ar. History The study of the origin and carly evolution of birds has never produced as much excitement and public attention as in the past decade. [Zhou 2004, p. 435) Vian history starts more than eransformation of rept with limived flying abilities. Birds then diversified in form and function first in the Mesozoic and then again as modern taxa in the ‘Tertiary. The evolution and adaptive radiation of birds paralleled the in- dependent evolution and rise of placental mammals to their own modern prominence, Increases in atmospheric oxygen over this same period of Earth history, with rapid increases in the early Jurassic and the Eocene, potentially favored the success of these two principal groups of highly active land vertebrates with aerobic metabolism (Falkowski et al. 2005). The details of the transformation of reptiles into birds. including the role of dinosaurs, have long been the focus of intense debates. A wealth of well-preserved new fossils of both early birds and dinosaurs, mostly tern China, provide a new and expanded scenario of the initial stages of the evolution of birds. Major episodes of extinction punctuated the long history of life on Earth. The Class Aves participated in several of them, starting in the lace Cretaceous. In another episode at the beginning of the Pleistocene epoch about 3 million years ago, clim 25 percent of the existing bird species. Recurrent tinued to alter habitats and, in curn, the distributions and viabilities of bird populations, In the past century, humans have become the primary foree changing and threatening the natural world, including global Birds now face a major new episode of species extinctions. This chapter first examines the reptilian features of birds and then Archaeopteryx lithegraphica, the earliest known bird. The array of new fos- sil dinosaurs and of the diverse bird species that followed Archacopteryy is 50 million y ancestors into feathered birds extinction of at least matic changes con ates,26 (CHAPTER TWO a source of additional insights into the evolution of feathers and avian flight. This chapter also reviews che main stages of the diversification of modern birds in the Mesozoic era in association with the breakup of Gondwanalind. the ancient southern continental landmass. The stage is then set for Chapter 3, which examines how ornithologists reconstruct evolutionary relationships among species and classify birds according to these relationships. Birds As Reptiles Birds evolved from reptiles (Figure 2-1). Thomas H. Housley. the great evolutionary biologist of the nineteenth century, asserted that birds were “mercly glorified reptiles” and accordingly classified them together in the taxonomic category Sauropsida (Huxley 1867). Indeed, birds and mod- em reptiles have many characters in common (Figure 2-2). The skulls of both articulate with the first neck vertebra by means of a single ball-and- socket device—the occipital condyle: mammals, which evolved from a different line of reptiles, have two of them. Birds and modem reptiles have a simple middle ear with only one ear bone—the stapes; mammals | A | \\ - Base reptiles. FIGURE 2-1 A simplified family tree of the vertebrates. Birds, dinosaurs, pterosaurs, ‘and crocodiles evolved from one group of reptiles, the thecodonts; mammals evolved from another, the therapsids, Other groups of early reptiles gave rise to turtles, snakes and lizards, and the iguana-like tuatara now found only on little islands near New Zealand, (The dashed lines indicate that detailed lineage between birds and dinosaurs is uncertain.)Sclerotic ring supports eye Expanded lateral braincase Single middle- ear bone Lower jaw composed Lower jaw articulates Single occipital of several bones on quadrate bone condyle FIGURE 2-2 Some reptilian features of the avian skull have three middle-car bones. The lower jaws, or mandibles, of both birds and moder reptiles are composed of five or six bones on & ch side: mam- mals have only one mandibular bone. The ankles of both birds and mod- em reptiles are sited in the tarsal bones (ee Figures 1-2 and 1-3), not be- tween the long lower leg bones, or tibia, and tarsi as in mammals. The scales on the legs of birds are similar in structure to the body scales of modern reptiles. Both birds and modern reptiles lay a yolked. polar egy in which the embryo develops by shallow divisions of the cytoplasm on the surface of the egg, In birds and in some reptiles, females have two different sex chro- mosomes, Zand W, and are referred to as the hetcrogametic sex (see Chapter 14); males are the heterogametic sex among mammals (with X and Y chromosomes). Both birds and reptiles have nucleated red blood cells, whereas the red blood cells of mammals lack nuclei Archaeopteryx: The Original Link Between Birds and Reptiles The simi ties between birds and reptiles leave no doubt of their evo- lutionary relationship to each other. Yet we are not content with tha We want w know which reptiles gave rise to birds and how the trans formation proceeded. For this knowledge. we must turn to the fossil record, There, an extiner creature, Archacoprerys lidhographica, first signaled the origin of birds trom reptiles, Fine-grained limestone deposits in central Europe contain a record of creatures that occupied that region during the age of dinosaurs—in the late Jurassic period, from 155 million to 135 million years ago (Table 2-1). At that time, central Europe was wopical, sporting palmlike plants, Great warm seas and lagoons covered parts of the European continent. The coastal lagoons attracted prerodactyls, or flying reptiles. some as small as 27 HISTORY28 CHAPTER TWO PITABLE 271 Ceotogidtine scale Million Years Era Period Epoch Before Present Quitemary Recent 001 Pleistocene =. 15-35 Pliocene Cenozoic ~ - 7 {age of birds Miocene and mammals) —— 6 Tertiary Oligocene ~ 36-38 Eocene 53-54 Paleocene 6 Cretaceous —— 100 on 135 Mesozoic Late {age of reptiles) — 135 Jurassic 170 1830-190 Triassic 230 From Feduccia 1980, sparrows and others as large as eagles, which flew on batlike wings made of stretched skin. Sometimes they perished in the lagoons, where gentle fossilization in che fine calcareous sediments preserved their features in exquisite anatomical detail, Also preserved in the same lagoons were the remains of the feathered reptile now called Archacoprery The firse evidence of the origin of birds was an impression of just single feather found in a Bavarian quarry. from which Jurassic limestone was mined for lithographic slabs. The impression was brought to the attention of German naturalist Hermann von Meyer of Munich in 1861. A complete skeleton of a small reptilelike animal with feathers also was found and brought to von Meyer's attention just a few months later. He named the fossil creature Arshacoptery (archaios, “ancient”; preryx. “wing”) lithographica. The discovery of a second complete specimen of Archacopteryx in another quarry near Eichstitt. Bavaria, followed in 1877 (Figure 2-3), Ic is fully articulated, revealing details of che wing bones. flight feathers and the pairs of feathers attached to each vertebra of its long tail. These feathers are indistinguishable from modern feathers.FIGURE 2-3 This fully articulated skeleton of Archaeopteryx lithographica was found in 1877 near Eichstitt, Bavaria. [Courtesy of J. Ostrom] Now known from seven specimens and that first feather, Archaeopteryx was a crow-sized, bipedal “reptile” with a blunt snout and many small, reptilian teeth. It bore feathers on both wings and til and probably also over most of its body. like modern birds. It possessed, however, numer ous reptilian features. Like the modem guans (Cracidae), it may have been a strong-running, terrestrial “bird” that could leap into trees, jump among large branches, and make short flights between trees. Paleontolog that Awhacopreryx was capable of gliding and weak flapping but not of long, sustained flights. Indications of Anacopreryx’s flight capa clude its large furcula, which probably anchored strong pectoralis mus eles. and the acute angle of its scapula. which supported dorsal elevator muscles that helped to life the wings, as they do in modem flying birds30 CHAPTER TWO aS Corn Crake AS Archacopteryx Weka FIGURE 2-4 The vanes of the primaries of Archacop- teryx were asymmetrical like those of modern flying birds such as the Corn Crake, a kind of ral; they were not symmetrical like those of flightless birds such as the Weka, a flightless ral of New Zealand. The asymmetry has an aerodynamic function and presumably evolved in relation to flight in this, primitive bird. Similar asymmetries are reported for a well-feathered dinosaur named Microraptor. [After Feduccia and Tordoff 1979] Additionally, the vanes of Archacopteryx’s primary wing feathers were asym= metrical. a character common to nearly all flying birds and most pro- nounced in strong fliers (Feduccia and Tordoff 1979). In flightless birds these vanes are symmetrical (Figure 2-4), Archaeopteryx: was intermediate between reptiles and birds not only in skeletal features (Figure 2-5), but also in its brain and inner ear (Alonso et al, 2004). The brain was three times larger and more advanced than that of similarly sized reptiles. though still smaller than the brains of mod- FIGURE 2-5 Skeletal features of (A) the reptilelike Archaeopteryx and (8) a modern bird, the domestic pigeon. In modern birds, (1) the braincase is expanded and the head bones are fused; (2) the separate hand bones of reptiles are fused into fewer rigid elements; (3) the separate pelvic bones of reptiles are fused into a single, sturdy structure; (4) the many tail vertebrae of Archaeopteryx are reduced in number and partly fused into a pygostyle; (5) the tiny cartilaginous sternum of Archaeopteryx has expanded to a large keeled bony structure for the attachment of flight muscles; and (6) the typical reptile rib cage is strengthened with horizontal uncinate processes. [From Evolution of Vertebrates by E. H. Colbert. Copyright 1955 John Wiley @ Sons, Inc. reprinted by permission of John Wiley @ Sons, Inc.|em birds. The brain included enlarged visual centers. Expanded inner-ear structures would haye enhanced hearing and spatial orientation, These features suggest that -irchacopterys had evolved the initial neural systems required for flight. The discovery of Anhucopterys linked the evolution of birds directly to reptiles, It was a timely discovery of an animal that was intermediate between two higher taxonomic categories, a transition from ancestral to descendant stocks. Darwin's prediction of intermediate evolutionary links in Ou the Origin of Species by Means of Natural Selection (1839). published only owo years before the discovery of the first two Archaeopteryx fossils, seemed to have been fulfilled, The intermediate morphology of Ariacopteryx quickly moved into the nter of the debate between opponents and supporters of evolution by natural selection, Creationists, defending their views of the separate and unchanging appearances of birds and reptiles. insisted that Darwinists w misinterpreting the apparent intermediacy of Archaeopteryx. On the other side of the debate, Thomas H. Huxley, Darwin’s most eloquent cham= pion, was convinced of the link between birds and birdlike reptiles and soon converted leading American paleontologists. Charles Marsh of Yale University was one of these converts. He wrote: The classes of Birds and Reptiles. as now living, are separated by a gulf so profound that a few years since it was cited by the opponents of evolution as the most important break in the animal series, and one which that doctrine could not bridge over. Since then. as Huxley has clearly shown, this gap has been virtually filled by che discovery of bird-like Reptiles and reptilian Birds. Compsaguatluus and Aschacopteryx: of the Old World . . . are the stepping stones by which the evolutionist of to-day leads the doubting brother across the shallow remnant of the gulf, once thought impassable. [Marsh 1877. p. Feduccia 1980, p. 15] Archaeopteryx contributed to the acceptance of Darwin's theory of evo- lution as well as t our initial understanding of the origin of birds. Despite a series of challenges, Achaeopyerys: remains tirmly positioned as the oldest and most primitive known bird and che outstanding link to reptilian ancestors, as originally proposed, Birds As Dinosaurs There is little doubt that birds evolved from a line of Mesozoic reptiles. Which line and when, however, continue to be matters of intense de~ bate (Prum 2002; Feduccia 2002). One possibility is that birds evolved carly, before true dinosaurs, and from a stem group of reptiles called 31 HISTORY32 CHAPTER TWO ‘Triassic Jurassic | Cretaceous ‘Crocodilians = ‘Theropod difgsaurs! Bird | Ornithischian dinosaurs Flyingireptiles,. FIGURE 2-6 Historical debate about the evolution of birds. (A) Some experts believe that birds evolved from small theropod dinosaurs. (8) Other experts believe that birds evolved directly from the thecodont ancestors of dinosaurs and crocodiles. New fossils found in the past decade have swayed this debate in favor of the theropod dinosaur ancestors. [After Ostrom 1975] thecodonts. The other possibility is that birds evolved later from small theropod dinosaurs (Figure 2-6) The thecodont hypothesis of the origin of birds looks to a large group of primitive reptiles that prevailed in the early years of the Mesozoic Among them were the lightly built thecodonts, a diverse group of rep- tiles that gave rise to dinosaurs of different sorts, some of which were arboreal; to fying reptiles called pterosaurs: and to crocodiles. Some the- codonts even had elongated s of feathers (Figure 2-7). The hypothesis that birds evolved fom small theropod dinosaurs goes back co the discovery of fossil Arhacopteryx. Thomas H, Huxley (1868) ‘was particularly impressed by the similarities between Archaeopteryx: and Compsagnathus, a small dinosaur preserved in the same Jurassic limestone deposits (see Figure 2-7). Although we usually think first of the large, spectacular species, dinosaurs varied greatly in size and habits. They evolved from thecodont ancestors in the Jurassic period and were domi- nant animals of the Cretaceous period from 136 million to 65 million years ago. One group. the theropod dinosaurs. included not only large carnivores such as Tysanmosanius rex but also many small ones close in size to modern igu le, lightly buile, bipedal, liele dinosaurs with many small, sharp teeth, They probably chased small vertebrates and large in- seets. Some may even have been warm-blooded. The raptorlike “dromacosauss” have many characters in common with che earliest birds, ales that seemed like the natural pri iorsFIGURE 2-7 Two possible relatives of birds. (A) Compsognathus was a small theropod dinosaur that was preserved in the same limestone deposits as Archaeapteryx (8) Longisquama was a lightly built, arboreal thecadont reptile with elongated scales. 1) From Heilmann 1927: (6) from Bakker 1975, with permission from Scientific American, Ine.) 33 HISTORY‘CHAPTER TWO These small dinosaurs include Velociraptor, which figured prominently in Michael Crichton’s book Jurassic Park, The weight of the evidence has caused the pendulum of the debate co swing powerfully toward early terrestrial theropod dinosaurs as the im= mediate ancestors of birds (Pandian and Chiappe 1998; Pram 2002), In this proposed scenario, dromaeosaurs such as Deionyncluts, are the closest relatives of birds. Some, such as Protarchavopreryx and Caudipteryx, even had feathers (Figure 2-8). Indeed. all of the specitic features once thought FIGURE 2-8 The existence of feathered theropod dinosaurs, such as Caudipterye (A), Confuciusornis (8), and Microraptor (©) leads many t0 conclude that birds were derived from dinosaur ancestors {(A) Photo from Philip}. Currie, University of Alberta. (8) After Martin er a. 1998, (© After Xu etal 2003; photo by Xinhua Photo/CORBIS]to define the Class Aves as unique—feathers, furcula, pygostyle. bill, and even flow-through ventilation of the lung (O'Connor and Claessens 200: see also Chapter 6)—were present in dinosaurs of the Cretaceous period. These traits of some dinosaurs and the advanced birdlike features of Archaeopteryx enabled the improved flying abilities and arboreal life styles of the next stage of avian evolution. Major issues remain, however, Alan Feduccia and his colleagues di agree with many interpretations. So the debate continues (Feduceia 20 Feduecia et al, 2005; Zhou 2004). One interpretation, yet to be accepted is that the dromaeosaurs were an early adaptive radiation of birds com- prising all stages of flight and flightlessness. including degenerate feather structures A different part of the debate concems the evolution of the avian hand versus the dinosaur hand. The typical vertebrate hand bears five fingers, or digits, numbered sequentially I, II, II], IV. V. Like the majority of ver- tebrates with three fingers. including pre-dinosaur thecodonts, the fingers on the bird hand are numbers Il, II1, IV due to the symmetical reduc tion or loss of numbers I and V (Feduceia and Nowicki 2002; Figure 2-9), Dinosaurs (the Dinosauria), in contrast, had only three fingers— Theropod dinosaur Bird 35 HISTORY FIGURE 2-9 The hand of a basal theropod dinosaur (Herrerasauris) illustrates the reduction of digits 1V and V. This condition ied to the unique three-fingered hand (htt) of later theropod dinosaurs. Birds lost digits 1 and V to a different three- fingered hand (i, I, 1V) [From Feduccia and Nowicki 2002)36 CHAPTER TWO digits 1, 11, [lowing to the reduction or loss of digits IV and V. Thus the central question is whether birds branched off before the dinosaurs evolved their [-II-III hand structure or whether birds somehow changed the unique hand structure of dinosaur ancestors to a more typical (of ver- tebrates) three-fingered arrangement. Tracking the activity of genes te- sponsible for digit development suggests that bird digit II is really digit [ that has shifted its position. siding with the theropod camp (Vargas and Fallon 2004), Feduccia and colleagues (2005; see also Galis et al. 2005) disagree with the interpretation of how gene expression controls the em- bryology of these digits, They stand by their view chat digit II is digit IT and that the three-fingered avian hand has the primitive, pre-theropod composition of digits II, II, IV, What's nexe? We can expect to sce a sharpening of the questions co be resolved and better resolution of the evolutionary transitions from rep- tiles to the earliest birds in the Jurassic period. Certainly the best is yet to come, because scholarly interest, public attention, and real evidence both fossil and developmental—are ac an all-time high and growing (Box 2-1). In time, resolution of the specific ancestry of birds will inform our interpretation of a whole range of adaptations of birds, from morphology to social behavior (Prum 2002). TB 20x 2-1 The sequence of the chicken THE AVIAN GENOME: ONE BILLION DNA BASE PAIRS STRONG genome—specifically that of the Red junglefowl, Gallus gallus—was published in December 2004 with ini- tial comparisons with those of other organisms (international Chicken Genome Sequencing Con sortium 2004; Schmutz and Grimwood 2004) This signature event in ornithology enables a novel perspective concerning what is a bird, and sets the stage for a new era of a broad range of research: from commercial egg production to evo- lutionary ecology. The chicken genome is only the fourth vertebrate genome to be sequenced The first avian genome: MIs one-third the size of the mammalian genome due to reduced repeat content, pseudo: genes, and segmental duplications Includes an estimated 20,000 to 23,000 genes Includes 38 pairs of large (macro-) and tiny (micro-) chromosomes; the latter are distin- guished by high levels of guanosine-cytosine (GC) base pairs compared with adenine-thymine (AT) base pairs Includes long blocks of conserved sequences (70 megabases total) that align well with human genome sequences and are likely to be functional in both species despite 310 million years of evo- lutionary divergence Has undergone a novel mode of evolution for some noncoding RNA genes | Differs from the mammalian genome in the expansion and contraction of multigene families ™ Is more amenable than the mammalian genome to classification of its content, owing to reduced pseudogene contentEarly Evolution of Birds Separate from the debate about whether birds are dinosaurs is the recently exposed substantial fossil history of Mesozoic birds. Following the appear~ ance of Archaeopreryx in the Jurassic period, birds evolved the definitive features of modern birds and diversified during the Cretaceous period (Figure 2-10). A wealth of new fossil birds from Spain, China, and Pata~ gonia now bridge the once troublesome gap in the fossil record that separated Archacopteryx from modern birds. Basal birds from the early Cre raceous, including Confitciusornis and Jeholornis, were intermediate between Archacopteryx and more advanced forms. Confiuciusornis bas a horny beak quite like that of modern birds. Jeliolomis has a long tail like that of Archacepterys and forelimbs with advanced flight capabilities, Beyond these important links were two major lineages that diversified during the Cretaceous: the Enantiomithes and the Omithurae. These substantial first avian radiations included all stages of flight and Hlightlessness The Enantiomithes dominated the first phase of early avian evolution (Chiappe 1995: Figure 2-11). Dozens of flight-capable species of diverse ecological forms ranged worldwide. They were as small as sparrows and as large as vultures. They laid their eggs on the ground and underwent annual growth cycles recorded as treelike growth tin: of their limb bones. Many were arboreal Sinornis santensis was a signature species of this radiation. Discovered in China in 1987, this amazing fossil from the carly Cretaceous period, 140 million years ago (Sereno and Chenggang 1992), was a toothed, sparrow-sized bird with many features of theropod dinosaurs and Auchaeop- teryx. Sinontis also exhibited features intermediate between Archacopteryx and modern perching birds, Advances over Acacopterys include strength- ening and modifications of the hand, forearm, and pectoral girdle for flight functions: the ability to raise the wings high over the body as well as to fold them; a large pygostyle for the support of a tail fan, which improves steering and braking in flight: and a perching foot with an oppo s in cross sections le rear tt 0 Ra 00% je lc eats st “at oo git Bel ce ees pat soot at toh es GsH aleOT We ing Ornithurae Grnithothoraces Pygostylia ‘Aves, FIGURE 2-10 Relationships among early groups of birds that followed Archaeopteryx in the fossil record of the Mesozoic era. [From Zhou 2004] 37 HISTORY38 CHAPTER TWO. FIGURE 2-11 Enantiornithine birds thrived during the Mesozoic but then disappeared. They diversified into a wide range of water birds and arboreal, perching birds that could fly well. The sparrow-sized species Sinornis santensis was a signature species of this now extinct radiation of early birds. It was intermediate berween Archaeopteryx and modern birds. [After Sereno and Chenggang 1992) toe. the hallux. These features suggest that avian flight and perching abil- ities evolved in small-bodied birds that followed Arcacoprery. None of the Enantiomnithes survived into the Tertiary. They disap- peared along with dinosaurs in the mass extinction that marked the end of the Mesozoic era. The other lineage. the toothed Ornithurae, ultimately gave rise to modern birds. Like the Enantiomnithes. the toothed Omithurse included small, finch-sized, arboreal species in the early Cretaceous. Later mem- bers had advanced wing structure and flight ability and a fully developed perching foot. By the late Cretaceous. ornithurine birds exhibited a wide range of sizes and life styles that mirrored those of modern wading birds, diving birds, perching birds, and even secondarily flightless (having evolved from “fighted” birds) terrestrial forms. Among the best known forms are toothed seabirds—Hesperomis, Idithyernis, and their relatives in the extinct Order Hesperomithiformes. They inhabited the Cretaceous seas that cov-ered the central parts of North America and Eurasia. Some resembled modern loons, They ranged in size from that of a small chicken to that of a large penguin. The largest was Hesperomis regalis. from 1 to 2 meters in length. All 13 known species of divers were flightless, with large, pow- erful, lobed feet. Flying above the same shallow seas were at least six species of toothed, terlike birds (chil yomis) Most of the Omithume disappeared along with dinosaurs in the mass extinction that marked the end of the Mesozoic era. Among the few sur- vivor, however, were the ancestors of modem birds. These ancestors in= cluded birds related certainly to modern chickens. waterfowl, and ratites. and pethaps also to shorebirds and cube-nosed seabirds (Clarke et al. 2005). Evolution of Feathers Ac first, the well-developed feathers of Archacopreryx separated it from small dinosaurs of similar form and so started the quest for the ancestor of birds, Ie turns out. however, that feathers and teatherlike structun unigue to birds, including Ardiacoprenyx. Theropod dinosaurs had them Iso. The new awareness started with the discovery of the first “feathered dinosaur,” the chicken-sized Sinosauropreryx with filamentous downlike feathers, and then the turkey-sized Caudipterys with a well-preserved fan sare not f of vaned feathers on its tail and forelimbs. Fossil feathers have now been found on more than a dozen theropod dinosiuss and dromagosaurs not closely related co Archaeoprerys: Ancient feathers included downlike filamentous structures, or “dino- 2,” and well-vaned, essentially modem feather structures. The relation of dino-fuzz to real feathers remains controversial: arguments range from their being unrelated structures to being precursors of feathers to being simplitied feathers of flightless birds (Pram and Brush 2002; Lingh: Soliar 2003; Feduccia et al. 2005). Less controversial are the well-preserved vaned feathers. A little dinosaur named Microraptor gui had front and hind wings that sported outer feath- ers with asymmetrical vanes, just as in the wings of modem flying birds (Xu et al. 2003; see also Figure 2-8). Feathers clearly evolved in modern form in theropod dinosaurs and then diversified in form and function We long presumed that feathers evolved from scales of some kind, centering the debate on what advantages promoted the evolution of feath- es from scales. More likely. feathers evolved not as modified scales but as a novel epidermal structure (Prum and Brush 2002: see also Chapter 4) The first feathers, even if they were frayed scales, likely aided tempera- ture regulation as insulation or heat shields, a hypothesis long favored by reptile experts (Regal 1975). Contrary to many early speculations, feathers did noc evolve initially in concert with the evolution of flight. Rather, avian flight followed the initial evolution of vaned feathers. Early forays by gliding and weak flap- flight fostered additional changes in feather form and fanetion on the wings and tail. 1 39 HISTORY40 ‘CHAPTER TWO Evolution of Flight How did avian flight evolve, and just how well could Archacopteryy fly? What caused the forelimbs of reptilian ancestors to evolve into proto~ wings in the first place? Two basic theories are in contest: an arboreal theory and a cursorial, or running. theory. The arboreal theory proposes that the evolution of fight started with gliding and parachuting from elevated perches. Most drawings of Archae- opteryx depict an arboreal reptile clambering around trees, grasping branches with clawed fingers. Extensions of the bones of the forelimb en- hanced by elongated (flight) feathers enabled the ancestor of Archaeopteryx to parachute and glide between trees. This arboreal theory has been favored for many years (Bock 1965: Feduccia 1980: Figure 2-12). A va- riety of dinosaurs, and even pre-dinosaur thecodonts, were arboreal, and some flew, The cursorial theory proposes that elongated forelimbs heightened leaping ability in a small, bipedal theropod dinosaur that ran and jumped . The cursorial theory is a working corollary of the accept to catch pre To modern birds Active flight iS Gliding parachuting vias tepingpetweentnes 2 ZF strove te-poais Ly Bipedal locomotion—thecodonts oP itr heed insu a Quadrupedat locomotion—ground-dwelling ean tecoaas FIGURE 2-12 The long-standing arboreal theory of the evolution of avian flight suggests that, after evolving bipedal locomotion, che reptilian ancestors of birds became arboreal and leaped between trees. Active flight evolved from earlier stages of parachuting and gliding flight that enhanced the leaping abilities of the ancestors of Archaeopteryx. [After Feduccia 1980, adapted from Bock 1965]ance of the theropod origin of birds (Pandian and Chiappe 1998: Pram 2002). Extensions of the forelimbs helped to control and extend leaps (Caple et al. 1983, 1984). Elongation of three extensions of the body— two wings and a ail—would not enable flight at first but would help to control the body's position. Faster running. higher jumping, greater reach, and enhanced maneuverability would be the result, The flight capabili- ties of modem birds would thus be a logical extension of the first small jumps by litle dinosaurs. The arboreal versus cursorial theories are not clear alter They likely pose a false dichotomy because the activities of the avian ancestors, as well as those of Archacopteryx itself, mixed these behav- iors. The most important step was the evolution of a wing stroke that could produce the main components of powered flight: lift and thrust. A powered wing stroke required transformation of the wrist and shoul- der from the skeletal wing-precursors of theropod or other ancestors (Ostrom 1997). What were the behavioral steps that fostered the needed transformation? Ken Dial (2003a) provided a logical answer. He suggested that flap- ping their feathered forelimbs helped early birds climb steep inc cluding tree trunks. Chickens and their relatives routinely improve foc traction and climbing ability through wing-assisted incline running (Fig- ure 2-13). Incipient wings could have served avian ancestors in the same way. Continued improvement of such aerodynamic assistance favored changes in wrist and shoulder structure that led to the powered stroke of the avian wing. Protowings, increased arboreal habits, and gliding with feeble flapping—as proposed for the life style of Arhaeopreryx—would be the next logical evolutionary st. The evolution of the bastard wing, or alula, provided the finale. This key to avian flight, a set of small extensible feathers on the wrist that help to prevent stalling at slow airspeeds (see page 119), was found on a 115 million-year-old toothed and goldiinch-sized fossil ornithurine bird, Eoalulavis hoyasi, discovered in Spain (Sanz et al. 1996). All the elements for modern avian flight were available and in place. The subsequent evo- lution of modern, powered flight overhauled both the aerodynamic struc- tures of the body and the physiology that provided energy. These changes opened the door for the diversification of modern birds tives, Modern Birds The Tertiary period that followed the Mesozoic era unleashed the diver- ity of modern birds as we know them. It also produced some huge, cat nivorous, semimodem birds that temporarily occupied some of the niches left vacant by bipedal dinosaurs. Two-meter-tall diatrymas with power- fill legs, clawed toes, massive horse-sized skulls, and tearing, eaglelike beaks must have terrorized many lesser creatures before becoming extinct in the al HISTORY42 CHAPTER TWO (A) Horizontal (8) Incline (©)ineline > 45 (Walk and run only, (Walk and run only, (Run—flapping) ‘no flapping) ro flapping) gare \ (Dyvertical (© Vertical fight (©) Horizontal fight (Run—flapping) (Flapping only) (lapping only) FIGURE 2-13 Overview of wing positions of a Chukar partridge during wing-assisted incline running, and the proposed transitions to powered flight. (A and 6) Birds running over level substrates or shallow inclines do not use their wings to assist running. However, even partial wing development provides assistance to birds climbing inclines greater than 45 degrees. (C and D) A part of the wingbeat cycle (as much as 30 percent) directs aerodynamic forces toward the inclined surface, not skyward, which improves traction. (D through #) Mastery of vertical inclines attains use of wings in ways required for flight. [From Dial 2003a} Eocene epoch (Figure 2-14). In the Eocene, long-legged vulturelike birds (Neocathartes) lived in Wyoming beside shorebirds with ducklike heads (Preshyomnis). From the Oligocene epoch to the Pliocene epoch, 12 known species of phorusthacids—predatory birds from 2 to 3 meters tall, with powerful, rapacious bills—ranged throughout South America and north to Florida. ‘As recently as the last ice age, huge vulturelike teratorns dominated the skies. One teratorn with a 4-meter wingspan was abundant in south- em California, Another, known fiom caves in Nevada, had a wingspan of 5 to 6 meters, and yet another, recently discovered in Argentina, had an 8-meter wingspan. They were the size of small airplanes! These enor- mous birds symbolize some of the extremes of past avian achievements. Two waves of explosive evolution of modern birds, however, were ry ornithology (Feduccia 2003; Figure 2-13). million years ago, spawned nonpasserine birds The first wave. starting 6 (Text continues on page 43.)FIGURE 2-14 Large flightless birds, including diatrymas, flourished during the Tertiary period. [From Heilmann 1927] Ratites and, tinamous Gobipteryx, | Avisauras, ete Nonpasserines Paleocene 65 mya + NX Lithornithids “Transitional © shorebirds, Cretaceous paleognaths, etc. Herero gf? Ichthyornithiforms \\ Enantiornithines Late 100 mya Cretaceous Ambiortus Ganstes karly 135 nya Nea gros Cretaceous iberomesornis, tate Ts ove hh srciocopter Diversification ———___________ FIGURE 2-15 Model of the evolution of modern birds Two major radiations, the Enantiornithes and the primitive ornithurines, dominated the Cretaceous period after Archaeopteryx but did not survive into the Tertiary. Three major radiations during the ‘Tertiary gave rise to the major groups of modern birds: ratites and tinamous, rnonpasserines: and passerines. [From Feduccia 2003] 4344 CHAPTER TWO 4 5 FIGURE 2—16 ‘The large flightless birds of the world, called ratites, and the related tinamous evolved early in the Tertiary period. (1) Elegant Crested Tinamou: (2) Southern Cassowary; (3) Northern Brown Kiwi, (4) Rhea; (5) Common Ostrich.FIGURE 2-17 Woodpeckers and their allies were a preeminent group of nonpasserine land birds in the Tertiary: (1) Great Spotted Woodpecker, (2) Greater Honeyguide; (3) Double-toothed Barbet; (4) White-chinned Jacamar, (5) White-eared Pulfbird, of most of the orders of birds present today, including ratites (Figure 2-16). Specialized water birds, such as loons. auks, gulls, ducks, cranes. and pe- els, invaded ing, the Eocene epoch, from 54 million to 36 million years ago. Primitive woodpeckers and their relatives also appeared during the early Eocene and became the predominant perching birds during the Miocene epoch (Figure 2-17). Hummingbirds, too, go. back to the same epochs of Earth history. Fossils from the early Oligocene of southern Germany reveal that hummingbirds, now restricted to the 45 HISTORY46 CHAPTER TWO FIGURE 2-18 Rollers, kingfishers, and their allies (Order Coracitformes) were a dominant group of modern nonpasserine land birds early in the Tertiary period. Modern species include: (1) Puerto Rican Tody, (2) European Bee-eater, (3) Lilac- breasted Roller, (4) Turquoise-browed Motmot; (5) Oriental Pied Hornbill, (6) Pied Kingfisher.Wester Hemisphere, once Relatives of rollers, kingfishers, habited the Old World, t00 (Mayr 2004). 1d hornbills diversified in the Oligocene epoch (Figure 2-18). By the end of the Tertiary, from 10 million to 5 rmillion years ago, birds had diversified into a broad range of forms that included many modem genera The radiation of passerine birds, or songbirds, produced the second wave of new bird taxa in the Tertiary (Barker et al. 2004). The rapid evo- lution of flowering plants and insects in the Miocene opened new niches for insect-eating, fruit-eating, and nectar-feeding birds; this diversity of ecological opportunities resulted in an explosive radiation of songbirds (Regal 1977). Now they constitute more than half of all existing bird species: more than 3700 by the most conservative estimates. Defining passerine birds are many unique ateributes—small size, sperm structure, vocal abilities, perching foot. and high metabolism—but which attributes. if any, were key adaptations that catalyzed their success is still an open question (Raikow and Bledsoe 2000). The early diversification of birds, both passerine and nonpasserine, took place on a very different Earth: neither the arrangement of the continen- tal landmasses nor their climates resembled those of today. Through much of the Tertiary period, the world’s climates were warm trom pole to pole there was no striking polar gradient from frigid to hot as there is today. Antarctica Tinamous Moas Kiwis Elephant Rheas Ostrich Cassowaries Emu birds FIGURE 2-19 Ratites and tinamous are distributed throughout the ice-free continents of the Southern Hemisphere that once composed Gondwanaland. [After (Crncraft 2002} 47 HISTORY48, CHAPTER THO For example, during the late Eocene and early Oligocene epochs (ee Table 2-1 for the geologic time scale), subtropical to tropical climates with abundant precipitation and no frost prevailed in the far north of both North America and Eurasia. The floras of Great Britain and of western Europe in the early Eocene resembled those of the modern rain forests of Southeast Asia. Tropical birds—trogons, parrots, hombills, barbets, broadbills, and mousebirds—once lived in central Europe. Alligators and large tortoises lived on Ellesmere Island above the Aretic Circle ‘The arrangements of continents and their connections also changed over the period of avian evolution. The modern continents have been moving apart since the late Jurassic and Cretaceous periods. Much of the major reorganization during the Mesozoic era of the single great landmass known as Pangaea, with Laurasia in the north and Gondwanaland in the south, preceded the evolution of modem bird taxa. Nevertheless. we now believe that Gondwanaland and its southem continent offpring—South America, Affica, Madagascar, and Australia—played a major role in the evolution and distribution of modern birds (Figure 2-19). Ancient species, including the oldest parrots (Kea, Kaka) and the oldest songbirds (New Zealand wrens), persist as relicts in New Zealand, The mobility of birds. augmented by changing global climates and connections of land or sea, fostered fusions of isolated avifaunas. The Gondwanaland association of Southem Hemisphere continents fostered the exchange of taxa among Africa, South America, Ancestral fowl—moundbuilders in Australia, guans in South America, and guineafowl in Afica—appear to have originated in the main pars of Gondwanaland. Radiations of pheasants, partridge, and grouse in North America came after the northward expansion of ancestral groups into Laurasia and the separation of Laurasia into North America and Eurasia in the Eocene. The birds of South America now include ancient elements from Gondwanaland plus more recent arrivals from North America. Rep- resentatives of the nt Gondwanaland avifaunas are also sprinkled among the modern bird communities of Africa, Madagascar, and south ern Asia. The diversity of modern birds is duc to the rich 65-million-year history of evolution, expansions, and contractions of new taxa. ind Australia, Summary Birds evolved from small, bipedal reptiles more than 150 million years ago in the Mesozoic era. Birds and reptiles have many anatomical features in common—features that distinguish them fiom mammals. including a single occipital condyle on the back of the skull, a single middle-ear bone, and nucleated red blood cells. Archaeopteryx lithographica, one of the most important fossils of all ime, was a crow-sized, toothed, bipedal reptile with two essential avian fea- tures: feathers and a furcula (wishbone). It could clamber around trees and could fly. Known from seven specimens preserved in fine limestone de- posited in the late Jurassic period in Bavaria, it represents an evolution-ary link between birds and reptiles. Because of its timely discovery, Archaeopteryx fostered acceptance of Darwin's theory of evolution, Exactly which group of reptiles gave rise to birds has been the topic of strong de- bates, New fossils from China point to small theropod dinosaurs, some of which had feathers, as the ancestors of birds. Feathers evolved in theropod dinosaurs most likely as a form of insu lation and possibly heat protection. Extensions of feathered forelimbs of terrestrial dinosaurs aided running and jumping and then climbing and gliding, The powered wing stroke. combined with the evolution of che alula for controlled slow-speed flight, completed the evolution of avian flight. One fossil species found in China in 1987, Sinomis santensis, re~ tained many primitive features but also had advanced features of modern avian flight and perching abilities. Another fossil bird, 115-million-year- old Eoululavis, had a well-developed alula that enabled controlled flight and landing. Once established, birds diversified in both form and fun major radiations of ancient birds, the Ornithurae and the prospered in the Cretaceous but then disappeared. The modern orders of birds diverged fiom one another near the beginning of the Tertiary period, 60 million years ago, followed by the radiation of water birds in the Eocene epoch and land birds in the Miocene epoch. Avifiunas are the grind resule of millions of years of evolution, adap tive radiation, dispersal, and extinction of avian taxa with varied ecolog- ical roles. Throughout the history of avian evolution, neither the world’s climates nor the arrangement of the continents were as we know them today. Gondwanaland and the southern continents that it produced were a central stage in the early evolution of modem birds. Now many birds occupy only remnants of their original discributions. 49 HISTORY