From extant to extinct: locomotorontogeny and the evolution ofavian flightAshley M. Heers and Kenneth P. Dial

Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA

Evolutionary transformations are recorded by fossils withtransitional morphologies, and are key to understandingthe history of life. Reconstructing these transformationsrequires interpreting functional attributes of extinctforms by exploring how similar features function in extantorganisms. However, extinct–extant comparisons are of-ten difficult, because extant adult forms frequently differsubstantially from fossil material. Here, we illustrate howpostnatal developmental transitions in extant birds canprovide rich and novel insights into evolutionary trans-formations in theropod dinosaurs. Although juvenileshave not been a focus of extinct–extant comparisons,developing juveniles in many groups transition throughintermediate morphological, functional and behavioralstages that anatomically and conceptually parallel evolu-tionary transformations. Exploring developmental transi-tions may thus disclose observable, ecologically relevantanswers to long puzzling evolutionary questions.

Evolutionary transformationsEvolutionary transformations are central to the history oflife. Throughout the 3–4-billion year saga of life on Earth,fossils with transitional morphologies have recorded large-scale evolutionary changes that are key for understandingthe origins of major clades and adaptations [1–3]. Toreconstruct these transformations, scientists attempt todeduce the functional attributes of extinct morphologicalforms by exploring how similar features function in oracross extant organisms. However, comparing extinctand extant organisms to interpret the functional capacitiesof fossils with transitional morphologies is often difficult,because transitional fossils occur as morphological mosaicsof ancestral and derived character states, with suites offeatures that are frequently absent in extant adults. There-fore, transitional fossils commonly appear to lack extanthomologs or analogs. Consequently, hypotheses concern-ing the functional attributes of such fossils often seemuntestable [4], constraining the ability to advance under-standing of evolutionary transformations.

Transitional features have long been known to occurin prenatal stages of extant organisms (e.g. gill slits inhumans [5]), but their functional significance is difficultto examine in these passive developmental stages. By

Review

Glossary

Asymmetric feathers: pennaceous feathers in which the vanes on either side of

the rachis (central shaft) are different widths, with the trailing edge vane

conspicuously wider than the leading edge vane; asymmetry is thought to help

stabilize primary flight feathers (along the metacarpals and phalanges) against

oncoming airflow.

Avialans: members of a group of theropod dinosaurs that has traditionally

included Archaeopteryx (the earliest ‘bird’) (cf. [80]) and living birds (Figure 1,

node E, main text).

Caudofemoral muscle: muscle that attaches to the tail and femur, and that

helps retract the hindlimb in non-avian reptiles.

Channelized wrist: wrist with restricted movement; in birds, a series of ridges

and grooves (ventral ridge of the carpometacarpus, V-shaped ulnare and

articular ridge of the ulna) in the wrist interlock and channelize movement.

Contour feathers: pennaceous feathers that cover the wings and body of a bird.

Controlled flapping descent (CFD): locomotor behavior used by juvenile birds

that involves flapping the wings to slow and control aerial descents.

Keel: large, bony structure projecting beneath the sternum of a bird, similar to

the keel on a boat; site for attachment of major flight muscles (pectoralis and

supracoracoideus).

Maniraptorans: members of a group of theropod dinosaurs (Figure 1, nodes B

and C, main text).

Manus: hand (metacarpals and phalanges); also known as the carpometacar-

pus in birds.

Ontogenetic transitional wing (OTW) hypothesis: hypothesis stating that

extinct theropods with protowings might have behaved similar to juvenile

birds, flapping their incipient wings to navigate three-dimensional environ-

ments by flap-running up steep terrains (wing-assisted incline running) and

using controlled flapping descents to come back down [66].

Ornithurines: members of a group of theropod dinosaurs, whose most basal

members are similar in appearance to extant birds (Figure 1, node H, main text).

Paravians: members of a group of theropod dinosaurs (Figure 1, node D, main

text).

Pennaceous feathers: feathers that have a rachis (central shaft) with barbs

attached to either side, forming vanes.

Plumulaceous feathers: ‘downy’ feathers that lack a rachis (central shaft).

Primary feathers: pennaceous feathers along the distal forelimb (metacarpals

and phalanges); in extant flight-capable adult birds, primary feathers are

asymmetric, whereas secondary feathers (along the ulna) are more symmetric.

Protowings: small, incipient wings that are often characterized by distally

unfurled and/or symmetric feathers, and that are often restricted to the distal

forelimb [secondary feathers (along the ulna) and/or tertial feathers (along the

humerus) not preserved].

Pygostyle: bony structure at the end of the tail in birds, formed by the fusion of

tail vertebrae; attachment site for the rectricial bulbs and associated muscles.

Pygostylians: members of a group of theropod dinosaurs (Figure 1, node F,

main text).

Rectricial bulbs: fibro-adipose structures, on either side of the pygostyle, that

encase the roots of the tail feathers; muscles associated with the rectricial

bulbs control tail fanning and orientation.

Symmetric feathers: pennaceous feathers in which the vanes on either side of

the rachis (central shaft) are approximately the same width.

Synsacrum: fused sacral vertebrae (in a bird).

Tertial feathers: pennaceous wing feathers that lie along the humerus,

between the elbow and the body.

Theropods: members of a group of dinosaurs that includes the most probable

ancestors of extant birds.

Triosseal canal: a bony channel typically formed by the coracoid, scapula and

furcula (bones in the shoulder girdle), through which the tendon of the

supracoracoideus (upstroke muscle) passes.

Corresponding author: Heers, A.M. (ashmheers@gmail.com).Keywords: ontogeny; paleontology; transitional stages; form-function; flight;evolution; birds; dinosaurs.

296 0169-5347/$ – see front matter � 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2011.12.003 Trends in Ecology and Evolution, May 2012, Vol. 27, No. 5

Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

Wing-assisted incline running (WAIR): a locomotor behavior used by juvenile

and adult birds that involves flapping the wings while running up steep slopes;

flapping generates aerodynamic forces that drive the feet into the substrate

and increase traction, thereby allowing birds to ascend steep obstacles within

their habitat.

contrast, postnatal ontogenetic trajectories among extantspecies offer rich opportunities for quantitatively investi-gating form and function in transitional stages [6–11,B.E. Jackson, unpublished results], yet are relatively unex-plored. Postnatal ontogeny has not been a focus of extinct–extant comparisons (Box 1), although many examplesdemonstrate that juveniles share unique similarities withtransitional fossils. Unlike passive prenatal stages, postna-tal juveniles make use of transitional morphologies to loco-mote and/or survive and thus actualize form–functionrelationships during morphological transformations. Forexample, during the transition from aquatic to terrestriallife, metamorphosing salamanders progress through sever-al morphological transformations (loss of tail fins, loss ofgills, etc.). These anatomical changes are similar to manyof those that occurred during the aquatic-to-terrestrial evo-lutionary transition in the ancestors of tetrapods [12].Therefore, investigating how morphological shifts influenceorgan function during developmental transitions in juvenilesalamanders might provide insight into the functioning oforgan systems during the evolutionary transition from fishto tetrapod. Similarly, immature mayflies rely on a transi-tional flapping behavior (surface-skimming) that requiresonly a small wing area and muscle power output, congruentwith the hypothesized small wings and muscles of earlywinged insects. Such a behavior might have facilitated the

Box 1. What is the relationship between ontogeny and

evolution?

For over a century, students of evolutionary biology have ridiculed

the Haeckelian slogan, ‘ontogeny recapitulates phylogeny’, to such

an extreme that any comparison between ontogeny and phylogeny

has been dangerous. Analyses have repeatedly demonstrated that a

literal or linear comparison of the ontogeny of a species and its

evolutionary history is unfounded and doomed to falsification [5].

Consequently, most extinct–extant comparisons have focused on

extant adult forms. In 1985, Stephen Jay Gould felt compelled to

recast the discussion into a more objective light, encouraging

scientists not to ‘throw the baby out with the bathwater’. Great

strides in the field of evo-devo have additionally demonstrated the

explanatory power of ontogenetic studies. After all, morphological

parallels between ontogeny and phylogeny are relatively common-

place: ‘the invalidity of (Haeckel’s) law has been demonstrated, so

often, and so conclusively, that it is easy to fall into the opposite

extreme and ignore the fact that many organisms that are highly

dissimilar as adults go through similar larval or embryonic stages’

[71]. Modern thinking thus regards evolution as a process that

modifies ontogeny, at any developmental stage, either by inserting

new characters or by altering existing characters [3]. Changes in

developmental timing can create parallels between ontogenetic and

evolutionary trajectories, coupled with differences because of the

addition or alteration of characters [5]. Development does not

progress through a linear sequence of ancestral adult stages as

Haeckel proposed, but immature organisms do retain subsets of

ancestral features that can be modified or lost later in ontogeny.

Developing organisms, in fact, might provide the only opportunity

for investigating form and corresponding function of transitional

morphologies and/or behaviors. The similarities between ontoge-

netic and evolutionary stages therefore offer a rich and relatively

unexploited opportunity for exploring the history of life.

evolution of insect flight [6]. Sea squirt larvae resemble ahypothesized stage of early chordate evolution and havebeen used to explore chordate and vertebrate origins [7],whereas marsupials use an ancestral amniote-like (quad-rate-articular) jaw joint for feeding early in postnatal devel-opment and can elucidate early mammalian evolution [9].Thus, ontogenetic trajectories and the functional capacitiesof juveniles with transitional morphologies can provide richand novel insight into a broad array of evolutionary trans-formations, by clarifying the potential functional capacitiesof fossils with similar transitional morphologies. This un-tapped utility of postnatal ontogeny is perhaps best illus-trated through one of the most highly debated and recentlyrejuvenated evolutionary discussions: the origin and evolu-tion of avian flight.

Ontogeny and evolution: a case studyThe origin of birds and of bird flight has attracted scientificattention since the advent of evolutionary theory [13].Based on numerous lines of evidence, it is now widelyaccepted that birds evolved from bipedal theropod dino-saurs [14–21] (see Glossary; Velociraptor and Tyrannosau-rus are well-known examples). By contrast, locomotorbehaviors (gliding, flap-running, etc.) that might havefacilitated the evolutionary acquisition of flight remain asource of contention (reviewed in [20]). Most origin-of-flightscenarios attempt to deduce behavioral attributes by qual-itatively comparing the morphologies of extinct theropodsto the morphologies of extant adult stages (birds, glidingmammals, etc.). However, relationships between morpho-logical form and locomotor function inferred by theseapproaches often lack the empirical evidence necessaryfor discriminating among alternative hypotheses. Thisconstraint stems from the fact that early winged theropodshad many transitional features [22] that are not repre-sented in extant adult animals. Juveniles have not com-monly been used for extinct–extant comparisons. Yet, aspost-hatching birds develop and acquire flight capacity,they transition through intermediate morphological, func-tional and behavioral stages [8,10,11] that conceptuallyand anatomically parallel the evolutionary acquisition offlight. These observable transitional stages provide aunique opportunity to assess empirically the functionalattributes of transitional features, and thereby improveunderstanding of early winged theropods and the evolutionof flight. Thus, developing birds might be underappreciat-ed but important homologs or analogs for transitionaltheropod fossils.

In this article, we explore recent advances in avianbiology and paleontology to demonstrate how ontogenetictransitions can elucidate evolutionary transformations. We(i) consolidate historical and recent origin-of-flight hypothe-ses to review existing frameworks for discussing theropodevolution; (ii) survey the richly expanding theropod–avianfossil record to highlight morphological trends most relevantto locomotor evolution; and (iii) set forth a quantitative,ontogenetic perspective for interpreting these trends andhelping to structure hypotheses on the origin and evolutionof avian flight. Our intention is to illustrate how locomotorontogeny can clarify potential locomotor capacities of tran-sitional theropod fossils, by elucidating relationships

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Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

between form, function and behavior during obligately bi-pedal to flight-capable transitions.

Hypotheses on the origin of avian flightBeginning with Williston (1879) [23] and Marsh (1880)[24], many hypotheses have been proposed to explainhow flight evolved in the theropod–avian lineage(Table 1, column A). However, no consensus has beenreached. This impasse seems to stem from two main fac-tors. First, hypotheses have historically been structuredthrough a highly polarized framework. Discussion haslargely focused on whether flight evolved in an arboreal

Table 1. Review of hypotheses on the evolution of avian flighta,b

A B

Hypothesis Behavioral context of incipient wings

Role of

hindlimbs

Wing-assisted incline

running (WAIR, OTW)

[1,2] Run

Thrust generation

for faster running

[3–6]

Running on water

(Jesus-Christ lizard)

[7,8]

Leaping biped [9,10] Run and jump

Insect net [11,12]

Predatory strike [13–15]

Wings for stability [16,17]

Running into headwind [18]

Intraspecific fighting [19] Stand and jump

Jumping model [20]

Ridge gliding [21–23] Run and jump

Controlled flapping

descent (CFD, OTW)

[2] Run

Arboreal gliding [24–44] Climb, � jump,

� aerodynamic

force

Pouncing predator [45] Climb, jump,

acquire prey

Flutter-gliding [46] Climb

aThe origin of bird flight has drawn scientific interest for more than a century, and seve

have mainly focused on whether flight evolved in an arboreal or terrestrial environmen

function relationships inferred by origin-of-flight hypotheses are not observed in li

experimental framework, it has been difficult to evaluate alternative hypotheses. Colu

locomotion. Sketch of theropod adapted from [79].

bNumbers in square brackets refer to sources listed in S1 in the supplementary mater

298

or terrestrial environment, via a gliding or flapping pre-cursor (arboreal and from ‘the trees-down’, or cursorial andfrom ‘the ground-up’?) (Table 1, column B; reviewed in[20]). However, this arboreal versus cursorial dichotomyis probably unrealistic and might be impeding researchprogress [25,26], given that extant birds (i) flap and glide;(ii) flap with and without hindlimb support; and (iii) oftenspend time in both terrestrial and arboreal habitats.

Second, experimental investigations and extant sup-port of proposed form–function relationships are ratherscant (Table 1, column C; see [27]). Because of the per-ceived lack of extant homologs or analogs, alternative

C

Proposed behavior

observed in extant

tetrapods?

Extant support for

inferred form–function

relationships?

Role of

forelimbs

Flap Yes: many birds [1,47–49]

No: birds do not

flap to run faster

No

Yes: basilisk lizards

(but do not flap),

aquatic birds

(takeoff, usually)

[8,50]

Flap No No

Flap, acquire

prey

Yes/No: some bats,

but not while running

and jumping

[51]

Yes: mammalian felids

jump and swipe, but

not birds or reptiles

No

Glide No No

No No

Flap Yes: many extant adult birds No

Yes: many extant birds

during takeoff, display,

or predator escape

[20]

Glide Yes: petrels, etc. [52,53]

Flap Yes: immature birds [2,54]

Glide, climb Yes: Draco, flying

squirrels, etc., but

not birds

[55,56]

Yes/No: swooping birds

do not climb to elevated

ambush sites

No

Glide, flap,

climb

Yes/No: immature birds

climb but do not glide

No

ral origin-of-flight hypotheses have been proposed (column A). These hypotheses

t, via a gliding or flapping precursor (column B). Many of the behaviors and form–

ving animals and/or lack experimental support (column C). Without an extant,

mn B images: solid lines, terrestrial (or aquatic) locomotion; dashed lines, aerial

ial online.

?

S

A+S

A+S

S

Variablefeathering

Pelvic fusion: 0→1

Unguals: 0→1Thoracic vertebrae: 0→1

Skeletal morphology

Compsognathidae: Ss,Sc

Ornithomimosauria

Therizinosauroidea: Be

Oviraptorosauria: Ca,Sm

Alvarezsauridae: Su

Troodontidae: Ji

Dromaeosauridae

Archaeopteryx

Confuciusornithidae:

Aves

Tyrannosauroidea: Di

Phylogeny Feathers Size

(C)

(A)

(B)

(D)

(E)S: Ji, Ar

A: Mi?: An, B, Je

S: Pe, B?: An

MiA+S:

?: So,Ve, RaS: An, B

Mi, Ar, JeA+S:

C (unnamed):Caudipteryx

H (Ornithurae) - Aves:Columba

(F)

~100 g - 25 kg

Zhongornis

Yixianornis, Yanornis

RaMiSoVe

Xi

JeDa

S: Ca, Sm1,Sm2 (also on ulna)

S: Ca, Sm1, Sm2,Pr

?: Eo, Co, Ch

Scapula: 0→ 1Glenoid fossa: 0→ 1

Coracoid:0 1Ulna shape: 0 →1

Semilunate carpal: 0→1Femur: 0→1Transition pt: 0→1

Thoracic vertebrae: 1→2

Tibiotarsus: 0→1Tarsometatarsus: 0→1

Pubis: 0→1Synsacrum: 0→~1

Tail: 1→ 2

Tail: 0→1

Tail: 2→3

Coracoid: 1→~2

Carpometacarpus: 0→1Metacarpals: 0→1

Keel: 0→1

(H)

A (Coelurosauria) - B (Maniraptora):Sinosauropteryx

~ 10kg - 100kg

~150 g - 100 kg

~100 g - 10 kg

~ 2 g - 12 kg(not including

flightlessspecies)

of featheredmembers

Feathers: 0

Feathers: 0→ 1

SapeornithidaeZj

Feathers: 2→ 3

Feathers: 3→ 4

Eo, Co, Ch

Tail: 3→4

Enantiornithes

A+S:

(G)

Pubis: 1→2

Tarsometatarsus: 1→2Metatarsals: 0→1

Tibiotarsus: 1→~2Digit III: 0→1

Sacral count: 0→1

Humeral condyles: 0→1

Ulna articulation: 0→1

?

Pr Yx

B

An

Feathers: 1→ 2

Pe

EnEx

Eo, Co, Ch

Uncinate: 0→1Sternal ribs: 0 →1

D (Paraves) - E (Avialae):

F (Pygostylia):

Archaeopteryx

Confuciusornis

Glenoid fossa: 1 →2 Triosseal canal: 0→1Keel: 1→2Humeral head: 0→1Metacarpals: 1→2→3Wrist: 0→1Digit II: 0 →1Unguals: 1→2

Sacral count: 1→ 2Synsacrum: 1→ 2Pelvic fusion: 1→ 2Metatarsals: 1→ 2Metatarsal V: 0→1

TRENDS in Ecology & Evolution

Figure 1. Trends in theropod–avian evolution. The evolution of flight in theropod dinosaurs was marked by many changes in skeletal morphology, feather morphology,

body size, and mass distribution (see main text, and S2–S6 for details). Clades indicated by capitalized letters, and feathered theropods by bold italics (all feathered

theropods up through the basal pygostylians included). Clade and theropod names, character state changes and sources listed in S2; though details of phylogenetic

relationships are unclear in some places (e.g. many basal taxa, Alvarezsaurids, Rahonavis, Archaeopteryx [80]), general trends appear to hold. Whole body images from

[81]; reprinted with permission of The Johns Hopkins University Press. Individual bone elements adapted from [81–84]; all individual bone elements correspond to the

featured theropod. Pennaceous and non-pennaceous feathers indicated by black and gray shading, respectively; (S): symmetric feathers, (A): asymmetric feathers, (?):

feather structure probably pennaceous but poorly preserved or not well documented. Body size estimates based on adult theropods (see S2 for details), though smaller

feathered juveniles have been described (e.g. Epidendrosaurus [77]).

Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

299

Box 2. Evolution of skeletal morphology in the theropod–

avian lineage

The evolutionary acquisition of avian flight involved many changes

in forelimb and hindlimb morphology. In the forelimb apparatus,

the pectoral (shoulder) girdle became larger and more rigid, the

shoulder joint was elevated and dorsolaterally rotated, and a

triosseal canal was formed. The forelimb was lengthened and

strengthened, and many bony elements were fused or lost distally

[14,16,40,72]. Simultaneously, the trunk was gradually shortened

and stiffened [40,73,74]. These skeletal transitions collectively seem

to indicate an increase in size and strength of the flight apparatus,

an increase in stroke amplitude and more channelized limb move-

ments coupled with a less grasping manus (see S4 in the

supplementary material online) [14,16,40,72]. Given that the assem-

bly of the flight apparatus began early (in wingless theropods;

Figure 1, node B, main text) and culminated relatively late (Figure 1,

node H, main text) long after the evolutionary appearance of wings,

skeletal changes might have initially occurred in conjunction with

non-flight behaviors (climbing trees [75], wing-assisted incline

running [8,53,66], etc.).

In the hindlimb apparatus, pelvic girdle elements were expanded

and fused, and the pubis shifted from being cranially to caudally

directed. Distal bony elements in the limb were fused or lost, and the

foot became more gracile and, in many cases, acquired features

associated with prehensility (see S5 in the supplementary material

online) [43–45,76]. Concurrently, tail length and caudofemoral muscle

mass were gradually reduced [41,42]. In combination, such changes

are probably indicative of an increase in pelvic strength, an increase in

stride length and knee-based movements, an increase in foot

prehensility, and a tail liberated from terrestrial locomotion while

beginning to contribute to aerial locomotion [41–45,76]. During these

shifts, the hindlimb apparatus remained a conspicuous component of

theropod anatomy, and might have facilitated the evolutionary

acquisition of flight through a variety of behaviors (flap-running

[8,53,66], climbing trees [77], launching and landing [78], etc.).

Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

origin-of-flight scenarios have been evaluated primarilythrough mathematical models and computer simulations,or reconstruction and physical manipulation of fossilizedmaterial [28–30]. Yet even models and simulations requirevalidation through analysis of extant organisms and sen-sitivity analyses of unknown parameters [27]. By growingconsensus, more experimental and more rigorous hypoth-esis tests using extant organisms are therefore key toprogressing beyond the current level of understanding[17,25,27,31–38]. Evolutionary hypotheses must not onlybe congruent with the fossil record [37], but also be sup-ported by experimental and ecological evidence concern-ing form–function relationships in and across extantorganisms.

The fossil record: morphological trends duringtheropod–avian evolutionOrigin-of-flight investigations were once impeded by a lackof fossil material. However, the morphological gap previ-ously left by Archaeopteryx (described in 1861) and ahandful of ornithurines (described during the 1870s) isnow being filled with discoveries of feathered dinosaursand early birds, especially from China [18,39]. Althoughlong elusive and still somewhat puzzling, such fossils arekey to understanding the evolution of bird flight. Thesenew finds illustrate how the evolutionary assembly of theavian body plan began in bipedal predatory theropods withsmall forelimbs and large hindlimbs and tails, and pro-gressed through a series of increasingly bird-like, transi-tional anatomical stages. This progression, and theresulting acquisition of flight, involved a complex mosaicof changes in skeletal morphology, feather morphology,body size and mass distribution (Figure 1).

Skeletal morphology

The evolutionary acquisition of avian flight was associatedwith numerous changes in the musculoskeletal system(Figure 1; see S3 in the supplementary material online).Most conspicuously, the pectoral (shoulder) and pelvicgirdles were enlarged and strengthened, the forelimbwas lengthened and lost its grasping capacity, while thehindlimb was liberated from the tail and, in some groups,acquired features associated with prehensility [14,16,40–

45]. These changes signify several shifts in fore- andhindlimb capacity and function, resulting in a forelimbapparatus capable of flapping flight, and a hindlimb appa-ratus that retained ambulatory capacity while shiftingfrom hip- to knee-based locomotion (Box 2). Overall, ithas become clear that evolutionary transitions towardthe skeletal structure of extant birds occurred graduallyand were completed relatively late, long after the evolu-tionary appearance of wings. As demonstrated by a grow-ing number of well-preserved fossils, bird-like wings werecoupled with transitional skeletons during the earlyphases of flight evolution.

Feather morphology

Both feathers and wings appeared in non-avian theropoddinosaurs. These fossils illustrate a trend of increasingfeather complexity and distribution (see S6 in the supple-mentary material online). Feathers initially appeared as

300

fibrous or plumulaceous structures (Figure 1, node A). Such‘downy’ feathers were complemented in maniraptorans byserially branched feathers or symmetric pennaceous feath-ers arranged in ‘fans’ along the distal tail and as ‘protowings’along the manus and sometimes ulna (Figure 1, node C).Possible contour feathers and asymmetric pennaceousfeathers appeared in paravians, with asymmetric feathersoccurring as bird-like wings on the distal forelimb (tertialsabsent or not preserved) and, occasionally, along the hin-dlimbs and tail (Figure 1, node D). Pennaceous featherstherefore became more widely distributed and more asym-metric in more derived theropods, although a fully moderncomplement of feathers (including tertials and a tail fanwith rectricial bulb) might not have evolved until theornithurines (Figure 1, node H). Although widely discussed,the functional implications of this progression remain some-what enigmatic, because extant flight-capable adult birdshave asymmetric primary feathers and fully feathered fore-limbs that are very different from the symmetric feathersand protowings of extinct theropods (reviewed in [18,46,47]).Feather and wing evolution thus proceeded through a seriesof transitional morphological stages in theropods with tran-sitional skeletal morphologies and, presumably, intermedi-ate locomotor capacities.

Body size and distribution of mass

In addition to changes in feather and skeletal morphology,it is becoming apparent that the debut of winged theropodswas preceded by weight reduction, and accompanied and

Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

followed by an anterior shift in the center of mass. Basaltheropods were often massive, whereas basal maniraptor-ans (Figure 1, node C) were often turkey-sized or smaller,and basal paravians (Figure 1, node D) were frequentlycrow-sized or smaller [48–52]. Following the appearance ofavialans (Figure 1, node E), the shoulder girdle becamemore robust and the tail was reduced, presumably result-ing in an anterior shift in the center of mass (from thepelvic girdle region towards the shoulder girdle region)[41]. Given that the evolution of a bird-like shoulder regionwith an abbreviated tail and pelvic musculature occurredafter the appearance of small body size and bird-like wings,aerodynamic capacity might have evolved in small ther-opods with distributions of mass that were very differentfrom those of extant adult birds. Hindlimb support (duringflap-running [53], four-winged flying [54], etc.) might havebeen necessary to: (i) compensate for inadequate lift pro-duction by incipient wings; (ii) compensate for limitedpower output by small flight muscles; and/or (iii) maintainbalance if the center of mass in incipiently flight-capable,long-tailed animals was located far posterior to the centerof lift of the wings.

In summary, the recent era of fossil discovery hasprovided a long elusive, yet rich illustration of morpholog-ical evolution in the theropod–avian lineage, by elucidat-ing trends in skeletal morphology, feather morphology,body size and mass distribution (Figure 1, Box 2, see S3–S6in the supplementary material online). Yet interpreta-tions of these trends generally lack empirical and experi-mental support, because of the perceived lack of extanthomologs or analogs for (i) transitional locomotor beha-viors and capacities; (ii) transitional skeletons coupledwith bird-like wings; (iii) protowings and symmetric feath-ers; and (iv) bird-like wings coupled with a relativelyposterior center of mass (large legs and tail, and smallflight apparatus). It is becoming evident, however, thatthese transitional features are all represented in develop-ing juvenile birds [8,10,11, B.E. Jackson, unpublishedresults]. Thus, locomotor ontogeny could greatly advanceunderstanding of theropod–avian evolution, by providingunique but underappreciated opportunities for quantify-ing form–function relationships in transitional stages(bullets below).

Locomotor ontogeny: form and function duringdevelopmental transitionsExtant adult birds have many diagnostic morphologicalfeatures that are probably adaptations for flight (largekeel, channelized wrist, rigid trunk, fused pelvic elements,pygostyle, asymmetric feathers, etc.), and that were absentin winged maniraptorans and early birds (Figure 1, ap-proximately nodes C–F) [20,40]. Origin-of-flight hypothe-ses have often assumed, in the absence of such features,that early winged theropods were not powerful flappers(unossified or non-existent keels), were not capable of amodern style wingstroke (unchannelized wrists) and didnot use their feathers for aerodynamic force production(symmetrically vaned feathers) [34,40,55–57]. However,these and other assumptions about transitional morphol-ogies have not been tested, and most origin-of-flight sce-narios remain conjectural.

One avenue for exploring questions that cannot beanswered using extant adult animals relies on computersimulations and biomechanical testing of models [58,59].This approach is particularly promising when coupledwith experimental data from live organisms in ecologicalsettings. Locomotor strategies used by developing birds,for example, are relatively unexplored (cf. [8,10,60–62]),yet potentially disclose credible locomotor strategies usedby incipiently flight-capable theropods for at least fourreasons:

� Stages of locomotor development conceptually parallelstages of locomotor evolution. Similar to extinct ther-opods with protowings and/or transitional skeletons(Figure 1, approximately nodes C–F), juvenile birds relyon behaviors that bridge the bipedal to flight-capabletransition (Figure 2). Immature birds often engage theirlegs and underdeveloped ‘protowings’ simultaneouslywhile swimming underwater [e.g. hoatzin (Opisthoco-mus hoazin) chicks] [63]), flap-rowing across water [e.g.mallard (Anas platyrhynchos), merganser (Mergusmerganser) (T.R. Dial, unpublished results) and passeri-form chicks (http://dbs.umt.edu/flightlab/)], or flap-running up slopes [8] to escape predators and reachrefugia. These and other transitional behaviors enableimmature birds to supplement their wings with theirlegs, until their flight apparatus becomes stronger andeffective enough to support their body weight complete-ly. In short, the developmental transition from obligate-ly bipedal to flight-capable reveals ecologically relevantbehaviors that might have facilitated the evolutionaryacquisition of flight.

� Stages of skeletal development approximately parallelstages of skeletal evolution. Similar to many fossilizedtheropods, but unlike their adult counterparts, imma-ture chukar (Alectoris chukar; and presumably juvenilesof other precocial species: see ‘puna tinamou’ and‘hoatzin’ at http://www.digimorph.org/) have unfusedthoracic vertebrae, an unfused synsacrum and smallpelvis, an extremely small keel, no V-shaped ulnare(wrist bone) and tarsal (ankle) bones that are not fusedto the tibia or metatarsus. These and other featuresgradually become more adult-like throughout ontogeny.Many transitional skeletal stages ‘unique’ to extincttheropods are therefore present in comparable form indeveloping birds (Figure 3).Skeletal development in precocial birds can help clarifythe evolution of musculoskeletal function, because post-hatching juvenile birds use their ‘dinosaur-like’, tran-sitioning skeletons to locomote and survive. Althoughtheir locomotor apparatus lacks many of the skeletalhallmarks of advanced flight capacity (large keel,channelized wrist, etc.), juveniles are neverthelesscapable of impressive flap-running behaviors(Figure 2a,b), and even engage in brief level flights(Figure 2b). Tracking skeletal morphology, skeletalmovement, bone loading and muscle activity duringthese behaviors and throughout ontogeny can revealform–function relationships of transitional features andelucidate possible functions of similar features in extincttheropods (see S7 in the supplementary material

301

P7

Toscale

P10P9

(a) Juvenile chukar(7-8 dph):

WAIR, CFD

(b) Juvenile chukar(18-20 dph):

WAIR, CFD, brief flight

(c) Adult chukar(~100 dph):

WAIR, flight

TRENDS in Ecology & Evolution

Figure 2. Functional locomotor stages during ontogeny. Precocial ground birds use transitional morphologies to perform impressive behaviors as they develop and acquire

flight capacity [8,10,11,60–62]. (a) 7–8-day-old chukar (Alectoris chukar) rely on distally unfurled, approximately symmetric feathers and extremely underdeveloped

skeletons for wing-assisted incline running (WAIR) and controlled flapping descent (CFD). (b) 18–20-day-old chukar, with mostly unfurled approximately asymmetric

feathers and slightly more developed skeletons, are capable of brief flight in addition to WAIR and CFD. (c) Adult, flight-capable chukar have fully unfurled, asymmetric

feathers and robust skeletons. These patterns suggest that the development of flight in birds conceptually parallels the evolution of flight in dinosaurs: during both

ontogeny and evolution (presumably), flight-incapable animals transition(ed) through intermediate morphological, functional and behavioral stages while acquiring flight

capacity. P7, P9, P10: primary feathers 7, 9, and 10, respectively. Pedal digits and tertial feathers not shown, for simplicity. Abbreviation: dph, days post-hatching.

Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

online). For instance, it has been hypothesized thatlocomotor strategies requiring less pectoral musclepower, lower wingstroke amplitudes and less complexkinematics were important during the early stages offlight evolution [40,56]. These hypotheses are based onthe fact that paravians with bird-like wings (Figure 1,node D) lacked the specialized joint morphologies ofextant flight-capable adult birds, and retained clawsand a relatively gracile flight apparatus compared withextant flight-capable adult birds (no ossified keel,slender coracoids, unfused metacarpals, etc. [40,56];Figure 1; see S3 in the supplementary material online).Hypothesized form–function relationships can beassessed in extant juvenile birds by quantifying musclepower output [B.E. Jackson, unpublished results] andwingstroke kinematics [11] in developmental stagesthat have adult-like wings but underdeveloped skele-tons (e.g. 15–20-day-old chukar). Thus, locomotorontogeny can be quantitatively assessed to help eluci-date the evolution of musculoskeletal function intransitional forms.

� Stages of feather development approximately parallelstages of feather evolution. Ontogenetic trajectories inthe feather morphology of chukar and other birds bear astriking resemblance to evolutionary trajectories infeather morphology of theropod dinosaurs (Figures 2and 3) [8,10]. Younger birds and more basal theropodshave protowings with distally unfurled (6–8-day-old

302

chukar; Similicaudipteryx STM4-1 [64]) and relativelysymmetric (6–14-day-old chukar; Caudipteryx [65] andSimilicaudipteryx [64]) primary flight feathers, whichare often oriented obliquely to airflow (6-day-old chukar;Caudipteryx [65]). By contrast, older birds and morederived theropods typically have wings with asymmet-ric and fully vaned flight feathers, and distal primariesoriented roughly parallel to the manus (>20-day-oldchukar; Microraptor [54] and Archaeopteryx [47]).Ontogenetic and evolutionary trajectories are thusremarkably similar.Given these similar morphological trajectories, wingand feather ontogeny can help illuminate the evolutionof aerodynamic capacity. Immature birds flap theirunderdeveloped feathers and protowings during anarray of behaviors (Figure 2), and generate usefulaerodynamic forces that increase with wing maturationand culminate in full flight capacity [10,62]. Using windtunnels, propeller models and particle image velocime-try (see S7 in the supplementary material online) toquantify ontogenetic trajectories in feather morphologyand aerodynamic performance can therefore clarify howsimilar-looking feathers might have functioned duringthe early phases of flight evolution. Preliminary workwith juvenile birds indicates that feathers might have:(i) initially provided thermal insulation (plumulaceousfeathers; <6-day-old chukar; Figure 1, node A) [18]; (ii)later become important for transitional locomotor

20dph

FeathersTrunk Pelvic girdle, tailManus AnklePectoral girdle

Extantjuvenilechukar

(7-8 dphunless specified)

Extantadult

chukar(~100 dph)

Extinctfeatheredtheropods

(b)

Cartilaginouskeel?

(c)

(a)

TRENDS in Ecology & Evolution

Figure 3. Anatomical similarities between juvenile birds and extinct theropods. Juvenile birds (a) have transitional skeletal and feather morphologies that are strikingly

similar to those of extinct theropods (b) but absent in adult birds (c) [8,10]. Although theropod fossils have been mainly compared to adult birds, the conceptual (Figure 2)

and anatomical similarities between extinct theropods and juvenile birds suggest that comparisons with juveniles are appropriate. Locomotor ontogeny provides a unique

and rich opportunity to explore form–function relationships of transitional features and to better understand theropod evolution. Extinct feathered theropods (b): pectoral

girdle of Archaeopteryx [40], manus of Archaeopteryx [17], trunk of Sapeornis [85], pelvic girdle and tail of Confuciusornis [82] and ankle of Caudipteryx [65,86]. Feathers of

Similicaudipteryx STM4-1 (left), Similicaudipteryx STM22-6 and Caudipteryx and Anchiornis (middle), and Microraptor and Archaeopteryx (right) [64]. Images adapted from

[17,40,64,65,82,85,86]. Abbreviation: dph, days post-hatching.

Review Trends in Ecology and Evolution May 2012, Vol. 27, No. 5

behaviors, such as wing-assisted incline running andcontrolled flapping descent (protowings with approxi-mately symmetric feathers on the ulna and/or manus; 6–

14-day-old chukar; Figure 1, node C) [8,53,66]; and (iii)eventually become co-opted for flapping and glidingflight (wings with asymmetric and symmetric feathersalong entire forelimb; approximately 20-day-old chukar;Figure 1, possibly nodes D, E or F). In short, developingbirds actualize potential functions of transitional wingsand feathers.

� Changes in body size during development help elucidatethe allometry of locomotor capacity. Extinct theropodsspanned a large range of body sizes [50], andcharacterizing the relationship between body sizeand locomotor capacity is therefore crucial for under-standing locomotor evolution. Although small non-avian theropods were not common discoveries untilrelatively recently, weight reduction has beenexpected to parallel the evolutionary transitiontowards powered flight because body mass constrainsflight performance (vertical flight, acceleration andmaneuverability) [67–69]. For example, extant flight-capable birds generally do not exceed 15 kg, and thepower margin (i.e. the difference between power

available and power required for flight) decreases asmass increases [67,70]. Similarly, ontogeneticincreases in wing loading in brush turkeys reduceflapping performance [61] (although different develop-mental trajectories probably occur in different spe-cies). These allometric relationships illustrate theconstraints of large body size on flight capacity, andsuggest that weight reduction in theropods (Figure 1)facilitated flight evolution.

In summary, the developmental acquisition of flight inbirds can provide a wealth of insight into the evolutionaryacquisition of flight in theropods. In both cases (presum-ably), flight-incapable animals transition(ed) through in-termediate morphological, functional and behavioralstages before becoming flight-capable. Developing birdsuse extremely underdeveloped, remarkably ‘dinosaur-like’skeletons and feathers to perform a variety of locomotorbehaviors, and thus help bring to life form–function rela-tionships of transitional morphologies that havehistorically been impossible to quantify in extant animals.When couched within the continuum of locomotor strate-gies among extant birds, insight from examining ontoge-netic transitions in form, function and behavior may

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greatly improve understanding of locomotor evolution intheropod dinosaurs.

Concluding remarksExploring ontogenetic trajectories and functional capabili-ties of extant juveniles can clarify the functional capacitiesof transitional fossils and provide rich insight into dinosaurevolution and a broad array of evolutionary transforma-tions. Developing juveniles of many taxa (birds, as well assea squirts, marsupials, etc. [5,7–11]) have subsets ofmorphological features that are often similar to subsetsof anatomical features in transitional fossils. These simi-larities offer unique opportunities for exploring form andfunction in transitional stages, and enriching the investi-gation of evolutionary history.

Postnatal ontogeny is only now beginning to become afocus of extinct–extant comparisons (Box 1). By using newtechniques (see S7 in the supplementary material online)to examine developmental transitions, scientists may beable to seek observable and ecologically relevant answersto long puzzling evolutionary questions. Here, we haveillustrated how locomotor ontogeny among extant birdscan clarify potential locomotor capacities of transitionaltheropod fossils, by elucidating relationships betweenform, function and behavior during obligately bipedal toflight-capable transitions. Juvenile birds share manyunique similarities with extinct theropod dinosaurs (Fig-ures 1-3), and perform an array of impressive behaviors byusing underdeveloped skeletons and protowings that areremarkably similar to the transitional skeletons and pro-towings of extinct theropods. These similarities betweendeveloping birds and extinct theropods are merely oneexample of many parallels between ontogeny and evolution[5–7,9]. Thus, future collaborations between scientists whostudy the extant (e.g. developmental biologists, behavior-alists, ecologists and experimental functional morpholo-gists) and extinct (paleontologists) will surely enhance theexploration of the history of life.

AcknowledgmentsThe authors wish to thank Brandon Jackson, Bret Tobalske, and RayCallaway for their valuable input. Special thanks are extended to TomMartin for help with manuscript revisions. Supported by NSF grantsGRFP-2007057068 (AMH) and NSF IOS 0822378 (KPD).

Appendix A. Supplementary dataSupplementary data associated with this article canbe found, in the online version, at doi:10.1016/j.tree.2011.12.003.

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