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The Chromosomes of Ten Species in the Avian Order Charadriiformes

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The Chromosomes of Ten Species in the Avian Order Charadriiformes AN ABSTRACT OF THE THESIS OF WILLIAM CHARLES RYAN for the DOCTOR OF PHILOSOPHY (Name) (Degree) in GENERAL SCIENCE presented on (Major) (Date) Title: THE CHROMOSOMES OF TEN SPECIES IN THE AVIAN ORDER cHARADR,r,p.rq ,---Redacted for Privacy Abstract approved ie,.......-,-,...,f ,- 1 u..---- ------ - IDald G.Humphy Chromosome complements of ten species of shorebirds, order Charadriiformes, were analyzed and compared.Mitotic chromosomes from the pigeon guillemot (Cepphus columba), Heermann's gull (Larus heermanni), the California gull (L. californicus), the western gull (L. occidentalis), the American avocet (Recurvirostra americana), the western willet (Catoptrophorus semipalmatus), Wilson's snipe (Capella gallinago), the wandering tattler (Heteroscelus incanum), and the black oystercatcher (Haematopus bachmani) were examined in this study. Short term cultures of bone marrow cells from each of these species provided a source of rapidly dividing cells.Mitosis was arrested with colchicine and the cells exposed to a hypotonic environ- ment prior to fixation in Carnoy's acetic-alcohol without chloroform. Fixed cells were resuspended in a 45% aqueous solution of acetic acid, air dried onto warmed cover slips and stained with lactic-acetic-orcein. In addition to these mitotic chromosomes, meiotic chromosomes of the black tern (Chlidonias niger) were fixed, air dried, stained and examined. Study of the slides of mitotic chromosomes revealed a marked similarity of karyotype in six of the ten species.These six were the oystercatcher, avocet, the three species of gulls and the pigeon guillemot.Study of the meiotic chromosomes of the black tern showed that it also had a chromosome complement similar to these six species. Three species, the western willet, Wilson's snipe and the wandering tattler, all members of the family Scolopacidae, were found to possess karyotypes quite different from the other members of the order.These last three species had diploid numbers between 90 and 100 and karyotypes which included many acrocentric elements but few metacentrics.This is in contrast to the other seven species which all had diploid numbers near 70 and karyotypes containing many non- acrocentric macrochromosomes. Finally, chromosomes of the domestic chicken (Gallus domes- ticus), a member of the closely related order Galliformes, were com- pared to the shorebird species.This comparison lead to the con- clusion that the seven species, with diploid numbers near 70 andmany non-acrocentric macrochromosomes, are evolutionarily descended along a common shorebird line and have many karyotypic characteris- tics in common with members of the closely related order Galliformes. Because of the markedly different karyotypes of the three members of the family Scolopacidae (snipe, willet and tattler) the suggestion is made that this family may have evolved from a different phylogenetic line than the other members of the order Charadriiformes. The Chromosomes of Ten Species in the Avian Order Charadriiformes by William Charles Ryan A THESIS submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy June 1971 APPROVED: Redacted for Privacy `professor of Geral Science in charge of major Redacted for Privacy Chairman of Department of General Science Redacted for Privacy Dean of Graduate School Date thesis is presented Typed by Nancy Kerley for William Charles Ryan ACKNOWLEDGMENTS I wish to express my sincere appreciation to my major professor, Dr. Donald G. Humphrey, for his invaluable advice, encouragement and direction in carrying out this investigation. To Dr. Paul Bernier of the Poultry Department must go special thanks for his generous assistance and advice on so many aspects of the study. I also am indebted to Miss Jamie C. Jenkins for her help in the preparation and analysis of karyograms and to Mrs. Jo Ann Ryan for her kind assistance in typing the various drafts of this dissertation. I am deeply indebted to numerous friends and colleagues of the General Science staff of Oregon State University and the Biology staff of Lewis and Clark College for encouragement, suggestions and assistance of every kind. Finally to my wife Marion, whose constant help, encouragement and understanding have been of immeasurable value throughout this study, go special thanks. TABLE OF CONTENTS Page INTRODUCTION 1 METHODS AND MATERIALS 19 Bone Marrow Culture Procedure 20 Harvesting of Arrested Cells 22 Fixation of Cells 24 Preparation of Slides 25 Slide Analysis and Preparation of Karyograms 27 RESULTS 29 DISCUSSION OF RESULTS 46 Structural Evolution of Karyotypes 48 Interpretation of Karyotypes 52 Phylogenetic Relationships in the Order Charadriiformes 69 SUMMARY AND CONCLUSIONS 75 BIBLIOGRAPHY 78 LIST OF TABLES Table Page 1 Chromosome arm ratios for five species of gull (Larus), 53 2 Pigeon guillemot - chromosome arm ratios. 57 LIST OF FIGURES Figure Page 1 Black Oystercatcher leAo1 bachmani Female karyotype 34 2 Wilson's Snipe Capella gallinago Male karyotype 35 3 Western Willet Catoptrophorus semipalmatus Male karyotype 36 4 American Avocet Recurvirostra americana Male karyotype 37 5 Western Gull Larus occidentalis Female karyotype 38 6 California Gull Larus californicus Female karyotype 39 Heermanns Gull Larus heermanni Male karyotype 40 8 Pigeon Guillemot Cepphus columba Female karyotype 41 9 Pigeon Guillemot Cepphus columba Male karyotype 42 10 Meiotic Chromosomes of Black Tern Chlidonias 43 11 Mitotic Chromosome Spread from Wandering Tattler Heteroscelus incanum 44 12 Domestic chicken Gallus domesticus Male karyotype 45 THE CHROMOSOMES OF TEN SPECIES IN THE AVIAN ORDER CHARADRIIFORMES INTRODUCTION For more than 70 years biologists have recognized that chromo- somes, the bearers of the hereditary particles (Sutton, 1903), per- haps more than any other structure reflect the phylogenetic history of a taxonomic group,White (1954, p.1) points out that evolutionary transformations have their origin in the chromosomes, and, being the physical basis of heredity, these bodies furnish the material source for evolutionary change. He goes on to say, The differences in chromosome number and chromosome shapes which frequently distinguish one species from its relatives throw new light on the problem of taxonomy, while the cytological characteristics of whole groups of organisms have a bearing on the differentiation of the higher categories of our classification and on the problem of their evolutionary patterns, plasticity, and adaptive- ness (White, 1954, p. 2). As early in the history of chromosome study as 1905, McClung (1905) suggested that advances in taxonomic knowledge would come about "by a comparison of the germ cells and body characters in nearly related species, by observing the differences in germ cells of in- dividuals that vary from the type of the species... It Since the beginning of the 20th century cytophylogeny, the study and comparison of the chromosome complements of different species 2 in an effort to elucidate phylogenetic relationships, has yielded signif- icant results in a large number of taxonomic groups.However, cyto- phylogeny of vertebrates, which, because of technical difficultieswas generally neglected during the first half of the 20th century, has only recently seen great progress.Yet in spite of this recent rapid ad- vance in vertebrate cytophylogeny one group, the birds, has continued to be neglected.This is somewhat surprising in light of the fact that of all vertebrate classes, Ayes is probably the best known taxonomi- cally and would provide an excellent opportunity to examine the value of cytotaxonomy by comparison with classification basedon morpho- logical characteristics, As Darlington (1957,p. 236) put it, In some ways, birds are the best known animals. Almost all existing species of them are probably known,some 8600 full species (Mayr, 1946; Mayr and Amadon, 1951) plus thousands of geographical subspecies, and the dis- tributions of many of the species are known in detail. The reasons for this lack of knowledge about the chromosomes of birds are two.First, the class Ayes has long been notoriousas being "exceptionally difficult" (White, 1954, p. 283) to work with cytogenetically. As a result many cytologists have, understandably, selected less refractory animals for study.Secondly, the presence of a large number of "microchromosomes" in every known bird karyo- gram has made determination of the exact chromosome number a virtual impossibility (Stenius et al,, 1963; Ohno, 1961; Itoh; 1969; Bhatnagar, 1968),In spite of these difficulties some species, 3 especially those of commercial importance, have been intensively studied. The domestic chicken, for example, has been a favorite subject throughout the brief history of cytogenetics,Between 1906 and 1950, there appeared in the literature at least 29 separate reports of studies of chicken chromosomes (Brant, 1952),Since then the total has at least doubled. And yet, when R. N. Shoffner (1965) summarized our knowledge about the chromosomes of the chicken he listed the fol- lowing eight points. 1. The chromosome number is uncertain. 2.The microchromosomes are unclassified as to number, size, shape, heterochromatic condition, random dis- tribution and function, 3.The constancy of either meiotic or mitotic division products for the microchromosomes is questionable. 4.There is little or no knowledge about the occurrence or the effects of aberrant chromosomes such as translocations or inversions in fowl populations, 5,There is little knowledge
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