Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society00244066The Linnean Society of London, 2006? 2006
881
1722
Original Article
BEAK DEVELOPMENT
P. R. GRANT
ET AL.
Biological Journal of the Linnean Society, 2006, 88, 17–22. With 1 figure
A developing paradigm for the development of bird beaks
PETER R. GRANT1*, B. ROSEMARY GRANT1 and ARKHAT ABZHANOV2
1
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544–1003, USA
Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
2
Received 9 September 2004; accepted for publication 29 April 2005
Some adaptive radiations are notable for extreme interspecific diversification in one or a few adult traits. How and
why have trait differences evolved? Natural and sexual selection often provide answers to the question of why. An
answer to the question of how is to be found in the genetic control of the phenotypic traits, especially in the early
stages of development, when interspecific differences first become expressed. Recent studies of the molecular genetic
control of beak development in Darwin’s finches have shown that a signalling molecule (BMP4) plays a key role in
the development of large and deep beaks. Expression of this molecule occurs earlier (heterochrony) and at higher levels in species with deep beaks compared with species with more pointed beaks. The implication of this finding is that
variation in the regulation of one or a few genes that are expressed early could be the source of evolutionarily significant variation that is subject to natural selection in speciation and adaptive radiation. This view is reinforced by
parallel findings with the same signalling molecule in the development of jaw morphology in cichlid fish of the Great
Lakes of Africa. Further research into regulatory mechanisms is to be expected, as well as extension to other examples of radiation such as honeycreepers in Hawaii and Anolis lizards in the Caribbean. © 2006 The Linnean Society
of London, Biological Journal of the Linnean Society, 2006, 88, 17–22.
ADDITIONAL KEYWORDS: adaptive radiation – beak shape – Bmp4 – cichlid fish – Darwin’s finches –
embryonic growth – gene regulation – heterochrony.
INTRODUCTION
Problems of phylogeny can have solutions in ontogeny.
An obvious starting point for understanding patterns
of species richness is to reconstruct their phylogeny,
and much research over the past 30 years has been
devoted to doing this rigorously with molecular data.
Phylogeny having been established to a statistically
acceptable degree, enquiries can then be directed
towards questions of how and why the phylogeny
developed in the way that it did: what were the key
elements in the evolutionary transitions; what was
the genetic basis of variation in those elements; where
were the constraints on evolutionary change and what
were the environmental circumstances that resulted
in evolutionary change? In this article we show with a
detailed example how new research findings on ontogeny at the molecular level can help us to understand
phylogeny at the adult phenotypic trait level. This is
an old topic (Gould, 1977) with new potential. It is
*Corresponding author. E-mail: prgrant@princeton.edu
being advanced rapidly through progress in unveiling
the molecular genetic control of development in
several organisms, for example, plants (Barrier,
Robichaux & Purugganen, 2001), invertebrates
(Simpson, 2002) and vertebrates (Shapiro et al., 2004).
Starting with the products of one case of adaptive
radiation we chart the links between the origin of different species, in phylogeny and the origin of their
phenotypic trait differences in ontogeny.
PHYLOGENY
Certain taxa are unusually suitable for investigations
of phylogenetic history, because they are unusually
tractable as experimental subjects (Carson, 1990;
Hodges & Arnold, 1994; Naisbit, Jiggins & Mallet,
2001) or have a rich fossil history (Alroy, 1998; Saunders, Work & Nikolaeva, 1999), or because several species have been produced from an ancestral species in a
short time and hence the gaps between the species are
small (Schluter, 2000; Seehausen, 2000; Gillespie,
2004). Darwin’s finches fall into the last category. Sev-
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 17–22
17
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P. R. GRANT ET AL.
eral species (14) evolved from a common ancestor in a
short time (2–3 Myr) on Galápagos and Cocos islands.
Their phylogeny has been estimated reasonably well,
and is more impressive for the general congruence of
morphological, allozyme, microsatellite and mtDNA
reconstructions than it is for the support for all nodes
(Grant, 1999; Sato et al., 1999; Petren et al., 2005).
Species have originated as a result of change in a
small number of phenotypic traits, principally the size
and shape of the beak, and to a lesser extent body size
and plumage colour. They are believed to have originated allopatrically, adapting to local food supplies as
indicated by associations between interisland variation in beak characteristics and food supply (Grant &
Grant, 2002a). Moreover, directional natural selection
on beak traits has been shown to occur when, as a
result of climatic fluctuations, the composition of local
food supplies changes (Grant & Grant, 2002b). The
behavioural basis of speciation is known in broad outline through studies of the role of song and beak morphology in mate choice (Grant & Grant, 1997a, 1997b).
Not all questions about speciation have been
answered, and one major area of ignorance is the
genetic control of the beak traits that have been
important in species diversification.
Some Darwin’s finch species are phenotypically so
similar that extreme members of two species can be
difficult to distinguish. Thus it is easy to envisage a
transition from one species to the other occurring
through directional selection on heritable phenotypic
variation. Indeed, additive genetic variation for beak
traits is known to be high; likewise, selection coefficients can be high when the environment changes, and
the result is a measurable evolutionary response in
the next generation (Grant & Grant, 2002b). However,
within the group as a whole there are some strong
phenotypic discontinuities between species, none
greater than those between the basal warbler finches
(Certhidea) and all other species (Grant, 1999). Such
discontinuities may be the end result of gradual divergence in individually small steps in accordance with
the above reasoning of directional selection on standing genetic variation. The current absence of intermediates is then explained by their replacement or
extinction. Another possibility is that a re-patterning
of development occurred, a temporal re-scheduling of
the development of different beak dimensions (heterochrony), as a result of new genetic variation being
introduced by mutation but being subject to the same
directional selection on adult phenotypes. This alternative overcomes the problem of strong positive
genetic correlations between adult beak dimensions
retarding evolutionary change in beak shape, because,
potentially at least, it explains how one trait may
change while another does not. Thus, a deeper understanding of how adaptive changes in adult beak shape
were brought about during speciation may lie in the
ontogenetic differences among extant species.
ONTOGENY
Embryonic beak growth has rarely been studied
directly (Cane, 1994). For birds in general it can be
said that growth rates are uniform over the embryonic
period, and are faster for larger species compared with
smaller ones (Ricklefs & Starck, 1998). After hatching,
nestlings of closely related species grow predominantly along a single multivariate size axis, with only
minor variation in growth rates and the timing of
growth cessation (Boag, 1984; Björklund, 1993, 1996;
Burns, 1993). These observations imply that morphological differences between species which cannot be
attributed to differences in size at hatching must arise
during embryonic growth. Indeed, this appears to be
the case in fox sparrows ( Passerella iliaca). The larger
(adult) birds on Newfoundland have a larger body
size at hatching but a shorter beak at hatching than
have their relatives in California (Burns, 1993).
After hatching the two groups grow along roughly
parallel pathways. Similar results at hatching
were found in two populations of house finch
(Carpodacus mexicanus) (Badyaev, Hill & Whittingham, 2001a; Badyaev, Whittingham & Hill, 2001b).
Darwin’s finch species differ in adult size and shape
of beak in relation to body mass first as a result of different sizes at hatching, associated with different
sizes of eggs, and then as a result of different posthatching growth trajectories (Grant, 1981; Boag, 1984;
Grant & Grant, 1989). For example, on the island of
Genovesa, four species differ profoundly in posthatching growth trajectories of beak length and depth
(Fig. 1). Their beaks grow longer following the same
growth curve, but they hatch at different sizes on this
common curve. This size corresponds to approximately
20% of the total beak length growth in all species. In
contrast, the species have different beak depth growth
curves and hatch at different depths on these curves.
Differences at hatching in depth are much greater
than are differences in length, and the differences in
depth (but not length) are magnified during nestling
growth. For example, at hatching, the largest species
Geospiza magnirostris (∼35 g) has completed about
20% of its growth in beak depth (as well as length),
whereas the smallest species Ce. fusca (∼8 g) has completed 50% of its beak depth growth.
Therefore, differences among species at hatching set
the stage for differential nestling growth. But how is
the stage set in the first place? The answer, or
answers, to this question bring us closer to the evolutionary origin of differences between species, and
reside in the black box of embryonic growth. Until
recently, they could only be inferred by extrapolation
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 17–22
Beak depth
A
Beak length
BEAK DEVELOPMENT
?
?
Mass
Beak depth
B
Beak length
Mass
19
Mass
Mass
Figure 1. A, four species of Darwin’s finch on Isla Genovesa differ in beak proportions at hatching, indicated by symbols.
The unknown embryonic growth of beaks in relation to body mass must be faster compared with nestling growth (solid
lines), otherwise, as shown by backward extrapolation (dotted lines), beaks would be larger initially than are body sizes!
B, recent research shows that the species acquire their differences due to differential production of a signalling molecule,
BMP4, during a phase of rapid beak growth in the middle of embryogenesis. , Certhidea fusca; , Geospiza difficilis; ,
G. conirostris; , G. magnirostris. Adapted from Grant (1981).
backwards from hatching to the point of beak initiation at about day 4, when body mass is still very small.
Extrapolation has revealed three characteristics of
embryonic beak growth (Fig. 1). First, the four species
grow in beak dimensions faster in relation to mass
before hatching than they do after hatching. Second,
the embryonic growth trajectories of beak depth in
relation to mass are either the same or very similar in
the four species. Third, for beak length in relation to
mass there are two possible embryonic growth trajectories; either the trajectories are the same in the four
species, in which case the larger species switch to a
posthatching trajectory before they hatch, or they are
slower in the larger species than they are in the
smaller species.
The only way to distinguish between the alternatives is to study embryonic growth directly, using
molecular tools to open the black box and investigate
the control of development.
MOLECULAR GENETICS
The molecular basis of beak development in these
finches is starting to be revealed (Abzhanov & Tabin,
2004; Abzhanov et al., 2004). At the start of avian beak
development, two signalling molecules, fibroblast
growth factor 8 (FGF8) and sonic hedgehog (SHH),
have adjacent, nonoverlapping domains in the
epithelium covering the neural crest-derived mesenchyme that gives rise to the skeletal projections of
upper and lower mandibles (Hu, Marcucio & Helms,
2003; Schneider & Helms, 2003; Abzhanov & Tabin,
2004; Tucker & Lumsden, 2004; Wu et al., 2004). At
stages 17–20 (∼ day 3–4) the FGF8 domain is the dorsal frontonasal primordium and the ventral mandibular nasal primordium. The intervening region is the
domain for SHH. By misexpressing these two genes
with retroviral vectors injected into the neighbourhood of the developing beak, Abzhanov & Tabin (2004)
were able to show that together, but not alone, the two
molecules induce cartilage outgrowth where the
domains meet, and even in some regions where they
do not. They also induce synergistically expression of
other factors, such as the signalling molecule BMP4
(bone morphogenetic factor 4) in the underlying neural crest mesenchyme.
Differences among the species arise and become
consolidated in a restricted period of embryonic
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 17–22
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P. R. GRANT ET AL.
growth. Differences in the sizes of beak primordia
begin to appear at day 5 (Abzhanov et al., 2004). Differences in morphological shape are first seen at
day 6, halfway in time towards hatching, when neural
crest-derived mesenchyme is condensing into cartilage. By day 7–8, the species have attained their distinct morphologies, and these are maintained until the
end of embryonic development.
An important factor in the origin of these differences is Bmp4. At day 5 its expression is detectable
at low levels in the subectodermal mesenchyme of
G. difficilis and other species, but at a dramatically
higher level in the largest species, G. magnirostris.
At day 6, Bmp4 expression is elevated in three
ground finch species (G. magnirostris, G. fortis and
G. fuliginosa) but not in the two cactus finches
(G. conirostris and G. scandens), which have relatively
long and shallow beaks. An effect of Bmp4 expression
on beak depth development in chickens was demonstrated using a retroviral vector to locally misexpress
Bmp4 in the distal mesenchyme of the upper beak at
day 6.5. This experiment mimicked the natural occurrence of elevated levels of BMP4 at the same stage in
G. magnirostris, and it produced very G. magnirostrislike beaks, both in width and in depth of the upper
mandible. Injecting Noggin retrovirally, which is a
Bmp4 antagonist, led to a dramatic decrease in the
size of the upper beak and to a much smaller skeletal
element in the beak (Abzhanov et al., 2004; Wu et al.,
2004).
Thus, the species with deeper, broader beaks relative to their length express Bmp4 in the mesenchyme
of their beak primordia at higher levels and at earlier
stages than do species with more narrow and shallow
beak morphologies. There is an interesting variation
on this theme that demonstrates the importance of
variation in site of action of the signalling molecule.
In G. difficilis, once the cartilage condensation has
occurred at about day 6.5 (stage 29), Bmp4 continues
to be expressed in mesenchymal cells surrounding the
most rostral part of the prenasal cartilage. This spatially restricted expression appears to be responsible
for a unique feature of the adults: the upper mandible
is basally deep, but becomes rapidly pointed from
beyond the nostrils to the tip (Grant, Grant & Petren,
2000).
Molecular genetic results resolve two issues arising
from embryonic growth trajectories inferred from
nestling growth patterns (Grant, 1981). First, with
regard to beak depth, they show that, in comparison
with the smaller species, the larger G. magnirostris
starts to grow earlier, grows faster, and grows further.
Also, it does not grow along the same trajectory as
supposed previously. The faster and further growth is
consistent with the first hypothesis to explain species
transitions in terms of standing genetic variation,
whereas the earlier growth (heterochrony) is more
compatible with the hypothesis of re-patterning of
growth. Second, the species are similar in growth of
beak length with respect to mass, and evidently switch
to a posthatching trajectory before they hatch.
CONCLUSIONS AND PROSPECTS
Speciation of Darwin’s finches involved a diversification in embryonic growth patterns. We have obtained
the first glimpses of that diversification. We now know
that differences between the species arise and are consolidated in a relatively brief period of no more than
1–2 days in a 12–14-day period of embryonic growth.
Moreover, an important gene implicated in these differences has been identified. Variation in Bmp4 regulation appears to be one of the principal molecular
factors that provided the morphological variation on
which natural selection acted in the evolution of the
beaks of Darwin’s finches (Abzhanov et al., 2004).
Selection on adult beak variation is, in effect, selection
on growth programs. It results in changes in growth in
the next generation because of genetic correlations
between adult and juvenile expression of the same
morphological characters (Grant, 1983; Price & Grant,
1985; Björklund, 1993). Genetic variation in beaks is
an integral of allelic variation at loci that govern beak
growth in size and shape both embyonically and after
hatching. Thus, we are beginning to understand better
what it means to say that birds differ genetically in
the size and shape of their beaks.
Results of studying phenotypic growth patterns and
molecular genetic control of beak size and shape in a
group of ground finches (Geospiza spp.) have clear
implications for the evolution of the other Darwin’s
finches. Tree finches (Camarhynchus spp.) and the
vegetarian finch Platyspiza crassirostris vary in adult
beak proportions in a manner that parallels the variation in Geospiza, yet in some ways is subtly different
from them (Grant, 1999). For example, the curvature
of the mandibles and the relative depths of lower and
upper mandibles are distinguishing features of Camarhynchus and P. crassirostris. Therefore, a hypothesis
to explain variation in beak morphology among
Geospiza in molecular genetic terms should be largely,
but not entirely, successful in accounting for variation
among Camarhynchus and P. crassirostris. In contrast, Ce. fusca differs strikingly from all other species
of Darwin’s finch in its warbler-like traits of small
body size and long, narrow and shallow beak. One
hypothesis to explain the beak traits is that the same
interacting signalling molecules are involved but their
proportional effects are different. For example, Bmp4
expression may be suppressed to a large degree by a
uniquely high level of expression of the antagonist
noggin. There are several alternatives, hence several
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 17–22
BEAK DEVELOPMENT
ways in which the hypothesis can be falsified, including the action of one or more unique signalling molecules in Ce. fusca and different patterns of gene
regulation.
These findings place a new tool in the hands of avian
embryologists that could be applied in other avian systems, for example, in the study of sexual dimorphism
(Badyaev et al., 2001a, 2001b) and the radical changes
in beak curvature and proportions that characterize
variation at the level of families or orders (e.g. Cane,
1994). Moreover, they provide a new foundation for
studies designed to reveal the mechanistic basis of
species differences in morphology at the adult level.
For the future, a clear need is to determine how Bmp4
is regulated differently in the different species. Do the
differences reside in cis-regulatory elements, in the
timing or amounts of upstream inductive factors, or in
differences in the transduction of signals such as SHH
and FGF8? Or do the differences reside in trans-regulatory changes that modify the expression or activity
of factors that interact with cis-regulatory sequences
(e.g. Morley et al., 2004; Wittkopp, Haerum & Clark,
2004)? We have yet to find other signalling molecules
that perform similar, or different, functions, at other
times or at other sites. Some candidate molecules have
been examined; retinoic acid (RA), members of the
WNT (wingless) family, and sprouty have been shown
not to play a significant role in beak development
(Abzhanov & Tabin, 2004; Abzhanov et al., 2004; Wu
et al., 2004). However, Bmp2 and Bmp7 may play a
role supplementary to that of Bmp4 by controlling
growth in the size of the beak as its shape changes
during development. The possible role of all these factors in postembryonic growth is completely unknown.
To answer these questions, future research may be
able to take advantage of the natural occurrence of
hybridization among species of Darwin’s finch (Grant
et al., 2004; Grant, Grant & Petren, 2005).
There are interesting parallels between our findings
and discoveries being made with another well-known
adaptive radiation, that of cichlid fish in the Great
Lakes of Africa (Terai, Morikawa & Okada, 2002;
Albertson, Streelman & Kocher, 2003; Albertson et al.,
2005). In a study of two species from Lake Malawi,
variation at the Bmp4 gene was found to segregate
with QTL (quantitative trait loci), associated with the
shape of the lower jaw (Albertson et al., 2003). In
another study of four species differing in jaw morphology, an unusually large number of substitutions in
Bmp4 were found. Variation among these species is
restricted to the prodomain of the signalling molecule,
leading Terai et al. (2002) to conclude that post-translational regulation of the protein, rather than the
function of Bmp4, had changed. Not only do these
results broaden the implications of the Darwin’s finch
study, they point to future research opportunities in
21
cloning and analysing Bmp4 and other interesting
genes in the finches and other vertebrates. Other vertebrates should include honeycreeper finches of
Hawaii (Lovette, Bermingham & Ricklefs, 2002) and
Anolis lizards of the Caribbean (Losos, 1998), because
both have diversified impressively in their respective
environments, as well as promising groups of amphibians and mammals, such as salamanders (Parra-Olea
& Wake, 2001) and bats (Racey & Swift, 1995).
ACKNOWLEDGEMENTS
This work was supported by NSF grants (to P.R.G. and
B.R.G.) and the Cancer Research Fund of the Damon
Runyon-Walter Winchell Foundation fellowship,
DRG1618 (to A.A.).
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