Ha, Systematics The ancients looked for « natural order (Rosines) which would explain the bewildering diversity of phenomena, [Mayr 1969, p. 1] comparative biological sciences such as ornithology help us to understand the evolution of diversity. Closely related species have immediate common ancestors, which. in turn, had earlier common ancestors. The mee of genealogical relationships among species—their phylogeny—provides a foundation for taxonomic classification and a framework for underst ior, ecology, and morphology. The challenge of reconstructing the history of life belongs to a field of scholarly endeavor called systematics. Systematists are scientists who evaluate evolutionary relationships a of fossils. preserved specimens. behavior, and, increasingly, the genetic code of life itself, DNA, This chapter presents an overview of avian sy: ding the evolution of behav- ong organisms through comparisons ystematies. Firse is a sum- mary of the nature of species. the fundamental units of biological classi~ fication, Then follow the relation between phylogeny and formal classi- fication and the attributes of birds that provide clues to evolutionary history. The chapter concludes with an introduction to some of the pri- mary methodologies of systematics, including cladisties—the study of evo- nd biochemical yenetics—the study of changes in an organism's DNA. Comparisons of DNA sequences now enable unprecedented reconstructions of the evolution of modern birds. lutionary branching sequences—a Species and Speciation The diversity of life is a result of three evolutionary processes: phyletic evolution, the gradual change of a single lineage: speciation, the splitting of one phyletic lineage into two or more: and extinction, the termination52 CHAPTER THREE Present A. c Deg F Extinction Time Speciation <—“hyletic evolution» FIGURE 3-1 Diversification of evolutionary lineages includes speciation (circled nodes), the splitting of lineages; extinction, the loss of lineages; and phyletic evolution, the gradual change of a lineage with time. Clusters of similar, related taxa, such as C, D, and E (present in modern times), result from these changes. Taxon A stands alone because its Taxon B went extinct. Taxon F is not related to the other taxa, which had 2 recent common ancestor. of a lineage (Figure 3-1). If we had a complete record of life on Earth, we could accurately reconstruct the historical patterns of speciation and phyletic evolution. Extinctions, however, fragment the historical record; they erase the connections between related lineages, Species are the fundamental units of biological classification. Bird species have characteristic sizes. shapes. songs. and colors. as well as ecological niches and geographical ranges. Different species may interact ecologi- cally, but they do not freely exchange genes or novel genetic-based adap- tations. By a definition called the biological species concept, “Species are groups of interbreeding natural populations that are reproductively iso- lated from other such groups” (Mayr 1970, p. 12). The criteria in the definition of biological species are the reproductive compatibility of in- dividual organisms and the potential for the blending of differences between two populations. ‘The evolutionary legacy of the earliest birds includes roughly 100,000 species, of which only 1 in 10 is now with us, Behind this legacy lies the process of speciation—the multiplication of species through the division of one species into two or more as a result of the genetic divergence of isolated populations. Geographical separation of populations reduces the exchange of genes, thereby allowing independent divergence and enabling speciation. Most species of birds evolve as geographical isolates, although other kinds of reproductive isolation may sometimes play a role Bird populations become geographically isolated in two principal ways First, pioneering individual birds may colonize an oceanic island, for esample, and thus are separated from their main population on the main- land oF on other islands, Classic examples of divergence and speciation come from remote ishands such as the Gakipagos and Hawaiian archipel- agos. The birds on the Channel Islands off the coast of southern Califor- nia also are distinct, as are the kingfishers on small satellite islands off the coast of New Guinea. On the mainland, islands of special habitats, such as desert oases or subalpine mountain forests, may set a similar stage for divergence tion of the populations that occupy them. Fragmentation of habitats chat were once continuous is the second way in which bird populations may become isolated, Some ornithologists be- lieve that the dry. cold climates of the Pleistocene epoch, for example. shrank the great Amazonian rain forests into much smaller fragments surrounded by grasslands, Restricted to these forest refuges, toucans, manakins, and flycatchers were ng the many kinds of birds that underwent isolation and speciation (Figure 3-2) Remnant populations are one of the consequences of historical changes. Ostriches, now restricted to Africa, once roamed throughout Asia, Hummingbirds, now restricted to North and South America, once hovered in what is now Germany. Tiny colorful relatives of kingfishers, called todies (see Figure 2-18-1), are currently found only on the Greater Antilles of the West Indies, but they once ako lived in Wyoming and France (Olson 1985). Similarly, the endangered Florida Scrub Jay is now separated from the Western Scrub Jay by more than 30000 kilometers (Fig- ure 3-3). Widely separated areas may consequently share peculiar taxa. The African River Martin inhabits the Congo River basin, whereas the closely related White-eyed River Martin inhabits only Thailan lated species are found between these locations. Although the general patterns of geographical speciation in birds are well known, the details of the process of speciation are not. Slow adap- tive divergence of fragments of large populations and rapid genetic reor= ganization in small populations appear to be the primary modes of spec ation. Still to be resolved are the roles of ecological and social adaptations, as well as the timing and nature of the related genetic changes. Concerns about the practical application of the biological species concept also prompt some omithologists to question its working, merits and co recommend new approaches to the study of speciation and geographical variation in birds (McKitrick and Zink 1988; Cracraft_ 1989), Chapter 19 considers both the process of speciation and the current debates about che species concept. ind speci 10 Tee Scientific Names A logical system of scientific namex for each species is an essential pre- requisite for the study of the biology of birds because nonscientific names of birds tend to vary with locale. The American Goldfinch, for example, is also locally called the yellow-bird, thistle-bird, wild canary, and beet-bird 53. ‘SYSTEMATICS54 Kilometers Pears seen ws Lettered Aracari | Lettered Aracari | Green Aracari (PA. inscriptus) | (P. L humboldti) FIGURE 3-2 The ranges in Amazonia of three small toucans (the Green Aracari and two subspecies of the Lettered Aracari) reflect past isolation in refuges of wet forest habitats. [After Haffer 1974. © Nuttall Ornithological Club] (Figure 3-4). Each human culture employs its local bird names, fostering the need for standardized names that allow ornithologists throughout the world co communicate efficiently and exactly. The science of naming and classifying organisms, including birds, ac~ cording to standardized rules is called taxonomy, and the scientists who do55. SYSTEMATICS FIGURE 3-3 Distributions of the Florida Scrub Jay (star), now restricted to central Florida, and of the related Western Scrub Jay (shading) in the western United States and Mexico, Past climate and habitat changes fragmented the continuous distributions of this species, isolating the Florida Scrub Jay as a relict and endangered species. [After Curry et al, 2002] FIGURE 3-4 The American Goldfinch has many local names, such as wild canary, yellow-bird, thistle-bird, and beet-bird. [Courtesy of A. CouickshanloVIREO]56 (CHAPTER THREE this work are taxonomists. A taxon (pl. taxa) is any group of animals that is recognized in a classification, The Class Aves is a taxon that includes all species of bireb The rules of taxonomy are based on the system of nomenclature ‘eloped from 1735 to 1758 by Carolus Li Swedish botanist. Linnaeus assigned two latinized names to each species: the first denotes the genus—a group of similar species: the second denotes the species. Thus, the American Goldfinch is known formally as Carduelis tristis, which is a taxon that includes all populations of chat species. This particular com- bination of names is unique; no other bird species—indeed, no other an- imal species—may have this same pair of names. Before the work of Linnaeus, names were not standardized in length but consisted instead of a string of descriptive Latin words. The Great Black-backed Gull, for ex- ample, was once Lanis maxims ex alba et nigro feu cacnuleo igrinte varius (Willoughby and Ray 1676). Now it is simply Larus marinus, In addition to their Latin scientific names, birds have English names, as well as names in other languages. The American Ornithologists’ Union establishes and regularly revises a list of valid names. both English and sci- entific, for all bird species in North America. The International Ornitho- logical Congress prepares lists of recommended standardized names in English, French, and Spanish (e.g., Gill and Wright 2006) If we examine an assortment of birds, we can see the possibility of constructing a hierarchy, or ranking, of differences. A cursory survey of North American birds will distinguish woodpeckers from owls. Less obvious are the differences between the Downy Woodpecker. the Red-bellied Woodpecker, and the Northern Flicker or the differences between the Great Horned Owl, the Barred Owl, and the Eastern Screech Owl. Recognition of the subtle differences between the Downy Wood- pecker and the Hairy Woodpecker (Figure 3-5) or between the Eastern Screech Owl and the Whiskered Screech Owl requires even more expertise Related taxa—those having a common evolutionary history or geneal- ogy. as do the species of woodpeckers or owls or as do birds as a whole— constitute a lineage. Ornithologists classify the diverse species of modem birds into 30 different major lineages. or orders. Owls and woodpeckers de TABLE 3-1 Classification of three species of Woodpeckers f= Downy Hairy Northern Woodpecker ‘Woodpecker Flicker Aves Aves Aves Order Piciformes. Piciformes Piciformes Family Picidae Picidae Picidae Genus Picoides Picoides Colapres Species pubescens villosus surarus Nove: Full scientific names include the ge stricly speaking, the scientific name of the Downy Woodpecker, for ex is Picodes pubescens us as well as the species and so, ple,@ ® FIGURE 3-5 Three species of woodpeckers: (A) Downy Woodpecker; (8) Hairy Woodpecker; (C) Northern Flicker. The Downy Woodpecker and the Hairy Woodpecker are more closely related to each other than either isto the Northern Flicker are in different orders, Strigiformes and Piciformes, respectively. Note that the name of each order ends in “formes.” In turn, each of the 30 or: comprises a hierarchical set of families and genera. All woodpeckers are classified in the same order and in the same family, the Picidae. Each bird family name ends in “-idae.” The very similar, closely related Downy Woodpecker and Hairy Woodpecker are classified in the genus Picoides, but the less closely related Northern Flicker is classified in the genus Colaptes, along with other species of flickers (Table 3-1) Classification and Phylogeny The process of naming and classifying birds is an ancient and continuing one. Omitholegiae, by Francis Willoughby and John Ray, published in 87 SYSTEMATICS58 CHAPTER THREE 1676, was the first formal classification of birds. This “comerstone of mod- ern systematic ornithology” (Zimmer 1926) arranged all birds then known into a logical, hierarchical classification, Nearly a century later, Linnaeus used this elementary classification as the model for subsequent classifica tions. These early efforts. however, classified birds according to supert cial adaptations to aquatic versus terrestrial habitats, for example, rather than according to evolutionary relationship. Charles Darwin’s theory of evolution by natural selection transformed the philosophical basis of systematics into one based on common ances- tries, In his classic work On the Origin of Species by Means of Nanural Selee- rion (1859), Darwin reflected on the hierarchy of similarity due (0 evo- lutionary relationships: 1 believe that the arrangement of the groups within each class. in due subordination and relation to each other, must be strictly genealogical in order co be natural: buc that the amount of difference in the several branches or groups. though allied in the same degree in blood to their common progenitor, may differ greatly, being due to the different degrees of modification which they have undergone; and this is expressed by the forms being ranked under different genera, families, sections, or orders. [Darwin 1859, p. 420] Prevailing classifications of birds attempt to portray the evolutionary relationships of the various lineages as proposed by Darwin. Theoreticall each taxon is monophyletic: that is, it contains sets of birds, called clades, related by evolutionary descent from a common ancestor. A hierarchical organization of taxa indicates the relative closeness or distance of the evo- lutionary relationships among those taxa. Taxonomic Characters Reconstruction of the evolutionary history of birds requires the analysis of specific traits, called characters, that are shared as a result of common ancestry. Conservative characters—those that do not easily change in the course of ecological adaptation—are of the greatest value because they re tain clues to ancestors. A constant challenge to accurate reconstruction is the possibility of convergence between unrelated species, which is preva~ lent in both external appearance and specific attributes (see page 19) Darwin's champion, Thomas H. Husley. helped to lay the founda tions of modern systematics in birds with his study of the arrangement of the bones of the avian bony palate, the skeletal partition between the nasal cavities and the mouth (Huxley 1867; Figure 3-6). Succeeding genera- tions of ornithologists added new characters to the taxonomic tool kit Some of the most important ones were the form of the nostrils, the seruc ture of the leg muscles and tendons of the feet, the arrangement of toes. and the morphology of the vocal apparatus. Behavior, vocalizations, andMaxillary Palatine \ parasphenoid ad i rostrum Joss [| Basipterygoid Prerygoid process Quadiatojugal Quadrate FIGURE 3-6 sony palate of the Rhea, showing the complex arrangement of bones that represent the unique paleognathous palace of ratite birds. Other orders of birds have different arrangements of the elements of the bony palate. [From Fundamentals of Ornithology, 2nd ed, by J. Van Tyne and A.J. Berger. Copyright 1976 John Wiley @ Sons, Ine reprinted by permission of Joli Wiley @ Sons, nc proteins yielded clues to evolutionary relationships among some birds. So did plumage patterns of downy young (Figure 3-7) Unique characters define related groups of species—chat is, those with 4 conmion ancestor. Songbirds, the members of the Order Passeriformes, for example, have several unique characters. They have a preen gland with a unique nipple structure (ee Figure 4-13) and unique sperm Gee Figure 14-9). They also have a specialized perching foot with a large hal- lux (rear-directed toe). uniquely arranged deep tendons, and simplified foot muscles that facilitate perching at the expense of more delicate toe movements (Raikow 1982). These features indicate that members of the Order Passeriformes evolved from a common ancestor; that is, they are monophyletic. Generally. the more complex the character, che less likely it is that anatomical details will be precisely the same, owing to convergence among unrelated species. The details of toot structure reveal how unrelated birds evolved similar, but not identical, arrangements of the four toes (Bock and Miller 1959). Although most perching birds have anisodactyl feet, with three forward toes and one rear toe (Figure 3-8, page 61), at least eight groups—including most woodpeckers and their allies, most parrots, cuckoos, owl, the Osprey, curacos, and some swiltshave zygodactyl feet, with two forward and two rear toes. Different orientations of the working surfaces (condyles) of cuckoo toe bones versus woodpec! 59 SYSTEMATICS,60 (CHAPTER THREE Avocet 47 ‘Charadtiidae. y \ Vy Thick-knee FIGURE 3-7 Plumage-color patterns of downy young shorebirds provide clues to their evolutionary relationships (represented by branching lines). [4fter Jeh! 1968] bones, for example, indicate that these unrelated birds have evolved the ygodactyl foot arrangement in different ways. Still other toe configurations are possible. The trogons appear to have the zygodactyl toe arrangement, but the trogon’s second toe, not its fourth, is directed backward, forming what is called the heterodactyl toe arrange- ment, The syndactyl foot, with two or three toes fused basally, charac terizes the Order Coraciiformes: and the pamprodaetyl toot, with all four toes directed forward, characterizes the mousebirds (Order Coliiformes) and some swifts (Order Apodiformes). Despite the advances in grouping birds on the basis of characters such as foot structure, progress in systematics started © stall in the first half of the twentieth century. Cases of convergence loomed large, and omnithol- ogists failed to discover new anatomical clues that would clarify che pre \gements of the higher categories of birds, Erwin Stresemiann, vailing among the greatest German ornithologists. said: But as far as the problem of the relationship of the orders of birds ned, so many distinguished investigators have labored in this field in vain, that litele hope is left for spectacular breakthroughs... . Science ends where comparative morphology. comparative physiology, comparative ethology have failed us after neary [sic] 200 years of efforts. The rest is silence. [Seresemann 1959, p. 277]Anisodacty! Syndactyl N N \ N a W @ 9 @ x . @ @ @ Pamprodacty! Zygodactyl Heterodacty! FIGURE 3-8 Toe arrangements of perching birds. Alternatives to the prevalent (anisodacty!) arrangement of three toes in front and the hallux (the first digit) pointing to the rear have evolved several times (solid arrows). The syndacty! foot, in ‘hich the bases of toes 2 and 3 are fused, characterizes the Coraciiformes. The zygodactyl arrangement, with two forward-pointing toes and two rear-pointing toes, has been achieved in different ways nine times in the evolution of birds. In trogons, toe 2, not toe 4, is rear directed (heterodacty)). In the pamprodactyl foot, the positions of toes 1 and 4 are not fixed; all four toes may point to the front. Dashed arrows indicate uncertain derivations. Two major revolutions overcame such despair by infusing new vigor into the analysis of evolutionary relationships among birds. Cladistic char- acter analysis launched one revolution, and new biochemical technolo- gies drove the other. Major advances then followed the adoption of fo! mal methods for wracking historical changes among lineages through comparisons of DNA sequences themselves. Cladistics Chadistic analysis—the study of evolutionary branching sequence— ables ornithologists to separate primitive characters from common derived characters and to sort them rigorously across (ax: Phylogenetic studies require homologous characters, which can be traced to the sime feature in the immediate common ancestor of both organisms (Bock 1973, p. 386) and which exist in both their original and their changed states. For example, the flipperlike wings of penguins evolved from the wings of their petrel ancestors, In this case, the wings of petrels represent the ancestral—or primitive—character state, whereas 61 SYSTEMATICS.62 CHAPTER THREE the flipperlike wings of penguins represent the advanced—or derived— character state. If ewo species have a character state in common. we can hypothesize that they have a common ancestor with the same character state. The flip- perlike wings common to all penguin species correspond 0 their com- mon ancestry, Simple hypothetical branching sequences, o cladograms. then portray the distribution of characters of extant species and their hypothet- ical ancestors. We assume that the cladogram with the fewest evolution- ary changes—the most parsimonious one—is the most likely or most plausible phylogeny. Consider three hypothetical bird species that have different feet, crests, and bills (Figure 3-9). In this case, cladogram Il, which assumes a common ancestor for A and B that looked like B. is most plausible A pionecring example of relationships based on primitive and derived facter states is that proposed by Alan Feduccia (1977) in his study of yy Species A: (6h. ) Species B: (0, fh, w) Species €: (0,0) ch. Possible cladograms: 1 " a © © ® ® @& ® © OOP ® © & @ ono one oko FIGURE 3-9 Possible cladograms for three hypothetical bird species, AB, and C, that have different combinations of three derived characters: , crest h, hooked bill and 1, webbed feet. Primitive character states (no crest, an unhooked bill, or unwebbed feet) are denoted by 0. The changes from primitive (0) to derived character states (6, h, or w) are indicated for the evolution of each lineage (species A. 8, or C) from the common ancestor (0, 0, 0). The center cladogram (N = 4) is the most parsimonious, requiring fewest total changes to account for the distribution of derived characters among the three species; it also has the advantage that it postulates no convergence between species A and species 8the pes (middie-ear bone) of perching birds. The wood hoopoes (Fam ily Phoeniculidae) and hoopoes (Family Upupidae) have a unique derived character state, an anvil-shaped stapes, in common, which supports the traditional hypothesis that the vo families are closely related (Figure 3-10). The other birds in the Order Coraciiformes—the Kingfishers and their allies—have the primitive, column-shaped stapes. Biochemical Systema With the use of new technologies. direct comparisons of DNA nucleotide sequences of species launched the second revolution in the analysis of evo~ lutionary relationships among birds. Rapidly increasing knowledge of DNA structure enables testing of earlier hypotheses based on morpho- Jogical characters. In general, biochemical studies tend to corroborate previous morphological evidence of relationships. Sometimes, however, I views, reveal overlooked cases of convergence. and suggest unsuspected relationships among taxa biochemical analyses challenge tradition FIGURE 3-10 Primitive (A) and derived (8) anvil forms of the middle-ear bone, the stapes. Both hoopoes (eft) ‘and wood hoopoes (right) have the derived character, which supports the hypothesis of their close ‘evolutionary relationship, (After Feduccia 1977] 63TH 0x 3-1 64 DNA-DNA HYBRIDIZATION COMPARES TOTAL DNA-DNA hybridization esti- GENETIC DIVERGENCE mates the amount of genetic change that has taken place in the entire genome since the time at which two groups diverged from their most recent common ancestor. The estimates of genetic change be- tween species are then used to cluster pairs of species that are most similar. To build a phy- logeny, the estimates of genetic change are con- verted into standardized “distances” that form the basis of @ hierarchical branching diagram, or evo- lutionary tree Proportion of DNA dissoci 60 65 70 75 DNA is composed of four primary units called nucleotides. Each of the four different nucleotides has a unique base—adenine (A), cytosine (C), thymine (T), or guanine (G). The linear sequence of the nucleotides forms the genetic basis of life. Hydrogen bonds between certain pairs of bases— guanine and cytosine, adenine and thymine— hold the double-stranded DNA molecule to gether. However, these bonds can be broken by high temperatures. Fragments of double-stranded avian DNA from two species form double-stranded hybrid 80 85 90 95 ‘Temperature (°C) FIGURE 1 Results of a DNA-DNA hybridization experiment. Curves a through a are examples of heron DNA thermal-dissociation profiles, which show the proportion of the ONA that dissociates at each temperature. Curve a is the melting profile of the control, the homodupiex, in which Great Blue Heron DNA is hybridized with itself. It separates at a higher temperature than do the other hybrid DNAs because the best possible match obtains when DNA is hybridized with itself. The other three profiles of hybrid DNAs of different species—heteroduplexes— demonstrate decreasing similarities between Great Blue Heron DNA and the DNAS of the Great Egret (cum 1), the American Bittexn (curve €), and the Glossy bis (cune #). ‘The difference in the modal, or peak, melting temperatures (ATmode) between the homoduplex profile and the heteroduplex profiles is used to estimate the genetic distance. Here, the distance between the Great Blue Heron and the Great Egret is 86.5°C — 85,0°C = 1.5. The genetic distance between the Great Blue Heron and the American Sittern or the Glossy ibs is 5.5 or 10.5, respectively. [after Sheldon 19870, 19876]complexes when the fragments are heated and separated into single strands and then allowed to reassociate under special laboratory conditions. The hybridized DNA complexes of two samples from a single species are stable and separate only at high temperatures, but hybrid ONA complexes of distantly related species, such as a penguin and a warbler, have few sequences in common and readily dissociate, even at low temperatures. Ge- nomic similarity—that is, the number of bases in a specific nucleotide sequence that two species have in common—is revealed by the degree of thermal stability of the DNA-DNA hybrid mole- cule, Each 1 percent increase in the match be- 0.80, tween the paired sequences of a hybrid complex requires a 1°C increase in temperature to sepa- rate them (see Figure 1), Fred Sheldon’s (1987a, 1987b) DNA-DNA hybridization experiments serve to illustrate this approach to biochemical systematics (see Figures 1 and 2), The experiments demonstrated that the Great Blue Heron is genetically more similar to the Great Egret than to the American Bittern and more similar to both these species than to the Glossy Ibis. The results of these studies also re- vealed different rates of genetic change among different lineages of herons. 0.68 Snowy Egret 0.56 1.40 0.58 0.83 0.62 Little Blue Heron ‘Whistling Heron 89 Great Blue Heron 0.80 a 170 0.09) 170 182 2.09 Great Egret 0.70 Cattle Egret Black-crowned Night Heron Yellow-crowned Night Heron Green Heron 129 ‘American Bittern 248 a 242 FIGURE 2. Branching diagram, or evolutionary tee, of heron ‘elationships based on DNA-DNA hybridization experiments conducted by Fred Sheldon and colleagues (19872, 1987b). Species are clustered according to theie similarity, which is defined by the hierarchy of branch lengths ‘The genetic distance between the Great Blue Heron and the Great Egret measured by AFimaie iM Figure 1 is epproximately the same as the branching distance in this tre, which is the sum of three intervening branch lengths (0.89 + 0.01 ~ 0.80 = 1.7) Least Bittern Lineated Tiger Heron Boat-billed Heron Glossy tis Notice that most branch tips on the tree line up with each other, because their DNAs diverged at approximately the same rate over time. The American Bittern and the Least Bittern, however, exhibit relatively long total branch lengths, because their DNA diverged (accumulated base-pair mutations) faster. Conversely, the DNAS of the Lineated Tiger Heron and the Boat-billed Heron changed more slowly than the other species in this study. [After Sheldon 19874, 19876) 6566 CHAPTER THREE Olé Word New World barbets Toucans barbers L_| FIGURE 3-11 Evolutionary relationships among Old World barbets, roucans, and New World berbets based on 2 parsimony analysis of sequence data for the cytochrome b gene of the ‘mitochondrial DNA. Despite their different morphologies, the toucans and New World barbets are sister taxa. The (Old World barbets and the New World barbets are similar by virtue of having folder ancestral traits in The use of biochemical characters in ornithology started in earnest with the analysis of egg white proteins by Charles Sibley (1970). His igural studies of egg-white proteins were soon superseded by com- parisons of enzymes called allozymes, which in curn yielded to com- parisons of DNA sequences themselves. Sibley and his colleague Jon Ahlquist (1990) assembled thousands of samples of DNA from birds throughout the world, representing species from all but three families, in an unprecedented effort to revise the entire Class Aves by a singu- lar molecular technique, called DNA-DNA hybridization (Box 3-1 pages 64-65). Their bold new phylogeny and classification of the birds of the world revitalized avian systematics and challenged many tradi- ions. Some of the challenges have proved to be correct; some have not. Among the revelations now supported by additional data were pre- viously unappreciated major continental radiations. Many Australian songbirds, for example, had been previously classified with similar Asian and European forms. DNA comparisons showed that diverse Australian re related to one another and that similarities in morphology and behavior to species elsewhere were examples of convergence. The adaptive radiation of Australian songbirds, so revealed. parallels the ex- traordinary diversity of marsupial mammals and eucalyptus plants on chat continent. Each year, comparisons of the DNA genomes of birds increase in power and efficiency. Especially fruitful have been comparisons of the nucleotide sequ a small circular NA molecule (mitochondrial DNA. or mtDNA) found in the mitochondria of the cytoplasm. Scott Lanyon and John Hall's (1994) sequence analysis of 888 nucleotides of the mtDNA ‘gene cytochrome b confirmed one of the interesting results of Sibley and Ablguist’s early DNA-DNA hybridization experiments regarding the re- Lationships of barbets. Barbets are brightly colored. tropical, fruit-eating relatives of the woodpeckers. The results of both biochemical studies i dicated independently that the New World barbets were more closely related to the toucans of Central and South America than they were to. barbets of the Old World (Figure 3-11). All barbets had been formerly considered most closely related to one another. Instead, the big-billed rou- cans diverged radically from New World barbets after the barbets had arrived in the tropics. Construction of a full phylogeny of modern birds, at least at the level of genera, is imminent, as one chapter of the ambitious Tree of Life proj- (Cracraft and Donoghue 2004). Automated gene sequencing and a growing selection of genes that evolve at different rates now allow the comprehensive construction of avian phylogenies. The proportion and pattern of large numbers of nucleotide substitutions define genealogical relationships among diferent clades of birds. Faster-evolving genes such as those encoded by mitochondrial DNA help to resolve relationships among closely related species. Slower-evolving nuclear genes help to re= solve more distant or ancient relationships. For example, List Mertz and her colleagues at the American MuseumHawk owls — —— oa | T Pyemy ows a FTE seminer ows Savanna owls If Northern Hawk-Ow! Old World owls TL L_] jungle ows LF oat ns I New World owls Eared owls tt lg Eagle owls ———— FIGURE 3-12 Phylogeny of the owis of che world (Strigiormes) based on the nuclear RAG-1 exon. Twelve major clades sequence from the oldest groups (barn owls, hawk owls) through the small owls (elf owls, pygmy owls, saw-whet ovis) to.a large cosmopolitan clade that includes New World screech owls and the big wood owls, eared owls, and eagle owls. [Courtesy of t. Mertz and colleagues at the American Museum of Natural History| Eurasian Fagle-Owl of Natural History deciphered the relationships among the genera of owls (Order Strigiformes) by using the powerfal nuclear RAG-1 gene (exon) (Figure 3-12) 6768 (CHAPTER THREE Among the results: & The bam owls (Tyconidae) and typical owls (Strigidae) are each mono- phyletic and have a common ancestor. The Strigidae comprise three major clades of owls: (1) all members of the Australasian hawk owls (genus Ninex}: (2) other small owls world wide including saw-whet owls (Acgolius), litle owls (Athene), and pygmy- owls (Glaucidium); and (3) a large assemblage of other owls including the big eagle owls (Buby), eared owls (Asio), ancl New World screech owls (Megascops). = The Snowy Ow! is related to the Great Horned Owl and eagle owls in the genus Buby. % The Long-whiskered Owlet, a tiny, extremely rare species of the cloud forests of Peru, is the sister species of the desert-living Elf Ow. Construction of phylogenies based on biochemical or morphological characters or on both is the first step toward understanding the evolution of birds. The next step is to map other information onto a phylogeny to explore evolutionary trends in behavior. ecology, and biogeography (Sheldon and Whittingham 1997). The analysis of nest construction by wallows is one such effort. Fred Sheldon and his colleagues (2008) ex- amined the relationships among most of the species of swallows (Family Hirundinidae) of the world by using a variety of techniques. including DNA-DNA hybridization, two mitochondrial genes, and a nuclear gene (Figure 3-13). Such packages of genes that evolve at different rates allow the construction of phylogenies for whole families of birds with resolu- tion of both recent and older branching sequences. Nest construction is extremely diverse among species of swallows. Some species burrow into hillsides, others adopt tree cavities, and still others build mud nests on cliffs. The use of pure mud to construct hanging nests is unique among all birds, The original DNA-DNA hybridization studies by Winkler and Sheldon (1993) revealed that nest-construction habits reflect the evolu- tionary history of species. The swallows divided cleanly into. mud nesters e.g. barn swallows (Hirundo) and cliff swallows (Petrochelidon|: cavity adopters [e-g., martins (Prague) and tree swallows (Tach ycineta)|: and excava tors [eg sand martins (Riparia)]. Analyses of the majority of swallow species representing all genera with the use of the full toolkit of both mitochon- drial and nuclear genes reaffirmed the basic split between mud-nesting species of swallows and the cavity adopters, or core martins, Mud nesting evolved only once in the evolutionary history of swallows and then diversified, prin— cipally in Africa where a dry climatic history favored this mode of nesting. ‘The obligate cavity-adoption behavior of the core martins appears to be tied to their evolution in the rich forest habitats of the New World. Three ger era (Pseudhirundo, Cheramoeca, and Psalidoproone) of excavators proved to be old basal lineages of swallows now restricted to Africa and Australia, The two living species of river martin. one from Congo and the other from Thailand (ee page 53). represent the most ancient lineage of all.{Ea PSeectidon sare Patina orboica a Punochelidoneyanoleuca 59 EO star meiaolenca “a0 thle Cia Noticias 1.0 LS a5 — Nechlidn maria upthtin ac oe LOTT Nenclden bias r 100 rate 1.00 ay Progte dominicensis {100 00 — prog suis Pscudochelidon eurystoming ‘Steloidonterys semipennis 00) |p Sedona ‘pine 3103 -Progne chalybea “00 Progne eles iparia riparia 1 riparia pata Tachycnetaleacorhoa oss} ose Ripariacincta ena bracae 0.67 To Tachycineta stolzmanni O58 chin atbinen 100 Tevet etl ie 1 Fe tein O86. Tachycineta euchrysea Pryanoprogne rapesti {E00 ptyonaprogne futigula | Hirano atrocaeraen 1.00 Hirundo tahitica 11.00 sirundo neoxena Hirando albigalaris irundo smhit 077 —sirundo rustica Hirundo angolensis ra z Hirano lucia ‘00 Hirundoaetbiopica Miro fevcosoma Hirando diidiate etichan webicumm 1.0/5 00, 1.00 Tan Sioa paw oa 7 0, Dalichon dasypus £00 Detchon nipalense erocheldon ytrhonota 1.00 Fron 1% petracetidon rufcelaris 7 Pehoctldon prem et . Ses Petrochelidon nigricans L__pygg — hea este i Petrockelidon ariel Pscudhirando griseopyaa Psalidoprocne prstopteraholomelas Psaldoprocne fuliginesa 1.004 Psatidoprocne prstoptera petit 1.00. ‘sions Tera FIGURE 3-13 Phylogeny of the four primary clades of 61 species of swallows (Hirundinidee) based on comparisons of a nuclear gene (ND2) and a mitochondrial gene (for eytochrome 1). The two disjunct species of river martins (Pseudochelidon) of “Thailand and Congo, respectively, are the ancient outgroup lineage of the family. Then follow two basal and relctual genera: the Gray-rumped Swallow (Pseuhirundo) of ‘Australia and the savwwing swallows (Psalidoprocre) of Africa, which have no known relatives. The rest of the swallow species divide cleanly into the mud nesters, such as the Barn Swallow (Hirundo) and allies, and the core martins (Prage, Tachycineta, Riparia) and alles. [From Sheldon etal. 2005] Barn Swallow 69 SYSTEMATICS.FIGURE 3-14 The fowl-ike birds Galliformes) (A) and waterfowl (Anseriformes) (8) were among the ‘earliest lineages of successful modern birds: (1) Lady Amherst’ Pheasant, 2) Red Junglefowt, (3) Great Currasow, (4) Vutturine Guineafowl, (5) Sage Grouse. (6) Musk Duck, (7) Smev, (8) Black-necked Swan, (9) Mallard, (10) Magpie Goose, and (11) Horned Screamer w72. (CHAPTER THREE FIGURE 3-15, Electrophoretic studies of proteins by Sibley and Ahlquist (1973) suggested that the Hoatzin might be related to Guira cuckoos, not to guans, as had been thought, But the relationships of this enigmatic species remain unresolved. Results of the latest DNA studies suggest that the Hoatzin represents an old basal lineage with no close living relatives. [From original by E Poole, courtesy of The Academy of Natural Sciences, Philadelphia] The use of mitochondrial genes allowed these researchers to finely re- solve the relationships among species in each major group of more re- cently evolved species. For example, the mud nesters divide cleanly into mud-cup nesters (barn swallows and crag martins), enclosed-mud nesters (cliff swallows and red-rumped swallows), and modified-mud-cup nesters (house martins). The concordance between phylogenetic relationships and nest-building behavior overturns the historical view that the nest-construction behav- ior of birds changes easily as an adaptation to local circumstances. Instead, we now have a strong foundation for the study of the divensty of the so- cial systems of swallows DNA analysis of slow-evolving (nuclear) genes has revealed some of the deepest roots of the evolution of modern birds. For example, chick enlike birds (Galliformes) and waterfowl (Anseriformes) are firmly posi tioned as being among the oldest modern birds (Cracraft et al. 2004; Figure 3-14, pages 70-71). The enigmatic Hoatzin is a remnant of an ancient basal lineage with no close living relatives, cuckoos included (G. Barrowclough, pers. comm.; Figure 3-15). One of the biggest surprises is that flamingos (Phoenicopteriformes) and grebes (Podicipediformes) ap- pear to be each other's closest living relatives but with an ancient com- mon ancestor (van Tuinen et al. 2001; Figure 3-16). This relationship was never included in past considerations of cither group, given their en~ tirely different morphologies.FIGURE 3-16 (A) The “ relationships of flamingos (Phoenicopteriformes) have Jong been debated, primarily about whether they are closer to waterfowl or to storks. (B) DNA comparisons suggest that flamingos are distantly related to grebes (Podicipeditormes). 7374 CHAPTER THREE IMiocene Petroicidge g 3 Tertiary ‘Cretaceous Acanihisittidae FIGURE 3-17 Phylogeny and diversification of songbirds (Passeriformes) based on ‘wo single-copy nuclear genes. The height of the bars on the right-hand edge of the branching diagram is proportional to the number of species in each clade. Projected divergence dates of clades in relation to the geologic time scale are based on assumptions of the rate of gene evolution, which are subject to criticism. [after Barker et al. 2008] The new DNA technologies also reveal more details of the evolution of songbirds (Passeriformes) in the Tertiary, including their phylogeny and their biogeography (Barker et al. 2004; Figure 3-17). This single largest radiation of modem birds originated in ancient Australasia perhaps as early as the late Cretaceous, followed by repeated worldwide expansions of suc- cessful groups. Three species of New Zealand wrens (Acanthisitidae), which represent the oldest lineage of all, still persist in New Zealand. The so-called suboscine songbirds, which have simpler vocal-muscle arrange- ments than those of the oscine songbirds, split early into New World and ‘Old World lineages. The New World suboscines—tyrant flycatchers, antbirds, and ovenbirds—became dominant members of the avifaunas of the New World tropics. The Old World suboscines—broadbills, pittas— did not. A host of Australasian families—lyrebirds (Menuridae), bower- birds (Peilonorhynchidae), honeyeaters (Meliphagidae), and others—evolved before the diversification of the two principal songbird clides—the Corvida and the Passerida.Summary The classitication of the kinds of birds of the world helps ornithologists to communicate with one another and serves as a tool in the continuing study of avian evolutionary relationships. The species is the primary unit of biological classification Formal taxonomic classifications comprise a hierarchical series of in- es. Orders, ic groupings of birds. all of clusive categories that indicate the relationships among line families, and genera are the principal taxonor which belong to the Class Aves. Theoretically each taxon is monophyletic and consists of species more closely related co one another than co species in other taxa. In theory, the hierarchy of the classification and the evolutionary history of birds are the same. The diversity of modern birds reflects historical pattems of speciation, extinction, and phyletic evolution. Conservative characters—attributes, that do noc change easily in the course of adaptation—enable omitholo~ common ancestor. Recog- nition of ancestral (primitive) versus changed (derived) character states aids. in the reconstruction of the sequences of past evolutionary events ists to decipher which groups of species have nvergence—the independent evolution of similar adaptations by un related species—can red species to y of convergence can be revealed by detailed study of complex characters, such ay the internal anatomy of the toes, and by biochemical evidence. Two recent revolutions, cladistic analysis a rel Use pear to be re id biochemical technology, have infused a new vitality into the study of the phylogenetic rela ships sorts the poharities of primitive and derived characters. Biochemical com- parisons of DNA compositions of species tend to confirm conclusions based on morphology, but they sometimes reveal unsuspected affinities andr mong species and among, major groups of birds. Cladistie analysis ew patterns of adaptive radiation, 75 SYSTEMATICS