Joel Cracraft Julie Feinstein Jaime García-Moreno F. Keith Barker Scott Stanley Michael D. Sorenson Michael Braun Alice Cibois Tamaki Yuri John Harshman Peter Schikler David P. Mindeli Gareth j. Dyke Pamela Beresford
Phylogenetic Relationships among Modern Birds (Neornitlies) Toward an Avian Tree of Life
Modem perceptions of the inonophyly of avian higher taxa and wfithin a few short years after Origin and a year before {modern birds, Neomiihes) and their interrelationships are Huxley's seminal paper, he produced the monumental the legacy uf systematic work undertaken in the 19th cen- Generelle Morphola^c der Organismen•the first com]5rehen- tury. Before Llie imroduttion of an evolutionary wo rid view sive depiction of the Tree of Life (Haeckel 1866). Haeckel's by Charles Darwin in 1859, taxonomists clustered laxa into interests were primarily with invertebrates, but one of his groups using similarities that reflected a vision of how God students was to have a singular impact on systematic orni- might have organized ilic world ai the time of Creation. Such thology that lasted more than 125 years. was the case with the Quinerian system of avian classifica- In 1888 Max Fürbringe r published his massive (1751 tion devised by Macleay (1819-1821) in which groups and pages, 30 plates) two-volume tome on the morjjhology and subgroups of five were recognized, or of Strickland (1841) systematics of birds. Showing his classical training with or Wallace (1856) in which affinities were graphed as un- Haeckel and the comparative anatomist Carl Gegenbaur, rooted networks (see O'Hara 1988), Fûrbringer meticulously buili the first avian Tree of Life• After Darwin, this worldview changed. For those com- including front and hind views of the tree and cross sections parative biologists struggling to make sense of Earth's hiotic at different levels in time. The vastness of his morphological diversity in naturalistic terms, Darwinism provided a frame- descriptions and comparisons, and the scope of his vision, work for organizing similarities and differences hierarchically, established his conception of relationships as the dominant as a pattern of aneestry and descent. The search for the Tree viewpoint within systematic ornithology. All classifications that of Life was launched, and it did not take long for the struc- followed can fairly be said to be variations on Fürbringer's ture of avian relationships to be addressed, The firsi to do so theme. Such was the magnitude of his insights. Indeed, as was no less a figure than Thomas Henry Huxley (1867), who Stresemann (1959: 270) noted: produced an important and influential paper on avian clas- sification that was explicitly evolutionary, tt was also Huxley On the whole all the avian systems presented in the who provided the first strong argument that birds were re- standard works in this century are similar to each lated to dinosaurs (Huxley 1868), other, since they are all based on Fûrbringer and Huxley was particularly influential in England and was Gadow |who followed Ftirbringer's scheme closely read widely across Europe, but the 'father of phylogeneiics" and, being fluent in German, was able to read the and phylogenetic "tree-thinking" was clearly Ernst Haeckel, 1888 tomej. My system of 1934 [Stresemann 1927- Darwin's conceptual framework had galvanized Haeckel, 1934] does not differ in essence from those which
468 Phylogenetic Relationships among Modern Birds (Neornithes) 469
Weimore (1951) and Mayr and Amadon (1951) have "new systematics" has opened up a field which is far recommended. more accessible lo accurate research and which is more apt to produce tangible and immediate results, (Mayr Furl?ringer (1888) thus estabîished the framework for vir- 1942: 291) lually all the major higher level taxa in use today, and the faci that subsequent classifications, with relatively minor A final answer was that, if phylogeny were essentially alterations, adopted his groups entrenched them within or- unknowable, it would inevitably be decoupled from classih- nithology so pervasively thai his classificatory scheme has cation.andthe latter would be seen as subjective. The archi- influenced how ornithologists have sampled taxa in system- tects of the synthesis clearly understood the power of basing atic studies to the present day. classifications on phylogeny (e.g., Mayr 1942: 280) but in Despite his monumental achievement in establishing the addition to lack of knowledge, "the only intrinsic difficulty first comprehensive view of the avian branch of the Tree of of the phylogenetic system consists in the impossibility of Life, a\ian phylogeny soon became of only passing interest to representing a 'phylogenetic tree' in linear sequence." systeraatists. Phylogenetic hypotheses•in the sense of taxa be- Twenty-seven years later, Stresemann summarized clas- ing placed on a branching diagram•^were largely abandoned sificatory history to that date in starkly harsh terms: until the last several decades of ihe 20th century. For more than 80 years after Fûrbringer the pursuit of an avian Tree of In view of the continuing absence of trustworthy Life was replaced by an interest in tweaking classifications, the information on the relationships of the highest most important being those of Wetmore (1930, 1934, 1940. categories [taxa] of birds to each other it becomes 1951, 1960), Stresemann (1927-1934), Mayr and Amadon smelly a matter of convention how to group them into (1951), and Storer (1960). Aside from reflecting relationships orders. Science ends where comparative morphology, in terms of overall similarity, these classifications also shaped comparative physiology, comparative ethology have contemporary views of avian phylogenetics by applying the failed us after nearly 200 years of effort. The rest is philosophy of evolutionary classification (Simpson 1961, Mayr silence. (Stresemann 1959: 277-278) 1969), which ranked groups according lo how distinct they were morphologically. The silence did not last, A mere four years after this indictment ofavian phylogenetics, Wilhelm Meise, whose office was next What happened to "tree thinking" in systematic orni- to that of the founder of phylogenetic systematics, Willi Hennig, thology between 1890 and 1970? The first answer to this published the first explicitly cladistic phylogenetic tree in or- question was that phylogeny became characterized as the nithology, using behavioral characters to group the ratite birds unknown and unknowable. Relationships were considered (Meise 1963). Avian systematics. like all of systematics, sooii impossible to recover without fossils and resided solely in became translbimed by three events. The first was the intro- the eye of the beholder inasmuch as there was no objective duction of phylogenetic (cladistic) thinking (Hennig 1966)and method for detennining them. Thus, Stresemann (1959: 270, a quantitative methodology for building trees using those prin- 277) remarked. ciples (Kluge and Farris 1969; the first quantitative cladistic The construction of phylogenetic trees has opened the analysis for birds was included in Payne and Risley 1976), At door to a wave of uninhibited speculation. Everybody the same lime, the rise of cladistics logically led to an interest may form his own opinion , , . because, as far as birds in having classifications represent phylogenetic relationships are concerned, there is virtually no paleomologica! more explicitly, and that too became a subject of discussion documentation. . ., Only lucky discoveries of fossils within ornithology (e.g., Cracraft 1972, 1974, 1981). This can help us. ,.. desire for classifications to reflect phylogeny had its most com- prehensive expression in the classification based on DNA-DNA A second answer is that phylogeny was eclipsed by a re- hybridization, a methodology, however, that was largely phe- definition of systematics, which became more aligned with netic(Sibleyetal. 1988, Sibley and Ahlquist 1990, Sibley and "population thinking." This view was ushered in by the rise Monroe 1990). of the so-called "New Systematics" and the notion that "the The second contribution that changed avian systemat- population . , , has become the basic taxonomic unit" (Mayr ics was increased use of molecular data of various types. 1942: 7). The functions of the systematist thus became iden- Techniques such as starch-gel electrophoresis, isoelectric- tification, classification ("speculation and theorizing"), and focusing electrophoresis, immunological comparisons the study of species formation (Mayr 1942: 8-11). Phylog- of proteins, mitochondrial DNA (miDNA) RFLP (restric- eny became passé [see also Wheeler (1995) for a similar in- terpretation). Thus, tion fragment length polymorphism) analy.sis, DNA hy- bridization, and especially mtDNA and nuclear gene The study of phylogenetic trees, of orthogenetic series, sequencing have all been used to infer relationships, from and of evolutionary trends comprise a held which was the species-level to thai of families and orders. Today, with the happy hunting ground of the speculative-minded few exceptions, investigators of avian higher level rela- taxonomist of bygone days. The development of the tionships use DNA sequencing, mostly of mtDNA, but 470 The Relationships of Animals: Deuterostomes
nuclear gene sequences are now becoming increasingly Archaeopteryx important Finally, not to be forgotten were the continuous innova- Neornithes tions in computational and bioinformatic hardware and soft- ware over the last three decades that have enabled invesiigaiors to tolled, store, and analyze increasing amounts of data. Ichthyornis This chapter attempts to summarize what we think we know, and don't know, about avian higher level relation- Hesperornis ships at this point in time. In the spirit of this volume, the chapter represents a collaboration of independent labora- Enantiornithes tories actively engaged in undcrsianding higher level rela- tionships, but it by no means involves all those pursuing •Confuciusornithidae this problem. Indeed, there is important unpublished mor- phological and molecular work ongoing that is not included iTroodontidae here. Nevertheless, it will be apparent I rom this synthesis thai significant advances are being made, and we can ex- pect the nexi five years of research lo advance measurably Dromaeosauridae our understanding of avian relationships. aCaudipteryx
Birds Are Dinosaurs tSinosauropteryx
Considerable debate has taken place in receñí years over •Alvarezsauridae whether birds are phylogeneiically linked to maniraptorian dinosaurs, and a small minority of workers have contested tStruthiomimus this relationship (e.g., Tarsitano and Hecht 1980, Martin 1983, Fed necia 1999. 20Ü2. Olson 2002). In contrast, all tTyrannosaurus rex researchers who have considered this problem over the last 30 years from a cladistic perspective have supported a Figure 27.1. Kclationships of birds to theropod dÍTios;mrs (after theropod relationship for modern birds (Ostrom 1976, Chiappe and Dyke 2002). Cracrafi 1977, 1986, Gauthier 1986, Padian and Chiappe 1998, Chiappe 1995, 2001, Chiappe et al. 1999, Sereno 1999, Norell et al. 2001, Holtz 1994, 2001, Prum 2002, DNA Hybridization and Beyond Chiappe and Dyke 2002, Xii el al. 2002), and that hypoth- esis appears as well corroborated as any in systematics The DNA hybridization work of Siblcy and Ahlquist (1990) (fig. 27.1). has had a major impact on avian systematics. Their tree• Having said this, droves of fossils•advanced theropods the so-called "Tapestry" shown tn figure 27.2•provided as well as birds•are being uncovered with increasing regu- a framework for numerous evolutionary interpretations of larity, and many of these are providing now insights into avian biolog)'. Avian systematists, however, have long noted character distributions, as well as the tempo of avian evoíu- shortcomings with the analytical methods and results of tion. Just 10 years ago, undersiandingof the early evolution Siblcy and Ahlquisi (Cracraft 1987, Houde 1987. Unyon of birds was based on a handful of fossils greatly separated 1992. Mindell 1992, Harshman 1994). Moreover, it is obvi- iem]îorally and phylogeneiically (e.g., Archaeopteryx and a ous that Sibley and Ahlquist, like many others before and few derived omithurines) Now, more than 50 individual taxa after, designed their experiments with significant precon- are known from ihroughoui the Mcsozoic (Chiappe and ceived assumptions of group monophyly (again, inany of Dyke 2002). and from this new information it is now clear which can be traced to FUrbringer 1888). that feathers originated as a series of modifications early in The spine of the DNA hybridization tree is character- the theropod radiation and thai flight is a later innovation ized by a plethora of short iniernodes, which is consistent (reviewed in Chiappe and Dyke 2002, Xu et al. 2003). with the hypothesis of an early and rapid radiation (dis- Numerous new discoveries of pre-neomithine fossils will cussed more below). The critical issue, however, is that most undoubtedly provide alternative interpretations to charac- of the deep intemodes on Sibley and Ahlquist's ( 1990) tree ter-state change throughout the line leading to modern were not based on a rigorous analysis of the data, and in birds (for summaries of pre-neornithine relationships, see fact the data are generally insufficient to conduct such analy- Chiappe and Dyke 2002), ses(,Lanyon 1992, Harshman 1994). Relationships implied emus DROMICEIDAE < cassowaries CASUARIIDAE kiwis APTERYGiDAE rheas RHEiDAE Palaeognathae ostrich STRUTHiOMDAE tinamcius TiNAMiDAE i duclts, geese ANATiDAE i screamers ANHIMIDAE Magpie Goose ANSERANATiDAE pheasants PHASiANIDAE Galloanserae guineafûwl NUMtDiDAE quail OOONTOPHORiDAE guans CRACIDAE mound buiiders MEGAP0D1DAE i buttonquaiis TURNiCiDAE woo(lpccl
6. A combined analysis of 74 "waterbird" taxa for 5300 cassowaries base pairs of miiochondrial and RAG-2 gene se- quences (S. Stanley, J. Feinstein, andj, Cracraft, emus unpubl. obs.) 7. An analysis of ]46 passeriform taxa for 4108 base rheas pairs of the RAG-1 and RAG-2 nuclear genes (F. K. Barker, J. F. Feinstein, P. Schikler, A. Cibois, and J. Cracraft, unpubl. obs.) ostrich 8. An analysis of 44 nine-primaried passeriforms Palaeognathae ("Fringillidae) using 3.2 kilobases of mitochondrial (kiwis sequence (Yuri and Mindeli 2002). •tinamous
Phylogenetic Relationships Galloanserae duclts, geese among Basal Neornithes Magpie Goose The Base of the Neornîthîne Tree
In contrast to the considerable uncertainties that exist regard- .screamers ing the higher level relationships among the major avian clades, the base of the neomithine tree now appears to be guans, curassows well corroborated by congruent results from both morpho- logical and molecular data (fig. 27,3; summarized in Cracraft ptieasants, quail, and Clarke 2001, Garcla-Moreno et al. 2003; see below). gulnealowl Thus, modem birds can be divided into two basal clades, •megapodes Palaeognathae (tinamous and the ratite birds) and Neo- gnaihae (all others); Neognathae, in turn, are composed of •Neoaves two sister clades, Galloanserae for the galliform (megapodes, guans, pheasants, and allies) and anseriform (dutjks. geese, Figure 27.3. The basal rciationships of modern iiirds swans, and allies) birds, and Neoaves for all remaining taxa. tNeomilhcs). Retalionships within Paleognathae arc those based on morphology (Lee el al. 1997). which do not agree wuh results This tripartite division of basal neomithines has been recov- from molecular sequences. See text for further discussion. ered using morphological (Livezey 1997a, Livezey and Zusi 2001, Cracraft and Clarke 2001, Mayr and Clarke 2Ö03; see below) and various types of molecular data (Groth and it also worth noting that palaeognaths and neognaths arc BaiTowcIough 1999, van Tuinen ei al. 2000, Garcia-Morcno readily distinguished by large homomorphic sex chromo- and Mindell 2000, GarcIa-Morcno ei al. 2003, Braun and somes in the former and strongly heteromorphic chromo- Kimball 2002, Edwards ct al. 2002, Chubb 2004; see also somes in the latter (Ansari et al. 1988, Ogawa et al. 1998). results below). The DNA hybridization tree also recovered this basal structure, but the root, estimated by assuming a Palaeognathae molecular clock without an outgroup, was placed incorrectly (fig. 27.2). In contras!, analyses using morphological or Monophyly of palaeognaths is well corroborated, but rela- nuclear sequences have sought to place the root through tionships within the ratites remain diffictilt to resolve. The outgroup analysis, and their results are consistent in placing relationships shown in figure 27.3 reflect those indicated by it between palaeognaths and neognaths (Cracraft 1986, Groth morphology (Cracraft 1974, Lee et al. 1997, Livezey and Zusi and Barrowclough 1999, Cracraft and Clarke 2001; see also 2001), and all the internodes have high branch support. studies discussed below). Small taxon samples of mitochon- Molecular data, on the other hand, have differed from this drial data have also been particularly prone to placing the view and. in general, data from different loci and methods presumed fast-evolving passerine birds at the base of the of analysis have yielded conflicting results, in most of these neomithine tree (Harlid and Amason 1999, Mindell et al. studies (Lee et al, 1997, Haddrath and Baker 2001, Cooper 1997, 1999), but larger taxon samples and analyses using et al, 2001) the kiwis group with the emu + cassowaries, and better models of e\'olution (e.g., Paton et al, 2002) have the rhea and ostrich diverge independently at the base of the agreed with the morphological and nuclear sequence analy- 11 ee. When the extinct New Zealand moas are included in ses. Recent studies of nuclear short sequence motif signatures studies using most of the mitochondrial genome (Haddrath support the traditional hypothesis (Edwards et al. 2002), and and Baker 2001. Cooper et al. 2001), they also tend to be 474 The Relationships of Animais: Deuterostomes pîaced toward the base of the tree. It can be noted that single ostrich gene trees often do not recover raiiie monophyly with strong rhftas support, all hough these taxa generally group together, kiwis tinamous Palaeognaihs appear to exhibit molecular rate heteroge- cassowaries neity. Tinanious, in particular, and possibly rheas and os- einu triches appear to have higher rates of molecular evolution New Worid vuitures than do kiwis, emus, and cassowaries (Lee et al, 1997, van nightjars faicons, caraca ras Tuinenet al, 2000, Haddiathand Baker 2001 XAddiiionally, hawlfrogmouths in base composition, which have made phytogenciit inter- oilbird pretations difficult (Haddrath and Baker 2001), Thus, rate cranes artifacts, nonstationarity, the existence of relatively few, rails deeply divergent species-poor lineages, and short internodal owls parrots distances among those lineages ail play a role in making ihe songbirds resolution of raiite relationships extremely difficult and con- potóos troversial. Although palaeognath relationships may be solved trogons with additional molecular and nioiphological data of the tra- owlet nightjars hummingbirds ditional kind, the discovery of major character changes in swifts molecular sec|uences such as indels or gene duplications may barbets, toucans also prove to be important, woodpeckers, honeyguides putfbirds jacamars Calloanserae kingfishers, motmots rollers Despite occasional debates that galliforms and anseriforms grebes arc not sister taxa (Ericson 1996, 1997, Ericsonci al,2001), flamingos loons the predominant conclusion of numerous workers using shearwaters morphological and/or molecular data is that they are (Livczey tro pic bird 5 1997a. Grot h and Banowciough 1999, Mi tide II et al. 1997, ibises shoebill 1999, Zusi and Livezey 2000, Livezey and Zusi 2001, Cracrafi pelicans and Clarke 2001, Mayr and Clarke 2003. Chubb 2004), herons Molecular studies questioning a monophylctic Galloanserae cormorants (e,g,, Ericson et al, 2001) have all employed small taxon gannets frigateblrds samples of mtDNA or nuclear DNA, but when samples are penguins increased, or nuclear genes are used, Galloanserae are sun bittern monophylctic and the sister group of Neoaves (Groih and storks Barrowclough 1999, Garcia-Moreno and Mindetl 2000, van buHonquail ^•C shorebirds Tuinen ct al. 2000, García-Moreno et al. 2003, Chubb 2004; tioatzin sec alsoj. Hai^shnian, M. J. Braun, and C, J, Huddlesion, pheasants, quail, guineafowl unpubl. obs); three indel events in sequences from i-myc chachalacas megapodes also support a monophylctic Galloanserae (hg. 27.4). The magpie goose DNA hybridization tree of Siblcy and Ahlcjuist (1990) rec- ducks ognized Galloanserae. but because the neormthme root was Figure 27.4. Phylogenetic tree based on approximately I 100 incorrectly placed, Galloanserae was resolved as the sister bases of the nuclear oncogenc c-niyt. incktdirig intrtm, cxon group of the palaeognaihs. With respect to relationships coding, and 3' untranslated region sequence, for 170 laxa within galliforms, a consistent pattern seems to have emerged CJ Harshman, M.J. Braun, and C. H Huddleston, unpubl. (Cracrafi 1972,1981,1988, Sibley and Ahlquist 1990, fig. 328, obs,). The tree shown is an unweighied parsimony majority rule Harshman 1994, Dimcheif ei al. 2000,2002, Dyke et al. 2003; bootstrap tree, plus other compatible branches. Thick branches see also J. Harshman. M. J. Braun, and C. J. Huddlesion, have 70% or greater bootstrap support; thin branches may have unpubl. obs.): (Megapodiidae (Cracidae (Numididae + very low support. Vertical tick marks represent phylogeiieiically Odomophoridac + Phasianidac))). The major questions re- informative indels. Mosi terminal branches represent several main centered around ihe relaiivc relationships among the species, and all those are strongly supponed. although ¡or claritv the branches are not shown as thickened. guinea fowl (numidids), New World quail (odontophorids), and pheasants (phasianids), as well as the phylogeny within the laitcr; recent sludies suggest that the numidids are out- Phyiogenelic Relationships among Modern Birds (Neornithes) 475 side quails and phasianids (Cracraft 1981, Dimcheff ei al. Eudromia tinamaus 2000,2002, Dyke et al, 2003). Struthio rheas, ostriches Relationships among ihc basal clades of anseriforms are also Rhea Dendrocygna ducks, geese not too controversial (IJvczcy 1986,1997a,; Sililey and Atit<:[uist Aythya 1990: fig. 328 contra the "tapestry", Harshinan 1994, Ericstm Chauna screamers 1997, Groth and îîarrowclough 1999; for views of rclaiionsKips Anseranas Magpie Goose Megapodiiis megapodes wiihinanatids,sceMadsenet al. 1988,Uvezey 1997b,Donne- Alectura Goussé et al. 2002). The screamers (AnhimidatO are the sister Gallus pheasants group 10 the magpie goose (Atiseratiaiidae) + dueks, geese, and Aery Ilium guinea fowl Crax guans, currasows swans (Anatitiae). We note, however, that the resolmion of the Otus owls basal nodes among screamers, magpie goose, and anatids has Tockus hornbllis been diffitult and thai mitoehondrial data sometimes unite the Buleo hawks screamers and magpie goose (fig. 27.5), a grouping not sug- Crinifer turacos Musophaga gested by nuclear, morphological, or combined data. The fact Columba pigeons thai bolh Livezey (1997a) and Ericson (1997) found the Late Treron Creiaceous-l'aleogene fossil Presbyomis to be the sister group Trogon trogon s Opisthocomus Hoatzin of Anatidae (see also Kurochkin et al. 2002) is important he- Phoenicipterus flamingos cause il sets the Laie Cretaceous as the minimum time of di- Scolopax shorebirds vergence for the anatids and all deeper nodes. Burhinus Mycteria storks Ciconia Relationships within Neoaves Colius mouseblrds Urocolius Relationships among the neoavian higher taxa have been Nandayus parrots Neophema discussed in a nuinber of studies over the past several de- Smlthornls broadbills cades (e.g., Cracraft 1981, 1988, Siblcy and Ahlquist 1990, Sayomis tyrant flycatchers Ericson 1997,Mindellei al. 1997, 1999. Fcduccia 1999, van Vidua finches Corvus crows Tuinenei al. 2000, 2001, among others), and ii is clear that Neomorphus relatively little consensus has emerged. The monophyly of Crotophaga cuckoos many groups thai have been accorded the taxonomic rank Centropus Coccyzus of "order" such as loons, grebes, penguins, parrots, cuckoos, Cuculus and the large songbird group (Passenformes) has not been Falco falcons seriously questioned but that of nearly all other higher taxa Coraciaa rollers has. Thus, it is now broadly accepted thai several traditional Figure 27.5, A ptiylogenetie hypothesis for 41 avian taxa based orders such as pelee ant forms, ciconiiforms, and capriinulgi- on about 4800 base pairs ol miWLhondrial sequence and &80 base forms are nonmonophyletic, whereas the status of others such pairs of PEPCK intron 9 nuclear gene using ihree paleognaths as as gruiforms, eoraciifonns, picifonns. and falconiforms remains ihe root (Soienson ci al. 2003). Nodes with bootstrap support uncertain in the minds of many workers. values ol 70% ;ire shown in hcav)' hlaek, based on maxiiiiiini If one had to summarize the current siaic of knowlcdge, likelihood and maximum probahiiity analyses of mitoehondrial the most pessimistic view would see the neoavian tree as a data and MP analyses of PEPCK intron 9. "comb," with little or no resolution among most traditional families and orders. Short and poorly supported iniemodes primary reason for the neoavian comb is suspected to be among major clades of neoavians are characteristic of recent insufficient character and/or laxon sampling. As noted above, studies using nuclear (Groth and Barrowclough 1999, van current evidence suggests that many of these divergences are Tulnen et al. 2000) or mitoehondrial data sets (van Tuinen old and occurred relatively close in time. Thus, we arc opti- eial. 2000, 2001, Johnson 2001, Hedges and Sibley 1994. mistic that most neoavian relationships will be resolved with Johansson et al. 2001), and the data sets discussed here also additional data (see Discussion, below). illustrate this point. The trees discussed below will be inter- preted within the framework of bootstrap resampling analy- Phylogenetic Relationships among ses that show sister lineages supported at the 70% leve! (heavy the "Waterbird Assemblage" lines in the figures). Using this approach, relationships among the avian higher taxa can be inteipretcd as largely unresolved, Ovcv the years, many autbors have suggested that some or producing the neoavian comb. Nevertheless, there are emerg- all of the waterbird orders, in particular, seabirds (Procet- ing .similarities in phyiogenelic pattem recovered acro,<;s some lariiformes), penguins (Spbenisciformes), loons (Gaviifonmes), of these different studies that suggest some commonality of grebes (Podicipediformes), storks, herons, flamingos and al- phylogenetic signal. In these and other published cases, the lies (Ciconiiformes), pelicans, cormorants, and allies (Pele- AU The Relationships of Animals: Deuterostomes
caniformes), shorebirds and gulls (Charadriiformes), and ing, and (3) various clades within traditional charadrii forms cranes, rails, and allies ( G m i formes), are related to one an- and gmiforms. Both i-myc and RAG-2 + morphology Imk other (see, e.g., Sibley and Alilcjuist 1990, Hedges and Sibley Irigaiebirds to the sulids, phalacrocoracids, and anhingids. 1994, Olson and Feduccia 1980a, 1980b, Cracrafl 1988). In an attempt to address problems of sparse laxon sam- Some authors have also linked various lalconifomi families pling seen in previous studies, S. Stanley,]. Feinstein, and J. to the waterbird assemblage (Jollie 1976-1977, Rea 1983), Cracrafl (unpubi. obs.) examined 57 waterbird taxa for 5319 including a supposedly close relationship between New base pairs of mitochondrial and nuclear RAG-2 sequences Wodd vultures (Caihanidae) and storks (Ligon 1967. Sibley (fig. 27.6). When paiaeognaihs and Galloanserae are used as andAhlquist 1990, Avise et al. 1994; but also see Jollie 1976- ouigroups, the root of the waterbird tree was placed on one 1977, Hackett et al. 1995, Heibig and Siebold 1996), As a of the [WO gruifonm lineages, thus suggesting, in agreement consequence of these and newer molecular studies, it is now with Sibley and Ahlquist (1990) and van Tuitien et al, (2001), widely ihoughi ihai several of the large traditional orders of that gruí forms arc outside the other waterbird taxa, although waterbirds may not be monophyletic, and this is especially this is not strongly supported given available data. This larger true of the peiccaniforms and ciconiiforms (Cottam 1957, analysis still provides little resolution fur higher level rela- Sibley and Ahlquist 1990, Hedges and Sibley 1994, Siegel- tionships among waterbirds, but it does hnd support for a Causey 1997, van Tuinen et al 2001). grebe + flamingo relationship, monopliyly of charadriiforms, The supposition that waterbirds are related to one an- and the shoebill + pelicans + hammerkop clade, in agreement other within neomithines as a whole is not well supported, with van Tuinen el al. (2001) and ihe c-m>'(; data (fig. 27,4). although the available data are suggestive of a relationship The buttonquails (Tumicidae) have traditionally been among some of ihem (see above). Only the DNA hybridiza- considered members of ihe order Gruiformes, Recent mo- tion tree of Sibley and Ahlquist (1990) covered all birds, and lecular analyses, however, now place them decisively with on their tree (fig. 27.2) the waterbirds and falconiforms are the charadriiforms, and indeed ihey are the sister-group of clustered together. Van Tuinen ei al. (2001) recently re- the Lari (Paton ei al, 2003). The t-myc data (fig. 27.4) are evaluated waterbird relationships and compared new DNA consistent with this topology and include a unique indel, hybridization data with results from about 4062 base pairs uniting tumicids and chradriiforms. of mitochondrial and nuclear sequence data for 20 and 19 The mitochondrial and RAG-2 data also appear to con- taxa, respectively. Their most general conclusion was iheie tain phylogenetic signal for other clades even though they was relatively little branch support across the spine of ihe do not have high bootstrap values. Thus, when the data are tree, indicating that relationships among waterbirds are siill explored using a vanety of methods (e.g., transversion pai- very much uncertain. They did, however, find support for simony), the following groups are generally found (fig, 27,6): several clades: (1) a grouping of (the shoebill ßciWniccps + (1) an expanded "pelecaniform" clade thai also includes taxa pelicans) + hammerkop (icopus). and these in lurn lo ibises formerly placed in ciconiifomis (shoebill, hammerkop, ibises, and herons, (2) penguins + seabirds (Procellariiformes), and and storks), (2) a grouping of grebes and flamingos with most surprisingly, (3) grebes + flamingos. charadriiforms and some falconiforms, and (3) often a mono- Previous studies have had insufficient laxon and charac- phyletic Falconiformes (although the family Falconidae ter sampling, or both. Even though large taxon samples based was not sampled), with no evidence of a relationship be- on mitochondrial genes (fig. 27.6), or on the c-myc and RAG- tween storks and New World vultures, Tropicbirds (phae- 2 nuclear genes (figs. 27.4, 27.7A), are an improvement on thoniids) and herons (ardeids) represent divergent taxa that previous work, by themselves or together (fig. 27.8), they are have no stable posirion on the nee. Some of these relaiion- still inadequate to provide strong character support for most sbips are also seen in other data sets such as the i~myc data clades. Nevertheless, some congruence among these various (fig, 27.4) and in the mitochondrial data of van Tiainen et al. studies is apparent The c-myi data (fig. 27.4; J. Harshman, (2001), M.J.Braun, and C.J, Huddleston, unpubi. obs.), for example, recover (1) (connorants + ganneis) + frigalebirds, (2) (shoe- Phylogenetk Relationships among the Owls bills + pelicans) + ibises, (3) grebes + flamingos, and (4) (Strigiformes), Swifts and Hummingbirds buttonquails + shorebirds. At the same time, groups such as (Apodiformes), and Nightjars and Allies loons, tropicbirds, penguins, and storks do not show any (Cap rjmu Ig ¡formes) clear pattern of relaúotiships in the '^-myt data or the nuclear/ mitochondrial tree of van Tuinen et al. (2001). What is clear The DNA hybridization tree (fig. 27.2; Sibley and Ahlquist in the L-myc data is thai New World vultures and storks arc 1990) recognizes a monophyletic Caprimulgi formes that is distantly removed from one another; New Wodd vultures the sister group of the owls; these two groups, in turn, are were not included in the van Tuinen et al. study. The RAG- the sister group of the luracos (Musophagidae), and finally, 2 data (fig. 27,7; J. Cracraft, P. Schikler. and J. Feinstein, all three are the sister clade of the swifts and hummingbirds unpubi. obs.) also strongly support (Da pelican/shoebitl/ (Apodiformes), There is now clear evidence that this hypoth- hammerkop clade, (2) a cormorant/anhinga/gannet group- esis is not correct. Phylogenetic Relationships among Modern Birds (Neornitíies) 477
Psophia Psophiidae: trumpeters Grus canadensis Aramus guarauna Gruidae; cranes, limpktn Gavia pad ficus Gavjjdae: loons Gavia immer Oceanodroma leucorhoa Halocyptena microsoma Procellariidae: petrels, Puftinus griseus diving-petrels Pterodroma cahow Pterodroma tesson! Petecanoides magellani Pelecanoides urinatrix Pachyptila crassirostn's Futmarus glacialoides Diomedea nig ripes Diamediidae: albatrosses Diomedea buiiert Oceanites oceánicas Fregetta graiteria Aechmaphorus occídentalls Podiceps auritus Podicipedidae; grebes Taciiybaptus rtificoUis Podylimbus podiceps Phoenicopterus minor Phoenicopterus ruber Phoenicopterldae: flamingos Aclophilornis africanus Jacanidae: Jacanas Stiltia isabelia Glareolidae: pratincoles Larus mar i nus Sterna hirundo Laridae: terns, gulls Alca torda Alcidae; murres, auks Charadrius metodius Vanellus chilensis Charadrlfdae: plovers Cattiartes aura Cathartidae: New World vultures Coragyps atratus Pandion tialiaetus Accipitridae; osprey Sagittarius serpentarius Saglttariidae: Secretarybird Figure 27.6. A phylogenetic Fregata magnlficens Fregatidae: frigate bird s Fragata minor (lypothesis I or "wiuerbird" Morus bassanus Morus serrator Sulidae: boobies, gannets higher taxa using 4164 base Su la sula pairs of mitochondrial sequence Phalacrocorax urlie Phalacrocoracidae: cormorants (cylochromt b, COi, COIJ, COllí) Anhinga anhinga Anhingidae: anhlngas Ciconia ciconia and 1155 base pairs of the RAG- Mycteria americana Ci con i Ida e; storks 2 nuclear gene (iransvcrsion Leptoptilos javanicus Balaeniceps rex Balaeniclpitldae: Shoebill weighted) using gruiform taxa as Pelecanus erythrorynctios Pelecanidae: pelicans the root (S. Stanley, J. Feinsiein, Scopus umbretta Scopidae: Hammerkop and J. Cracrafi, unpubt. obs.). Eudocimus ruber Threskiornithidae: ibises Pygoscelis antárctica Thick brandies represent Pygosceiis papua Spheniscidae: penguins äpheniscus humbotdti intcrfamiliaj cladcs supported by Phaethon rubricauda Phaethontidae: tropic birds bootstrap values greater than Pbaethon lepturus 70% (all families had high Butorldes virescens Egretta tricolor Ardeidae: heron« bootstrap values but are not Ixobrychus sinensis shown for simplicity).
Both published and unpublished data have recently in- caprimulgiform taxa are also not supported by available se- dicaied that caprimulgiforms are not mouophyletic. Itistead C[uence data (figs. 27.4, 27.7, 27.8; Johansson ei al. 2001. of their traditional placement within caprimulgifonns, owlet- Mindell et al. 1997); however, one subsi^cjuenl DNA hybrid- nightjars (Aegothelidae) are most cîosely related to the swifts ization Study has supported this hypothesis, in addition to and hummingbirds, a hypothesis hrst recognized in t-myt linking owls, caprimulgiforms, and apodiforms (Bleiweiss nuclear sequences (Braun and Huddleston 2001; fig. 27.4). et al. 1994). Preliminary morphological data also suggest a This relationship is supported by morphological characters relaiionship (Livezey and Zusi 2001). (May r 2002) as well as by combined morphological and RAG- 2 data (fig. 27.7B) and by combined c-myc and RAG-2 data Phylogenetic Relationships among "Higher Land (fig. 27.8). Even with the aegothelids removed from the Birds": Cuculiformes, Coraciiformes, Trogoniformes, caprimulgiforms there is presently httle support for the Coliiformes, and Piciformes monophyly of the remaining families. The available molecu- lar data for c-myc, RAG-2, or combined c.-myc/RAG-Z (figs. Few avian relationships are as interesting as those associated 27.4, 27,7A, 27.8) do not unite them, nor do combined c- with the "higher lancl bird" question, and it is a problem with myc and RAG-1 fragments (Johansson et al. 2001) or mor- important imphcations for the overall topolog)' of the neomi- phology (Mayr 2002). The relationships of owls to various thine tree. Historically, groups such as the piciforms, coraci- tinamous tinamous emus, cassowaries ernus, cassowanes KIWIS ostriches KIWIS rheas ostriches pheasants, chickens pheasants, chickens mound builders mound builders nnagpif emboóse le ducKs, geese se ream ef s screamers Toons . penguins Ms storm-petrels shearwaters, petrels albatrosses 01VI nq-petrels diving-petrels priorS '^ penguins shearwaters albatrosses petrels [imp kin storm-petrels trumpeters grebes cranes rails, Sun-grebes rails, sungrebes cranes, limpkins bustards trumpeters mesites mesites sen a mas Sunbittern, Kagu Sunbittern, Kagu sen amas iacanas -ratincoles fa'è^^Îs^ ulls, terns, auks pratincoles plovers gulls, terns, auks oystercatchers plovers, oystercatchers stilts, avocets, thick-knees buttonquails buttonquails stilts, avocets, ttiick-knees frigatebirds boobies, gannetç tri gate birds cormorants, anhingas boobies, qannets tropicbirds cormorants, an hing as pelicans, Shoebill tropicbirds Hammerkop pelicans, Shoeblll storks" hammerkop pises flamingos herons ibises New World vultures slorlis osprey nerons falcons New world vultures osprey hawks, eagles falcons Secretary Bird secretary bird owls aw|(s¡^ragles Hoatzin turacos cucKoos sandgrouse igrouse parrots barn owls owls pigeons swifts Lcnminqbirds swifts \ir.ti mf hummingbirds X''-, . nighljars owlet-niqhtiars frog mouths Oilblrd potóos rogón s nightjars, potóos bee-eaters frogmouths rollers, g round-rollers trogons kingfishers horn bills, hoopoes bee-eaters todies ground-rollers mouseoirds rollers puffbirds, jaca mars kingfishers moimots _, woodpeckers, indicatorblrds mou se bird s Old World barbets puffbirds, jacamars toucans. New World barbets woodpeckers, indicatorblrds Acanlhisilta Old World barbets Old & New World, su bo seines toucans basal Australian ÔcorvidansO New World barbets passerldan oscines horn bills, hoopoes Australian robins OcorvidansO passeriforms B Figure 27.7. (A) A ph y loge net if hypothesis for ncoa\1an taxa using 11 ^2 base piiirs oí the RAG-2 cxon. i,li) A pli y loge ne tic tree based on 1152 base pairs ot tht ]i/\C-2 exon and 166 morphologi- cal characters. Analyses arc all unweighted parsimony. Thick branches have greater than 70% bootstrap support. Data frornj. Cratraft, P. Sehiklcr. J, Feinstein, P. Beresford. ;irid G.J. Dyke (unpubl. obs,). Phylogenetic Relationships among Modern Birds (Neornithes) 479 strong support from: iforms, passerifoims, caprimulgiforms, and cuculiforms have combined data and both data sets been associated with one another iti various classifications combined data only (e.g., Huxley 1867, Garrod 1874, Fürbringer 1888) and have combined data and one separate data set been loosely called "higher land birds" (e.g., Ülson 1985, Aptéryx Feduccia 1999. Johansson el al. 2001), Here we discuss the Casuarius Dromaius novaehollandige relationships within and among the corad i form and piciform Rhea americana birds, their placement on the neomithine tree, and their re- Struthio camelus Tinarnus maior lationships to the passehforms. Coragyps atraWs Although the cuculiforms, coraciiforms, and piciforms Calhartes Tockus have long been seen as higher" neornithines and often Upupa epops closely related lo passcri forms, this view was turned upside Ctiordeiles Eurostopodus down by the DNA hybridization tree (Sibley and Ahlquist Batrachostomus 1990), which postulated that all three groups were at the base Podargus papuensis of the neoavian tree (fig. 27.2). One of the two traditional strigid Tyto alba groups of piciforms, Pici, was placed near the base of the oscine neoavian tree adjacent to the tumicids, whereas the other, Pitta Sleatornis canpensis the jacamars and puffbirds (Galbulae), was placed as the sis- Nyctibius ter group to a monophyletic "Coraciae," including traditional Podiceps Phoenicopterus coraciilomis and irogons. The passeriforms were placed as Spheniscus humboldti the sister group to the entire waterbiid assemblage but were Gavia Pu/fin us not found to have any dose relationship with either piciform Columbia or coraciiform taxa. pteroclid Colius At present, none of these relationships can be confirmed Grus canadensis or refuted. Available nuclear sequence data for RAG-l (Groth ratlid Eurypyga h&lias and Barrowclough 1999) as well as the c-myc and fíAC-2 data Ciconia (figs. 27.4, 27.7) cannot resolve the base of Neoaves, indi- Opisthocomus hoazin threskiornithid cating that the placement of these (or other) groups within psittacine neornithines remains an open question. Recent morphologi- cacatuine Turnix cal and molecular studies, however, are identifying some well- Stiltia isabella supported clades within these groups. The two major clades Burhinus ardeid of the picifoiTns, Pici and Galbulae, are each strongly mono- Phalacrocorax phyletic in all studies (see figs. 27.4,27.7A,B, 27.8; Johansson Sula Phaethon ruiyricauda et al. 2001), and evidence increasingly indicates that they are Balaeniceps rex sister taxa. Some data, including RAC-2 (fig. 27.7A) and frag- Petecar)us ments of c-myc and RAC-J (Johansson et al. 2001 ), cannot picid indicator resolve this issue, but a monophyletic Piciformes is supported Lybius by moq^hology (Cracraft and Simpson 1981, Swierczewski ramphastid Buceo and Raikow 1981, Raikow and Cracraft 1983, Mayr et at. H Gálbula musophagid cuculitorm Chloroceryle Momotus coracild Figure 27.8. Ph y logent tic hypothesis from combined c-niyc Trogon and RAG-2 data for 69 taxa, analyzed by unweighted parsi- Micrastur gilvicollis mony. Branches with bootstrap support greater than 50% are Sagittarius serp&ntarius Buteo shown. Thick branches have greater than 70% bootstiap Fregata magnificerts suppon. To maximize the lyxon overlap between data sets, Amazilia equivalent species were combined, and this is reflected in the phaethornithine ChaetLira name given to the terminal node; for example, Gallus gallus was Aegotheles sequeneed for boih genes, but iwn different species were Galtus gallus scquenced from Afgothelcs, and species were seciueneed from megapodid Anseranas semipalrnata two different genera of megapodes. Data fromj. Harshman, M. Anas platyrtiynchos J, Braun, andj. Cracraft (uiipubl. ohs). ^titO The Relationships of Animals: Deuterostomes
2003), longer c-myc sequences (fig. 27.4), RAG-2 + morphol- seriforms has long been accepted and is strongly supponed ogy (fig, 27.7B), combined c-myc/RAG-2 data (fig. 27.8), and bya variety of studies, including those using morphological by other nuclear sequences Qohansson and Ericson 2003). or molecular data (Feduccia 1974, 1975, Raikow 1982,1987; Within Pici, it is now clear that the barbets are paraphyletic see also figs, 27,4,27.5,27.7,27.8). Our current understand- and that some or all of the New World taxa are more closely ing of their basal relationships and biogeographic distribu- related to toucans (Burton 1984, Sibley and Ahlquist 1990, iion,s strongly suggests that the group is old, with an origin Lanyon and Hall 1994, Prum 1988, Barkerand Unyon 2000, probably more than 79 million years ago, well before the Moyle 2004) than to other barbets; interrelationships within Cretaceous-Tertiary extinction 65 million years ago (e.g., the barbet and toucan clade still need additional work. Paton et al, 2002) and on a late-stage Gondwana (Cracraft DNA hybridization data were interpreted as supporting a 2001, Barker et al. 2002, Ericson et al, 2002), Recent mo- monophyleiic coraciiforms (Sibley and Ahlquist 1990). Al- lecular work using nuclear genes (Barker et al. 2002,Encson though recent DNA sequences arc insufficient to test coraci- et al. 2002) supports the hypothesis that the New Zealand ifonn monophyly, they do show support for groups of families wrens (Acanihisittidae) are the sister group to the remain- traditionally placed within coraciiforms. There is now congru- der of the passerines, and that the latter clade can be di\ided ent suppon, for example, for the monophyly of (1) hombills into TWO sister lineages, the suboscines (Tyranni) and the + hoop(>es/woodhoopoes(rig.';. 27.4,27.7A,B, 27.8; Johansson oscines (Passeii). Resolving relationships within the subo- et al 2001), (2) moimot5+ todies Qohansson et al. 2001), and scines and oscines has been complex, not only because of (3) kingfishers + motmots (figs. 27.4A, 27,7B, 2 7.8; Johansson the huge diversity (about 1200 and 4600 species, respec- et al. 2001), and support for (4) the kinghsher/motmot ciade tively) but also because many of the traditional families are with the rollers (figs. 27.4,27,7B, 27.8; Johansson et al. 2001 ). neither monophyleiic nor related as depicted in Sibley and Although they are clearly monophyleiic (Hughes and Ahlquist's (1990) tree. Nucleargene sequences, however, are Baker 1999), the relationships of the cuckoos are very un- beginning to clarify phylogenetic patterns within this large certain, with no clear pattern across different studies. The group. The results presented here summarize some ongoing distinctive Hoatzin {Opiaihommim hoazin) has been variously studies of the passerines, primarily using two nuclear genes placed with galliforms (Cracraft 198Î), cuculiforms (Sibley (RAG-1 and MG-2; F. K. Barker, J, F, Feinstein, P. Schiklfer, and Ahlquist 1990, Mindellei al. 1997), or turacos (Hughes A, Cibois, and j. Cracraft, unpubl, obs.) with dense taxon and Baker 1999), yet there is no firm suppon in the c-myc sampling, and represent the most comprehensive analysis of (fig. 27.4), mitochondrial and PEPCK data (hg. 27,5), or in passeriform relationships to date (4126 aligned positions for those from RAG-2 and morphology (fig. 27,7B; see also 146 laxa). Livezey and Zusi 2001) for any of these hypotheses. A rela- The DNA hybridization data were interpreted by Sibley tionship to galliforms at least can be rejected: hoatzins are and Ahlquist (1990) as showing a division between suboscine clearly members of Neoaves, not Galloanserae (figs, 27.4, and oscine passerines with the New Zealand wrens being the 27,5, 27,7A,B, 27,8; see also Sorenson et al. 2003). sister group to the remaining suboscines. Within the oscines, Trogons and mousebirds are each so unique morphologi- there were two sister clades. Córvida, which consisted of all cally that they have been placed in their own order, bul both Australian endemics and groups related to crows (the so- have been allied to coraciiform and/or picifoma birds by many called "corvine assemblage"), and Passerida for all remain- authors (lor reviews, see Sibley and Ahlquist 1990, Espinosa ing taxa. The phylogenetic hypothesis shown in figure 27.9A, de los Monteros 2000), In recent years trogons have generally which is based on nuclear gene data (F, K, Barker, J, F, been associated with various coraciiforms on the sti'ength of Fcinsiein, P. Schikler, A. Cibois, and J, Cracraft, unpubl. stapes morphology (Feduccia 1975), myology (Maurer and obs.), depicts a substantially different view of passeriform Raikow 1981), and osteology (Ijvezey and Zusi 2001), Mouse- history. Thus, although the subdivision into suboscines and bird relationships have l^een more difficult to ascertain, and no oscines is corroborated, the New Zealand wrens are the sis- clear picture has emerged. In the mitochondrial-PEPCK data ter group of all other passerines. In addition, numerous taxa mousebirds group with parrots (fig, 27,5), whereas the RAG-2 of the Australian "co^v^dans" are complexly paraphyletic rela- gene is uninlormative. The study of Espinosa de los Monteros tive to the passeridans and a core "Corvoidea," (2000) linked mouselîirds with trogons and then that clade with The suboscine taxon sample is small, but these nuclear parrots. The problem is that all these groups are old, divergent data are able to resolve a number of the major clades with taxa with relatively little intrataxon diversity. Much more data strong support (fig, 27,9B), New World and Old World will be needed to resolve their relationships, clades are sister groups (Irestedl et al, 2001, Barker et al, 2002). Within the Old World group, the data strongly sup- Phylogenetic Relationships within port ilic pillas as being the sister group of the paraphyletic the Perching Birds (Passeriformes) broadbills and the Malagasy asilies (see also Prum 1993), The New Worid suboscines are divisible into two large clades. The The perching birds, order Passeriformes, comprise almost first includes nearly 550 species of New World flycatchers, 60% of the extant species of birds. The monophyly of pas- manakins, and coiingas; although this clade is strongly sup- New Zealand wrens New Zealand wrens
New World suboscines oscines
broadbills, aslties Old World subosclnes pittas 0. W. suboscines lyrebirds, scrub-birds pipromorphlne flycatchers Australian treecreepers cotingas oscines bowerbirds I tltyrine flycatchers fairy wrens manakins tyrant flycatchers honey eaters wood creepers í parda I otes, scrubwrens L í oven birds Australian babblers formicarlineantbirds
logrunners tapaculos Australia thamnophiline antbirds crows and allies (Córvida)
B N. W. suboscines t finches and allies (Passerida)
Australian robins passeridan songbirds bald crows, Chaetops ta mud-nest builders dippers 0) melampittas thrushes •D birds of paradise 0) O. W. flycatchers "5 Q. monarch flycatchers mockingbirds, thrashers u(B o starlings crows, jays '3 ot waxwings w shrikes o kinglets rhipldurine flycatchers drongos nutnatches n tree-creepers Ö wattle-eyes, batises wrens loras •D sugarbird and allies 0) helmet&hrikes O fairy bluebirds Ü vanga shrikes c flowerpeckers bush shrikes uo sunbirds currawongs, butcherbirds m w weavers, widowbirds wood-swallows accentors O. W. orioles cardinals tanagers whistlers, shrike-thrushes buntings, sparrows cuckooshrikes orioles, blackbirds tit berrypecker N. W. warblers shrike-tits chaffinches, bramblings erpornis wagtails, pipits víreos titmice, chickadees pitohuls larks n crested be 11 bird swallows •a •whipblrds cisticoltd warblers Ö Lslttellas bulbuls '_> ^ berry peckers, longbllls sylviid warblers • New Zealand wattlebirds whtte-eyes Lcnemophillnes babblers
Figure 27.9. Phylogenetic analyses from an analysis of 146 passeriform laxa for 4126 base pairs of RAG-1 and RAG-2 exons using maximum parsimony. (A) Relationships among the basal lineages. (B) Re latí uns hips among the suboscine passerilorms. (C) RL4;ilii.inships among the passeridan songbirds. (D) Relationships among the basal oscines and curvidan songbirds. Data from F. K, Barker, J. F. Feinstem, i\ Schikler, A. Cibois, and J. Craeraft (unpubl, ohs ). 482 The Relationships ai Animals: Deuterostomes ported, relationships within the group are still uncertain (see 2000. Lovette and Bermingham 2002, Yuri and Mindell 2002). also Johansson ei al, 2002), The remaining 560 species of The last group of core passeridans is Muscicapoidea, which New World suboscines are split into the thamnophiline ant- encompasses the kinglets, wax wings, starlings, thrashers and birds and their sister clade, the formicarinine antbirds and mockingbirds, and the large thrush and Old Worid flycatcher the ovenbirds and woodcreepers. The most thorough study clade of .some 450 species. of New World suboscine relationships to date is thai of With the elimination of the early "corvidan" clades dis- Irestedt et al. (2002), which examined more than 3000 base cussed above (fig. 27.9A), the remainder of Sibley and pairs of nuclear and mitochondrial sequences for 32 ingroup Ahlquist's "Córvida" do appear to form a monophyletic as- taxa of woodcreepers, ovenbirds, and antbirds; our results semblage, although it is not well supported at this lime, and are congruent with those reported in their study. we restrict the name "Córvida" to this clade (fig. 27.9D). As noied, the oacines, or songbirds, have been subdivided Although relationship,!; among family-level taxa within this into two large assemblages, the Córvida and Passerida, based complex cannot be completely resolved with RAG-J and on inferences from DNA hybridization. This simple partition RAG-2 sequences, these data do identify several well-defined has been shown to be incorrect (Barker ct al. 2002, Ericson clades, and they partition relationships more satisfactorily ei al. 2002), but we are now able to tell a much more inter- than previous work. esting story because oía larger taxon sample. No fewer than Two of the corvidan clades are well supported. The first five distinctive Australian "corvidan" clades arc sequential we term here Corvoidea, which include the crows and jays sister groups to the core corvoid and passeridan clades (Corvidae) and their sister group, the true shrikes (Lîniidae), (Barker et al. 2002; see also F. K. Barker, J. F. Feinstein, the monarch and rhipidnrine flycatchers, drongos, mud-nest P. Schikler, A. Cibois, and J. Cracraft, unpubl, obs,): the lyre- builders (Struihidea. Corcorax), the two speciesof Mf («mpiiw, birds (Menuridae), the bowerbirds and Australian treecreepers and the birds of paradise (Paradisaeidae), The second wcll- (Ptilonorhynchoidea), the diverse meliphagoid assemblage, the supponed lineage of the corvidans we term Malaconotoidea. pomotostomine babblers, and the onhonychid logninners This "shrike-like" assemblage is comprised of the African bush- (fig. 27.9A). This phylogeneiic paiiem firmly anchors the ori- shrikes (Malaconotidae). the helmet shrikes (Prianops), Balis, gin of the oscines in East Gondwana. the Asian ioras (Aegithinidae), and the vanga shrikes (Vangi- But the story of corvidan paraphyly is not yet exhausted. dae) of Madagascar. Also included in this clade are the wood- The passeridan clade has three basal clades (fig. 27.90, one swallows (Artamidae) and their sister group the Australian of which is the Australian robins (Eopsaltridae), included by magpies and currawongs (Cracticidae). DNA hybridization data within the corvidans. A second clade All other corvidans appear to be basal to the corvoids and is the peculiar African genus Picathanes, the bald crows or malaconotoids but are, on present evidence, unresolved rela- rock-fowl, also placed toward the base of the passerines by tive to these two clades. Most of these groups, including the hybridization data (see Sibley and Ahlquist 1990: 625-626), pachycephalids, orioiids, campephagids, daphoenosittids, and its sister taxon, the rock-jumpers (Chaetopi). Finally, falcunculids, and other assorted genera are mostly Australasian there are the core passeridans (Ericson etal. 2000, Barker in distribution, and presumably in origin. Also included in this et al. 2002; see also F. K. Barker, J. F. Feinstein. P. Schikler, melange are the víreos and their Asian sister group, Erpomis A. Cibois, and J, Cracraft, unpubl. obs.). It is not clear from zanthokuca. the available data whether the Picaífiíirtes + Chaetopa clade Outside of all these corvidan groups is a clade compris- or the eopsaltrids is the sister group of the core passeridans, ing some ancient corvidans that appear to be related; the New although present data suggest the robins are more closely Zealand wattlebirds (Callaeaiidae), the cnemophilines (for- related. mally placed in the birds of paradise), and the berrypeckers The basal relationships of the core passeridans are still (Melanocharitidae). The basal position of these groups rela- unclear. There are four moderately well-dehned clades within tive to the remaining Córvida provides persuasive evidence the group (fig. 27.9C; see also Ericson and Johansson 2003). that the group as a whole had its origin in Australia (and The first, Sylvioidea. includes groups such as the titmice and perhaps adjacent Antarctica), further lying the origins of the chickadees, larks, bulbuls. Old World warblers, white-eyes, oscine radiation to this landmass. babblers, and swallows. The second, here termed Cenhioidea, consists of the wrens, nuthatches, and treecreepers. The third is a very large group, Passeroidea, that includes various Old Discussion World laxa basally•the fairy bluebirds, sunbirds, flower- peckers, sparrows, wagtails, and pipits•and the huge (almost Where We Are 1000 species) so-called nine-primaried oscine assemblage (Fringillidae of Monroe and Sibley 1993), most of which are To judge from the large numbers of papers reviewed above, New World (Emberizinae: buntings, wood warblers, tana- research on the higher level relationships of birds has made gers, cardinals, and the orioles and blackbirds; for recent significant progress over the last decade, yet it is obvious from discussions of relationships, see Groth 1998, Klicka et al. the results of these studies that compelling evidence for re- Phylogenetic Relationships among Modem Birds (Neornitlies) 483 la lions Kips among mosi major clades of Neoaves is still lack- ing. Nevertheless, a function of this chapter is to serve as a riidae) benchmark of our current understanding ol avian relation- QSl.._ ...,^ ,_.,_..,.._ 'dae) rpeas (Rbfeidae) ships, and one way expressing this progress is to propose a ducks., geese, sWai MagpieT3oose,(An: eranatidae) summary hypothesis that attempts to reflect the improve- screamers (Aohimn meoabodes Megao ments in our knowledge of avian relationships, even though guans; ciirrasowsT( the underlying evidence may be imperfect. Different inves- 3a'¿f^' tigators, including the authors of this chapter, will disagree guineaTQwr{hJurTjmrdiaaej EirrtpKinWrar-''' about what constitutes sufficient evidence for supporting the cranes (GruiL , . frumpeters rPsûphiic monophyly of a clade, and most would no doubt prefer to sun-g•5eg XHelfornr see a tree that is biised on all avian higher laxa and a very Jae) large data set of molecular and morphological characters Terrias ' busfaros i tidjaae,^.,, numbering in the tens of thousands. That ideal is 5-10 years mesites. I esitornifnid ae) :eskiorntfhia away, however, yei ii is still useful to examine how far have alaenicipiti! we come over the last decade. pelicanskim el IC icrae Ramme; ead tiopi''dae) Fig;ure 27 10 depicts a summary phylogenetic hypoth- herons,! rdeii storKS iconii esis for the avian higher taxa. It represents an estimate of avian iODie anr;ie1 anninc history at this point in time and is admittedly spéculative in a number of places that we note below; it represents, more- over, a compromise among the auihors. We therefore have no illusions that all of these relationships will stand the test thick-kneesiBurhinidae) of time and evidence, but a number will. The thick lines are sinealnb|ir{Çtiionididae) raíl neo le AJareolidaareoiïdaé) meant to identify clades in which relatively strong evidence 8u îs, Ve rn slEàcidae) for their monophyly has been discovered in one or more utton-quails (Tyrnipidae) lacanas^rj^caniaaeí individual studies. The thin lines depict clades that have been painted-snipe (Rostratulidae), , plairiS'Wanaerèr (Pedtongmiaae) recovered in various studies, even though the evidence for seedsnipe rroinocoridaeï. these individual hypotheses may be weak. Congruence across Sanapipers iScoiopaciaaeJ flamingos (Phçieniçoptçncfae) studies suggests that with more data, many of these clades grebes (Podici edidáe). nawks, gaqles idae) will gain increased support. ósprey (Párioioi secretary-bird jagitiahidae) As already noted, the base of the neomithine tree is no N.W. vuftures (.Çafnarlidae) longer particularly controversial, with palaeognathsand then falcons TFalconiaaeí Galloanserae being successive sister groups to Neoaves. Re- lationships wat hin rat i tes arc unsettled, however, because of oons füayiidäe). ._, , conflict among the molecular data and with the morphologi- ^ßliSi-jJosJSpnehiscidae) nucnmingBirps (Trochilidae cal evidence. swi owl.(lef _ . - n. lati'iârs. .fAegothel idae) Neoavian relationships, on the other hand, are decid- DOtoos edly uncertain, although new information becomes avail- Caprimijfgidae) wm eafermthraael' able with each new study. The base of the neoavian tree is roqmou ïlPogaraigaè) iracas osopriadldaej , a complete unknown, but within Neoaves evidence for re- oatzm pistnocpmi^dae epns lationships among a number of major groups is emerging. Jgro. There is a suggestion thai many of the traditional "water- Olí , ^,.bir•• o lia bird" groups are related, although a monophylelic assem- lalbulidae) blage that includes all "waterbird" taxa itself is unlikely. (Rarñphastidae) Thus, some "waierbird" taxa are definitely related, others loneyquidos (Indicatoridae) wooctpècSersYPicipae) probably so, but other nonwaterbird taxa will almost cer- mousebirds (Conipae) tainly be found to be embedded within waierbirds. It now fegggSes^^P-^ûn« seems clear that some traditional groups such as Pelc- wo culidae) hornbiils caniformes and Ciconiiformes arc not monophyletic, but bee-ea qlmol many of their constituent taxa are related. Thus there is now fPsI dinidae) . , , evidence for a shoebill + pelican + hammerkop clade and CLtdkoor epíosorfiatidae) rolfers • for an anhinga + cormorant + gannet + (more marginally) around I-rol le, rachypteraciidae) Irigaiebird clade, and these two clades are probably related id Vforid áubpsc ines ew WorTcfsuboscines to each other, along wit h ibises, herons, and storks. Tropic- ew Zeafana wrens (Acanthisittidae) birds Cphacthoniids) are a real puzzle as this old, long- Figure 27.10, Summury hypothesis for avian higher level branch taxon is quite unstable on all trees. relationships (see discussion in text). 484 The Relationships of Animals: Deute rosto m es
There is a core group oí gruiform taxa with well sup- and suggests we know very little about avian relationships. ported reliUionships, induding rails + sungrebes, on the one Viewed more optimistically, however, the tree is a working hand, and cranes + limpkins + trumpeitrs, on ihe other. hypothesis that suggests progress is being made. Critically, Moreover, the kagu and sunbittem are strongly supported this representation oí our state of knowledge contradicts the sister taxa. Aside from some morphological character data false notion that the broad picture of avian phylogcnetics has (e.g., Livezey Í998), there is little current evidence to sup- been drawn, and only the details remain to be filled (e,g,, port monophyly of traditional Gruiformes. This is an old Mooers and Cotgreave 1994), Given the state of cUKcnt ac- group, with basal divergences almost certainly in the Creta- tivity in many laboratories around the world, we predict that ceous (Cracraft 2001) that cannot be resolved given the char- in little more than hve years a similar figure, whatever its acter data currently available; yet, there is no firm evidence configuration, will have a substantially larger proportion of that any of these groups is related to a nongruiform taxon, well-supported clades. so we retain the traditional order. Ongoing work in various labs is confirming the mono- The Future phyly of the charadriiforms, including the buttonquails, of- ten placed in gruiforms. Current sequence data tl^aton et al. These are exciting and productive times for avian system- 2003) indicate the relationships shown in figure 27,10. There atists. We are witnessing the growth of molecular databases, is also a suggestion in the molecular data presented earlier containing sequences from homologous genes across most that charadriilorms are associated with flamingos + grebes, avian taxa. As recently as 10 years ago the availability of such and possibly with some or all of the falconiforms. The latter comprehensive, comparative, discrete character data sets was group consists of three well defined clades (falcons, little more than a dream. Within the next several years large cathartids, and accipitrids + osprey + secretary bird), but data sets for both molecular and morphological data will be whether these are related to each other is still uncertain. published that span all the major clades of nonpasseriform Morphology indicates that they are, but molecular data can- birds. At the same time, avian systematics is becoming in- not yet confirm or deny this creasingly collaborative with groups of researchers pooling Relationships among the "higher land birds" remain coti- resources and publishing together. These collaborations in- troversial in many cases. Swifts, hummingbirds, and owlet- volve both molecular and morphological data and extend nightjars are monophyletic but their relationships to other back across time through the incorporation of fossils. taxa traditionally called caprimulgiforms are unsupported; Ali of these data will soon be publicly available on the aswithgruifonns. we have no clear evidence that any of them Internet as a result of these collaborations, and these data are more closely related to other taxa, and so we retain the should greatly accelerate avian systeinatic research. Discrete- group. Whether owls cluster with these families is also un- character data sets lend themselves to continual growth and certain. Again, all of these taxa are veiy old groups and reso- addition in a manner entirely absent from the early compre- lution of their relationships will require more data. hensive work based on DNA hybridization distances (Sibley The three "orders" Picifonnes, Coraciifomnes, and Pas- and Ahlquist 1990). These data sets will variously confirm, seriformes may or may not be related to one another, but in challenge, or ovenum earlier hypotheses of a\'ian phylogeny, many studies subgroups of them are clustered together. More and this may be expected to continue as both character and and more data sets are showing a monophyletic piciforms. laxon sampling increase. We view the continued collection Passeriforms are strongly monophyletic, and relationships of comparative data as imperative notjusi for avian system- among their basal clades are becoming well understood (see atics, but for elaborating the insight into evolutionary his- discussion above). Finally, the traditional coraciiforms group tory and processes at multiple hierarchical levels that only into two clades whose relationships to each other are nei- phylogeny can provide. ther supported nor refuted by our data, The relationships of mousebirds and trogons are also still obscure. The Challenge In contrast to many of the above groups, there are some highly distinctive taxa such as turacos, parrots, pigeons, the Just how difficult will it be to build a comprehensive avian hoatzin, and cuckoos that have been notoriously difficult to Tree of Life (ATOL)? Several observations suggest it will be associate with other groups using both molecular and mor- extremely so. First, there are about 20.000 nodes on the phological data. Deciphering their relationships will require extant avian Tree of Life. Fossil taxa only add to that num- larger amounts of data than are currently available. ber. Then, there is the challenge presented by the history of Despite the appearance of substantial structure, the hy- birds itself It is now evident that there have been many epi- pothesis of figure 27,10 could be interpreted pessimistically sodes of rapid radiation across the neoavian tree, perhaps by examination of those clades subtended by thin branches• involving thousands of nodes, and resolving these will re- indicating insufficient support•versus those with thick- quire unprecedented access to specimen material (including branched clades we judge to be either moderately or strongly anatomical preparations and fresh tissues) as well as large supported. Seen in this way, the tree is mostly a polytomy character sampling to establish relationships. Gone are the Phylogenetic Relationships among Modern Birds (Neomithes) 485 days when a single person or laboratory might hope to solve the studies discussed here illustrates this point. Evidence now the problem of avian relationships. The problem is too diffi- indicates owlet-nightjars are ihe sister group of swifts and cult and complex for single laboratories in which time and hummingbirds. Depending on the sister group of this clade, money are hmited. The scientific challenge presented by the it implies either that adaptation to nocturnal lifestyle arose avian Tree of Life will call for large taxon and character sam- multiple times in aegothelids and other birds, or that noc- pling, goals best achieved by a communitywide effort. turnal habits are primitive and swifts and hummingbirds are There are also conceptual roadblocks. One is the prob- secondarily diurnal. Phylogeny thus provides important in- lem of uncertain knowledge, More taxa and characters may sight into understanding avian diversification. not guarantee a "satisfying" answer, by which we mean hav- Finally, our perspectives on avian evolution will not be• ing resolution of nodes with sufficiently strong branch sup- shovild noi be•built on one kind of data. Tree topologies pon that additional data will merely confirm what has already should reflect the most comprehensive description of char- been found. Ihn issue is that more taxa guarantee (some) acter evolution over time, which means that all forms of char- uncertainty. More taxa are good, of course, but they also acter information•genetic, morphological, behavioral, and means more character data will likely be required to attain so forth•should be incorporated into analyses. They may strong support for any particular node. Measuring phyloge- not only contribute to phylogenetic resolution in their ovm netic understanding on very large trees such as the avian Tree right, but will give us a richer picture of the history of avian of Life will also be a complex challenge. Measures of support evolution. are ambiguous in their own right, and whatever answer we get depends on the taxon and character sampling•that is, on the available data. Thus, what are the boundaries of a Acknowledgments study? How will we know when to stop (because it has been F.K.B., G.j.D.. S.S., PB., and A.C. all received su ppon from the determined we "know" relationships) and move on to an AMNH F M, Clmpman Fimd, Much of the research presented unresolved part of the tree? This isa nonirivial problem, but in this chapter is supported by the AMNII Monell Molecular as we erect a scaffold that identifies strongly supported mono- Laboratory and Lewis B, and Dorothy Cullman Program Tor phyletic groups, perhaps that will make it easier to circum- Molecular Sysiemaiics Studies, Work on the c-myc gene scribe studies and resolve the tree more finely. was aided by the able assistance of Chris Huddleston and Another conceptual roadblock is the problem of investi- a Smithsonian postdoctoral lellowship toJ.IL M.S. acknowl- gator tenacity. It should be straightforward to build the scaf- edges the help of Elen Oneal and support from the National fold of the a\nan Tree of Life, Sysieraatists are doing that now. Science Foundation. Work by J,G.-M., D.P.M., M.D.S., and There will be•and already are•lots of trees that are mod- T.Y. was supported by NSF grants DKB-9762^27 and DBI- erately resolved but still have little satisfactory branch sup- W74523. port {remember that the DNA hybridization tree was nearly "fully" resolved). So how much do we, the investigators, re- Literature Cited ally warn to know relationships? If the object is to publish more papers, then as more and more taxa are added, and if Ansari, H. A., N. Takaj;i. and M. .Sasaki. 1988. Morphological character sampling does not also increase, more and more diftcrentiation ol sex eh rom oso m es in three species of ratile nodes are likely to be supported rather poorly, especially birds. Cyiogenet. Cell Genet. 47:185-188. across those parts of the tree representing rapid radiations Avise, J. C. W, S, Nelson, and C. G. Sibley, 1994, DNA- (short in te modes). Resolving these nodes with some mea- sequencc suppon for a close phylogenetic relationship between some storks and New-World vultures, Proc. Nad. sure of confidence will require substantial amounts of data Acad, Sei, USA 91:5173-5177. (much more than is currently collecied in typical studies). Barker, F, K., G. F. Barrowclough, andj, G, Groth. 2002, A In the near future, this may not be an issue as technical in- phylogenetic hypothesis for passerine birds: taxonomic and novations allow systematisis to gather more data more rap- biogeographic implications of an analysis of nuclear DNA idly. However, many investigators will not necessarily have seqtience data, Proc, R, Soc. Lond, B 269:295-308. easy access to these technologies, and ü is already becoming Barker, F, K., and S. M, Lanyon, 2000. The impact ol parsimony apparent that being able to collect large volumes of data (ge- weighting schemes on inferred relationships among toucans nomes) does not necessarily mean that the data themselves and neotropical barbets (Aves: Piciformes), Mol. Phylogenet. are going to be phylogenetically useful for the problem at Evol. 15:215-234, hand. Blciwciss, R• J. A. W. Kirsch, and F -J. bipointe. 1994 DNA- Although many phylogenetic problems in birds, at all DNA hybridization-based phylogeny lor "higher" nonpas- serines: reevaluating a key portion of the avian family tree. taxonomic levels, will be quite difficult to resolve, we must Mol. Phylogenet Evol, 3:240-255. be resolute. Resolving relationships is crucial for answering Braun, M.J., and C,J, Huddleston, 2001, Molecular phylo- numerous questions in evolutionary biolog}', and to the ex- gencticsof caprimulgiform nighthirds. P. 51 in Abstracts of tent that these questions are worth pursuing we should not the 1 lyth Stated Meeting, American OmithoIogisls' Union, settle for not knoviñng phylogeny, One result emerging from Seattle, WA, 16-19 August 2001. 486 The Relationships of Animals; Deuterostomes
Braun. E, L, and R. T. Kimball. 2002, Examining basal avian Dimcheff. D. E., S, V, Drovetski, M. Krishnan. and D. P. divergences witîi miiochondrial sequences: model complex- Mindell. 2ÛÛÛ. Cospeciation and horizontal transmission of iiy, laxon sampling, and sequence lengih. Syst. Biol. avian sarcoma and leukosis virus gag genes in galliform 51:6H-625. birds. J. Virol, 74:3984-3995. Bunon, P. J. K. 1984. Anatomy and evolution of the feeding Dimcheff, D. E., S. V. Drovetski, and D. P. Mindell. 2002. apparatus in the avian orders Coraciiformcs and Piciformcs. Molecular evolution and systematics of teiraoninae and Bull Br. Mus Nal Hisi. Zool. 47C6):331-443. other Galliformes using miiochondrial 12S and ND2 genes. Chiappe, L. M 1995. The first 85 million years of avian Mol, Phybgenet. Evol. 24:203-215. evolmion. Nature 378:349-355. Donne-Goussé, C, V. Laudet, and C. Hanni. 2002. A molecular Chiappe, L. M. 2001. Phylogeneiic relationships among basal phylogeny of Anseriformes based on mitochondrial DNA birds. Pp. 125-139 in New perspectives on the origin and analysis. Mol. Phylogenei. Evol, 23:339-356. early evolution of birds (J. Gauthier and L F, Gall, eds.). Dyke, G. J. 2001. The evolution of birds in the early Tertiary: Peabody Museum of Natural History, Yale University. New systematics and patterns of diversification. Geol. Jour. Haven, CT. , 36:305-315. Chiappe, L. M., and G. J. Dyke. 2002. The Mesozoic radiation Dyke, G. J,, B. E. Gulas, and T. M. Crowe. 2003, The supra- of birds. Annu. Rev Ecol. Sysl. 33:91-124. generic relationships of galliform birds (Aves, Galliformes), Chiappe, L. M., J. Shu'an, J. Qiang, and M. A. Norell. 1999. a cladistic analysis of morphological characters. Zool J. Anatomy and systematics of the Confuciusorniihidae Linn. Soc. 137:227-244. (Theropoda: Aves) from the late Mesoioic of northeastern Edwards, S. V., B. Fértil, A. Giron, and P. J. Deschavannc. 2002, China. Bull. Am. Mus. Naí. Hist. 242:1-89, A genomic schism in birds revealed by phylogenetic analysis Chubb, A L 20Ú4. New nuclear evidence for the oldest of DNA strings. Syst. Biol, 51:599-613. divergence aong neognath birds: the phylogenetic utility of Ericson, P. G. P. 1996. The skeletal evidence for a sister-group ZENK ([), Mol. Phylogen, Evol, 30:140-151, relationship of anseriform and galliform birds•a critical Cooper, A., C. Lalueza-Fox, S. Anderson. A. Rambaut, J. Austin, evaluation. J. Avian Biol. 27:195-202. and R. Ward, 2001. Complete mitochondrial genome Ericson, P. G. P. 1997, Systematic relationships of the Palaeo- sequences of two extinct moas clarify raiite evolution, gene family Presbyomithidae (Aves: Anserilormes). Zool, J. Nature 409:704-707. Linn. Soc, 121:429-483. Cooper, A,, and D. Penny. 1997. Mass survival of birds across Ericson, P. G. P., L. Chrisiidis, A. Cooper, M, Irestedt, J, the Cretaceous-Tertiary boundary: molecular evidence. Jackson, U. S.Johansson, andj. A. Norman. 2002. A Science 275:1109-11)3. Gondwanan origin of passerine birds supported by DNA Cottam, P. A. 1957. The pclecaniform characters of the skeleton sequences of the endemic New Zealand wrens. Proc. R, Soc, of the shoebill stork Baiaeniceps rex. Bull. Br. Mus. Nat. Hist. Lond. B 269:235-241. 5:51-72. Ericson, P. G. P., and U. S Johansson. 2003. Phylogeny of Cracrafi.J. 1972. The relationships of the higher taxa of birds: Passerida (Aves: Passeriformes) based on nuclear and problems in phylogenetic reasoning. Condor 74:379-392. mitochondrial sequence data. Mol, Phylog. Evol, 29:126- Cracraft, J. 1974. Phylogeny and evolution of the ratite birds. 138, Ibis 116:494-521. Ericson, P. G. P., U. S. Johansson, and T, J. Parsons. 2000. Cracraft, J. 1977. John Ostroms studies on Archcmoptciyx, the Major divisions in oscines revealed by insertions in the origin of birds, and the evolution of avian flight, Wilson nuclear gene c-m^c: a novel gene in avian phylogeneiics. Bull. 89:488-492. Auk 117:1069-1078. Cracraft, J. 1981. Toward a phylogenetic classificaiion of the Ericson, P. G. P., T.J. Parsons, U. S.Johansson. 2001. Morpho- Recent birds of the world (Class Aves), Auk 98:681-714. logical and molecular support for nonmonophyly of the Cracraft, J. 1986 The origin and early diversification of birds, Galloanserae. Pp. 157-168 in New perspectives on the Paleobiology 12:383-399. origin and early evolution of birds (J. Gaiuhier and L. F. Cracraft, J. 1987. DNA hybridiiation and avian phylogeneiics. Gall, eds.). Peabody Museum of Natural History, Yale Evol, Biol. 21:47-96. University, New Haven, CT. Cracraft, J, 1988. The major dades of birds. Pp. 339-361 in The Espinosa de los Monteros, A. 2000. Higher-level phylogeny of phylogeny and clas.'iification of ihe tetrapods. Vol. 1: Trogoniformes. Mol. Phylogenei. Evol. 14:20-34. Amphibians, reptiles, birds (M. J. Benton, ed.). Clarendon Feduccia, A. 1974. Morphology of the bony stapes in New and Press, Oxford, Old Worid suboscines: new evidence for common ancestry. Cracraft. J. 2001. Avian evolution, Gondwana biogeography and Auk 91:427-429. the Cretaceous-Tertiary mass extinction event, Proc. R. Soc. Feduccia, A, 1975. Morphology of the bony stapes (columella) in Lond. B 268:459-469. the Passeriformes and related groups: evolutionary implica- Cracrafi.J., and J. Clarke. 2001. The basal clades of modem tions. Univ. Kans. Mus. Nat, Hist, Misc. Publ. 63:1-34. birds. Pp. 143-156 in New perspectives on the origin and Feduccia, A, 1995. F.xplosive evolution in Tertiary birds and early evoltition of birds (J. Gauthier and L. F. Gall, eds.). mammals. Science 267:637-638. Peabody Museum of Natural History, Yale University, New Feduccia, A, 1999. The origin and evolution of birds. 2nd ed. Haven, CT. Yale University Press, New Haven, CT, Darwin, C. R. 1859. On ihc ori^n of species. John Murray, Feduccia, A. 2002. Birds are dinosaurs: simple answer to a London. complex problem. Auk 119:1187-1201. Phylogenetic Relationships among Modern Birds (Neornithes) 4S7
Feduccia, A. 2003. 'Big bang' for Tcniary birds? Trends Ecol. Hughes, J. M., and A. J, Baker, 1999. Phylogenetic relationships Evol, 18:172-176. of the enigmatic hoatzin (Opisthocomus hoazin) resolved Fùrbringer, M. 1888. Untersuchungen zur Morphologie und using mitochondrial and nuclear gene sequences. Mol. Biol. Systematik der Vögel. 2 vols, von Holkema. Anisterdani. Evol. 16:1300-1307. Garcia-Moreno, J,, and D. P. Mindcll. 2000. Using homologous Huxley, T, H, 1867. On the classification of birds; and on the genes on opposite sex chromosomes (gamctologs) in taxonomic value of the modiftcations of certain of the phylogenetic analysis: a case study with avian CHD. Mol. cranial bones observable in the class. Proc. Zoot. Soc. Lond. Biol. r-vol. 17:1826-1832. 1867:415-472. Gartia-Moreno, J., M. D. Sorcnson, and D. P. Mindell. 2003. Huxley, T. H. 1868. On the animals which are luost nearly Congruent avian phylogenies inferred From mitochondrial intermediate between birds and reptiles, Geol, Mag. 5:357- and nuclear DNA sequences. J. Mol, Evol. 57:27-37. 365. Garrod, A. H. 187*1. On certain muscles of birds and their value Irestedt, M•J. Fjeldsa, U. S.Johansson, and P. G. P. Ericson. in classification, Proc. Zool. Soc. Lond. 1874:3.39-348. 2002. Systematic relationships and biogeography of the Gauthier, J, A, 1986. Saurischian monophyly and the origin of tracheophone suboscines (Aves: Passe ri formes). Mol. birds. Pp. 1-55 in The origin of birds and the évolution of Phylogenet. Evol. 23:499-512. flight (K. Padian, ed,). Memoirs of the California Acadetny Irestedt, M.. U. S.Johansson, T.J. Parsons, and P. G. P. Ericson. of Sciences 8. San Francisco, CA. 2001. Phyiogeny of major lineages of suboscines (Pas- Groih, J. G. 1998. Molecular phylogenetics of finches and seriformes) analysed by nuclear DNA sequence data. sparrows: consequences of character state removal in J. Avian Biol. 32:15-25. cytocbrome b sequences. Mol. Phylogenei. Evol. 10:377-390. Johansson, U. S., and P. G. P. Ericson. 2003. Molecular support Groth, J. G,. and G. F. lïarrowclough. 1999. Basal divergences in for a sister group relaiiot^ship between Pici and Galbulae birds and the phylogenetic utility of the nuclear RAG-1 (Piciformes sensu Wetmore 1960). J. Avian Biol. 34:185- gene. Mol. Phylogenet. Evol. 12:115-123. 197. Hackett, S.J., C S, Griffiths,]. M. Bates, and N. K. Klein. 1995. Johansson, U. S., M. Irestedt, T. J. Parsons, and P. G. P. Ericson. A commentary on the use of sequence data for phylogeny 2002. Basal phyiogeny of the Tyrannoidea based on reconstruction. Mol. Phylogenet. Evol. 4:350-356. comparisons of cytoehroiue b and exons of nuclear c-myc Haddrath. O., and A. J. Baker. 2001. Complete mitochondrial and RAG-1 genes. Auk 119:984-995. DNA genome sequences of extinct birds; ratite phylo- Johansson, U. S.. T.J. Parsons, M. Irestedt. and P. G. P. Ericson. genetics and the vicariance biogeography hypothesis. Proc, 2001. Glades within the 'higher land birds', evaluated by R. Soc. lond. 268:939-^45. nuclear DNA sequences. J. Zool. Syst. Evol. Res. 39:37-51. Haeckel, E. 1866. Generelle Morphologie der Organismen: Johnson, K. P, 2001. Taxon sampling and the phylogenetic allgemeine Grundzüge der organischen Formen- positioti of Passeriformes: evidence from 916 avian Wissenschaf 1, mechanisch begründet durch die von Charles cytocbrome b sequences. Syst. Zool. 50:128-136. Darwin reformine Descendens-Theorie. G. Reimer, Berlin. Jolhc, M. 1976-1977. A contribution to the morphology and Härltd, A., and U Amason 1999. Analyses of mitochondrial phyiogeny of the Falconifomies. Evol, Theory 1:285-298, DNA nest ratite birds within the Neognathae: supporting a 2:115-300, 3:1-141, neotenous origin of ratite morphological characters. Proc. R. Klicka, J., K. P. Johnson, and S. M. Lanyon. 2000. New world Soc. Lond. 266:305-309. nine-prima ried oscine relationships: constructing a Harsh m an, J. 1994. Re weaving the Tapestry: what can we leam mitochondrial DNA framework. Auk 117:321-336. from Sibley and Ahlquisi (1990)? Auk 111:377-388. Kluge, A. G., and J. S. Farris. 1969, Quantitative phyletics and Hedges, S. B., Parker, P. H.. Sibley, C. G., and S. Kumar. 1996. the evolution of anurans. Sysl. Zool. 18:1-32, Continental breakup and the ordinal diversification of birds Kurochkin, E. N,. G. J. Dyke, and A, A, Karhu. 2002. A new and mammals. Nature 381:226-229. presbyorniihid bird (Aves, Anserifonues) from the Lite Hedges, S. B., and CG. Sibley. 1994. Molecules vs. morphol- Cretaceous of southern Mongolia. Am. Mus. Nov. 3386:1• ogy in avian evolution; the case of the "peleeaniform" birds. 17. Proc. Nati. Acad. Sei. USA 91:9861-9865. Unyon, S. M. 1992. Review of Sibley and Ahiquist 1990. Helbig, A. ].. and I. Seibold. 1996. Are storks and New World Condor 94:304-307. vultures paraphyletic? Mol. Phylogenet. Evol. 6:315-319. Lanyon, S. M., andj. G. Hall. 1994 Reexaiui nation of barbet Hennig, W. 1966. Phylogenetic sysiemaiics. University of monophyly using mitochondria I-DNA sequence data. Auk Illinois Press, Urbana. 111:389-397. Holtz, T. R.,Jr. 1994. The phylogenetic position of the Lee, K.,J. Feinstein, and J. Cracraft. 1997. Phylogenetic Coelurosauria (Dinosauria: Theropoda). J. Paleontol. relationships of the ratite birds: resolving conllicts between 68C5):1100-1117. molecular and morphological data sets. Pp. 173-211 in Holtz. T. R., Jr. 2001. Arciometatarsalia revisited: the problem of Avian molecular evolution and systematics (D. P. Mindell, homoplasy in reconstructing theropod phybgeny. Pp. 99- ed.). Academic Press, New York. 122 in New perspectives on the origin and early evolution of Ligon, J. D. 1967. Relationships of the caihariid vultures. Occ. birds (J- Gauthier and L F, Ciall, eds.), Peahody Museum of Pap. Mus. Zool. Univ. Mich. 651:1-26. Natura! History, Yale University, New Haven. CT. Livezey, B. C. 1986 A phylogenetic analysis of recent anseriform Houdc, P. 1987. Critical evaluation of DNA hybridization genera using morphological characters. Auk 103:737-754. Studies in avian systematics. Auk 31:17-32. Livezey, B. C. 1997a. A phylogenetic analysis of basal Anscri- 488 The Relationships of Animals: Deuterostomes
formes, the fossil Presbyomis, and the inierordinal relation- molecular evolution and systematics (D, P, Mindell, cd,). ships of waterfowl, Zoo). J. l.inii. Soc. 121:361-428. Academic Press, San Diego, Livezey, B, L, IWTb. A phylogeiietic classification ol waierfüwl Monroe, B, L,and C, G, Sibiey. 1993, A world checklist of (Aves: A n se ri form es), including selected fossil species, Ann. birds, Yale University Press, New Heaven, CT, Carnegie Mus. 66:457-496. Mooers, A. O,, and P Cotgreave, 1994. Sibley and Ahlquisi's Livezey, B. C. 1998. A phyiwgcnetic analysis of the Gruiformes tapestry dusted off. Trends Ecol, Evol. 9:458-459 (Aves) based on morphological characters, with an emphasis Moyle, R, G, 2004, Phylogenetics of barbets (Aves: Piciformes) on rails (Rallidae). Philos. Trans. R, Soc. Lond. 353:2077- based on nuclear and mitochondrial sequence data. Mol, 2151. Phylogen, Evol, 30:187-200. Uvezey, B, C, and R 1.. Zusi. 2001, Higher-order phylogenetics Norell, M. A.,J, M, Clark, and P, J. Makovicky 2001, Phyloge- of modem Aves based on comparative anatomy. Neth, J. netic relationships among coclurosauitan ihcropods. Zool. 51:179-205. Pp. 49-67 in New perspectives on the origin and early Loveiie, 1. J., and El. Benningham. 2ÜD2. Wtiat is a wood evolution of birds 0- Gauthier and L. F. Gall, eds.), Peabody warbter? Molecular characterization of a monophyletic Museum of Natural History, Yale University, New Haven, Parulidae. Auk 119:695-714. CT. Macleay. W, S, 1819-1621, Horae eniomologicac: or essays on Ogawa, A,, K, Murata, and S, Mizuno, 1998, The location of (he annulose animals. S. Bagster. London. Z- and W-linked marker genes and sequence on the Madscn, C. S., K. P. McHugh, and S, R. D. Kloet. 1998. A homomorphic sex chromosomes of the ostrich and the emu, partial classification of waterfowl (Anatidae) based on Proc, Nail. Acad. Sei. USA 95:4415-4418, single-copy DNA. Auk 105:452-459. O'Hara. R. J. 1988. Diagrammatic classifications of birds, 1819- Martin, L. D. 1983, The origin of birds and of avian flight. Curr, 1901: views of the natural system in 19th-century British Omiihol. 1:106-129. ornithology. Pp, 2746^2759 in Acta XIX Congressus Maurer, D. R., and R J. Raikow. 1981. Appendicuiar myology, Inicmationalis Omiîhologici (H, Quellet, cd). National phylogeny and classification of the avian order Coraci- Museum of Natural Sciences, Ottawa. iformcs (including Trogon i formes), Ann. Caniegie Mus. Olson, S. L, 19fi5, The fossil records of birds. Pp. 79-238 in 50:417-434. Avian biology (D. S, Earner, J, King, and K, C. Parkes, eds), Mayr, E. 1942. Systematics and the origin of species: from the vol, 8. Academic Press, New York, viewpoint of a zoologist. Columbia University Press, New Olson, S. [• 2002. Review of "New Perspectives on the Origin York. and Eady Evolution of Birds, Proceedings of the Imcma- Mayr, E. 1969. Principles of systematic zoology. McGraw Hill, tional Symposium in Honor of John H. Ostrom," Auk New York. 119:1202-1205, Mayr, E., and D. Amadon. 1951. A classification of recent birds. Olson, S. L,, aod A, Feduccia. )980a, Presbyomis and the origin Am. Mus. Nov. 1946:453-473. of the Anseriformes (Aves: Charadriomorphae), Smithson, Mayr, G. 2002. Osteological evidence for paraphyly of the avian Contnb, Zool, 323:1-24, order Caprimulgiformes (nightjar and allies). J. Omithol, Olson, S. L,, and A, Feduccia, 1980b, Relationships and 143:82-97. evolution of flamingos (Aves: Phocnicopieridae). Smithson, Mayr, G., and }. Clarke. 2003. The deep divergence of modem Contrib, Zool 316:1-73, birds: a phylogeneiic analysis of tnorphological characters. Ostrom, j. H. 1976. Archaeopteryx and the origin of birds, Biol, Cladistics 19:527-553. J, Linn, Soc, 8:91-182, Mayr, Ü., A. Manegold, and U. S.Johansson. 2003. Monophyl- Padian, K., and L, M. Chiappc, 1998. The origin and early etic groups within "higher land birds"•comparison of evolution of birds, Biol, Rev. 73:1-42, molecular and morphological data. Z Zool. Syst. Uvol, Res. Paton, T. A,, A, J, Baker, J, G. Groth, and G, F, Barrowclough. 41:233-248. 2003. RAG-1 sequences resolve phylogenetic relationships Meise, W, 1963, Verhalten der straussartigen Vogel und within charadriifonn birds. Mol. Phylogen, Evol, 29:268- Monophylic der Ratitae. Pp. 115-125 m Proceedings of the 278 13th International Ornithological Congress (C, G. Sibley, Paton, T. A, O. lladdrath, and A ). Baker, 2002. Complete ed,). American Ornithologists' Union, Baton Rouge, LA. mitochondrial DNA genome sequences show that modem MindcU, D., ed. 1997, Avian molecular evolution and systemat- birds are not descended from transitional shorebirds, Proc, ics. Academic Press, San Diego. R. Soc. Lond. B 269:839-846, Mmdell, D. P. 1992. DNA-DNA hyhndization and avian Payne, R. B,, and C, ), Risley, 1976, Systematics and evolution- phylogeny, Syst, Biol. 41:126-134. ary relationships among the herons (Ardeidae). Mise, Publ, Mindell, D, P., M, D, Sorenson, D, E. Dimcheff, M. Hasegawa, Mus, Zool. Univ. Michigan 150:1-115. J. C. Ast, and T. Yuri. 1999, Interordinal relationships of Prum, R, O, 1988, Phylogenetic interrelationships of the barbels birds and other reptiles based on whole mitochondrial (Capllonidae) and toucans (Ramphastidae) based on genomes. Syst. Biol. 48:138-152. morphology with comparisons to DNA-DNA hybridization, Mindell, D. P., M. D. Sorenson, C. J. Huddleston, H. C. ZoolJ. Linn. Soc, Lond. 92:313-343, Miranda, Jr., A. Knight, S. J. Sawchuk, and T. Yuri, 1997, Prum, R, O. 1993 Phylogeny, biogeography, and evolution of Phylogenetic relationships among and within select avian the broadbills (Eurylaimidae) and asites (Philepiitidae) orders based on miiochondrial DNA, Pp, 213-247 in Avian based on morphology. Auk 110:304-324, Phylogenetic Relationships among Modern Birds (Neornithes) 489
Prum, R. O. 2002. Why urnilhologists should care about the Strickland. H. E. 1841, On the true method of discovering the theropod origin of birds. Auk 119:1-17. natural system in zoology and botany, Ann, Mag, Nat, Hist. Raikow, R. 1987 t lindlimb myology and evolution of the Old 6:184-194, World suboscine passenne birds (Acantliisitiidac, Pitiidac. Swierczewski. E. V,, and R. J. Raikow, 1981. Hindlimb Philepittidae, Eurylaimidat). Am, Ornithol. Unioti Ümith. morphology, pbyiogeny. and classification of the Pici- Monogr. 41:1-81. formes. Auk 98:466-480. Raikow, R.J. 1982. Monophyly of the Passeriformes: test oía Tarsitano, 5.. and M, K, Hecht, 1980, A reconsideration of the phylogunttif hypothcsis. Auk 9<í:431-445. reptilian relationships oi AychaeopUryx. Zool.J Linn. 5oc. Raikow. R. J , andj. Cratrah. 1983. Monophyly of the Pici- 69:149-182. formes: a reply to Olsoti. Auk 100:134-138, van Tuinen, M, D. B. Butvill.J. A. W. Kirsch, and S. B. Hodges. Rea, A, M, 1983. Catharlid affinities: a brief overview. Pp. 26- 2001. Convergence and divergence in the evolution of 54 in Vulture biology and management (S. R. Wilbur and aquatic birds. Proc. R, Soc. Lond. B 268:1-6. J. A. Jackson, cds.). University of Calilbniia Press, Berkeley. van Tuinen, M,. C, G, Sibley, and S, B, Sibley, 2000 The early Sereno, P. C. 1999, The evolution of dinosaurs. Science hisiorj' of modern birds inferied from DNA sequences of 284:2137-2147, nuclear and mitochondrial ribosotnal genes. Mol, Biol. Evol, Sheldon, V. H,, and A, H, Bledsoe, 1993. Avian molecular 17:451-4'57, systcmatics, 1970s to 1990,s, Annu. Rev, Ecol. Syst, Waddell, P J., Y. Cao, M. Hasegawa, and D. P. Mindell. 1999. 24:243-278, Assessing ihe Cretaceous superordinal divergence times Sibley, C. G., and Ahlquist. J. E. 1990. Phylogcny and classifica- within birds and placental mammals using whole mitochon- tion of birds: a study in molecular evolution. Yale University drial protein sequences and an extended statistical frame- Press, New Haven, CT. work. Syst, Biol, 48:119-137, Sibley, C, G•J, E. Ahlquist, and B. L. Monroe. 1988. A Wallace, A, R 1856. Attempts at a natural arrangement of birds, classification of the living birds ol the world based on DNA- Ann. Mag. Nat. Hist. 18:193-216. DNA hybridiiation studies. Auk 105:409-423. Wet mo re, A. 1930. A systematic classification for the birds of Sibley, C. G., and B. L, Monroe. Jr. 1990. Distribution and the world. Proc, U,S, Nati, Mus, 76:1-8. taxonomy of the birds of the world. Yale University Press, Wet m ore. A, 1934, A systematic classification for the birds of New Heaven. CT. the world/revised and amended. Smithson. Inst, Mise, Coll, Siegel-Causey, D. 1997. Phy logen y of the Pele cam formes: 89(:i3):l-ll, molecular systcmatics of a primitive group, Pp. 159-172 in Wet m ore. A, 1940, A systematic classification for the birds of Avian molecular evolution and sysiemaiics (D, P, Mindell, the world. Smithson. Inst. Misc. Coll. 99(7):]~11, cd,). Academic Press, New York, Wetmore, A. 1951. A revised classification for the birds of the Simpson. G. G, 1961 Principles of animal taxonomy. Columbia world. Smithson. Inst. Misc. Coll. U7t4):l-22. University Press, New York, Wetmore, A. 1960. A classification for the birds of the world, Simpson. S. F,. and J, Cracraft, 1981, The phylogenetic Smithson. Inst. Misc. Col!. 139(11): 1-37. relationships of the picifoiroes (Class Aves), Auk 98:481- Wheeler, Q. D. 1995. The "old systematics*': classification and 494, phylogeny. Pp.31-62 in Biology, phytogeny, and classifica- Sorenson, M, D., E. Oneal.J. Garcia-Mo reno, and D. P. Mindell tion of Coleóptera: papers celebrating the 80th birthday of 2003. More taxa, more characters: the hoaizin problem is Roy A, Crowson (J, Pakaluk and S, A, Slipirtski, eds.), still unresolved. Moi, Biol. Evol, 20:1484-1499. Muieum i Instytut Zoologii PAN, Warsaw, Stanley, S, E,. andJ, Cracrafi, 2002, Uighcr-lcvcl systematic Xu. X,. M. A. Norell, X-L. Wang, P. J. Makovicky, and X.-C. analysis of birds; current problems and possible solutions. Wu, 2002, A basal troodontid from the Early Cretaceous of Pp. 31-43 in Molecular systematics and evolution: theory China. Nature 415:780-784. and practice (R. DeSalle, G. Giribet, and W. Wheeler, eds.). Xu, X,. Z. Zhou, X. Wang, X, Kuang, F. Zhang, and X. Du, Birkliäuser Verlag, Basel. 2003, Four-winged dinosaurs from China, Nature 421:335- Storcr, R. W, 1960. Evolution in the diving birds. Pp. 694-707 340, in Proceedings of the XII International Omuhological Yuri, T,, and D. M, Mindell. 2002, Molecular pbylogenelic Congress (G. Bergman, K. O. Donner, and L von Haartman, analysis of Fringillidae, "New World nine-primaried eds). Tilgirtanmn Kirjapaino, Helsinki. oscines" (Aves: Passeriformes). Mol, Phylogenet, Evol. Siresemann. E. 1927-1934. Aves. Pp. 1-899 in Handbuch der 23:229-243. Zoologie (W. Kûkenthal and T. Krumbach, eds.), vol. 7, Zusi. R. L, and B, C, Livezey, 2000, Homolog)' and phyloge- pt. 2. Walter de Gruyter, Berlin, netic implications of some enigmatic cranial features in Stresemann, E. 1959. The status of avian systematics and its galliform and anseriform birds, Ann. Carnegie Mus. unsolved problems. Auk 76:269-280. 69:157-193.