A Phylogenomic Study of Birds Reveals Their Evolutionary History
Shannon J. Hackett et al.
Science 320, 1763 (2008);
DOI: 10.1126/science.1157704

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A Phylogenomic Study of Birds
Reveals Their Evolutionary History
Shannon J. Hackett,1* Rebecca T. Kimball,2*† Sushma Reddy,1* Rauri C. K. Bowie,1,3,4
Edward L. Braun,2 Michael J. Braun,5,6 Jena L. Chojnowski,2 W. Andrew Cox,2
Kin-Lan Han,2,5,6 John Harshman,1,7 Christopher J. Huddleston,5 Ben D. Marks,8Kathleen J. Miglia,9 William S. Moore,9 Frederick H. Sheldon,8 David W. Steadman,10
Christopher C. Witt,8,11 Tamaki Yuri2,5
Deep avian evolutionary relationships have been difficult to resolve as a result of a putative
explosive radiation. Our study examined ~32 kilobases of aligned nuclear DNA sequences from 19
independent loci for 169 species, representing all major extant groups, and recovered a robust
phylogeny from a genome-wide signal supported by multiple analytical methods. We documented
well-supported, previously unrecognized interordinal relationships (such as a sister relationshipbetween passerines and parrots) and corroborated previously contentious groupings (such as
flamingos and grebes). Our conclusions challenge current classifications and alter our
understanding of trait evolution; for example, some diurnal birds evolved from nocturnal ancestors.
Our results provide a valuable resource for phylogenetic and comparative studies in birds.
lthough well studied, the evolutionary
relationships among major avian groups
are contentious (1–6). Recovering deep
evolutionary relationships in birds is difficult,probably reflecting a rapid divergence early intheir evolutionary history (1–3, 7, 8) that has
resulted in many distinctive, morphologically cohesive groups (e.g., owls, parrots, and doves) withfew, if any, extant intermediary forms linking
them to other well-defined groups. This extreme
radiation also makes it difficult to place fossil taxa,
which further contributes to the difficulty in precisely timing avian divergences (3, 9).
Only two nodes at the base of the avian tree
are consistently supported by both molecular andmorphological phylogenetic studies (2–5, 10–14).
The first divides the Paleognathae (ratites andtinamous) and Neognathae (all other birds), andthe second splits the neognaths between the
Galloanserae (chickens, ducks, and allies) andNeoaves (other neognaths). Although the Neoaves
represents the majority of avian diversity (95% ofA

1
Zoology Department, Field Museum of Natural History,
1400 South Lake Shore Drive, Chicago, IL 60605, USA.
2
Department of Zoology, University of Florida, Gainesville,
FL 32611, USA. 3Museum of Vertebrate Zoology andDepartment of Integrative Biology, University of California,
Berkeley, CA 94720, USA. 4Department of Science andTechnology–National Research Foundation Centre of
Excellence at the Percy FitzPatrick Institute, Departmentof Botany and Zoology, Stellenbosch University, Matieland
7602, South Africa. 5Department of Vertebrate Zoology,
Smithsonian Institution, 4210 Silver Hill Road, Suitland,
MD 20746, USA. 6Behavior, Ecology, Evolution, andSystematics Program, University of Maryland, College Park,
MD 20742, USA. 7Pepperwood Way, San Jose, CA 95124,
USA. 8Museum of Natural Science, 119 Foster Hall,Louisiana State University, Baton Rouge, LA 70803, USA.
9
Department of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI 48202, USA.
10
Florida Museum of Natural History, University of Florida,
Gainesville, FL 32611, USA. 11Department of Biology andMuseum of Southwestern Biology, University of New
Mexico, Albuquerque, NM 87131, USA.

*These authors contributed equally to this work.
†To whom correspondence should be addressed. E-mail:rkimball@ufl.edu

extant species) and is the focus of most comparative studies, little consensus exists regarding relationships within this clade (1–5, 8). The absence ofintermediate forms linking well-defined groups,
combined with the difficulty of resolving relationships, led to hypotheses that the base of Neoaves
represents an unresolved evolutionary radiation(polytomy) (7, 8). Previous efforts to reconstructthese phylogenetic relationships have been limited
by taxon sampling, the number of loci, and/or
slowly evolving loci with limited power to resolve short internodes [e.g., (3, 4, 10, 12, 14)].
Moreover, conflicting results have been obtainedwith morphology (13, 15), DNA-DNA hybridization (6), whole mitochondrial genomes (16–18),
and different nuclear exon, ribosomal RNA, andintron sequences (1, 3, 4, 10, 12, 14).
Phylogenomics is useful for resolving difficult phylogenies and for verifying or overturning
relationships created on the basis of single genes(19–21). We collected a large DNA sequence
data set to address avian phylogenetic relationships from 171 species representing all but three
nonpasserine families, all major passerine clades,
and two crocodilian outgroups (22). Our alignmentof 32 kb represents 19 nuclear loci located on 15
different chromosomes in the chicken genome (22),with introns (74%), coding exons (23%), and untranslated regions (UTRs) (3%). Data quality andsequence alignments were assessed before analyses (22). We analyzed the data using different optimality criteria and distinct tree-search algorithms (22).
Our sampling of many loci allowed us to assess whether relationships were supported by a signal across the genome or were driven by a single
locus. We (i) analyzed individual loci, (ii) conducted“gene-jackknifing” (excluding one locus at a time,then analyzing the remaining data) to determine
whether conclusions were driven by a single locus,(iii) conducted a partitioned–maximum likelihood(ML) analysis (where each locus had a distinctive
set of parameters), and (iv) coded the data as R
(purine) or Y (pyrimidine) to avoid conclusions
driven by base-compositional biases [e.g., (16)].

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Analyses of individual loci showed that no
single gene was able to recover all nodes identified
with the concatenated data (Fig. 1). The low powerof individual loci was the most pronounced in shortand slowly evolving genes, which generally did
not resolve any interordinal relationships (Fig. 1).
Consistent with previous studies, we recovered genome-wide support for basal divergences
between Paleognathae and Neognathae andbetween Galloanserae and Neoaves (Fig. 2) withrobust support. The topology at the base of
Neoaves, with extremely short internodes, indicated a rapid radiation (Fig. 3) that likely explains
conflicts among previous studies. However, weconsistently found several, well-supported, deep
divisions within Neoaves (highlighted in different
colors in Figs. 2 to 4).
Our study (i) revealed robust higher-levelgroupings within Neoaves, (ii) suggested several
previously unrecognized interordinal relationships, (iii) supported previously proposed clades,(iv) reinforced established relationships not consistently recovered in previous studies, and (v)found well-supported groupings at the tips ofmajor clades. The results discussed below focus
on groups that are found with multiple analyticalmethods and partitions and that exhibit strong
support (ML bootstrap support ≥ 70%) (23).
The largest clade in Neoaves was a wellsupported land bird clade (green, node F, Fig. 2)(3) that contained the Passeriformes (perchingbirds, representing more than half of all avian
species), which is allied with several morphologically diverse orders. These included Piciformes(woodpeckers and allies), Falconiformes (hawks
and falcons), Strigiformes (owls), Coraciiformes(kingfishers, hornbills, rollers, and allies), Psittaciformes (parrots), Coliiformes (mousebirds), andTrogoniformes (trogons). One of the most unexpected findings was the sister relationshipbetween Passeriformes and Psittaciformes (nodeA, Fig. 2), with Falconidae (falcons) sister to thisclade. This relationship varied slightly among
analyses and gene-jackknifing (Fig. 1), yet theclose relationship between passerines with parrots and/or falcons appeared consistently.
Sister to the land birds is the Charadriiformes(shorebirds, gulls, and alcids; yellow, node G,
Fig. 2). This grouping seems to be driven primarily by the b-fibrinogen gene (FGB), because
it was present in analyses of only this gene anddisappeared when the gene was removed throughjackknifing (Fig. 1). Regardless of the exact
placement of the Charadriiformes in our analyses, we consistently support that this order is notbasal within Neoaves (24) and thus refute thehypothesis that transitional shorebirds gave riseto all modern birds (7). Our phylogeny revealed ahighly supported water bird clade (blue, node H,
Fig. 2) (3, 14), including members of thePelecaniformes (totipalmate birds), Ciconiiformes (storks and allies), Procellariiformes (tubenosed birds), Sphenisciformes (penguins), andGaviiformes (loons). Basal to the water birds
were two clades of terrestrial and arboreal taxa

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Fig. 1. Congruence of clades as determined fromconcatenated analyses and multiple data partitions. Nodes
refer to groups in Fig. 2. Dark blue or dark gray cells
indicate those with relationships present in maximum
parsimony (MP) and ML [GARLI (31) and RAxML (32)]analyses (A) or in ML (B and C); light blue or light graycells indicate relationships present with the exception of or
inclusion of one taxon; and striped cells indicate relationships found by either GARLI or RAxML, but not both. The
size of each data partition is listed below its name. (A)major partitions (BS, bootstrap support; dashes represent
clades with less than 50% bootstrap support); (B)individual locus analyses; (C) gene-jackknifing analyses.
n/a, not applicable.

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72

81

68

89

98

H

99

*

*

**
* *
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J

86

*
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96
68

I

98

61

L

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96

M

O

66

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*
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98

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65

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96

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97

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Struthioniformes

62

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Coraciiformes

*
*

98

*

Caprimulgiformes**

K 98 *

58

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81

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Passeriformes

94

One of our most important findings was thatseveral well-accepted orders were not monophyletic. Our analyses provided strong support
that (i) Tinamiformes (tinamous) are foundAnhinga
Phalacrocorax
Acanthisitta
Morus
54
BombycillaFregataRegulus
Ardea
Sylvia60
Cochlearius
TurdusEudocimus
Fringilla
Balaeniceps Ciconiiformes
PasserScopusOscines
PloceusPelecanus
Vidua
Ciconia
Picathartes
Diomedea
Corvus
Oceanodroma
MalurusPelecanoides Procellariiformes
Climacteris
Puffinus
MenuraOceanites
98
Dendrocolaptes
Eudyptula Sphenisciformes
Scytalopus
Gaviiformes
Gavia
Grallaria
Corythaeola Musophagiformes
Thamnophilus
Tauraco77
Mionectes
AramusSuboscines
Tyrannus
A
Grus
Pipra
Psophia
67
Pitta
Heliornis"Gruiformes"
Smithornis
Sarothrura
Sapayoa
Himantornis
81
Alisterus
Rallus73
Psittacula
Centropus
Micropsitta
B
Coua
Chalcopsitta Psittaciformes
Coccyzus
Platycercus
Phaenicophaeus Cuculiformes
Psittacus
Cuculus64
Cacatua
Crotophaga
Daptrius
Geococcyx
Falco
Choriotis
Herpetotheres Falconidae
Otididae
Eupodotis
Micrastur
Opisthocomus
CariamaCariamidae
Aegotheles
AlcedoAerodramus
MomotusStreptoprocne
69
Todus
Hemiprocne
Apodiformes
Brachypteracias
Colibri
Coracias
Phaethornis
Merops98
Caprimulgus
Bucco
Eurostopodus
GalbulaBatrachostomus
Capito98
Podargus
98
Megalaima Piciformes
Nyctibius bracteatus
F
Dryocopus
C
Nyctibius grandis
Indicator
Steatornis
Bucorvus
71
Eurypyga Gruiformes
TockusRhynochetos Gruiformes
Phoeniculus
Columba85
Upupa
Geotrygon
Pharomachrus TrogoniformesD
TreronTrogonColumbiformes
Columbina
Leptosomus
Otidiphaps
Colius
Mesitornis
Urocolius Coliiformes
Mesitornithidae
MoniasPhodilus
Pterocles
Tyto
81
Strigiformes
Syrrhaptes Pteroclididae
Speotyto
Phaethon lepturus
Strix
G
Phaethon rubricauda Phaethontidae
Buteo
Phoenicopterus Phoenicopteriformes
Gampsonyx Accipitridae
Podiceps
Podicipediformes
Pandion
Alectura
61
Sagittarius
Megapodius
Cathartes
E
ColinusSarcoramphus Cathartidae
Coturnix
Galliformes
Arenaria
GallusJacanaRollulus
Rostratula
NumidaPedionomus
Crax
Thinocorus
Anas
DromasCharadriiformes
AythyaLarus
BiziuraTurnixAnser
Anseriformes
Burhinus
Malacorhynchus
Charadrius
OxyuraPhegornis
Anseranas
Haematopus
ChaunaApteryxCasuarius
Fig. 2. ML analysis of the 19-locus data set (ln = –866017.07). ML bootstrap
Dromaius
values > 70% from GARLI are indicated on the cladogram by thicker branches andCrypturellus
Tinamus
are listed at nodes, with values of 100% designated by asterisks. Diamonds at
Tinamiformes
Eudromia
nodes indicate congruence with MP analysis, and black vertical bars refer toNothoprocta
Rhea
ordinal designations (those that are dashed indicate paraphyly). The phylogenetic
Struthio
Pelecaniiformes

88

*
**
*
*
*

typically considered as belonging to Gruiformes).
These latter relationships were also largely
dependent on the presence of FGB (Fig. 1) andrequire further study to determine their validity.

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(node J, Fig. 2): Musophagiformes (turacos) anda clade (gray, node I, Fig. 2) including core
Gruiformes (rails, cranes, and allies), Cuculiformes (cuckoos), and Otididae (bustards, which aretree was rooted to crocodilian outgroups (not shown). Genera in bold are icertae
sedis. Branch colors represent major clades supported in this study: land birds (green), charadriiforms (yellow), water birds (blue), core gruiforms andcuckoos (gray), apodiforms and caprimulgiforms (brown), galloanserae (orange), and paleognaths (purple). Large capital letters indicate groups
discussed in the text and Fig. 1.
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SCIENCEVOL 32027 JUNE 20081765

within Struithioniformes (ostriches and allies;
purple, node Q, Fig. 2), (ii) Apodiformes (hummingbirds and swifts) are found within Caprimulgiformes (nightjars and their allies; brown,node L, Fig. 2), and (iii) Piciformes are found within Coraciiformes (node C, Fig. 2). Typical Pelecaniformes and Ciconiiformes [sensu (13, 25)]
were intermixed in a clade (Fig. 2) that excludes
one traditional pelecaniform family: the Phaethontidae (tropicbirds). The Gruiformes represented atleast four distinct clades in our tree (Fig. 4), depending on the circumscriptions of this order[reviewed in (6)]. Finally, Falconidae and Accipitridae (hawks and osprey) formed distinct clades inall analyses, rather than a monophyletic Falconiformes (Fig. 2) (18).
Several disparate taxa were robustly placed in
our analyses. Cariamidae (seriemas) has traditionally been classified as a gruiform, althoughconvergence with Falconiformes was noted (6).
We found strong support for placing Cariamidae
within land birds near other raptorial groups.
Leptosomus (cuckoo roller) is generally placed
within Coraciiformes, though a relationship with
Falconiformes has also been suggested (6). Ourdata set placed Leptosomus sister to a clade including Piciformes, Coraciiformes, and Trogoniformes (node D, Fig. 2).
Our results suggest resolution of some controversial groupings. For example, Cathartidae (NewWorld vultures)—traditionally placed within
Falconiformes—were previously allied with Ciconiidae (storks) (6). However, our phylogeny
demonstrated no affinity with storks [see also
(3, 18, 26)] and instead strongly supported
placement of Cathartidae within the land birds(usually with Accipitridae). We support that Turnix(buttonquail) belongs within the Charadriiformes(3, 4, 27) and that Podicipediformes (grebes) andPhoenicopteriformes (flamingos; node N, Fig. 2)(14) are sister taxa. Finally, we recovered a sister
relationship between Rhynochetos (kagu) andEurypyga (sunbittern) (node M, Fig. 2) (28): twomonospecific and geographically disparate families that grouped outside of the core Gruiiformes.
The previously proposed division of Neoaves
into Coronaves and Metaves is driven by two loci(4) in our analyses (Fig. 1) and may not represent
the species tree. Many taxa assigned to Metaves
are composed of small numbers of closely related
extant species, including Mesitornithidae (mesites), Phaethontidae, Pteroclididae (sandgrouse),
and Columbiformes (pigeons and doves). The difficulty in placing them may be driven by long,unbreakable branches leading to the tips (Fig. 3).
The enigmatic Opisthocomus (hoatzin) still cannot
be confidently placed, but some putative sister
relationships can be rejected (29).
Modern birds occupy a wide diversity ofniches and exhibit a variety of behaviors. The
broad structure of our phylogeny suggested diversification along general ecological divisions,such as water birds, shorebirds, and land birds.
However, adaptations to these environments clearly arose multiple times (4), because many aquatic

1766

birds were not part of the water bird clade (e.g.,
tropicbirds, flamingos, and grebes) and terrestrial
birds were found outside of the land bird clade(e.g., turacos, doves, sandgrouse, and cuckoos).
Our phylogeny also indicated several distinctive
niches, such as nocturnal (owls, nightjars, andallies), raptorial (falcons, hawks, eagles, New
World vultures, seriema, and owls), or pelagic(tubenosed birds, frigatebirds, and tropicbirds)
lifestyles, have evolved multiple times. Furthermore, our results reinterpret the evolution ofvarious adaptations (e.g., the diurnal Apodiformes evolved from nocturnal/crepuscular Caprimulgiformes, and flighted Tinamiformes arose
within the flightless Struthioniformes) and biogeographic patterns (e.g., the New Caledoniankagu and Neotropical sunbittern are sister taxa).
Given the number of nonmonophyletic groups
in our study, we compared our results withmajor classifications [supporting online material (SOM) text]. Unexpectedly, roughly thesame percentage (35%) of orders defined bydifferent classifications (13, 25, 30) was notmonophyletic relative to the results of our study(Fig. 4). Some orders, such as Gruiformes andthe broadly encompassing Ciconiiformes [sensu(30)], were particularly problematic. Other traditional orders were not monophyletic because of the exclusion or inclusion of one ora few taxa (e.g., placing Turnix within Charadriiformes contradicts all three classifications). Only six orders were defined consistently
across taxonomies and monophyletic in ourstudy (Fig. 4). Given our results, conclusions
from comparative studies that depended
upon these classifications may need to be
re-evaluated in light of this understanding of
avian evolution.
Deciphering the roots of the avian tree oflife has been a lingering problem in evolutionary biology. The inclusion of multiple lociwith diverse rates of evolution, particularly
the large proportion of rapidly evolving introns, yielded a well-supported phylogenetic
tree at multiple taxonomic depths. Althoughsome higher-level avian relationships remainunresolved, simulations suggest that additional sequence data from rapidly evolving locimay resolve these remaining questions (1). It
is also evident that future classifications will

0.1

Fig. 3. ML phylogram demonstrating the short internodes at the base of Neoaves and highlighting
certain extreme examples of rate variation across avian lineages. Colors are as in Fig. 2. Scale bar
indicates substitutions per site. Figure S1 shows the phylogram with taxon names.

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Fig. 4. Our phylogeny differs from and agrees with previous classifications. We merged well-supported(>70% bootstrap values) monophyletic clades at the tips with the same ordinal designation across all
three classifications (e.g., 24 species called Passerines). Only higher relationships supported by bootstrap
values >50% are shown. Colors are as in Fig. 2. Color bars to the right of the tree show membership in
three different classifications: Peters’ (25) (left), Sibley and Monroe’s (30) (middle), and Livezey and Zusi’s(13) (right). Black text within the bars indicates monophyletic orders in our phylogeny, whereas white text
within the bars indicates nonmonophyletic orders. Ordinal name codes: ANS (Anseriformes), APO(Apodiformes), APT (Apterygiformes), ARD (Ardeiformes), BAL (Balaenicipitiformes), BUC (Bucerotiformes), CAP (Caprimulgiformes), CAS (Casuariiformes), CHA (Charadriiformes), CIC (Ciconiiformes), CLM(Columbiformes), COL (Coliiformes), COR (Coraciiformes), CRA (Craciformes), CUC (Cuculiformes), FAL(Falconiformes), GAL (Galliformes), GAV (Gaviiformes), GLB (Galbuliformes), GRU (Gruiformes), MUS(Musophagiformes), OPI (Opisthocomiformes), PAS (Passeriformes), PEL (Pelecaniformes), PIC (Piciformes), POD (Podicipediformes), PRO (Procellariiformes), PSI (Psittaciformes), RAL (Ralliformes), RHE(Rheiformes), SPH (Sphenisciformes), STH (Struthioniformes), STR (Strigiformes), TIN (Tinamiformes), TRC(Trochiliformes), TRO (Trogoniformes), TUR (Turniciformes), and UPU (Upupiformes).
change dramatically, based on our phylogenetic study, and that our results will stimulatecomparative studies to address the growing
number of questions regarding the evolutionof birds.

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of Birds of the World (Yale Univ. Press, New Haven, CT,
1990).
31. D. J. Zwickl, thesis, University of Texas at Austin (2006).
32. A. Stamatakis, Bioinformatics 22, 2688 (2006).
33. This work is a contribution of the Early Bird project,supported by NSF’s Assembling the Tree of Life program(DEB-0228675, DEB-0228682, DEB-0228688, and
DEB-0228617). We thank the American Museum of
Natural History, Australian National Wildlife Collection,
Burke Museum of Natural History and Culture (Universityof Washington), Field Museum of Natural History,
University of Kansas Natural History Museum andBiodiversity Center, L. Densmore private collection,Louisiana State University Museum of Natural Science,
Marjorie Barrick Museum (University of Nevada, Las
Vegas), Museum of Southwestern Biology (University of
New Mexico), Museum of Vertebrate Zoology (Universityof California, Berkeley), Museum Victoria, National
Museum of Natural History, San Francisco Zoological
Garden, and Zoological Museum University of
Copenhagen, as well as many different collectors fortissue samples (table S1). We appreciate support from
D. Zwickl and R. Ree for analysis; the DePaul
Bioinformatics Group, part of the Illinois Bio-grid at
DePaul University, for access to their supercomputing
facilities; and J. Bates, D. Levey, P. Makovicky,
T. Schulenberg, and P. Soltis for comments. Z. Bear,
N. Block, B. Burkley, M. Burns, Z. Burns, S. Coplowitz,
R. Flynn, K. Hammons, V. Heimer-Torres, E. Sackett-Hermann,

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REPORTS1767

REPORTS
Supporting Online Materialwww.sciencemag.org/cgi/content/full/320/5884/1763/DC1
Materials and Methods
SOM Text
Figs. S1 to S3

A Significant Upward Shift in
Plant Species Optimum Elevation
During the 20th Century
J. Lenoir,1* J. C. Gégout,1 P. A. Marquet,2,3,4 P. de Ruffray,5 H. Brisse6
Spatial fingerprints of climate change on biotic communities are usually associated with changes inthe distribution of species at their latitudinal or altitudinal extremes. By comparing the altitudinal
distribution of 171 forest plant species between 1905 and 1985 and 1986 and 2005 along theentire elevation range (0 to 2600 meters above sea level) in west Europe, we show that climate
warming has resulted in a significant upward shift in species optimum elevation averaging
29 meters per decade. The shift is larger for species restricted to mountain habitats and forgrassy species, which are characterized by faster population turnover. Our study shows thatclimate change affects the spatial core of the distributional range of plant species, in addition
to their distributional margins, as previously reported.
ecent warming has induced biologicaland ecological responses from animals
and plants throughout the world (1–3).
Consistent responses to global warming or “fingerprints” are apparent in the phenology and distribution of species (1–5). For plants, invertebrates,and vertebrates, climate change has strongly influenced distribution and abundance at range margins both in latitude (polar margins) (5–8) and inelevation (upper margins) (5, 9–11), and even in
depth for marine fishes (8). Shifts at the upperedge of altitudinal range agree with the hypothesis of an upward trend to escape rising temperatures (12–14). Changes in range limits, however,are just one, albeit important, expression of thelikely consequences of climate change. More subtle changes within the ranges of species are also
likely and, although poorly explored as yet, might
have important ecological and evolutionary consequences. Assuming niche conservatism overevolutionary time (15), we tested for large-scale(across temperate and Mediterranean mountain
forests in west Europe), long-term (over the 20th
century), and multispecies (through an assem-

R

1
AgroParisTech, UMR 1092, Laboratoire d'Etude des RessourcesForêt-Bois (LERFoB), 14 rue Girardet, F-54000 Nancy, France.
2
Center for Advanced Studies in Ecology and Biodiversity(CASEB), Departamento de Ecologia, Pontificia Universidad
Católica de Chile, Alameda 340 C.P. 6513677, Santiago,
Chile. 3Institute of Ecology and Biodiversity (IEB), Casilla653, Santiago, Chile. 4Santa Fe Institute, 1399 Hyde Park
Road, Santa Fe, NM 87501, USA. 5CNRS, Institut de Biologie
Moléculaire des Plantes (IBMP), Université Louis Pasteur, 12
Rue du Général Zimmer, F-67084 Strasbourg Cedex, France.
6
CNRS, UMR 6116, Institut Méditerranéen d'Ecologie et dePaléoécologie (IMEP), Faculté des Sciences de Saint Jérôme,case 461, F-34397 Marseille Cedex 20, France.

blage of 171 species) climate-related responses inforest plant altitudinal distributions. We analyzed
species responses by measuring shifts in the altitudinal position of species’ maximum probability of presence within their distribution, insteadof focusing on distributional extremes. Additionally, we tested for the effect of ecological and life
history traits on the magnitude of the response to
climate warming (16). In particular, we tested
whether species restricted to mountain areas

Tables S1 to S3
References
12 March 2008; accepted 29 May 2008
10.1126/science.1157704(10–12, 17, 18) and/or fast generation times (19)are particularly sensitive to temperature changes.
We studied species in forest communities
found between lowland to the upper subalpine
vegetation belt (0 to 2600 m above sea level) over
six mountain ranges in west Europe (the Western
Alps, the Northern Pyrenees, the Massif Central,the Western Jura, the Vosges, and the Corsican
range). Climatic change in France has been characterized by increases in average temperature of
far greater magnitude than increases in the world
mean annual temperature, of about 0.6°C overthe 20th century (20), reaching up to 0.9°C (21)and even close to 1°C in the alpine region since
the early 1980s (22). From two large-scale floristic inventories (about 28,000 surveys) (23), we
extracted two well-balanced subsamples, including 3991 surveys each, carried out across thestudied mountain ranges (see fig. S1 for surveys
location). The first subsample included surveys
carried out before the mid-1980s (1905–1985),
and the other one, after 1985 (1986–2005) (seefig. S2 for altitudinal distribution of surveys). We
chose this temporal threshold because the analysis of yearly mean surface temperature anomalies between 1965 and 2005 shows that in 1986
the studied mountain ranges experienced a temperature regime shift (Fig. 1A), staying above theaverage baseline conditions. In contrast, analysisof annual precipitation anomalies between 1965

Fig. 1. Climatic trends from 1965 to 2006.
(A) Yearly mean surface temperature anomalies (using overall mean temperature asbaseline) and (B) annual precipitation anomalies (using overall mean annual precipitation as baseline) averaged for 73 elevationsites in the French mountains ranging inaltitude from 10 to 2010 m above sea level.
Solid gray bars refer to positive anomalies,
whereas open bars refer to negative ones.
The solid curve is the smoothed averagewith use of a 10-year filter. The verticaldotted lines mark the split between the twostudied periods. Data have been gatheredfrom the French National Climatic Network(Météo-France).

*To whom correspondence should be addressed. E-mail:jonathan.lenoir@agroparistech.fr

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A. Hudson, S. Hunter-Smith, S. Kearney, L. Kimball,
K. Rozofsky, J. Smith, and P. Tester provided assistancein the lab. Sequence accession numbers in GenBank are
EU737149 to EU740386, EF521416 to EF521576, andEU302706 to EU302748.