27 Phylogenetic Relationships among Modern Birds (Neornithes) Toward an Avian Tree of Life

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Joel Cracraft

F. Keith Barker

Michael Braun

John Harshman

Gareth J. Dyke

468

Modern perceptions of the monophyly of avian higher taxa

(modern birds, Neornithes) and their interrelationships are

the legacy of systematic work undertaken in the 19th century.

Before the introduction of an evolutionary worldview

by Charles Darwin in 1859, taxonomists clustered taxa into

groups using similarities that reflected a vision of how God

might have organized the world at the time of Creation. Such

was the case with the Quinerian system of avian classification

devised by Macleay (1819–1821) in which groups and

subgroups of five were recognized, or of Strickland (1841)

or Wallace (1856) in which affinities were graphed as unrooted

networks (see O’Hara 1988).

After Darwin, this worldview changed. For those comparative

biologists struggling to make sense of Earth’s biotic

diversity in naturalistic terms, Darwinism provided a framework

for organizing similarities and differences hierarchically,

as a pattern of ancestry and descent. The search for the Tree

of Life was launched, and it did not take long for the structure

of avian relationships to be addressed. The first to do so

was no less a figure than Thomas Henry Huxley (1867), who

produced an important and influential paper on avian classification

that was explicitly evolutionary. It was also Huxley

who provided the first strong argument that birds were related

to dinosaurs (Huxley 1868).

Huxley was particularly influential in England and was

read widely across Europe, but the “father of phylogenetics”

and phylogenetic “tree-thinking” was clearly Ernst Haeckel.

Darwin’s conceptual framework had galvanized Haeckel,

and within a few short years after Origin and a year before

Huxley’s seminal paper, he produced the monumental

Generelle Morphologie der Organismen—the first comprehensive

depiction of the Tree of Life (Haeckel 1866). Haeckel’s

interests were primarily with invertebrates, but one of his

students was to have a singular impact on systematic ornithology

that lasted more than 125 years.

In 1888 Max Fьrbringer published his massive (1751

pages, 30 plates) two-volume tome on the morphology and

systematics of birds. Showing his classical training with

Haeckel and the comparative anatomist Carl Gegenbaur,

Fьrbringer meticulously built the first avian Tree of Life—

including front and hind views of the tree and cross sections

at different levels in time. The vastness of his morphological

descriptions and comparisons, and the scope of his vision,

established his conception of relationships as the dominant

viewpoint within systematic ornithology. All classifications that

followed can fairly be said to be variations on Fьrbringer’s

theme. Such was the magnitude of his insights. Indeed, as

Stresemann (1959: 270) noted:

On the whole all the avian systems presented in the

standard works in this century are similar to each

other, since they are all based on Fьrbringer and

Gadow [who followed Fьrbringer’s scheme closely

and, being fluent in German, was able to read the

1888 tome]. My system of 1934 [Stresemann 1927–

1934] does not differ in essence from those which

Julie Feinstein

Scott Stanley

Alice Cibois

Peter Schikler

Pamela Beresford

Jaime Garcнa-Moreno

Michael D. Sorenson

Tamaki Yuri

David P. Mindell

Phylogenetic Relationships among Modern Birds (Neornithes) 469

Wetmore (1951) and Mayr and Amadon (1951) have

recommended.

Fьrbringer (1888) thus established the framework for virtually

all the major higher level taxa in use today, and the

fact that subsequent classifications, with relatively minor

alterations, adopted his groups entrenched them within ornithology

so pervasively that his classificatory scheme has

influenced how ornithologists have sampled taxa in systematic

studies to the present day.

Despite his monumental achievement in establishing the

first comprehensive view of the avian branch of the Tree of

Life, avian phylogeny soon became of only passing interest to

systematists. Phylogenetic hypotheses—in the sense of taxa being

placed on a branching diagram—were largely abandoned

until the last several decades of the 20th century. For more

than 80 years after Fьrbringer the pursuit of an avian Tree of

Life was replaced by an interest in tweaking classifications, the

most important being those of Wetmore (1930, 1934, 1940,

1951, 1960), Stresemann (1927–1934), Mayr and Amadon

(1951), and Storer (1960). Aside from reflecting relationships

in terms of overall similarity, these classifications also shaped

contemporary views of avian phylogenetics by applying the

philosophy of evolutionary classification (Simpson 1961, Mayr

1969), which ranked groups according to how distinct they

were morphologically.

What happened to “tree thinking” in systematic ornithology

between 1890 and 1970? The first answer to this

question was that phylogeny became characterized as the

unknown and unknowable. Relationships were considered

impossible to recover without fossils and resided solely in

the eye of the beholder inasmuch as there was no objective

method for determining them. Thus, Stresemann (1959: 270,

277) remarked,

The construction of phylogenetic trees has opened the

door to a wave of uninhibited speculation. Everybody

may form his own opinion . . . because, as far as birds

are concerned, there is virtually no paleontological

documentation. . . . Only lucky discoveries of fossils

can help us. . . .

A second answer is that phylogeny was eclipsed by a redefinition

of systematics, which became more aligned with

“population thinking.” This view was ushered in by the rise

of the so-called “New Systematics” and the notion that “the

population . . . has become the basic taxonomic unit” (Mayr

1942: 7). The functions of the systematist thus became identification,

classification (“speculation and theorizing”), and

the study of species formation (Mayr 1942: 8–11). Phylogeny

became passй [see also Wheeler (1995) for a similar interpretation].

Thus,

The study of phylogenetic trees, of orthogenetic series,

and of evolutionary trends comprise a field which was

the happy hunting ground of the speculative-minded

taxonomist of bygone days. The development of the

“new systematics” has opened up a field which is far

more accessible to accurate research and which is more

apt to produce tangible and immediate results. (Mayr

1942: 291)

A final answer was that, if phylogeny were essentially

unknowable, it would inevitably be decoupled from classification,

and the latter would be seen as subjective. The architects

of the synthesis clearly understood the power of basing

classifications on phylogeny (e.g., Mayr 1942: 280) but in

addition to lack of knowledge, “the only intrinsic difficulty

of the phylogenetic system consists in the impossibility of

representing a ‘phylogenetic tree’ in linear sequence.”

Twenty-seven years later, Stresemann summarized classificatory

history to that date in starkly harsh terms:

In view of the continuing absence of trustworthy

information on the relationships of the highest

categories [taxa] of birds to each other it becomes

strictly a matter of convention how to group them into

orders. Science ends where comparative morphology,

comparative physiology, comparative ethology have

failed us after nearly 200 years of effort. The rest is

silence. (Stresemann 1959: 277–278)

The silence did not last. A mere four years after this indictment

of avian phylogenetics, Wilhelm Meise, whose office was next

to that of the founder of phylogenetic systematics, Willi Hennig,

published the first explicitly cladistic phylogenetic tree in ornithology,

using behavioral characters to group the ratite birds

(Meise 1963). Avian systematics, like all of systematics, soon

became transformed by three events. The first was the introduction

of phylogenetic (cladistic) thinking (Hennig 1966) and

a quantitative methodology for building trees using those principles

(Kluge and Farris 1969; the first quantitative cladistic

analysis for birds was included in Payne and Risley 1976). At

the same time, the rise of cladistics logically led to an interest

in having classifications represent phylogenetic relationships

more explicitly, and that too became a subject of discussion

within ornithology (e.g., Cracraft 1972, 1974, 1981). This

desire for classifications to reflect phylogeny had its most comprehensive

expression in the classification based on DNA–DNA

hybridization, a methodology, however, that was largely phenetic

(Sibley et al. 1988, Sibley and Ahlquist 1990, Sibley and

Monroe 1990).

The second contribution that changed avian systematics

was increased use of molecular data of various types.

Techniques such as starch-gel electrophoresis, isoelectricfocusing

electrophoresis, immunological comparisons

of proteins, mitochondrial DNA (mtDNA) RFLP (restriction

fragment length polymorphism) analysis, DNA hybridization,

and especially mtDNA and nuclear gene

sequencing have all been used to infer relationships, from

the species-level to that of families and orders. Today, with

few exceptions, investigators of avian higher level relationships

use DNA sequencing, mostly of mtDNA, but

470 The Relationships of Animals: Deuterostomes

nuclear gene sequences are now becoming increasingly

important.

Finally, not to be forgotten were the continuous innovations

in computational and bioinformatic hardware and software

over the last three decades that have enabled investigators

to collect, store, and analyze increasing amounts of data.

This chapter attempts to summarize what we think we

know, and don’t know, about avian higher level relationships

at this point in time. In the spirit of this volume, the

chapter represents a collaboration of independent laboratories

actively engaged in understanding higher level relationships,

but it by no means involves all those pursuing

this problem. Indeed, there is important unpublished morphological

and molecular work ongoing that is not included

here. Nevertheless, it will be apparent from this synthesis

that significant advances are being made, and we can expect

the next five years of research to advance measurably

our understanding of avian relationships.

Birds Are Dinosaurs

Considerable debate has taken place in recent years over

whether birds are phylogenetically linked to maniraptorian

dinosaurs, and a small minority of workers have contested

this relationship (e.g., Tarsitano and Hecht 1980, Martin

1983, Feduccia 1999, 2002, Olson 2002). In contrast, all

researchers who have considered this problem over the last

30 years from a cladistic perspective have supported a

theropod relationship for modern birds (Ostrom 1976,

Cracraft 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,

Chiappe and Dyke 2002, Xu et al. 2002), and that hypothesis

appears as well corroborated as any in systematics

(fig. 27.1).

Having said this, droves of fossils—advanced theropods

as well as birds—are being uncovered with increasing regularity,

and many of these are providing new insights into

character distributions, as well as the tempo of avian evolution.

Just 10 years ago, understanding of the early evolution

of birds was based on a handful of fossils greatly separated

temporally and phylogenetically (e.g., Archaeopteryx and a

few derived ornithurines). Now, more than 50 individual taxa

are known from throughout the Mesozoic (Chiappe and

Dyke 2002), and from this new information it is now clear

that feathers originated as a series of modifications early in

the theropod radiation and that flight is a later innovation

(reviewed in Chiappe and Dyke 2002, Xu et al. 2003).

Numerous new discoveries of pre-neornithine fossils will

undoubtedly provide alternative interpretations to character-

state change throughout the line leading to modern

birds (for summaries of pre-neornithine relationships, see

Chiappe and Dyke 2002).

DNA Hybridization and Beyond

The DNA hybridization work of Sibley and Ahlquist (1990)

has had a major impact on avian systematics. Their tree—

the so-called “Tapestry” shown in figure 27.2—provided

a framework for numerous evolutionary interpretations of

avian biology. Avian systematists, however, have long noted

shortcomings with the analytical methods and results of

Sibley and Ahlquist (Cracraft 1987, Houde 1987, Lanyon

1992, Mindell 1992, Harshman 1994). Moreover, it is obvious

that Sibley and Ahlquist, like many others before and

after, designed their experiments with significant preconceived

assumptions of group monophyly (again, many of

which can be traced to Fьrbringer 1888).

The spine of the DNA hybridization tree is characterized

by a plethora of short internodes, which is consistent

with the hypothesis of an early and rapid radiation (discussed

more below). The critical issue, however, is that most

of the deep internodes on Sibley and Ahlquist’s (1990) tree

were not based on a rigorous analysis of the data, and in

fact the data are generally insufficient to conduct such analyses

(Lanyon 1992, Harshman 1994). Relationships implied

Figure 27.1. Relationships of birds to theropod dinosaurs (after

Chiappe and Dyke 2002).

Archaeopteryx

Neornithes

Ichthyornis

Hesperornis

Enantiornithes

Confuciusornithidae

Troodontidae

Dromaeosauridae

Caudipteryx

Sinosauropteryx

Alvarezsauridae

Struthiomimus

Tyrannosaurus rex

Phylogenetic Relationships among Modern Birds (Neornithes) 471

Figure 27.2. The “tapestry” of Sibley

and Ahlquist (1990) based on DNA

hybridization distances. The tree was

constructed by hand from incomplete

data matrices. The topology shown here

is that of Sibley and Ahlquist (1990),

but their classification and nomenclature

are modified in some instances to

use more familiar names.

emus DROMICEIDAE

cassowaries CASUARIIDAE

kiwis APTERYGIDAE

rheas RHEIDAE

ostrich STRUTHIONIDAE

tinamous TINAMIDAE

ducks, geese ANATIDAE

screamers ANHIMIDAE

Magpie Goose ANSERANATIDAE

pheasants PHASIANIDAE

guineafowl NUMIDIDAE

quail ODONTOPHORIDAE

guans CRACIDAE

mound builders MEGAPODIDAE

buttonquails TURNICIDAE

woodpeckers PICIDAE

honeyguides INDICATORIDAE

Old World barbets MEGALAIMIDAE

toucans RAMPHASTIDAE

New World barbets CAPITONIDAE

kingfishers ALCEDINIDAE

todies TODIDAE

motmots MOMOTIDAE

bee-eaters MEROPIDAE

rollers CORACIIDAE

cuckoo-roller LEPTOSOMATIDAE

trogons TROGONIDAE

hornbills BUCEROTIDAE

woodhoopoes PHOENICULIDAE

hoopoe UPUPIDAE

jacamars GALBULIDAE

puffbirds BUCCONIDAE

mousebirds COLIIDAE

cuckoos CUCULIDAE

hoatzin OPISTHOCOMIDAE

anis CROTOPHAGIDAE

parrots PSITTACIDAE

potoos NYCTIBIIDAE

oilbird STEATORNITHIDAE

nightjars CAPRIMULGIDAE

frogmouths PODARGIDAE

owlet nightjars AEGOTHELIDAE

owls STRIGIDAE

barn owls TYTONIDAE

turacos MUSOPHAGIDAE

swifts APODIDAE

hummingbirds TROCHILIDAE

songbirds PASSERIFORMES

pigeons COLUMBIDAE

sungrebes, limpkin HELIORNITHIDAE

cranes GRUIDAE

trumpeters PSOPHIIDAE

kagu RHYNOCHETIDAE

seriemas CARIAMIDAE

bustards OTIDIDAE

sunbittern EURYPYGIDAE

rails RALLIDAE

seedsnipe THINOCORIDAE

plains-wanderer PEDIONOMIDAE

sandpipers, snipes SCOLOPACIDAE

jacanas JACANIDAE

paintedsnipe ROSTRATULIDAE

plovers CHARADRIIDAE

thick-knees BURHINIDAE

sheathbill CHIONIDIDAE

pratincoles, crab-plover GLAREOLIDAE

gulls, terns LARIDAE

sandgrouse PTEROCLIDIDAE

falcons, caracaras FALCONIDAE

secretarybird SAGITTARIIDAE

hawks, eagles ACCIPITRIDAE

grebes PODICIPEDIDAE

tropicbird PHAETHONTIDAE

boobies, gannets SULIDAE

anhinga ANHINGIDAE

cormorants PHALACROCORACIDAE

herons ARDEIDAE

hammerhead SCOPIDAE

flamingos PHOENICOPTERIDAE

ibises THRESKIORNITHIDAE

storks, New World vultures CICONIIDAE

pelicans PELECANIDAE

frigatebirds FREGATIDAE

penguins SPHENISCIDAE

albatrosses DIOMEDEIDAE

shearwaters, petrels PROCELLARIIDAE

storm-petrels OCEANITIDAE

loons GAVIIDAE

Palaeognathae

Galloanserae

PICI

(Piciformes part)

Coraciiformes

Galbulae

(Piciformes, part)

Caprimulgiformes

Strigiformes

Apodiformes

Gruiformes

Charadriiformes

Falconiformes part

Ciconiiformes part

Pelecaniformes part

Falconiformes part

Pelecaniformes part

472 The Relationships of Animals: Deuterostomes

by the tree therefore have ambiguous reliability. In addition,

because of the manner in which experiments were

designed, and possibly because of artifacts due to rate heterogeneity

in hybridization distances, instances of incorrect

rooting occur across the tree. Thus, although the DNA

hybridization data have yielded insight about both novel

and previously proposed relationships, they are difficult to

interpret and compare with other results except as assertions

of relationships.

The tree derived from DNA hybridization data postulated

a specific series of relationships among taxa traditionally assigned

ordinal rank, as well as among families. It is relevant

here to summarize the overall structure of this tree as some

of the major groupings it implies will be addressed in subsequent

sections of this chapter. Suffice it to say at this point,

the emerging morphological and molecular data confirm

some of these relationships but not others, both among traditional

“orders” but among families as well.

Among its more controversial claims, the DNA hybridization

tapestry (fig. 27.2):

1. Recognizes a monophyletic Palaeognathae (ratites and

tinamous) and Galloanserae (galliform + anseriform)

but unites them, thus placing the neornithine root

between them and all other birds: this rooting renders

the Neognathae (all birds other than palaeognaths)

paraphyletic, a conclusion refuted by substantial data

(see below). Oddly, Sibley and Ahlquist (1990)

contradicted this in their classification and grouped

Galloanserae within their “Neoaves” (equivalent to

Neognathae here).

2. Places Turnicidae (buttonquail), Pici (woodpeckers

and their allies), and Coraciiformes (kingfishers,

rollers, and allies) + Galbulae (traditionally united

with the Pici) at the base of the Neoaves.

3. Identifies mousebirds, then cuckoos + Hoatzin, and

finally parrots as sequential sister groups to the

remaining neognaths.

4. Makes the large songbird (Passeriformes) assemblage

the sister group to the remaining neognaths; this

latter clade has the pigeons as the sister group of a

large, mostly “waterbird,” assemblage.

5. Depicts monophyly of Gruiformes (cranes, rails, and

allies) and Charadriiformes (shorebirds, gulls, and

allies) within the waterbirds: the falconiforms are also

monophyletic, except that the New World vultures

(Cathartidae) are placed in a family with the storks

(Ciconiidae). Within the remainder of the waterbirds,

the traditional orders Pelecaniformes (pelicans,

gannets, cormorants) and Ciconiiformes (flamingos,

storks, herons, ibises) are each rendered paraphyletic

and interrelated with groups such as grebes, penguins,

loons, and the Procellariiformes (albatrosses,

shearwaters).

The Challenge of Resolving Avian Relationships

Initial optimism over the results of DNA hybridization has

given way to a realization that understanding the higher level

relationships of birds is a complex and difficult scientific

problem. There is accumulating evidence that modern birds

have had a relatively deep history (Hedges et al. 1996, Cooper

and Penny 1997, Waddell et al. 1999, Cracraft 2001,

Dyke 2001, Barker et al. 2002, Paton et al. 2002, contra

Feduccia 1995, 2003) and that internodal distances among

these deep lineages are short relative to the terminal branches

(Sibley and Ahlquist 1990, Stanley and Cracraft 2002; the

evidence is discussed below). To the extent these hypotheses

are true, considerable additional data will be required

to resolve relationships at the higher levels. This conclusion

is supported by the results summarized here.

Although the base of Neoaves is largely unresolved at

this time, recent studies are confirming some higher level

relationships previously proposed, and others are resolving

relationships within groups more satisfactorily than

before (the songbird tree discussed below is a good example).

At the same time, novel cladistic hypotheses are

emerging from the growing body of sequence data (e.g., the

proposed connection between grebes and flamingos; van

Tuinen et al. 2001). So, even though our ignorance of avian

relationships is still substantial, progress is being made, as

this review will show.

In addition to summarizing the advances in avian relationships

over the past decade (see also Sheldon and Bledsoe

1993, Mindell 1997), the following discussion of neornithine

relationships is largely built upon newly completed studies

from our various laboratories that emphasize increased taxon

and character sampling for both molecular and morphological

data. These studies include:

1. An analysis of the c-myc oncogene (about 1100

aligned base pairs) for nearly 200 taxa that heavily

samples nonpasseriform birds (J. Harshman, M. J.

Braun, and C. J. Huddleston, unpubl. obs.)

2. An analysis broadly sampling neornithines that uses

4800 base pairs of mitochondrial sequences in

conjunction with 680 base pairs of the PEPCK

nuclear gene (Sorenson et al. 2003)

3. An analysis of the RAG-2 [recombination activating

protein] nuclear gene for approximately 145

nonpasseriform taxa and a sample of passeriforms

( J. Cracraft, P. Schikler, and J. Feinstein, unpubl. obs.)

4. A combined analysis of the RAG-2 data and a sample

of 166 morphological characters for 105 family-level

taxa (G. J. Dyke, P. Beresford, and J. Cracraft, unpubl.

obs.)

5. A combined analysis of the c-myc and RAG-2 data for

69 taxa, mostly nonpasseriforms (J. Harshman, M. J.

Braun, and J. Cracraft, unpubl. obs.)

Phylogenetic Relationships among Modern Birds (Neornithes) 473

6. A combined analysis of 74 “waterbird” taxa for 5300

base pairs of mitochondrial and RAG-2 gene sequences

(S. Stanley, J. Feinstein, and J. Cracraft,

unpubl. obs.)

7. An analysis of 146 passeriform taxa for 4108 base

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.)

8. An analysis of 44 nine-primaried passeriforms

(“Fringillidae) using 3.2 kilobases of mitochondrial

sequence (Yuri and Mindell 2002).

Phylogenetic Relationships

among Basal Neornithes

The Base of the Neornithine Tree

In contrast to the considerable uncertainties that exist regarding

the higher level relationships among the major avian

clades, the base of the neornithine tree now appears to be

well corroborated by congruent results from both morphological

and molecular data (fig. 27.3; summarized in Cracraft

and Clarke 2001, Garcнa-Moreno et al. 2003; see below).

Thus, modern birds can be divided into two basal clades,

Palaeognathae (tinamous and the ratite birds) and Neognathae

(all others); Neognathae, in turn, are composed of

two sister clades, Galloanserae for the galliform (megapodes,

guans, pheasants, and allies) and anseriform (ducks, geese,

swans, and allies) birds, and Neoaves for all remaining taxa.

This tripartite division of basal neornithines has been recovered

using morphological (Livezey 1997a, Livezey and Zusi

2001, Cracraft and Clarke 2001, Mayr and Clarke 2003; see

below) and various types of molecular data (Groth and

Barrowclough 1999, van Tuinen et al. 2000, Garcнa-Moreno

and Mindell 2000, Garcнa-Moreno et al. 2003, Braun and

Kimball 2002, Edwards et al. 2002, Chubb 2004; see also

results below). The DNA hybridization tree also recovered

this basal structure, but the root, estimated by assuming a

molecular clock without an outgroup, was placed incorrectly

(fig. 27.2). In contrast, analyses using morphological or

nuclear sequences have sought to place the root through

outgroup analysis, and their results are consistent in placing

it between palaeognaths and neognaths (Cracraft 1986, Groth

and Barrowclough 1999, Cracraft and Clarke 2001; see also

studies discussed below). Small taxon samples of mitochondrial

data have also been particularly prone to placing the

presumed fast-evolving passerine birds at the base of the

neornithine tree (Hдrlid and Arnason 1999, Mindell et al.

1997, 1999), but larger taxon samples and analyses using

better models of evolution (e.g., Paton et al. 2002) have

agreed with the morphological and nuclear sequence analyses.

Recent studies of nuclear short sequence motif signatures

support the traditional hypothesis (Edwards et al. 2002), and

it also worth noting that palaeognaths and neognaths are

readily distinguished by large homomorphic sex chromosomes

in the former and strongly heteromorphic chromosomes

in the latter (Ansari et al. 1988, Ogawa et al. 1998).

Palaeognathae

Monophyly of palaeognaths is well corroborated, but relationships

within the ratites remain difficult to resolve. The

relationships shown in figure 27.3 reflect those indicated by

morphology (Cracraft 1974, Lee et al. 1997, Livezey and Zusi

2001), and all the internodes have high branch support.

Molecular data, on the other hand, have differed from this

view and, in general, data from different loci and methods

of analysis have yielded conflicting results. In most of these

studies (Lee et al. 1997, Haddrath and Baker 2001, Cooper

et al. 2001) the kiwis group with the emu + cassowaries, and

the rhea and ostrich diverge independently at the base of the

tree. When the extinct New Zealand moas are included in

studies using most of the mitochondrial genome (Haddrath

and Baker 2001, Cooper et al. 2001), they also tend to be

Figure 27.3. The basal relationships of modern birds

(Neornithes). Relationships within Paleognathae are those based

on morphology (Lee et al. 1997), which do not agree with results

from molecular sequences. See text for further discussion.

cassowaries

emus

rheas

ostrich

kiwis

tinamous

ducks, geese

Magpie Goose

screamers

guans, curassows

pheasants, quail,

guineafowl

megapodes

Neoaves

Palaeognathae

Galloanserae

474 The Relationships of Animals: Deuterostomes

placed toward the base of the tree. It can be noted that single

gene trees often do not recover ratite monophyly with strong

support, although these taxa generally group together.

Palaeognaths appear to exhibit molecular rate heterogeneity.

Tinamous, in particular, and possibly rheas and ostriches

appear to have higher rates of molecular evolution

than do kiwis, emus, and cassowaries (Lee et al. 1997, van

Tuinen et al. 2000, Haddrath and Baker 2001). Additionally,

paleognath mitochondrial sequences, which have been the

primary target of molecular studies, exhibit significant shifts

in base composition, which have made phylogenetic interpretations

difficult (Haddrath and Baker 2001). Thus, rate

artifacts, nonstationarity, the existence of relatively few,

deeply divergent species-poor lineages, and short internodal

distances among those lineages all play a role in making the

resolution of ratite relationships extremely difficult and controversial.

Although palaeognath relationships may be solved

with additional molecular and morphological data of the traditional

kind, the discovery of major character changes in

molecular sequences such as indels or gene duplications may

also prove to be important.

Galloanserae

Despite occasional debates that galliforms and anseriforms

are not sister taxa (Ericson 1996, 1997, Ericson et al. 2001),

the predominant conclusion of numerous workers using

morphological and/or molecular data is that they are (Livezey

1997a, Groth and Barrowclough 1999, Mindell et al. 1997,

1999, Zusi and Livezey 2000, Livezey and Zusi 2001, Cracraft

and Clarke 2001, Mayr and Clarke 2003, Chubb 2004).

Molecular studies questioning a monophyletic Galloanserae

(e.g., Ericson et al. 2001) have all employed small taxon

samples of mtDNA or nuclear DNA, but when samples are

increased, or nuclear genes are used, Galloanserae are

monophyletic and the sister group of Neoaves (Groth and

Barrowclough 1999, Garcнa-Moreno and Mindell 2000, van

Tuinen et al. 2000, Garcнa-Moreno et al. 2003, Chubb 2004;

see also J. Harshman, M. J. Braun, and C. J. Huddleston,

unpubl. obs.); three indel events in sequences from c-myc

also support a monophyletic Galloanserae (fig. 27.4). The

DNA hybridization tree of Sibley and Ahlquist (1990) recognized

Galloanserae, but because the neornithine root was

incorrectly placed, Galloanserae was resolved as the sister

group of the palaeognaths. With respect to relationships

within galliforms, a consistent pattern seems to have emerged

(Cracraft 1972, 1981, 1988, Sibley and Ahlquist 1990, fig. 328,

Harshman 1994, Dimcheff et al. 2000, 2002, Dyke et al. 2003;

see also J. Harshman, M. J. Braun, and C. J. Huddleston,

unpubl. obs.): (Megapodiidae (Cracidae (Numididae +

Odontophoridae + Phasianidae))). The major questions remain

centered around the relative relationships among the

guinea fowl (numidids), New World quail (odontophorids),

and pheasants (phasianids), as well as the phylogeny within

the latter; recent studies suggest that the numidids are out-

Figure 27.4. Phylogenetic tree based on approximately 1100

bases of the nuclear oncogene c-myc, including intron, exon

coding, and 3' untranslated region sequence, for 170 taxa

( J. Harshman, M. J. Braun, and C. H. Huddleston, unpubl.

obs.). The tree shown is an unweighted parsimony majority rule

bootstrap tree, plus other compatible branches. Thick branches

have 70% or greater bootstrap support; thin branches may have

very low support. Vertical tick marks represent phylogenetically

informative indels. Most terminal branches represent several

species, and all those are strongly supported, although for

clarity the branches are not shown as thickened.

ostrich

rheas

tinamous

kiwis

cassowaries

emu

New World vultures

nightjars

falcons, caracaras

hawks

hornbills

hoopoes

frogmouths

oilbird

cranes

rails

owls

parrots

songbirds

potoos

trogons

owlet nightjars

hummingbirds

swifts

barbets, toucans

woodpeckers, honeyguides

puffbirds

jacamars

kingfishers, motmots

rollers

grebes

flamingos

loons

shearwaters

tropicbirds

ibises

shoebill

pelicans

herons

cormorants

gannets

frigatebirds

penguins

sunbittern

storks

buttonquail

shorebirds

hoatzin

pheasants, quail, guineafowl

chachalacas

megapodes

magpie goose

ducks

Phylogenetic Relationships among Modern Birds (Neornithes) 475

side quails and phasianids (Cracraft 1981, Dimcheff et al.

2000, 2002, Dyke et al. 2003).

Relationships among the basal clades of anseriforms are also

not too controversial (Livezey 1986, 1997a,; Sibley and Ahlquist

1990: fig. 328 contra the “tapestry”, Harshman 1994, Ericson

1997, Groth and Barrowclough 1999; for views of relationships

within anatids, see Madsen et al. 1988, Livezey 1997b, Donne-

Goussй et al. 2002). The screamers (Anhimidae) are the sister

group to the magpie goose (Anseranatidae) + ducks, geese, and

swans (Anatidae). We note, however, that the resolution of the

basal nodes among screamers, magpie goose, and anatids has

been difficult and that mitochondrial data sometimes unite the

screamers and magpie goose (fig. 27.5), a grouping not suggested

by nuclear, morphological, or combined data. The fact

that both Livezey (1997a) and Ericson (1997) found the Late

Cretaceous-Paleogene fossil Presbyornis to be the sister group

of Anatidae (see also Kurochkin et al. 2002) is important because

it sets the Late Cretaceous as the minimum time of divergence

for the anatids and all deeper nodes.

Relationships within Neoaves

Relationships among the neoavian higher taxa have been

discussed in a number of studies over the past several decades

(e.g., Cracraft 1981, 1988, Sibley and Ahlquist 1990,

Ericson 1997, Mindell et al. 1997, 1999, Feduccia 1999, van

Tuinen et al. 2000, 2001, among others), and it is clear that

relatively little consensus has emerged. The monophyly of

many groups that have been accorded the taxonomic rank

of “order” such as loons, grebes, penguins, parrots, cuckoos,

and the large songbird group (Passeriformes) has not been

seriously questioned but that of nearly all other higher taxa

has. Thus, it is now broadly accepted that several traditional

orders such as pelecaniforms, ciconiiforms, and caprimulgiforms

are nonmonophyletic, whereas the status of others such

as gruiforms, coraciiforms, piciforms, and falconiforms remains

uncertain in the minds of many workers.

If one had to summarize the current state of knowledge,

the most pessimistic view would see the neoavian tree as a

“comb,” with little or no resolution among most traditional

families and orders. Short and poorly supported internodes

among major clades of neoavians are characteristic of recent

studies using nuclear (Groth and Barrowclough 1999, van

Tuinen et al. 2000) or mitochondrial data sets (van Tuinen

et al. 2000, 2001, Johnson 2001, Hedges and Sibley 1994,

Johansson et al. 2001), and the data sets discussed here also

illustrate this point. The trees discussed below will be interpreted

within the framework of bootstrap resampling analyses

that show sister lineages supported at the 70% level (heavy

lines in the figures). Using this approach, relationships among

the avian higher taxa can be interpreted as largely unresolved,

producing the neoavian comb. Nevertheless, there are emerging

similarities in phylogenetic pattern recovered across some

of these different studies that suggest some commonality of

phylogenetic signal. In these and other published cases, the

primary reason for the neoavian comb is suspected to be

insufficient character and/or taxon sampling. As noted above,

current evidence suggests that many of these divergences are

old and occurred relatively close in time. Thus, we are optimistic

that most neoavian relationships will be resolved with

additional data (see Discussion, below).

Phylogenetic Relationships among

the “Waterbird Assemblage”

Over the years, many authors have suggested that some or

all of the waterbird orders, in particular, seabirds (Procellariiformes),

penguins (Sphenisciformes), loons (Gaviiformes),

grebes (Podicipediformes), storks, herons, flamingos and allies

(Ciconiiformes), pelicans, cormorants, and allies (Pele-

Figure 27.5. A phylogenetic hypothesis for 41 avian taxa based

on about 4800 base pairs of mitochondrial sequence and 680 base

pairs of PEPCK intron 9 nuclear gene using three paleognaths as

the root (Sorenson et al. 2003). Nodes with bootstrap support

values of 70% are shown in heavy black, based on maximum

likelihood and maximum probability analyses of mitochondrial

data and MP analyses of PEPCK intron 9.

Eudromia

Struthio

Rhea

Dendrocygna

Aythya

Chauna

Anseranas

Megapodius

Alectura

Gallus

Acryllium

Crax

Otus

Tockus

Buteo

Crinifer

Musophaga

Columba

Treron

Trogon

Opisthocomus

Phoenicipterus

Scolopax

Burhinus

Mycteria

Ciconia

Colius

Urocolius

Nandayus

Neophema

Smithornis

Sayornis

Vidua

Corvus

Neomorphus

Crotophaga

Centropus

Coccyzus

Cuculus

Falco

Coracias

tinamous

rheas, ostriches

ducks, geese

screamers

Magpie Goose

megapodes

pheasants

guinea fowl

guans, currasows

owls

hornbills

hawks

turacos

pigeons

Hoatzin

trogons

flamingos

shorebirds

storks

broadbills

tyrant flycatchers

finches

crows

parrots

mousebirds

rollers

cuckoos

falcons

476 The Relationships of Animals: Deuterostomes

caniformes), shorebirds and gulls (Charadriiformes), and

cranes, rails, and allies (Gruiformes), are related to one another

(see, e.g., Sibley and Ahlquist 1990, Hedges and Sibley

1994, Olson and Feduccia 1980a, 1980b, Cracraft 1988).

Some authors have also linked various falconiform families

to the waterbird assemblage (Jollie 1976–1977, Rea 1983),

including a supposedly close relationship between New

World vultures (Cathartidae) and storks (Ligon 1967, Sibley

and Ahlquist 1990, Avise et al. 1994; but also see Jollie 1976–

1977, Hackett et al. 1995, Helbig and Siebold 1996). As a

consequence of these and newer molecular studies, it is now

widely thought that several of the large traditional orders of

waterbirds may not be monophyletic, and this is especially

true of the pelecaniforms and ciconiiforms (Cottam 1957,

Sibley and Ahlquist 1990, Hedges and Sibley 1994, Siegel-

Causey 1997, van Tuinen et al. 2001).

The supposition that waterbirds are related to one another

within neornithines as a whole is not well supported,

although the available data are suggestive of a relationship

among some of them (see above). Only the DNA hybridization

tree of Sibley and Ahlquist (1990) covered all birds, and

on their tree (fig. 27.2) the waterbirds and falconiforms are

clustered together. Van Tuinen et al. (2001) recently reevaluated

waterbird relationships and compared new DNA

hybridization data with results from about 4062 base pairs

of mitochondrial and nuclear sequence data for 20 and 19

taxa, respectively. Their most general conclusion was there

was relatively little branch support across the spine of the

tree, indicating that relationships among waterbirds are still

very much uncertain. They did, however, find support for

several clades: (1) a grouping of (the shoebill Balaeniceps +

pelicans) + hammerkop (Scopus), and these in turn to ibises

and herons, (2) penguins + seabirds (Procellariiformes), and

most surprisingly, (3) grebes + flamingos.

Previous studies have had insufficient taxon and character

sampling, or both. Even though large taxon samples based

on mitochondrial genes (fig. 27.6), or on the c-myc and RAG-

2 nuclear genes (figs. 27.4, 27.7A), are an improvement on

previous work, by themselves or together (fig. 27.8), they are

still inadequate to provide strong character support for most

clades. Nevertheless, some congruence among these various

studies is apparent. The c-myc data (fig. 27.4; J. Harshman,

M. J.Braun, and C. J. Huddleston, unpubl. obs.), for example,

recover (1) (cormorants + gannets) + frigatebirds, (2) (shoebills

+ pelicans) + ibises, (3) grebes + flamingos, and (4)

buttonquails + shorebirds. At the same time, groups such as

loons, tropicbirds, penguins, and storks do not show any

clear pattern of relationships in the c-myc data or the nuclear/

mitochondrial tree of van Tuinen et al. (2001). What is clear

in the c-myc data is that New World vultures and storks are

distantly removed from one another; New World vultures

were not included in the van Tuinen et al. study. The RAG-

2 data (fig. 27.7; J. Cracraft, P. Schikler, and J. Feinstein,

unpubl. obs.) also strongly support (1) a pelican/shoebill/

hammerkop clade, (2) a cormorant/anhinga/gannet grouping,

and (3) various clades within traditional charadriiforms

and gruiforms. Both c-myc and RAG-2 + morphology link

frigatebirds to the sulids, phalacrocoracids, and anhingids.

In an attempt to address problems of sparse taxon sampling

seen in previous studies, S. Stanley, J. Feinstein, and J.

Cracraft (unpubl. obs.) examined 57 waterbird taxa for 5319

base pairs of mitochondrial and nuclear RAG-2 sequences

(fig. 27.6). When palaeognaths and Galloanserae are used as

outgroups, the root of the waterbird tree was placed on one

of the two gruiform lineages, thus suggesting, in agreement

with Sibley and Ahlquist (1990) and van Tuinen et al. (2001),

that gruiforms are outside the other waterbird taxa, although

this is not strongly supported given available data. This larger

analysis still provides little resolution for higher level relationships

among waterbirds, but it does find support for a

grebe + flamingo relationship, monophyly of charadriiforms,

and the shoebill + pelicans + hammerkop clade, in agreement

with van Tuinen et al. (2001) and the c-myc data (fig. 27.4).

The buttonquails (Turnicidae) have traditionally been

considered members of the order Gruiformes. Recent molecular

analyses, however, now place them decisively with

the charadriiforms, and indeed they are the sister-group of

the Lari (Paton et al. 2003). The c-myc data (fig. 27.4) are

consistent with this topology and include a unique indel,

uniting turnicids and chradriiforms.

The mitochondrial and RAG-2 data also appear to contain

phylogenetic signal for other clades even though they

do not have high bootstrap values. Thus, when the data are

explored using a variety of methods (e.g., transversion parsimony),

the following groups are generally found (fig. 27.6):

(1) an expanded “pelecaniform” clade that also includes taxa

formerly placed in ciconiiforms (shoebill, hammerkop, ibises,

and storks), (2) a grouping of grebes and flamingos with

charadriiforms and some falconiforms, and (3) often a monophyletic

Falconiformes (although the family Falconidae

was not sampled), with no evidence of a relationship between

storks and New World vultures. Tropicbirds (phaethontids)

and herons (ardeids) represent divergent taxa that

have no stable position on the tree. Some of these relationships

are also seen in other data sets such as the c-myc data

(fig. 27.4) and in the mitochondrial data of van Tuinen et al.

(2001).

Phylogenetic Relationships among the Owls

(Strigiformes), Swifts and Hummingbirds

(Apodiformes), and Nightjars and Allies

(Caprimulgiformes)

The DNA hybridization tree (fig. 27.2; Sibley and Ahlquist

1990) recognizes a monophyletic Caprimulgiformes that is

the sister group of the owls; these two groups, in turn, are

the sister group of the turacos (Musophagidae), and finally,

all three are the sister clade of the swifts and hummingbirds

(Apodiformes). There is now clear evidence that this hypothesis

is not correct.

Phylogenetic Relationships among Modern Birds (Neornithes) 477

Both published and unpublished data have recently indicated

that caprimulgiforms are not monophyletic. Instead

of their traditional placement within caprimulgiforms, owletnightjars

(Aegothelidae) are most closely related to the swifts

and hummingbirds, a hypothesis first recognized in c-myc

nuclear sequences (Braun and Huddleston 2001; fig. 27.4).

This relationship is supported by morphological characters

(Mayr 2002) as well as by combined morphological and RAG-

2 data (fig. 27.7B) and by combined c-myc and RAG-2 data

(fig. 27.8). Even with the aegothelids removed from the

caprimulgiforms there is presently little support for the

monophyly of the remaining families. The available molecular

data for c-myc, RAG-2, or combined c-myc/RAG-2 (figs.

27.4, 27.7A, 27.8) do not unite them, nor do combined cmyc

and RAG-1 fragments (Johansson et al. 2001) or morphology

(Mayr 2002). The relationships of owls to various

caprimulgiform taxa are also not supported by available sequence

data (figs. 27.4, 27.7, 27.8; Johansson et al. 2001,

Mindell et al. 1997); however, one subsequent DNA hybridization

study has supported this hypothesis, in addition to

linking owls, caprimulgiforms, and apodiforms (Bleiweiss

et al. 1994). Preliminary morphological data also suggest a

relationship (Livezey and Zusi 2001).

Phylogenetic Relationships among “Higher Land

Birds”: Cuculiformes, Coraciiformes, Trogoniformes,

Coliiformes, and Piciformes

Few avian relationships are as interesting as those associated

with the “higher land bird” question, and it is a problem with

important implications for the overall topology of the neornithine

tree. Historically, groups such as the piciforms, coraci-

Figure 27.6. A phylogenetic

hypothesis for “waterbird”

higher taxa using 4164 base

pairs of mitochondrial sequence

(cytochrome b, COI, COII, COIII)

and 1155 base pairs of the RAG-

2 nuclear gene (transversion

weighted) using gruiform taxa as

the root (S. Stanley, J. Feinstein,

and J. Cracraft, unpubl. obs.).

Thick branches represent

interfamilial clades supported by

bootstrap values greater than

70% (all families had high

bootstrap values but are not

shown for simplicity).

Psophia

Grus canadensis

Aramus guarauna

Gavia pacificus

Gavia immer

Oceanodroma leucorhoa

Halocyptena microsoma

Puffinus griseus

Pterodroma cahow

Pterodroma lessoni

Pelecanoides magellani

Pelecanoides urinatrix

Pachyptila crassirostris

Fulmarus glacialoides

Diomedea nigripes

Diomedea bulleri

Oceanites oceanicus

Fregetta gralleria

Aechmophorus occidentalis

Podiceps auritus

Tachybaptus ruficollis

Podylimbus podiceps

Phoenicopterus minor

Phoenicopterus ruber

Actophilornis africanus

Stiltia isabella

Larus marinus

Sterna hirundo

Alca torda

Charadrius melodius

Vanellus chilensis

Cathartes aura

Coragyps atratus

Pandion haliaetus

Sagittarius serpentarius

Fregata magnificens

Fregata minor

Morus bassanus

Morus serrator

Sula sula

Phalacrocorax urile

Anhinga anhinga

Ciconia ciconia

Mycteria americana

Leptoptilos javanicus

Balaeniceps rex

Pelecanus erythrorynchos

Scopus umbretta

Eudocimus ruber

Pygoscelis antarctica

Pygoscelis papua

Spheniscus humboldti

Phaethon rubricauda

Phaethon lepturus

Butorides virescens

Egretta tricolor

Ixobrychus sinensis

Gruidae: cranes, limpkin

Gaviidae: loons

Procellariidae: petrels,

diving-petrels

Podicipedidae: grebes

Phoenicopteridae: flamingos

Jacanidae: jacanas

Glareolidae: pratincoles

Laridae: terns, gulls

Charadriidae: plovers

Cathartidae: New World vultures

Accipitridae: osprey

Sagittariidae: Secretarybird

Fregatidae: frigatebirds

Sulidae: boobies, gannets

Phalacrocoracidae: cormorants

Anhingidae: anhingas

Ciconiidae: storks

Balaenicipitidae: Shoebill

Pelecanidae: pelicans

Scopidae: Hammerkop

Threskiornithidae: ibises

Spheniscidae: penguins

Phaethontidae: tropicbirds

Ardeidae: herons

Psophiidae: trumpeters

Diomediidae: albatrosses

Alcidae: murres, auks

478 The Relationships of Animals: Deuterostomes

Figure 27.7. (A) A phylogenetic hypothesis for neoavian taxa using 1152 base pairs of the RAG-2

exon. (B) A phylogenetic tree based on 1152 base pairs of the RAG-2 exon and 166 morphological

characters. Analyses are all unweighted parsimony. Thick branches have greater than 70%

bootstrap support. Data from J. Cracraft, P. Schikler, J. Feinstein, P. Beresford, and G. J. Dyke

(unpubl. obs.).

tinamous

emus, cassowaries

kiwis

ostriches

rheas

pheasants, chickens

mound builders

ducks, geese

magpie goose

screamers

loons

storm-petrels

albatrosses

diving-petrels

prions

shearwaters

petrels

storm-petrels

grebes

rails, Sun-grebes

cranes, limpkins

trumpeters

mesites

Sunbittern, Kagu

seriamas

bustards

jacanas

pratincoles

gulls, terns, auks

plovers, oystercatchers

buttonquails

stilts, avocets, thick-knees

frigatebirds

boobies, gannets

cormorants, anhingas

tropicbirds

pelicans, Shoebill

Hammerkop

flamingos

ibises

storks

herons

New World vultures

osprey

falcons

Secretarybird

hawks, eagles

Hoatzin

turacos

cuckoos

parrots

pigeons

sandgrouse

barn owls

owls

swifts

hummingbirds

Oilbird

nightjars

owlet-nightjars

frogmouths

potoos

trogons

bee-eaters

rollers, ground-rollers

kingfishers

hornbills, hoopoes

todies

motmots

mousebirds

puffbirds, jacamars

woodpeckers, indicatorbirds

Old World barbets

toucans, New World barbets

Acanthisitta

Old & New World suboscines

basal Australian ТcorvidansУ

passeridan oscines

Australian robins

ТcorvidansУ

penguins

tinamous

emus, cassowaries

kiwis

ostriches

rheas

pheasants, chickens

mound builders

ducks, geese

screamers

loons

albatrosses

diving-petrels

shearwaters, petrels

grebes

rails, sungrebes

limpkin

cranes

trumpeters

mesites

Sunbittern, Kagu

seriamas

bustards

jacanas

pratincoles

gulls, terns, auks

plovers

oystercatchers

buttonquails

stilts, avocets, thick-knees

frigatebirds

boobies, gannets

cormorants, anhingas

tropicbirds

pelicans, Shoebill

Hammerkop

flamingos

ibises

storks

herons

New World vultures

osprey

falcons

Secretarybird

hawks, eagles

Hoatzin

turacos

cuckoos

parrots

pigeons

sandgrouse

owls

swifts

hummingbirds

Oilbird

nightjars, potoos

owlet-nightjars

frogmouths

trogons

bee-eaters

ground-rollers

kingfishers

hornbills, hoopoes

motmots

mousebirds

puffbirds, jacamars

woodpeckers, indicatorbirds

Old World barbets

toucans

New World barbets

passeriforms

penguins

rollers

A B

Phylogenetic Relationships among Modern Birds (Neornithes) 479

iforms, passeriforms, caprimulgiforms, and cuculiforms have

been associated with one another in various classifications

(e.g., Huxley 1867, Garrod 1874, Fьrbringer 1888) and have

been loosely called “higher land birds” (e.g., Olson 1985,

Feduccia 1999, Johansson et al. 2001). Here we discuss the

relationships within and among the coraciiform and piciform

birds, their placement on the neornithine tree, and their relationships

to the passeriforms.

Although the cuculiforms, coraciiforms, and piciforms

have long been seen as “higher” neornithines and often

closely related to passeriforms, this view was turned upside

down by the DNA hybridization tree (Sibley and Ahlquist

1990), which postulated that all three groups were at the base

of the neoavian tree (fig. 27.2). One of the two traditional

groups of piciforms, Pici, was placed near the base of the

neoavian tree adjacent to the turnicids, whereas the other,

the jacamars and puffbirds (Galbulae), was placed as the sister

group to a monophyletic “Coraciae,” including traditional

coraciiforms and trogons. The passeriforms were placed as

the sister group to the entire waterbird assemblage but were

not found to have any close relationship with either piciform

or coraciiform taxa.

At present, none of these relationships can be confirmed

or refuted. Available nuclear sequence data for RAG-1 (Groth

and Barrowclough 1999) as well as the c-myc and RAG-2 data

(figs. 27.4, 27.7) cannot resolve the base of Neoaves, indicating

that the placement of these (or other) groups within

neornithines remains an open question. Recent morphological

and molecular studies, however, are identifying some wellsupported

clades within these groups. The two major clades

of the piciforms, Pici and Galbulae, are each strongly monophyletic

in all studies (see figs. 27.4, 27.7A,B, 27.8; Johansson

et al. 2001), and evidence increasingly indicates that they are

sister taxa. Some data, including RAG-2 (fig. 27.7A) and fragments

of c-myc and RAG-1 (Johansson et al. 2001), cannot

resolve this issue, but a monophyletic Piciformes is supported

by morphology (Cracraft and Simpson 1981, Swierczewski

and Raikow 1981, Raikow and Cracraft 1983, Mayr et al.

Figure 27.8. Phylogenetic hypothesis from combined c-myc

and RAG-2 data for 69 taxa, analyzed by unweighted parsimony.

Branches with bootstrap support greater than 50% are

shown. Thick branches have greater than 70% bootstrap

support. To maximize the taxon overlap between data sets,

equivalent species were combined, and this is reflected in the

name given to the terminal node; for example, Gallus gallus was

sequenced for both genes, but two different species were

sequenced from Aegotheles, and species were sequenced from

two different genera of megapodes. Data from J. Harshman, M.

J. Braun, and J. Cracraft (unpubl. obs.).

Apteryx

Casuarius

Dromaius novaehollandiae

Rhea americana

Struthio camelus

Tinamus major

Coragyps atratus

Cathartes

Tockus

Upupa epops

Chordeiles

Eurostopodus

Batrachostomus

Podargus papuensis

strigid

Tyto alba

oscine

Pitta

Steatornis caripensis

Nyctibius

Podiceps

Phoenicopterus

Spheniscus humboldti

Gavia

Puffinus

columbid

pteroclid

Colius

Grus canadensis

rallid

Eurypyga helias

Ciconia

Opisthocomus hoazin

threskiornithid

psittacine

cacatuine

Turnix

Stiltia isabella

Burhinus

ardeid

Phalacrocorax

Sula

Phaethon rubricauda

Balaeniceps rex

Pelecanus

picid

Indicator

Lybius

ramphastid

Bucco

Galbula

musophagid

cuculiform

Chloroceryle

Momotus

coraciid

Trogon

Micrastur gilvicollis

Sagittarius serpentarius

Buteo

Fregata magnificens

Amazilia

phaethornithine

Chaetura

Aegotheles

Gallus gallus

megapodid

Anseranas semipalmata

Anas platyrhynchos

strong support from:

combined data and both data sets

combined data only

combined data and one separate data set

480 The Relationships of Animals: Deuterostomes

2003), longer c-myc sequences (fig. 27.4), RAG-2 + morphology

(fig. 27.7B), combined c-myc/RAG-2 data (fig. 27.8), and

by other nuclear sequences (Johansson and Ericson 2003).

Within Pici, it is now clear that the barbets are paraphyletic

and that some or all of the New World taxa are more closely

related to toucans (Burton 1984, Sibley and Ahlquist 1990,

Lanyon and Hall 1994, Prum 1988, Barker and Lanyon 2000,

Moyle 2004) than to other barbets; interrelationships within

the barbet and toucan clade still need additional work.

DNA hybridization data were interpreted as supporting a

monophyletic coraciiforms (Sibley and Ahlquist 1990). Although

recent DNA sequences are insufficient to test coraciiform

monophyly, they do show support for groups of families

traditionally placed within coraciiforms. There is now congruent

support, for example, for the monophyly of (1) hornbills

+ hoopoes/woodhoopoes (figs. 27.4, 27.7A,B, 27.8; Johansson

et al. 2001), (2) motmots + todies (Johansson et al. 2001), and

(3) kingfishers + motmots (figs. 27.4A, 27.7B, 27.8; Johansson

et al. 2001), and support for (4) the kingfisher/motmot clade

with the rollers (figs. 27.4, 27.7B, 27.8; Johansson et al. 2001).

Although they are clearly monophyletic (Hughes and

Baker 1999), the relationships of the cuckoos are very uncertain,

with no clear pattern across different studies. The

distinctive Hoatzin (Opisthocomus hoazin) has been variously

placed with galliforms (Cracraft 1981), cuculiforms (Sibley

and Ahlquist 1990, Mindell et al. 1997), or turacos (Hughes

and Baker 1999), yet there is no firm support in the c-myc

(fig. 27.4), mitochondrial and PEPCK data (fig. 27.5), or in

those from RAG-2 and morphology (fig. 27.7B; see also

Livezey and Zusi 2001) for any of these hypotheses. A relationship

to galliforms at least can be rejected: hoatzins are

clearly members of Neoaves, not Galloanserae (figs. 27.4,

27.5, 27.7A,B, 27.8; see also Sorenson et al. 2003).

Trogons and mousebirds are each so unique morphologically

that they have been placed in their own order, but both

have been allied to coraciiform and/or piciform birds by many

authors (for reviews, see Sibley and Ahlquist 1990, Espinosa

de los Monteros 2000). In recent years trogons have generally

been associated with various coraciiforms on the strength of

stapes morphology (Feduccia 1975), myology (Maurer and

Raikow 1981), and osteology (Livezey and Zusi 2001). Mousebird

relationships have been more difficult to ascertain, and no

clear picture has emerged. In the mitochondrial-PEPCK data

mousebirds group with parrots (fig. 27.5), whereas the RAG-2

gene is uninformative. The study of Espinosa de los Monteros

(2000) linked mousebirds with trogons and then that clade with

parrots. The problem is that all these groups are old, divergent

taxa with relatively little intrataxon diversity. Much more data

will be needed to resolve their relationships.

Phylogenetic Relationships within

the Perching Birds (Passeriformes)

The perching birds, order Passeriformes, comprise almost

60% of the extant species of birds. The monophyly of passeriforms

has long been accepted and is strongly supported

by a variety of studies, including those using morphological

or molecular data (Feduccia 1974, 1975, Raikow 1982, 1987;

see also figs. 27.4, 27.5, 27.7, 27.8). Our current understanding

of their basal relationships and biogeographic distributions

strongly suggests that the group is old, with an origin

probably more than 79 million years ago, well before the

Cretaceous–Tertiary extinction 65 million years ago (e.g.,

Paton et al. 2002) and on a late-stage Gondwana (Cracraft

2001, Barker et al. 2002, Ericson et al. 2002). Recent molecular

work using nuclear genes (Barker et al. 2002, Ericson

et al. 2002) supports the hypothesis that the New Zealand

wrens (Acanthisittidae) are the sister group to the remainder

of the passerines, and that the latter clade can be divided

into two sister lineages, the suboscines (Tyranni) and the

oscines (Passeri). Resolving relationships within the suboscines

and oscines has been complex, not only because of

the huge diversity (about 1200 and 4600 species, respectively)

but also because many of the traditional families are

neither monophyletic nor related as depicted in Sibley and

Ahlquist’s (1990) tree. Nuclear gene sequences, however, are

beginning to clarify phylogenetic patterns within this large

group. The results presented here summarize some ongoing

studies of the passerines, primarily using two nuclear genes

(RAG-1 and RAG-2; F. K. Barker, J. F. Feinstein, P. Schikler,

A. Cibois, and J. Cracraft, unpubl. obs.) with dense taxon

sampling, and represent the most comprehensive analysis of

passeriform relationships to date (4126 aligned positions for

146 taxa).

The DNA hybridization data were interpreted by Sibley

and Ahlquist (1990) as showing a division between suboscine

and oscine passerines with the New Zealand wrens being the

sister group to the remaining suboscines. Within the oscines,

there were two sister clades, Corvida, which consisted of all

Australian endemics and groups related to crows (the socalled

“corvine assemblage”), and Passerida for all remaining

taxa. The phylogenetic hypothesis shown in figure 27.9A,

which is based on nuclear gene data (F. K. Barker, J. F.

Feinstein, P. Schikler, A. Cibois, and J. Cracraft, unpubl.

obs.), depicts a substantially different view of passeriform

history. Thus, although the subdivision into suboscines and

oscines is corroborated, the New Zealand wrens are the sister

group of all other passerines. In addition, numerous taxa

of the Australian “corvidans” are complexly paraphyletic relative

to the passeridans and a core “Corvoidea.”

The suboscine taxon sample is small, but these nuclear

data are able to resolve a number of the major clades with

strong support (fig. 27.9B). New World and Old World

clades are sister groups (Irestedt et al. 2001, Barker et al.

2002). Within the Old World group, the data strongly support

the pittas as being the sister group of the paraphyletic

broadbills and the Malagasy asities (see also Prum 1993). The

New World suboscines are divisible into two large clades. The

first includes nearly 550 species of New World flycatchers,

manakins, and cotingas; although this clade is strongly supPhylogenetic

Relationships among Modern Birds (Neornithes) 481

Figure 27.9. Phylogenetic analyses from an analysis of 146 passeriform taxa for 4126 base pairs

of RAG-1 and RAG-2 exons using maximum parsimony. (A) Relationships among the basal

lineages. (B) Relationships among the suboscine passeriforms. (C) Relationships among the

passeridan songbirds. (D) Relationships among the basal oscines and corvidan songbirds. Data

from F. K. Barker, J. F. Feinstein, P. Schikler, A. Cibois, and J. Cracraft (unpubl. obs.).

New Zealand wrens

New World suboscines

Old World suboscines

lyrebirds, scrub-birds

Australian treecreepers

bowerbirds

fairy wrens

honeyeaters

pardalotes, scrubwrens

Australian babblers

logrunners

crows and allies (Corvida)

finches and allies (Passerida)

Australia

oscines

A N. W. suboscines

O. W. suboscines

New Zealand wrens

oscines

broadbills, asities

pittas

pipromorphine flycatchers

cotingas

tityrine flycatchers

manakins

tyrant flycatchers

woodcreepers

ovenbirds

formicariine antbirds

tapaculos

thamnophiline antbirds

B gnateaters

passeridan songbirds

mud-nest builders

melampittas

birds of paradise

monarch flycatchers

crows, jays

shrikes

rhipidurine flycatchers

drongos

wattle-eyes, batises

ioras

helmetshrikes

vanga shrikes

bush shrikes

currawongs, butcherbirds

wood-swallows

O. W. orioles

whistlers, shrike-thrushes

cuckooshrikes

tit berrypecker

shrike-tits

erpornis

vireos

pitohuis

crested bellbird

whipbirds

sittellas

berrypeckers, longbills

New Zealand wattlebirds

cnemophilines D

Malaconotoidea Corvoidea

Australian robins

bald crows, Chaetops

dippers

thrushes

O. W. flycatchers

mockingbirds, thrashers

starlings

waxwings

kinglets

nuthatches

tree-creepers

wrens

sugarbird and allies

fairy bluebirds

flowerpeckers

sunbirds

weavers, widowbirds

accentors

cardinals

tanagers

buntings, sparrows

orioles, blackbirds

N. W. warblers

chaffinches, bramblings

wagtails, pipits

titmice, chickadees

larks

swallows

cisticolid warblers

bulbuls

sylviid warblers

white-eyes

C babblers

Muscicapoidea

Sylvioidea Passeroidea Certhioidea

482 The Relationships of Animals: Deuterostomes

ported, relationships within the group are still uncertain (see

also Johansson et al. 2002). The remaining 560 species of

New World suboscines are split into the thamnophiline antbirds

and their sister clade, the formicarinine antbirds and

the ovenbirds and woodcreepers. The most thorough study

of New World suboscine relationships to date is that of

Irestedt et al. (2002), which examined more than 3000 base

pairs of nuclear and mitochondrial sequences for 32 ingroup

taxa of woodcreepers, ovenbirds, and antbirds; our results

are congruent with those reported in their study.

As noted, the oscines, or songbirds, have been subdivided

into two large assemblages, the Corvida and Passerida, based

on inferences from DNA hybridization. This simple partition

has been shown to be incorrect (Barker et al. 2002, Ericson

et al. 2002), but we are now able to tell a much more interesting

story because of a larger taxon sample. No fewer than

five distinctive Australian “corvidan” clades are sequential

sister groups to the core corvoid and passeridan clades

(Barker et al. 2002; see also F. K. Barker, J. F. Feinstein,

P. Schikler, A. Cibois, and J. Cracraft, unpubl. obs.): the lyrebirds

(Menuridae), the bowerbirds and Australian treecreepers

(Ptilonorhynchoidea), the diverse meliphagoid assemblage, the

pomotostomine babblers, and the orthonychid logrunners

(fig. 27.9A). This phylogenetic pattern firmly anchors the origin

of the oscines in East Gondwana.

But the story of corvidan paraphyly is not yet exhausted.

The passeridan clade has three basal clades (fig. 27.9C), one

of which is the Australian robins (Eopsaltridae), included by

DNA hybridization data within the corvidans. A second clade

is the peculiar African genus Picathartes, the bald crows or

rock-fowl, also placed toward the base of the passerines by

hybridization data (see Sibley and Ahlquist 1990: 625–626),

and its sister taxon, the rock-jumpers (Chaetops). Finally,

there are the core passeridans (Ericson et al. 2000, Barker

et al. 2002; see also F. K. Barker, J. F. Feinstein, P. Schikler,

A. Cibois, and J. Cracraft, unpubl. obs.). It is not clear from

the available data whether the Picathartes + Chaetops clade

or the eopsaltrids is the sister group of the core passeridans,

although present data suggest the robins are more closely

related.

The basal relationships of the core passeridans are still

unclear. There are four moderately well-defined clades within

the group (fig. 27.9C; see also Ericson and Johansson 2003).

The first, Sylvioidea, includes groups such as the titmice and

chickadees, larks, bulbuls, Old World warblers, white-eyes,

babblers, and swallows. The second, here termed Certhioidea,

consists of the wrens, nuthatches, and treecreepers. The third

is a very large group, Passeroidea, that includes various Old

World taxa basally—the fairy bluebirds, sunbirds, flowerpeckers,

sparrows, wagtails, and pipits—and the huge (almost

1000 species) so-called nine-primaried oscine assemblage

(Fringillidae of Monroe and Sibley 1993), most of which are

New World (Emberizinae: buntings, wood warblers, tanagers,

cardinals, and the orioles and blackbirds; for recent

discussions of relationships, see Groth 1998, Klicka et al.

2000, Lovette and Bermingham 2002, Yuri and Mindell 2002).

The last group of core passeridans is Muscicapoidea, which

encompasses the kinglets, waxwings, starlings, thrashers and

mockingbirds, and the large thrush and Old World flycatcher

clade of some 450 species.

With the elimination of the early “corvidan” clades discussed

above (fig. 27.9A), the remainder of Sibley and

Ahlquist’s “Corvida” do appear to form a monophyletic assemblage,

although it is not well supported at this time, and

we restrict the name “Corvida” to this clade (fig. 27.9D).

Although relationships among family-level taxa within this

complex cannot be completely resolved with RAG-1 and

RAG-2 sequences, these data do identify several well-defined

clades, and they partition relationships more satisfactorily

than previous work.

Two of the corvidan clades are well supported. The first

we term here Corvoidea, which include the crows and jays

(Corvidae) and their sister group, the true shrikes (Laniidae),

the monarch and rhipidurine flycatchers, drongos, mud-nest

builders (Struthidea, Corcorax), the two species of Melampitta,

and the birds of paradise (Paradisaeidae). The second wellsupported

lineage of the corvidans we term Malaconotoidea.

This “shrike-like” assemblage is comprised of the African bushshrikes

(Malaconotidae), the helmet shrikes (Prionops), Batis,

the Asian ioras (Aegithinidae), and the vanga shrikes (Vangidae)

of Madagascar. Also included in this clade are the woodswallows

(Artamidae) and their sister group the Australian

magpies and currawongs (Cracticidae).

All other corvidans appear to be basal to the corvoids and

malaconotoids but are, on present evidence, unresolved relative

to these two clades. Most of these groups, including the

pachycephalids, oriolids, campephagids, daphoenosittids,

falcunculids, and other assorted genera are mostly Australasian

in distribution, and presumably in origin. Also included in this

melange are the vireos and their Asian sister group, Erpornis

zantholeuca.

Outside of all these corvidan groups is a clade comprising

some ancient corvidans that appear to be related: the New

Zealand wattlebirds (Callaeatidae), the cnemophilines (formally

placed in the birds of paradise), and the berrypeckers

(Melanocharitidae). The basal position of these groups relative

to the remaining Corvida provides persuasive evidence

that the group as a whole had its origin in Australia (and

perhaps adjacent Antarctica), further tying the origins of the

oscine radiation to this landmass.

Discussion

Where We Are

To judge from the large numbers of papers reviewed above,

research on the higher level relationships of birds has made

significant progress over the last decade, yet it is obvious from

the results of these studies that compelling evidence for rePhylogenetic

Relationships among Modern Birds (Neornithes) 483

lationships among most major clades of Neoaves is still lacking.

Nevertheless, a function of this chapter is to serve as a

benchmark of our current understanding of avian relationships,

and one way expressing this progress is to propose a

summary hypothesis that attempts to reflect the improvements

in our knowledge of avian relationships, even though

the underlying evidence may be imperfect. Different investigators,

including the authors of this chapter, will disagree

about what constitutes sufficient evidence for supporting the

monophyly of a clade, and most would no doubt prefer to

see a tree that is based on all avian higher taxa and a very

large data set of molecular and morphological characters

numbering in the tens of thousands. That ideal is 5–10 years

away, however, yet it is still useful to examine how far have

we come over the last decade.

Figure 27.10 depicts a summary phylogenetic hypothesis

for the avian higher taxa. It represents an estimate of avian

history at this point in time and is admittedly speculative in

a number of places that we note below; it represents, moreover,

a compromise among the authors. We therefore have

no illusions that all of these relationships will stand the test

of time and evidence, but a number will. The thick lines are

meant to identify clades in which relatively strong evidence

for their monophyly has been discovered in one or more

individual studies. The thin lines depict clades that have been

recovered in various studies, even though the evidence for

these individual hypotheses may be weak. Congruence across

studies suggests that with more data, many of these clades

will gain increased support.

As already noted, the base of the neornithine tree is no

longer particularly controversial, with palaeognaths and then

Galloanserae being successive sister groups to Neoaves. Relationships

within ratites are unsettled, however, because of

conflict among the molecular data and with the morphological

evidence.

Neoavian relationships, on the other hand, are decidedly

uncertain, although new information becomes available

with each new study. The base of the neoavian tree is

a complete unknown, but within Neoaves evidence for relationships

among a number of major groups is emerging.

There is a suggestion that many of the traditional “waterbird”

groups are related, although a monophyletic assemblage

that includes all “waterbird” taxa itself is unlikely.

Thus, some “waterbird” taxa are definitely related, others

probably so, but other nonwaterbird taxa will almost certainly

be found to be embedded within waterbirds. It now

seems clear that some traditional groups such as Pelecaniformes

and Ciconiiformes are not monophyletic, but

many of their constituent taxa are related. Thus there is now

evidence for a shoebill + pelican + hammerkop clade and

for an anhinga + cormorant + gannet + (more marginally)

frigatebird clade, and these two clades are probably related

to each other, along with ibises, herons, and storks. Tropicbirds

(phaethontids) are a real puzzle as this old, longbranch

taxon is quite unstable on all trees. Figure 27.10. Summary hypothesis for avian higher level

relationships (see discussion in text).

tinamous (Tinamidae)

kiwis (Apterygidae)

cassowaries (Casuariidae)

emus (Dromiceidae)

ostriches (Struthionidae)

rheas (Rheidae)

ducks, geese, swans (Anatidae)

Magpie Goose (Anseranatidae)

screamers (Anhimidae)

megapodes Megapodiidae)

guans, currasows (Cracidae)

grouse, pheasants (Phasianidae)

N. W. quails (Odontophoridae)

guinea fowl (Numididae)

Limpkin (Aramidae)

cranes (Gruidae)

trumpeters (Psophiidae)

sun-grebes (Heliornithidae)

rails (Rallidae)

Sun-bittern (Eurypygidae)

Kagu (Rhynochetidae)

seriemas (Cariamidae)

bustards (Otididae)

mesites (Mesitornithidae)

ibises (Threskiornithidae)

Shoebill (Balaenicipitidae)

pelicans (Pelicanidae)

Hammerhead (Scopidae)

herons (Ardeidae)

storks (Ciconiidae)

boobies, gannets (Sulidae)

anhingas (Anhingidae)

cormorants (Phalacrocoracidae)

frigate-birds (Fregatidae)

tropicbirds (Phaethontidae)

flamingos (Phoenicopteridae)

grebes (Podicipedidae)

hawks, eagles (Accipitridae)

osprey (Pandionidae)

Secretary-bird (Sagittariidae)

N. W. vultures (Cathartidae)

falcons (Falconidae)

albatrosses (Diomediidae)

shearwaters, petrels (Procelariidae)

storm-petrels (Oceanitidae)

loons (Gaviidae)

penguins (Spheniscidae)

owls (Strigidae)

hummingbirds (Trochilidae)

swifts (Apodidae)

owlet-nightjars (Aegothelidae)

potoos (Nyctibiidae)

nightjars (Caprimulgidae)

Oilbird (Steatornithidae)

frogmouths (Podargidae)

turacos (Musophagidae)

Hoatzin (Opisthocomidae)

pigeons (Columbidae)

sandgrouse (Pteroclidae)

parrots (Psittacidae)

cuckoos (Cuculidae)

puffbirds (Bucconidae)

jacamars (Galbulidae)

O. W. barbets

toucans (Ramphastidae)

N. W. barbets

honeyguides (Indicatoridae)

woodpeckers (Picidae)

mousebirds (Coliidae)

trogons (Trogonidae)

hoopoes (Upupidae)

woodhoopoes (Phoeniculidae)

hornbills (Bucerotidae)

bee-eaters (Meropidae)

motmots (Momotidae)

todies (Todidae)

kingfishers (Alcidinidae)

cuckoo-roller (Leptosomatidae)

rollers (Coraciidae)

ground-rollers (Brachypteraciidae)

Oscine songbirds

Old World suboscines

New World suboscines

New Zealand wrens (Acanthisittidae)

button-quails (Turnicidae)

sandpipers (Scolopacidae)

sheathbill (Chionididae)

painted-snipe (Rostratulidae)

plains-wanderer (Pedionomidae)

seedsnipe (Thinocoridae)

pratincoles (Glareolidae)

auks (Alcidae)

gulls, terns (Laridae)

jacanas (Jacanidae)

plovers (Charadriidae)

oystercatchers (Haematopodidae)

thick-knees (Burhinidae)

stilts, avocets (Recurvirostridae)

484 The Relationships of Animals: Deuterostomes

There is a core group of gruiform taxa with well supported

relationships, including rails + sungrebes, on the one

hand, and cranes + limpkins + trumpeters, on the other.

Moreover, the kagu and sunbittern are strongly supported

sister taxa. Aside from some morphological character data

(e.g., Livezey 1998), there is little current evidence to support

monophyly of traditional Gruiformes. This is an old

group, with basal divergences almost certainly in the Cretaceous

(Cracraft 2001) that cannot be resolved given the character

data currently available; yet, there is no firm evidence

that any of these groups is related to a nongruiform taxon,

so we retain the traditional order.

Ongoing work in various labs is confirming the monophyly

of the charadriiforms, including the buttonquails, often

placed in gruiforms. Current sequence data (Paton et al.

2003) indicate the relationships shown in figure 27.10. There

is also a suggestion in the molecular data presented earlier

that charadriiforms are associated with flamingos + grebes,

and possibly with some or all of the falconiforms. The latter

group consists of three well defined clades (falcons,

cathartids, and accipitrids + osprey + secretary bird), but

whether these are related to each other is still uncertain.

Morphology indicates that they are, but molecular data cannot

yet confirm or deny this.

Relationships among the “higher land birds” remain controversial

in many cases. Swifts, hummingbirds, and owletnightjars

are monophyletic but their relationships to other

taxa traditionally called caprimulgiforms are unsupported;

as with gruiforms, we have no clear evidence that any of them

are more closely related to other taxa, and so we retain the

group. Whether owls cluster with these families is also uncertain.

Again, all of these taxa are very old groups and resolution

of their relationships will require more data.

The three “orders” Piciformes, Coraciiformes, and Passeriformes

may or may not be related to one another, but in

many studies subgroups of them are clustered together. More

and more data sets are showing a monophyletic piciforms.

Passeriforms are strongly monophyletic, and relationships

among their basal clades are becoming well understood (see

discussion above). Finally, the traditional coraciiforms group

into two clades whose relationships to each other are neither

supported nor refuted by our data. The relationships of

mousebirds and trogons are also still obscure.

In contrast to many of the above groups, there are some

highly distinctive taxa such as turacos, parrots, pigeons, the

hoatzin, and cuckoos that have been notoriously difficult to

associate with other groups using both molecular and morphological

data. Deciphering their relationships will require

larger amounts of data than are currently available.

Despite the appearance of substantial structure, the hypothesis

of figure 27.10 could be interpreted pessimistically

by examination of those clades subtended by thin branches—

indicating insufficient support—versus those with thickbranched

clades we judge to be either moderately or strongly

supported. Seen in this way, the tree is mostly a polytomy

and suggests we know very little about avian relationships.

Viewed more optimistically, however, the tree is a working

hypothesis that suggests progress is being made. Critically,

this representation of our state of knowledge contradicts the

false notion that the broad picture of avian phylogenetics has

been drawn, and only the details remain to be filled (e.g.,

Mooers and Cotgreave 1994). Given the state of current activity

in many laboratories around the world, we predict that

in little more than five years a similar figure, whatever its

configuration, will have a substantially larger proportion of

well-supported clades.

The Future

These are exciting and productive times for avian systematists.

We are witnessing the growth of molecular databases,

containing sequences from homologous genes across most

avian taxa. As recently as 10 years ago the availability of such

comprehensive, comparative, discrete character data sets was

little more than a dream. Within the next several years large

data sets for both molecular and morphological data will be

published that span all the major clades of nonpasseriform

birds. At the same time, avian systematics is becoming increasingly

collaborative with groups of researchers pooling

resources and publishing together. These collaborations involve

both molecular and morphological data and extend

back across time through the incorporation of fossils.

All of these data will soon be publicly available on the

Internet as a result of these collaborations, and these data

should greatly accelerate avian systematic research. Discretecharacter

data sets lend themselves to continual growth and

addition in a manner entirely absent from the early comprehensive

work based on DNA hybridization distances (Sibley

and Ahlquist 1990). These data sets will variously confirm,

challenge, or overturn earlier hypotheses of avian phylogeny,

and this may be expected to continue as both character and

taxon sampling increase. We view the continued collection

of comparative data as imperative not just for avian systematics,

but for elaborating the insight into evolutionary history

and processes at multiple hierarchical levels that only

phylogeny can provide.

The Challenge

Just how difficult will it be to build a comprehensive avian

Tree of Life (ATOL)? Several observations suggest it will be

extremely so. First, there are about 20,000 nodes on the

extant avian Tree of Life. Fossil taxa only add to that number.

Then, there is the challenge presented by the history of

birds itself. It is now evident that there have been many episodes

of rapid radiation across the neoavian tree, perhaps

involving thousands of nodes, and resolving these will require

unprecedented access to specimen material (including

anatomical preparations and fresh tissues) as well as large

character sampling to establish relationships. Gone are the

Phylogenetic Relationships among Modern Birds (Neornithes) 485

days when a single person or laboratory might hope to solve

the problem of avian relationships. The problem is too difficult

and complex for single laboratories in which time and

money are limited. The scientific challenge presented by the

avian Tree of Life will call for large taxon and character sampling,

goals best achieved by a communitywide effort.

There are also conceptual roadblocks. One is the problem

of uncertain knowledge. More taxa and characters may

not guarantee a “satisfying” answer, by which we mean having

resolution of nodes with sufficiently strong branch support

that additional data will merely confirm what has already

been found. The issue is that more taxa guarantee (some)

uncertainty. More taxa are good, of course, but they also

means more character data will likely be required to attain

strong support for any particular node. Measuring phylogenetic

understanding on very large trees such as the avian Tree

of Life will also be a complex challenge. Measures of support

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

study? How will we know when to stop (because it has been

determined we “know” relationships) and move on to an

unresolved part of the tree? This is a nontrivial problem, but

as we erect a scaffold that identifies strongly supported monophyletic

groups, perhaps that will make it easier to circumscribe

studies and resolve the tree more finely.

Another conceptual roadblock is the problem of investigator

tenacity. It should be straightforward to build the scaffold

of the avian Tree of Life. Systematists are doing that now.

There will be—and already are—lots of trees that are moderately

resolved but still have little satisfactory branch support

(remember that the DNA hybridization tree was nearly

“fully” resolved). So how much do we, the investigators, really

want to know relationships? If the object is to publish

more papers, then as more and more taxa are added, and if

character sampling does not also increase, more and more

nodes are likely to be supported rather poorly, especially

across those parts of the tree representing rapid radiations

(short internodes). Resolving these nodes with some measure

of confidence will require substantial amounts of data

(much more than is currently collected in typical studies).

In the near future, this may not be an issue as technical innovations

allow systematists to gather more data more rapidly.

However, many investigators will not necessarily have

easy access to these technologies, and it is already becoming

apparent that being able to collect large volumes of data (genomes)

does not necessarily mean that the data themselves

are going to be phylogenetically useful for the problem at

hand.

Although many phylogenetic problems in birds, at all

taxonomic levels, will be quite difficult to resolve, we must

be resolute. Resolving relationships is crucial for answering

numerous questions in evolutionary biology, and to the extent

that these questions are worth pursuing we should not

settle for not knowing phylogeny. One result emerging from

the studies discussed here illustrates this point. Evidence now

indicates owlet-nightjars are the sister group of swifts and

hummingbirds. Depending on the sister group of this clade,

it implies either that adaptation to nocturnal lifestyle arose

multiple times in aegothelids and other birds, or that nocturnal

habits are primitive and swifts and hummingbirds are

secondarily diurnal. Phylogeny thus provides important insight

into understanding avian diversification.

Finally, our perspectives on avian evolution will not be—

should not be—built on one kind of data. Tree topologies

should reflect the most comprehensive description of character

evolution over time, which means that all forms of character

information—genetic, morphological, behavioral, and

so forth—should be incorporated into analyses. They may

not only contribute to phylogenetic resolution in their own

right, but will give us a richer picture of the history of avian

evolution.

Acknowledgments

F.K.B., G.J.D., S.S., P.B., and A.C. all received support from the

AMNH F. M. Chapman Fund. Much of the research presented

in this chapter is supported by the AMNH Monell Molecular

Laboratory and Lewis B. and Dorothy Cullman Program for

Molecular Systematics Studies. Work on the c-myc gene

was aided by the able assistance of Chris Huddleston and

a Smithsonian postdoctoral fellowship to J.H. M.S. acknowledges

the help of Elen Oneal and support from the National

Science Foundation. Work by J.G.-M., D.P.M., M.D.S., and

T.Y. was supported by NSF grants DEB-9762427 and DBI-

9974525.

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