Iturria: Science Daily
ScienceDaily (Sep. 24, 2012) —
It has long been known that diversity of form and function in birds'
specialized beaks is abundant. Charles Darwin famously studied the
finches on the Galapagos Islands, tying the morphology (shape) of
various species' beaks to the types of seeds they ate. In 2010, a team
of Harvard biologists and applied mathematicians showed that Darwin's
finches all actually shared the same developmental pathways, using the
same gene products, controlling just size and curvature, to create 14
very different beaks.
Antillean bullfinches (Loxigilla violacea) use their deep and wide beaks
to crush seeds and hard fruits. Harvard researchers have found that the
molecular signals that produce a range of beak shapes in birds show
even more variation than is apparent on the surface. (Credit: Photo by
José M. Pantaleón)
Now, expanding that work to a less closely related group of birds,
the Caribbean bullfinches, that same team at Harvard has uncovered
something exciting -- namely, that the molecular signals that produce
those beak shapes show even more variation than is apparent on the
surface. Not only can two very different beaks share the same
developmental pathway, as in Darwin's finches, but two very different
developmental pathways can produce exactly the same shaped beak.
"Most people assume that there's this flow of information from genes
for development to an inevitable morphology," says principal
investigator Arhat Abzhanov, Associate Professor of Organismic and
Evolutionary Biology (OEB). "Those beaks are very highly adaptive in
their shapes and sizes, and extremely important for these birds. In
Darwin's finches, even one millimeter of difference in proportion or
size can mean life or death during difficult times. But can we look at
it from a bioengineering perspective and say that in order to generate
the exact same morphological shape, you actually require the same
developmental process to build it? Our latest research suggests not."
The findings have been published in the Proceedings of the National Academy of Sciences
The Caribbean bullfinches, geographic and genetic neighbors to
Darwin's finches, are a group of three similar-looking species that
represent two different branches of the evolutionary tree. These
bullfinches have very strong bills that are all exactly the same
geometric shape but slightly different sizes.
"They specialize in seeds that no one else can touch," explains
Abzhanov. "You'd actually need a pair of pliers to crack these seeds
yourself; it takes 300 to 400 Newtons of force, so that's a really nice
niche if you can do that. But the question is, what developmental
changes must have occurred to produce a specialized beak like that?"
A new and highly rigorous genomic analysis by coauthor Kevin J.
Burns, a biologist at San Diego State University, has shown that among
the three Caribbean bullfinch species, this crushing type of beak
actually evolved twice, independently. Convergent evolution like this is
common in nature, and very familiar to biologists. But understanding
that phylogeny enabled Abzhanov, lead author Ricardo Mallarino (a former
Ph.D. student in OEB at the Graduate School of Arts and Sciences), and
colleagues in applied mathematics at the Harvard School of Engineering
and Applied Sciences (SEAS) to perform a series of mathematical and
morphogenetic studies showing that the birds form those identical beaks
in completely different ways. Such studies must, by their nature, be
performed early in the embryonic stage of the birds' development, when
the shape and tissue structure of the beak is determined by the
interactions of various genes and proteins.
"In the small bullfinch you have almost a two-stage rocket system,"
says Abzhanov. "Cartilage takes you halfway, and then bone kicks in and
delivers the beak to the right shape. Without either stage, you'll fail.
In the larger bullfinches, the cartilage is not even employed, so it's
like a single-stage rocket, but it's got this high-energy, synergistic
interaction between two molecules that just takes the bone and drives
its development straight to the right shape."
In embryos of the small bullfinch, Loxigilla noctis
, the control genes used are Bmp4
, followed by TGFβIIr
, and Dkk3
, the same combination used in Darwin's finches. Embryos of the larger bullfinches, L. violacea
and L. portoricensis
, use a novel combination of just Bmp4
"Importantly," Abzhanov says, "despite the fact that these birds are
using different systems, they end up with the same shape beak, and a
different shape beak from Darwin's finches. So that reveals a surprising
amount of flexibility in both the shapes and the molecular interactions
that support them."
The finding offers new insight into the ways birds -- the largest and
most diverse group of land vertebrates -- have managed to adaptively
fill so many different ecological niches.
"It is possible that even if the beak shape doesn't change over time,
the program that builds it does," explains Abzhanov. "For evolution,
the main thing that matters for selection is what the beak actually
looks like at the end, or specifically what it can do. The multiple ways
to build that beak can be continually changing, provided they deliver
the same results. That flexibility by itself could be a good vehicle for
eventually developing novel shapes, because the developmental program
is not frozen."
Following a standard process in studies of developmental biology,
Abzhanov's team began with measurements of the morphological differences
between species, followed by observations of gene expression in
bullfinch embryos and functional experiments using chicken embryos.
Along the way, mathematical models helped the team to quantify and
categorize the beak shapes they were seeing.
"We used geometric morphometric analysis, looking at these beaks as
curves," says coauthor Michael Brenner, Glover Professor of Applied
Mathematics and Applied Physics at SEAS and Harvard College Professor.
"The beak shapes would turn into contours, contours were digitized into
curvatures, and curvatures were turned into representative mathematical
formulas. This provided our biology colleagues with an unbiased way of
determining which of the different species had beak shapes that were
identical up to scaling transformations, and which were in a completely
In order to observe gene expression in the developing bullfinch
embryos, Mallarino and a team of undergraduate field assistants had to
collect eggs from wild nests in the Dominican Republic, Barbados, and
Puerto Rico. The birds breed in dome-shaped nests with small side
entrances, often in the tops of tall cacti. In accordance with strict
fieldwork regulations, Mallarino's team collected only every third egg
laid, which required them to return to the nests daily, climbing dozens
of trees and cacti to carefully label every new egg. Laden with radios,
notebooks, markers, heavy ladders, and a special foam crate for the
delicate eggs, the team ventured into remote field sites at the crack of
dawn and returned to camp before noon to incubate those they collected.
"They're much more fragile than a chicken egg, and extremely small," says Mallarino. "We just walk very carefully."
"It's a big logistical operation," he adds. "It's five months of
really, really hard work under the sun in crazy conditions, but when it
works it's really rewarding. At day 6 or 7 you have a perfect, live
embryo with a beak beginning to form, and you can learn so much about
The next step in this work is to widen the lens yet again and compare the morphological development of a broader group of birds.
"In time, hopefully we'll see how the great diversity that you see
among all these highly adaptive bird beaks may actually evolve at the
genetic level," says Mallarino. "That's the greater challenge."
In addition to Abzhanov, Mallarino, and Brenner, coauthors included
Otger Campàs, a former postdoctoral associate at the School of
Engineering and Applied Sciences (SEAS); Joerg A. Fritz, a graduate
student in applied mathematics at SEAS; and Olivia G. Weeks, a graduate
student in organismic and evolutionary biology at the Graduate School of
Arts and Sciences.
This work was supported by several grants from the National Science
Foundation, as well as the Kavli Institute for Bionano Science and
Technology at Harvard and the National Institutes of Health.