalachian Mountains? What causes annual fluctuations in the size of the fall migrations? Beautiful and mysterious, the monarch's overwintering colonies in Mexico rank as one of the great biological wonders of the world. Unfortunately, these colonies are the monarch's Achilles' heel because of human population growth and deforestation in the tiny Oyamel fir forest enclaves. Additional risks arise from the increasing use of herbicides across North America which kill both larval and adult food resources. As a result, the migratory and overwintering biology of the eastern population of the monarch butterfly has become an endangered biological phenomenon. Without immediate implementation of effective conservation measures in Mexico, the eastern migration phenomenon may soon become biological history. In writing this paper for Charles Remington's honorarial issue of the Journal of the Lepidopterists' Society, fond memories flood forth of my days as his graduate student at Yale University from 1953 to 1957. My very first seminar lecture was on the migration of the monarch butterfly, Danaus plexippus (L.), and this set the stage for what will soon be 40 years of studying diverse aspects of the biology of this VOLUME 49, NUMBER 4 305 fascinating creature (reviews in Brower 1977a, 1984, 1985a, 1985b, 1986, 1987b, 1988, 1992). The present paper reconstructs the history of understanding the migration of the monarch butterfly in North America. To my knowledge, a detailed analysis of the ideas and the people who developed them has never been attempted. The story, a result of the combined observations of professional and amateur lepidopterists over more than a century, reflects the spirit in which Charles Remington, then a graduate student at Harvard, and his friend and colleague Harry Clench founded The Lepidopterists' Society in 1947 (Clench 1977). My purpose is to weave together the strands, to follow some of the red herrings, and to discuss several aspects of the migration biology that are still incompletely understood. Timely resolution of these questions should enhance efforts to preserve the monarch's mass migratory and overwintering behaviors which, regrettably, have become an endangered biological phenomenon (Brower & Pyle 1980, Brower & Malcolm 1989, 1991). The first great student of the monarch butterfly was Charles Valentine Riley, who emigrated from England and rose to lead midwestern, and then national entomology in the USA (Packard 1896, Essig 1931). In addition to being a first rate scientist, Riley was a talented artist who beautifully illustrated his descriptions of insect natural histories, and he fostered the English tradition of collating and publishing letters from a diversity of field observers, including many on the migration of the monarch. Anecdotal science on the monarch predominated well into the 20th century. In 1930, C. B. Williams of Edinburgh University reviewed monarch migration in his book, The Migration of Butterflies, which he periodically updated (Williams 1938, 1958, Williams et al. 1942). Shortly after the founding of The Lepidopterists' Society, Williams (1949:18) called for information from members and defined questions for much of the migration research that would follow: \"What happens to the butterflies that fly through Texas in the fall? Do they go on to Mexico? If so, do they hibernate there, or remain active, or breed?\" University of Toronto entomologist Fred A. Urquhart and his wife Norah took up the Williams challenge in 1940 and began tracing the fall migration of the monarch via a long-term tagging program, which would come to involve more than 3,000 research associates (Urquhart 1941,1952,1960,1978,1979,1987, Anon. 1955). The Urquharts communicated with their collaborators through an annual newsletter, published numerous papers on monarch biology, and carried on the tradition of incorporating amateurs' notes in their writings. According to Urquhart and Urquhart (1994), the final newsletter to their Insect Migration Association was issued as Volume 33 in 1994. Speculations about the destination of the eastern monarch migration 306 JOURNAL OF THE LEPIDOPTERISTS' SOCIETY became increasingly confused throughout the first three quarters of the 20th century because of the mysterious disappearance of what had to be vast numbers of butterflies that annually bred over an area of at least three million square kilometers. Many tortuous hypotheses were devised until resolution came in Urquhart's August 1976 National Geographic article announcing the discovery of the phenomenal overwintering aggregations in Mexico. This culmination of the Urquharts' lifetime efforts was one of the great events in the history of lepidopterology. FIRST OBSERVATIONS OF THE FALL MIGRATION: REPORTS FROM KANSAS TO CONNECTICUT Aside from a possible sighting of monarchs migrating in eastern Mexico during one of Christopher Columbus's expeditions (Doubleday & Westwood 1846-1852:91), D'Urban (1857) was apparently the first to report a migration of monarch butterflies. He described the butterflies appearing in the Mississippi Valley in \"such vast numbers as to darken the air by the clouds of them\" (p. 349). During September 1867 in southwestern Iowa, Allen (in Scudder & Allen 1869) described monarchs gathered in several groves of trees bordering the prairie \"in such vast numbers, on the lee sides of trees, and particularly on the lower branches, as almost to hide the foliage, and give to the trees their own peculiar color\" (p. 331). Although this clustering behavior was initially interpreted as a means of avoiding strong prairie winds, it soon became evident that it was associated with large southward movements of monarchs in the fall. The first collated evidence of massive fall migrations was published in 1868 by two American entomologists, Benjamin Dann Walsh and Charles Valentine Riley, who had independently emigrated from England to Illinois and were both keen to establish entomology as a science useful to farmers. Additionally, as evidenced in Darwin's correspondence (in F. Darwin and Seward 1903a:248-251, 1903b:385-386), Walsh and Riley were both influenced by The Origin of Species (Darwin 1859). Walsh, born in 1808, developed his interest in insects when he was nearly 50 years old, and launched his career in 1865 as associate editor of the Practical Entomologist in which he wrote, reprinted and edited numerous articles and letters, and answered letters from curious people and farmers besieged by insect pests. Within a decade he became the first Illinois State Entomologist (Riley 1870, Darwin and Seward 1903a). In contrast, Riley, born in 1843, had left his family home in England at the age of 17. By the time he was 20, he had begun publishing entomological notes in the Chicago-based Prairie Farmer (Ashmead 1895) and shortly thereafter became the journal's prolific entomological editor. In September 1868 the two men founded The American Entomologist, which Riley continued after Walsh died prematurely in VOLUME 49, NUMBER 4 307 1869 (Riley 1870). In 1868 Riley was appointed State Entomologist of Missouri, in 1876 he moved to Washington, D.C. to become Chief of the newly founded U.S. Entomological Commission, and shortly thereafter he founded the Smithsonian Institution's insect collections. Beginning in 1864, Riley used the Prairie Farmer to establish a correspondence network with midwestern farmers who were plagued by the migratory Rocky Mountain Locust. Combining his observations and high quality drawings with the information in hundreds of letters from farmers and lay
268 citations
TL;DR: The trees indicate that the genus Cryptosporidium has a closer phylogenetic affinity with the gregarines than with the coccidia, and these results do not support the present classification of the cryptosporidiidae in the suborder Eimerioirina Léger, 1911.
Abstract: Morphological and life cycle features of the tissue cyst-forming coccidia have been difficult to interpret in devising taxonomic classifications for the various genera. In this study, we amplified the full small subunit rRNA gene sequence of Isospora robini McQuistion and Holmes, 1988, and the partial sequence of Isospora gryphoni Olsen, Gissing, Barta, and Middleton, 1998 by PCR. Both of these species vary from Isospora species of mammals in having Stieda bodies on the sporocysts. The sequences were cloned and sequenced and were incorporated into an alignment with other Isospora species lacking Stieda bodies as well as with other coccidia. Maximum parsimony analysis of these sequences produced a single most parsimonious tree that placed I. robini and I. gryphoni in a clade containing various other eimeriid species. The Isospora species lacking Stieda bodies were in the sarcocystid clade. Similar results were found by maximum likelihood analysis. These findings indicate that the genus Isospora as defined by several authors is polyphyletic. Taxonomic changes to the genus Isospora would have to incorporate the 2 major clades found by molecular phylogenetic analysis. Isospora species with Stieda bodies should be classified in the family Eimeriidae, whereas those without Stieda bodies should remain in the family Sarcocystidae.
260 citations
Cites methods from "Ophryocystis elektroscirrha sp. n.,..."
...Oocysts of the neogregarine Ophriocystis elektroscirrha McLaughlin and Myers, 1970, were collected from monarch butter¯ies (Danaus plexippus L.), which were kindly provided to us by Sonia M. Altizer, University of Minnesota....
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...They were identi®ed as O. elektroscirrha based on an oocyst length of 14 lm, consistent with the original species description by McLaughlin and Myers (1970)....
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TL;DR: Results showed that parasitized butterflies exhibited shorter flight distances, slower flight speeds, and lost proportionately more body mass per km flown, suggesting that poorer flight performance among parasitized hosts was not directly caused by morphological constraints.
Abstract: Monarch butterflies (Danaus plexippus) are parasitized by the protozoan Ophryocystis elektroscirrha throughout their geographical range. Monarchs inhabiting seasonally fluctuating environments migrate annually, and parasite prevalence is lower among migratory relative to non-migratory populations. One explanation for this pattern is that long-distance migration weeds out infected animals, thus reducing parasite prevalence and transmission between generations. In this study we experimentally infected monarchs from a migratory population and recorded their long-distance flight performance using a tethered flight mill. Results showed that parasitized butterflies exhibited shorter flight distances, slower flight speeds, and lost proportionately more body mass per km flown. Differences between parasitized and unparasitized monarchs were generally not explained by individual variation in wing size, shape, or wing loading, suggesting that poorer flight performance among parasitized hosts was not directly caused by morphological constraints. Effects of parasite infection on powered flight support a role for long-distance migration in dramatically reducing parasite prevalence in this and other host‐pathogen systems.
232 citations
References
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TL;DR: A new systematic division of the suborder Schizogregarina is proposed on the basis of the comparative morphology of the different stages of the life-cycle of theDifferent genera.
Abstract: SUMMARY. The author proposes a new systematic division of the suborder Schizogregarina on the basis of the comparative morphology of the different stages of the life-cycle of the different genera. Two families, Dischizae and Monoschizae, are divided into a total of 6 tribes: The Dischizae into Ophryocystinae with the genera Ophryocystis, Mattesia, Menzbieria, Lipocystis and Sawayella, and Machadoellinae with the genera Machadoella and Farinocystis; Monoschizae into the tribe Caulleryellinae with genera Caulleryella, Tipulocystis and Merogregarina, the tribe Syncystinae with the genera Syncystis and Lipotropha, the tribe Schizocystinae with the genera Schizocystis and Siedleckia and the tribe Selenidiinae with the genera Selenidium and Meroselenidium.
31 citations
TL;DR: This is the first report of a virus infection in this family of butterflies, Danaus plexippus, and its possible role as a principal factor in populations fluctuations is discussed.
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