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Peter R. and B. Rosemary Grant lecture – Darwin’s Finches
Darwin’s Finches
October 28, 2009
Peter R. and B. Rosemary Grant lecture presented as part of the Darwin Distinguished
Lecture Series. These events are sponsored by Arizona State University, Office of the
President, College of Liberal Arts and Sciences, School of Life Sciences, and the
Center for Biology and Society.
Transcript
Quentin Wheeler: [0:00] Good evening, welcome. My name is Quentin Wheeler. I'm university
vice president and Dean of the College of Liberal Arts and Sciences, and I'm delighted to
welcome you here this evening. [0:10] This is the Darwin Distinguished Lecture Series, and it's
part of a continuing celebration of the 150th anniversary of the publication of "The Origin of
Species" that we've been having for, well, a little bit over the last year. And we've just had a
fantastic series of events and tonight will be no exception.
[0:29] Before I begin, I want to remind you that there will be a book signing afterwards at the
back of the room. And if I could ask you to muzzle your cellphones for the benefit of everyone,
I'd appreciate that.
[0:42] Perhaps no group of species on earth is more immediately and universally associated with
the theory of evolution than Darwin's finches. And certainly no scientists are more immediately
or universally associated with Darwin's finches than the Grants. So this is a superb opportunity to
have insight into the on-the-ground kind of studies that they have made a career of.
[1:06] Peter and Rosemary Grant are professors emeriti at Princeton University, fellows of the
National Academy of Sciences, the American Academy of Arts and Sciences and the Association
for the Advancement of Science.
[1:20] I had the pleasure of leading a tour in May of the Galapagos Islands, my first visit there,
and it was a joint fund raising venture of an institute that I run called the International Institute
for Species Exploration, and our Institute for Human Origins. And experiencing the Galapagos is
just a life altering event, and we'll have the pleasure of seeing some images of that tonight. But I
certainly recommend it to you.
[1:44] And our vessel did do one lap around Daphne Major. And I was thinking of the fortitude
of field biologists working for more than three decades on that island. This requires considerable
love and devotion, I think, to one subject matter.
[1:59] Beginning some 35 years ago, the Grants went to the Galapagos to study the birds that had
so intrigued Darwin. They lived there part of each year, they banded, tracked and observed
literally thousands of finches, and raised two daughters in the process.
[2:14] Darwin, like most of us today, did not fully recognize the variability inherent in the
finches of the Galapagos. These birds vary from vegetarians to vampires, and reveal adaptations
of a range rarely matched in other groups that have been studied.
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Peter R. and B. Rosemary Grant lecture – Darwin’s Finches
[2:31] During Darwin's brief visit to the Galapagos, he didn't appreciate what these birds might
tell us about evolution, and regrettably his notes and his labeling of his specimens was not quite
what it might have been. And upon returning to London, it became obvious as he worked with
ornithologists just the full implication of what these birds might mean in terms of revealing
something to us of their evolutionary history.
[2:54] But it was the Grants who would pick up where Darwin left off and reveal the full
potential of the Galapagos finches to tell us about evolution. Their powers of observation are
legendary. The staff at the Darwin Research Institute in the Galapagos reported to have said that
only God and Peter Grant can recognize Darwin's finches.
[3:14] It was the Grants' careful observations that elevated the finches to the paradigmatic case
study for natural selection that they are today. Meticulously measuring beak sizes and shapes,
and tracing such traits through genetic lineages for literally generations, the Grants have elevated
natural selection in the field laboratory from theory to incontrovertible fact.
[3:37] The Grants and their finch studies formed the basis of a non-fiction book, "The Beak of
the Finch: A Story of Evolution in Our Time" by Jonathan Weiner, which won the Pulitzer Prize
in 1995. In his book, Weiner writes that the Grants are the first scientists equipped with enough
patience, stubbornness, ground and sea support, computer power, airplane power and staying
power to watch the process actually happen.
[4:03] For their scientific contributions, Peter and Rosemary Grant have been recognized this
year with a Kyoto Prize for lifetime achievement. They have received the Darwin-Wallace Prize,
given only once every 50 years by the Linnean Society of London. They were awarded the
American Institute of Biological Sciences Outstanding Scientist Award, and Balzan Prize for
population biology in 2005. The Balzan Prize is reputed to be equivalent to the Nobel Prize,
created to honor scientific fields not recognized by the Nobel committee. And both received the
Senior Scientist Award of the Humboldt Foundation, the highest given to foreign scientists by
the German government.
[4:42] So please join me in extending a warm Darwinian welcome to Peter and Rosemary Grant
as they share with us what they've learned about evolution through the study of Darwin's finches.
[4:51] [applause]
Peter Grant: [5:07] Well thank you very much for that over-the-top introduction. [laughs] It's
been a great pleasure to come back to Phoenix after an absence of no less than 55 years. That
time, we experienced 115 degree temperatures. I could not believe it at 3:00 one afternoon. And
it's much more comfortable to be here at whatever it is, 62 degrees, today. [5:27] Anyway, it's a
great pleasure to be here, and to tell you about what we know about evolution as a result of the
studies that we and our associates have done on Darwin's finches.
[5:37] Now the title of this book is simply a restatement of "On the Origin of Species." The fact
that 150 years ago, there was a title to a book written by this man tells us that we are still
confronted by the same series of questions that Darwin was 150 years ago, namely, how as
modern evolutionary biologists do we explain the enormous biological diversity in the world?
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Peter R. and B. Rosemary Grant lecture – Darwin’s Finches
[6:05] And I'm really referring to two aspects of diversity as illustrated by these Hawaiian honey
creeper finches. One is the variety of them, they look very different. And the other one is the
numbers. More than 50 species evolved in a relatively short space of time.
[6:22] And evolutionary biologists like Rosemary and myself would like to be able to understand
this diversity. How is it that so many species have evolved from a common ancestor in a
relatively short space of time?
[6:34] Well the core process of that generation of biological diversity is speciation, and I'm going
to illustrate that with an oversimplified diagram of how speciation occurs. It is the process of
splitting of a single population or lineage into two, which diverge, and after a period of time they
are no longer capable of interbreeding, at which point they are unequivocally two species.
[7:03] Darwin was familiar, or rather he understood the early stages of this process much better
than the later ones. And I'm going to give a quote to show his understanding. Those cases he
wrote in which a speciation splits into two or three or more new species, I should think near
perfect separation would greatly aid in their specification, to coin a new word.
[7:29] Well fortunately the word "specification" did not catch on. We now say "speciation" but
the fundamental importance of geographical separation of derived populations has persisted to
the modern day in the process of speciation.
[7:45] How then does it end? To obtain a succinct statement of a general understanding by
biologists of how that process ends, one has to move fast forward into the modern era of
Mendelian genetics.
[8:00] And here I'm going to show a quotation from Hermann Muller, a population geneticist
who put it like this: "Thus, a long period of non-mixing of two groups is inevitably attended by
the origination of actual immiscibility, that is to say genetic isolation." And he was referring
specifically to random processes alone. Random genetic drift would do it, aided and abetted
perhaps and probably by natural selection.
[8:29] Now the theme of our talk is that there are many more interesting things going on
evolutionarily between the starting point and the end point than is reflected in these two
statements. And I make that assertion on the basis of our long-term study of Darwin's finches.
On the Galapagos Islands there are 14 species in total, one on Cocos Island off the coast of Costa
Rica derived from a communal ancestor in, again, a short space of time, two to three million
years only.
[9:00] None of the species have become extinct as far as we know as a result of human activity,
and we can't say that about many groups of birds elsewhere in the world. And not only that, but
there are some islands that are in as close to a natural or pristine state as it is possible to find.
And therefore, whatever we can find out through out studies about the relationship between
organisms, the finches, and the environment in contemporary time can be extrapolated -- without
any qualification about human influence -- can be extrapolated backwards in time to the times
when the evolutionary diversification took place.
[9:40] So, here then, is an outline of our talk. I will first introduce the diversity of the species
with an illustration of four only. Talk about speciation and the adaptive radiation. Give you
evidence for evolution when the environment changes. And then Rosemary will address the
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Peter R. and B. Rosemary Grant lecture – Darwin’s Finches
highly important critical question of what exactly constitutes the barrier to interbreeding between
two species. Well, that barrier occasionally leaks, species hybridize, and she will tell you what
we know about the causes of hybridization as well as the consequences.
[10:16] So, here then, is a brief overview of diversity, starting with perhaps the most famous of
all of the species, the woodpecker finch. The woodpecker finch uses a tool, a stick it fashions
itself in order to obtain a cryptic larvae from the environment. But the beak itself can be
considered a tool. And the beaks amongst the species vary enormously, and I'd like you to
concentrate on the beaks, their sizes, and their shapes, less on the plumage. There's a little bit of
variation in plumage color, hardly any unpatterned, but the beaks undoubtedly are the
centerpiece of the radiation because they vary so much. Here's a water finch, little eight gram
bird. Another bird bird, a large tree finch, has a completely different beak, and it functions in a
very, very different way. And then finally, here's the beak of a cactus finch with a tool
appropriate for probing cactus flowers.
[11:11] Now, it's called an adaptive radiation because one can easily see a correspondence, or a
match, between the nature of the beaks, the tools for dealing with foods, and the foods
themselves. A few years ago, Dosch Luter and I tried to go a little bit further than just making
that kind of matching correspondence. We asked, "Is it possible to be able to take information
from what is available in the matter of food supply on each of the islands and so understand the
way in which birds use the foods that we could predict, island by island, how many species there
would be on that island and which particular beaks they would have?"
[11:53] So it seems like a very difficult task. To be able to do that, you take the birds out of the
system and use the system itself minus the birds to predict what the birds would be doing. We,
never the less, managed to do this by developing an index of ecological opportunity on each of
the islands, and it is an index composed of two relationships. The first one is the relationship
between the size of seeds eaten by the graniferous species and their beak sizes. And
unsurprisingly big beak birds can crack open bigger seeds than small beak birds. And then the
second relationship is between the amount of food supply in the environment and the number, or
biomass, of finches supported by that food. And here, the data are summarized by islands and
you can see the unsurprising positive correlation between the two.
[12:46] So putting these two together, we came up with an expected population density of
finches of the graniferous sort in relation to beak sizes along that horizontal axis. Looking at
what would be the expected density a small beak bird, a medium beak bird, and a large beak bird
on these three islands. And the first thing that strikes you straight away is that the profiles of
ecological opportunity, sometimes we refer to those by the jargon term of adaptive landscapes,
the first thing that strikes you is that they're peaked. It's not a flat distribution, but there are one,
two, even three peaks or more on an island.
[13:31] So now the question is, where do these finches fit into these islands given the expected
peak population densities, and the answer is very close alignment, as indicated by the symbols
put underneath these peaks. There are three other features I would like to point out about this
figure. First of all, there is only one species aligned with each peak. You don't see two species
for any one peak. Secondly, there's no major peak that lacks a species. The ecological
opportunity has been responded to in evolutionary time by the diversification of the finches. And
the third thing is that the same peak on different islands may be occupied by different species.
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Peter R. and B. Rosemary Grant lecture – Darwin’s Finches
And that you can see by the different symbols under the small peak, the peak associated with
small beak size, on the middle and lower profiles.
[14:25] So I think there's a very strong, controversial argument that in the course of the radiation
multiple speciations have resulted in several species exploiting different aspects of the food
environment. It's much more difficult though to answer the question, "How exactly did
speciation take place?"
[14:46] And so, now I'm going to move to that topic and give you a simple Darwinian
cartoon-type diagram of the major views, not the sole views, but the major view about how
speciation takes place. It involves, in Darwin's language, three steps: colonization of a new area
through dispersal, adaptation to the new environment, and then finally, the coming together of
two derived products of this process separated by a barrier to interbreeding. Now what is that
barrier? How is it constituted?
[15:22] Well in this little cartoon, I have shown this with an arbitrarily chosen example on the
right-hand island of San Cristobal with a small figure of a finch and a large figure. So these are
symbols for two populations that have come together. And now the barrier to breeding may have
arisen solely as a result of adaptive change in allopatry, that is geographical isolation. And so,
when they came together they were fully formed different species.
[15:51] But more likely when they came together, there would be some adjustment. They
wouldn't be so completely different that they did not recognize each other as potential mates.
And then natural selection might be expected to work to the disadvantage of the intermediate
birds because they might interbreed with each other with low fitness and then might compete
with their parental species and suffer as a disadvantage because they are in the minority. That
second process, that divergence as a result of competitive interactions, is known as character
displacement, and I'm going to give you an example of that at the end of what I'm going to say.
[16:30] Now Rosemary's going to talk about the reproductive interactions at this crucial stage of
secondary contact. I'm going to start by giving you an example of the allopatric phase with a
species that is on the northern islands, not on the southern islands, as we see them here. So, bear
in mind on different islands, within the same species, populations are likely to differ according to
the nature of the food supply. That's the theme that I'm now going to develop.
[16:58] We start with this example of a sharp beaked ground finch -- that's the name of the
species -- high up on the island of Pinta occupying a forest where there's a predominance of hard
seeds, hard, cuticled insects, and mollusks - little snails - that this bird eats with a robust... it's
sharp, pointed, but it is, nevertheless, a robust beak.
[17:22] So, that's on that island, but on the low northeast island of Genovesa, there is no such
food. Another population of the same species feeds in a different way. Here the seeds are much
smaller, and they're softer, and the birds probe cactus flowers for nectar and pollen.
Correspondingly, and here's the association between morphology and diet, correspondingly,
these birds are small and with small beaks.
[17:48] Now, on the island of Wolf in the northwest of the archipelago, another population of the
same species has adapted to a different food supply. Here they have a rather robust beak, and
they use that as a tool for breaking open the eggs of sea birds that are called boobies.
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[18:07] If that doesn't work, if hammering away at this egg doesn't work, they use behavioral
stratagems to achieve the same end. Can you imagine that egg rolling along, and then falling off
a cliff, smashing, and thereafter, there is a free-for-all for the food.
[18:24] Well, if that's not bizarre enough, on this same island, the same species does the
following. It drinks blood, which it draws by pecking at the base of developing wing feathers of
this hapless bird, called a booby, sprouting forth blood as a result, and the bird will then drink the
blood. A habit we believe, and I think it's a reasonable supposition, that this probably derived
from feeding on hippoboscid flies.
[18:53] Now, hippoboscid flies are like mosquitoes. They fly up inside the feathers of sitting
birds, boobies in particular, and suck the blood. So, they're blood-filled insects that finches
probably fed on initially, and then since sometime later, and who knows how, they switched to
feeding on the boobies themselves, and in so doing, they shortened the food chain.
[19:18] So, you get the point. Different islands have different food supplies, different
opportunities for exploiting those different foods, and the species have changed in beaks as a
result of evolutionary processes in an adaptive way with a corresponding match between the
nature of the tool, and the nature of the task to be completed by it.
[19:39] That's the kind of argument that many of us evolutionary biologists make because we
can't go any further. But, it would be much better if we could show that natural selection as a
process producing the adaptive change that we only infer as a result of our studies to have
occurred in history with this comparison that I've just made.
[19:59] And as a process, natural selection has been demonstrated on this little island that
Quentin Wheeler circled once and wondered how anybody could want to go there. This is the
island of Daphne Major in the center of the archipelago, and people ask us, "What is it like to
work on this island?" So, the first two slides before I get back to science, I'm going to show you
brief little views of what it's like to be working on this island.
[20:25] The first one shows the bedroom -- I was going to nearly say the bathroom [laughs] -- the
bedroom, the dining room, and the laboratory where we do the work. And the second slide shows
how we do it. We put up nets. We capture birds. We take them out. We measure them in various
ways. Beak dimensions, we measure. Leg, wing, and we weigh them.
[20:48] And then having banded them with a unique combination of color bands and a numbered
metal band, we release them. We started in 1973. In 1988, we developed a technique for taking
blood without the need of liquid nitrogen, and since that year, from 1988 onward, we've been
bringing blood specimens, a single drop of blood, a minute amount, back to the United States for
DNA analysis. But when we started in 1973, that technique hadn't been invented, and we
measured and watched the birds to see what they did.
[21:21] Now, one of the questions right at the beginning was this. The finches differ markedly in
morphology. They've evolved divergently from common ancestors, so there must have been
some genetic variation for that process to take place because the species must be genetically
different. So, that implies any one population had genetic variation and could be added on by the
forces of selection shifting the population one way or the other.
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[21:51] How would we know about genetic variation governing traits like beak size, for
example? Well, the obvious way is to look for an association between parents and their offspring
because if there are traits that are inherited from parents by offspring, that should show up as a
positive relationship between, in this case, beak size of the offspring and the parents.
[22:15] So, we did a lot of work to establish the following relationship -- the average of the
mother's and the father's in beak depth, in this case. The average beak depth of the mother's and
the father's is a very good predictor of the average beak depth of the sons and the daughters.
[22:34] That relationship has a slope of .74, which is a measure of the inheritability of the trait, is
very high, and comparable to the inheritability height in humans. We humans have the same kind
of propensity to transmit genetic factors to our offspring to that degree, approximately three
quarters of the total maximum.
[22:59] So, there's a high degree of inheritance, therefore, in beak depth and other traits as well,
and then one can then take the question a little bit further and ask, "Well, what are the genetic
factors involved?" I'd like a pointer here, but I don't have it. Anyway, I don't need pointer to ask
you to look at the vertical scale and the high end of the vertical scale. I thank you very much. So,
well, I can't...I need another one. [laughs]
[23:26] [laughter]
Peter: [23:26] I'm sorry, that's greedy, isn't it? OK, notice the low end of the spectrum there
again. [23:33] [laughter]
Peter: [23:34] So, what is it that is genetically different about these individuals here from those
individuals at the top end of the spectrum here? We don't know. We don't know, but we're
heading in the right direction with a study of contrasting species to find out the genetic
differences between small-beaked and large-beaked species, and that is a stepping stone towards
being able to find out what makes the genetic difference within species, the genetic propensity,
therefore to evolve. [24:05] So, I'll tell you a little bit about what we know about genetic
differences between species. And here I'm referring to collaborative work that we have done with
two geneticists, Cliff Tabin and Arhat Abzhanov at the University of Harvard Medical School of
Genetics. They are the professionals. We've collaborated with them on everything except doing
the molecular work.
[24:27] And the question outstanding right at the beginning was, "What are the genes that make a
difference between a big-beaked bird like the large ground finch on the top, and the cactus finch
down at the bottom. So, they started by taking the known list of genetic factors responsible for
cranio-facial feature development in vertebrates, mammals in particular, and us humans even in
particular within that particular category.
[24:56] And they found one, a factor called a bone morphogenetic protein number four -- Bmp4,
for short -- that is expressed in our early embryonic development and mice and chickens and a
lot of other things as well. And they found that the expression at Day five in embryological
development is graded in a fashion exactly parallel with the variation in adult beaks between the
large beaks on the top and the most shallow beak of the cactus finch on the bottom, suggesting
there's more than just association.
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Peter R. and B. Rosemary Grant lecture – Darwin’s Finches
[25:34] I'll show you the pattern that shows that. Here's a diagram, and I'd like you to ignore the
right-hand panel, concentrate on the left one, and notice that Bmp4 expression at day five in the
upper mandible only -- we're looking at a plain, vertical slice through the upper mandible -- is
very intense at day five in that one, you hardly see any expression in that one, and you have to
imagine a graded variation in both of those. Cause and effect, or just simply correlation? A
perennial question for biologists.
[26:10] Well, to get at the possibility of a causal relationship, our collaborators did a nifty thing
of injecting, with a retroviral vector, Bmp4 from magnirostris, into a chicken at the same stage of
development to see if the Bmp4 from magnirostris, would convert a normal chicken into a kind
of magnirostris chicken. It did, as you can see from the middle one of these three panels.
[26:38] The top one is the control. The red double-headed arrow shows the normal beak, there is
the experimental treatment, and this bizarre horrible thing at the bottom, unfortunate thing has
been treated with another gene called noggin that antagonizes Bmp4. So the evidence is very
strong of a causal relationship, therefore, between Bmp4 and beak expression in this dimension
as well as, not shown in this picture, in the width.
[27:04] That leaves the question of what governs legs. Here they use the micro-ray technique to
go on a fishing expedition for genes that might be involved, and they found one, a very strongly
operating one. It's called calmodulin. It is expressed very intensely in these two species with very
long beaks; The Cactus and the Large Cactus Finch as you can see from there. It is graded, you
can hardly see that in this picture, but it is graded all the way from the long beak ones to the deep
beak ones.
[27:37] So two genes make a difference in beak shape, and it turns out that this one is operating
exactly the same time as Bmp4, but completely independently. So, any beak shaped different can
be achieved by a change of just one genetic factor. I'm not suggesting that there are only two
genes involved in the development of beaks there are lots, and lots, and lots. So this is really only
just the beginning of an investigation into genetic factors controlling beak size and beak shape
variations.
[28:07] This will eventually allow us to understand why there is this genetic variation within a
single population. Our guess is that the significant genetic variation doesn't lie in Bmp4 exactly;
we think that Bmp4 is probably very structurally similar amongst the species, but it's in the
whole complex regulatory apparatus governing the expression of this gene; that core ingredient
resulting in different adult sizes, lies in the regulation rather than the gene itself.
[28:42] Anyway, a very exciting beginning. That then tells you that the traits are heritable. They
genetically, therefore, potentially, malleable or labile. Now, what about environmental factors
that might be operating on this genetically variable trait? We're right at the beginning of our
study. As I said earlier, we banded off the birds, we watched them without having to capture
them again, we saw what they did; here's one cracking his seed, we new by his bands what his
beak dimensions were. We found the unsurprising thing that big beak birds could crack open
seeds that the small beak birds could not.
[29:19] Then in 1977, four years after we began, there was a severe drought in the archipelago.
Eighty-five percent of the medium ground finch population on the Island of Daphne died, and the
15 percent that survived were a non-random sample of the total. Large beak birds survived much
better than small beak birds, as shown in this diagram. Owing to the fact that they were able to
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crack open the large and hard seeds of Tribulus, this thing here measuring about a centimeter
long, a woody tissue in which there are hidden some seeds.
[29:58] Darwin would not have been at all surprised. He was challenged by one of his
correspondents to explain exactly what he meant by natural selection. Darwin chose an example
of birds to give an answer, and this was his answer: "I would now say," he said, "that of all birds
annually born, some will have a beak shape longer and some shaped shorter. And that under
conditions or habitats favoring longer beaks, all the individuals with beaks a little longer, will be
more apt to survive than those with beaks shorter than average.
[30:38] Well substitute beak depth for length, and basically that's what we found. One can ask
rhetorically, was it worth our while doing all that work if he knew it back in 1867? He also knew
that natural selection, which, by the way, is measured as that difference there between the start
and the finish of an episode like that; he knew that natural selection would have no evolutionary
consequences if the trait was not heritable. And I said earlier on the trait is highly heritable;
there's a high degree of genetic characterization underpinning the variation in beak. And so, with
that information it is possible to predict what the evolutionary change would be from one
generation to the next. And here is the so-called breeders equation that gives away a predicting.
[31:28] R, the evolutionary response to S selection is a function of selection strength and the
heritability or degree of inheritance. What you see above the dotted line, are the surviving adults.
They reproduced and produced a set of offspring, which, when fully grown, we measured in
order to compare the actual offspring average beak depth whereas the predicted one, which is the
broken line here, and there is the answer. Extraordinarily close, the prediction of an evolutionary
change was very closely matched by observations. Evolution therefore, had occurred by natural
selection on a genetically varying trait; functionally significant, functionally interpretable, when
the environment changed. But we learned a lot more about natural selection by following the fate
of this population through many environmental changes.
[32:27] And the one I am now going to talk about is the change that took place as a result of the
extraordinary amount of rain that fell in 1983, associated with an El Nio event, unprecedented in
the last 400 years, according the coral core data. But notice that two years later there's virtually
no rain; and then things changed.
[32:49] So first of all, rather than show you figures, or tables of numbers, here's some pictures to
show you what happened. Here's the normal dry season view of Daphne. The rain comes about
January, February, March, or April. The island becomes green, and in the foreground, one can
see Tribulus. This is the plant whose fruits, woody things like this, made the difference between
survival and non-survival in 1977. Only the big beak birds can crack open and get out the seeds.
[33:21] Well that plant was smothered in El Nio by the growth of grasses, first of all, but then
vines, and vines grew upon vines; vines grew over the bushes, they grew over the trees. They
grew over the bushes so much that the bushes disappeared. And even in the year after El Nio,
one could still see the aftermath of this extraordinary production of plants; principally small-seed
producing plants.
[33:49] So the island environment have been converted from one dominated by large and hard
seeds, to one dominated by small, soft seeds. And now the selective pendulum swung the other
way. Now the birds that have the selective advantage were the small beak birds. Small body
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sizes, birds with big tools for picking up and processing little seeds, small, soft seeds, at a rapid
rate to meet their daily energy requirements. And that happened repeatedly.
[34:17] And I'm now going to finish, before handing over to Rosemary, with a summary of the
long-term view of natural selection in this environment. The orange arrows indicate droughts.
They occur about as often as El Nios, and at each drought, there are high levels of mortality, and
survival depends upon the nature of the food supply produced in the wet years immediately
before the drought years.
[34:43] So, that pattern of recurring droughts implies oscillating directional selection, and that is
actually observed. The figure here is a little complicated, so I ask you to follow me through.
Fortis at the top and scandens are the medium ground finch and the cactus finch. And the panels
indicate selection coefficients -- the strength of selection on body size and beak size and beak
shape.
[35:11] If there were no selection, you would see a line from zero running all the way across
each panel, but you don't. You see histogram bars above and below the zero line indicating
fluctuating selection, and that in turn implies that morphologically these birds are not static.
They're not unchanging. Rather, they do change as a result of this oscillating selection, and once
again, that is matched by observations.
[35:40] The observations here laid out in the same panel, only instead of selection coefficients,
what you're looking at here are the mean values for body size, beak size, and so on. They would
stay within these parallel lines if there were no change across the time, but, in fact, they don't.
They move out of the initial confidence intervals, and so the remarkable thing is the birds now on
the island are not the same that they were when we started our study. Morphologically, they've
underdone change with this exception here, which I will put in a different frame here.
[36:17] Here is the one and only exception. This is a trait that increased the beak size, increased
markedly in the drought of '77, and then relaxed back again later. But, actually, this exception is
more apparent than real, because we had a drought on the island in 2004 -- 2003, 2004, into early
2005 -- and by coincidence, the amount of rain that fell in 2004 was exactly the same as in 1977.
So, all other things being equal, we would expect here another rise in the average beak size, but
instead, what we saw was an unprecedented drop in average beak size of the finches. This is the
medium ground finch population. And why?
[37:02] Well, all other things were not equal. There had been an invasion of another species onto
the island. Starting in 1983, the large ground finch established a breeding population built up in
numbers, I'll put it here, very gradually, and then getting faster and faster towards the year 2007,
so that by the time the drought struck, there were more than a couple of hundred large ground
finches on the island.
[37:28] So what happened was this. As the food crunch hit those populations, magnirostris, a
super competitor at crunching those Tribulus fruits, out-competed the larger members of the
medium ground finch population, so that the survivors, the ones who survived best...all the
individuals were at risk of dying, but the small beaked individuals in the medium ground finch
population had the survival advantage.
[37:55] So, here's the summary statement. I'll do it in two parts, one on this side. It goes like this.
Under stressful conditions where feeding on Tribulus makes a difference between survival and
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non-survival, in the absence of magnirostris, the large beak members of the medium ground
finch population have the selective advantage over the small beak members, and the average
population size of beak depth goes up.
[38:23] Now in the presence of magnirostris, on the other hand, under the same conditions, now
these ones are at a selective disadvantage. They're out-competed by these ones, and although the
small ones are dying, they're dying at a slower rate, so that the average beak size goes down.
[38:37] And the difference between medium ground finches and the large ground finches has
now expanded. It's increased. That is character displacement as envisaged in that little cartoon I
showed you of the speciation cycle. So, at this point, I'm going to hand over to Rosemary. This is
the point on the island which is the easiest one to climb on.
Rosemary Grant: [39:02] So, Peter has left us with two questions. How is the genetic
variability maintained, because he's shown that a selection oscillates backwards and forwards,
and under those conditions you would expect genetic variability to be eroded, but it's not. [39:18]
So, the next question is, "What is the barrier to interbreeding between these two species, fortis on
one hand and scandens on the other?" And the answer to both these questions is completely
related, as I will be about to show you.
[39:33] So, first, what is the barrier to interbreeding between species? Well, a very quick answer
is song and morphology, because the two species differ in song, and as Peter has shown you, in
morphology. They're very similar in all other respects. They build similar nests. They have
similar courtship display. And they're similar in plumage - males are black, and females are
brown.
[39:56] So, we first asked, "Can individuals discriminate on the basis of beak shape and body
size in the absence of any vocal cues?" And to do this, what we did is, we took two dead, stuffed
museum specimens -- a female fortis, and a female scandens -- and put them on either side of a
pole, took that pole into a territory, and asked if the territory owner could discriminate between
his own species female and the other species female.
[40:28] And the answer was a resounding, "Yes." They courted vigorously their own species,
and completely ignored the other one. So, we then asked, "Can individuals discriminate on the
basis of song in the absence of any morphological cues?"
[40:43] And we took recorded song, and we played back first of all fortis song. Fortis came into
the loudspeaker; scandens completely ignored the loud speaker. Played back scandens song,
scandens came in, and fortis ignored the song. So, clearly they can discriminate both on
morphology and song.
[41:04] And it turns out that between these two species, fortis and scandens, that song is very
important. So, what do we know about song? Well, song differs between a species. Scandens on
the left-hand side sings, "Cha cha cha cha cha," and fortis we call the "Swiss bird" because he
sings "mosly, musly, mosly, musly, mosly, musly."
[41:27] [laughter]
Rosemary: [41:28] [laughs] These birds sing just a short, simple song. There is individual
difference, so in the "musly, musly" one you get variations of "muesli, muesli" -- some are faster,
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some are slower. And in scandens you get variations in this "cha cha cha cha cha," and some are
faster and some are lower. But each individual bird only sings one song. [41:52] We also know
more, and this is work done by Bob Bowman many years ago, when you could take finches off
the Galapagos, and he took some to California and had a breeding population going. And he
found that song is learnt in association with morphology during a very short sensitive period of
time early in life between Day 10 and Day 40.
[42:15] And this period, Day 10 to Day 40, corresponds with the last few days that the birds are
in the nest, and when they are outside their nest being fed by their parents and mainly their
father.
[42:32] Now, once this song is learnt, it is absolutely retained for life. We have many hundreds
of birds recorded every single year, and we have never known one change its song, and lifetime
can last for as long as 16 years. So this is a typical Laurentian imprinting process whereby
species specific song is learned in association with parental morphology early in life and it
influences behavior later in life because a bird's mate according to their species specific song.
[43:14] So the consequence of this is a pre-mating barrier between the species. But we can ask
how robust is this barrier, does it ever leak? Because after all song is learnt and this imprinting
process would be very vulnerable to disruption if a young bird hears and learns another species'
song during its short, sensitive period. And this does happen, it happens very occasionally, it
happens typically if, scandens being a bit larger than fortis, sometimes takes over the fortis' nest,
usually it turfs out all the eggs, but occasionally an egg is left and that egg grows up as a fortis in
a scandens' nest and learns its foster father's song.
[44:01] It also happens with death of the father. Females do not sing, so if the father dies, and the
rest of the plutch is reared by the mother then what the birds will hear and learn is their
neighbor's song, their natal neighbor's song, and if that natal neighbor is a bird of another
species, it will learn that species' song. So we get these occasional learning of the wrong species'
song. And this rare learning of another species' song has led to hybridization. And I want to
stress at this point, hybridization has occurred throughout our whole study at this rare low rate.
And it is low, it is usually about one percent or perhaps even less. And these individuals mate
according to their song type so we get hybridization. And this hybridization gives us the
opportunity to test the degree of genetic incompatibility between the species which is
post-mating isolation.
[45:06] So we asked how fit are the hybrids? Are they viable? Are they fertile? And for the first
ten years of this study we had these hybrids -- one percent of each breeding time we got these
hybrids -- but none of the hybrids survived to breed. So we thought oh maybe this is because
they are genetically incompatible. Scandens and fortis are not sister species so they're not very
closely related. So we thought maybe this was genetic incompatibility but we also thought there
could be another reason. Hybrids are intermediate in beak size between the parental species and
during this time, as Peter showed you, the majority of seeds in the seed bank during the drought
were these large, hard Tribula seeds. And we watched hybrids trying to crack these large, hard
Tribula seeds, but none of them were successful. They could crack opuntia seeds, which is what
scandens will eat in the dry season, but they took two to three times as long as scandens did to do
this.
[46:12] And it seems that this was the correct explanation because after the El Nio of 1983 when
the island was converted from a large hard seed producer to the small soft seed and they became
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very abundant, hybrids survived. And they survived extremely well. But we can still ask, how
well did the hybrids survive relative to their parental species? So what we did is we took all the
birds that were born in 1983, 1987 and 1991 and we chose these years because there was a large
amount of rainfall, large numbers of birds were produced and we had a decent number of
hybrids.
[46:57] And this is a survival curve for these three cohorts of the parental species and fortis and
scandens over their lifetime and the cohort 1983, 1987, and 1991. Now if the hybrids survived
less well than the parental species we would expect the survival curve of the hybrids to lie below
that of the parental species, and instead, this is what we found. Hybrids survived very well, they
survived as well as the parental species if not better, and I say that because there was no
statistical significance between the survival, they also produced as many eggs, as many offspring
and as many recruits. So hybrids were doing extremely well and clearly there was no evidence of
incompatibility.
[47:51] So how did these hybrids mate? Let me just take you through this. We take this one
fortis-scandens here, and this is the result of a fortis father that had learnt a scandens song and so
his son also sang the scandens song and mated with a scandens female to produce the first back
cross generation, also singing a scandens' song mated with a scandens female to produce the
second back cross generation and the same on the fortis side. Now if this fortis-scandens was a
daughter and not a son, even though females do not sing, they do actually learn their father's
song and they still mated with the scandens. So the pattern is exactly the same whether it's for
males or for females.
[48:43] So the message is hybrids back cross according to the song pipe of their father, genes
will trickle from one species to another but the two species are kept apart by song. So this
implies that fortis and scandens are converging genetically and to test this what we did was to
standardized the difference, we took out 16 micro satellite loci, we standardized the difference
between the species in 1982 before there was any intragression, hybridization and intragression
to one. And then we followed the population through. And we found that the scandens'
population became increasingly similar to fortis in genetic composition and we did exactly the
same with our morphological measurements and we found exactly the same that scandens
population became increasingly similar in morphology. And the two lines almost exactly parallel
each other.
[49:41] So does this mean that the process of speciation is collapsing? Well, yes it does, but it
doesn't mean that it will go to complete collapse because the ecological food conditions,
allowing the hybrids to survive only occur episodically. For the first ten years of our study, the
food was not suitable for birds of intermediate condition, and they died. So what we see is a
fission in the first ten years of our study and a fusion in the last 20 years of our study.
[50:13] And so we have this fission/fusion dynamics. And during times of fusion, a fusion we
feel is genetic variation and this top slide shows an increase in heterozygocity and it also
enhances the morphological variation and you can see this through the beak shape variation
increase and so today scandens, and actually it's the same with fortis but I'm using scandens as an
example, it's really as though you were looking at a three foot or seven foot human, that is the
amount of variation by which it has increased. And this increase in genetic and morphological
variation on which selection can act, explains the answer to my first question, so it's episodic
intragression will explain why the genetic variation is not eroded.
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[51:08] So we can then ask, when does the pre-mating barrier never leak? When does
hybridization never occur? And the answer is after the species have become substantially
different in morphology and I can give you an example of this from the colonization of the big
beak bird, Geospiza magnirostris, that arrived on the island, as Peter said, in 1983, and the
population built up so that now there are over 200 individuals on the islands.
[51:38] And during this time, eight fortis imprinted or learnt a magnirostris song, but none
actually bred with a magnirostris and we were at first a little surprised about this, because fortis
and magnirostris are sister species. Genetically they're very closely related, much closer than
scandens and fortis.
[51:58] So we thought that it could be recognition. When the species are very different in size,
and magnirostris is almost twice the size of fortis, that they do not interbreed.
[52:10] But it could also be harassment, because when these poor little eight fortis opened their
mouths and sang magnirostris's song instead of singing "mosly, musly, mosly, musly," they went
"chee-a, chee-a" and every time they open their mouth to sing "chee-a" a magnirostris would
whip in from nowhere and just beat the living daylights out of them.
[52:33] [laughing]
[52:35] Now there was one poor little fortis that sang a magnirostris song and he sang and got
beaten up, he sang and he got beaten up, he sang a little quieter, he still got beaten up. He went
behind a bush and he sang a little quieter and he did this for years. And after about, I think it was
after about four or five years, he stopped singing altogether and then he got a mate. He got a
fortis mate but not a magnirostris. So the pre-mating barrier is robust when the size difference
between species is large, even learning the heterotypic song didn't lead to hybridization.
[53:16] But let's go back to this case where the barrier leaks when the size difference between the
species is small. But this only happens when the ecological conditions are suitable for survival of
birds with intermediate bill size.
[53:31] So how general is this process of episodic hybridization and introgression. We asked,
"Does it only happen on Daphne?" We saw that it also happened on Genovesa, another island
where we had done a long-term study. But we asked, "Could we see the footprints of
hybridization and introgression in the recent past on other islands in the Galapagos
Archipelago?"
[53:53] And we asked the question in the following way, or tried to answer it in the following
way - we said, "If the transfer of genes occurs episodically, species A should be genetically more
similar at neutral loci, like microsatellite loci, to closely related species B on the same island,
than to species B on a different island."
[54:14] That was a mouthful, but I can explain it a little bit better. I can say that if fortis and
scandens, who know have been introgressing genes on Daphne, so would fortis and scandens on
Daphne be more similar genetically at these microsatellite loci than fortis is to scandens on any
other island?
[54:36] And we did this for all species pairs of ground finches and we found most species of
ground finches are genetically more similar to a closely related sympatric species than they are to
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that species in allopatry. We also did it with tree finches and we found exactly the same pattern.
All or most of the dots are lying below the line.
[55:01] So it looks as though episodic introgression has been widespread in the Galapagos
Archipelago in all species pairs. So how important is this episodic gene exchange in the process
of speciation? Well, the radiation of the finches are very young. We estimate it to be about 2.8 to
three million years old. And so they lie around here. After lineages have become diagnosably
different, but long before the point where lineages cannot interbreed for the reasons of genetic
incompatibility.
[55:39] And this is not too surprising because Prager and Wilson showed that in birds and
reptiles, the average point at which genetic incompatibility arises is after they've been separated
for as long as 32 million years. So it's not too surprising that most of what we're seeing is
pre-mating isolation. This is an order of magnitude less for primates and mammals.
[56:08] So how important is episodic gene exchange in the process of speciation? We think it
could really be quite important and we argue that episodic introgression can be a rapid route to
change because it augments the genetic and phenotypic variation on which selection can act.
[56:29] So how general is this episodic hybridization and introgression in the wild? Well, if it is
important, we should see fission-fusion dynamics in the radiation, or amongst recently derived
species. So we looked at a variety of species and a variety of papers which have shown this, and
we find that hybridization and introgression is very common. You can think of it from bacteria,
the horizontal gene transfer, in plants, in insects, in fish, in amphibians, reptiles, birds, mammals
and primates.
[57:06] So in summary, how and why do species multiply? What have we been able to add to
this question? Well, why? Places like the Galapagos Archipelago, the environment with a large
number of islands with different ecological conditions, allows the independent evolution of
populations.
[57:26] How? Species differ in morphology. We now have some understanding of the genetics
underlying deep variation in work done by Cliff Tabin and Arhat Abzhanov, with the two
signaling molecules, Bmp4 and the calmodulin. Peter showed you that divergence in beak
morphology occurs through the cracking of environmental change by natural selection.
[57:50] And the pre-mating barrier is built from song, which is learnt, and morphology, which is
under genetic control. Birds mate according to the song they learn early in life in association
with parental morphology, and the barrier leaks when size differences between the species are
small. Rare learning of heterotypic song leads to hybridization and this is followed by
introgression, but only when ecological conditions are suitable for hybrid survival.
[58:20] And we think that episodic introgression can be important at early stages in the
speciation process, because it augments the genetic and phenotypic variation on which selection
acts, and in changing or new environments, this allows a population to move along a new
evolutionary trajectory.
[58:41] So we thank our many graduate students, post-doctoral fellows, collaborators and our
daughters who joined us on the island for many, many years. All our funding agencies, NSF
particularly has been a huge... nearly the whole of the study has funded us.
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[58:59] But I don't know about you, but whenever we are working on something we tend to see it
everywhere, so even in Picasso's eye, we see our Y-diagram with fortis on the left and
magnirostris on the right.
[59:14] But if that is a little bit too fanciful and a little bit too farfetched, let me leave you to
looking into the future, and with one message, which is a conservation message, that neither
species nor environments are static entities but they're dynamic, they're constantly changing, and
to conserve species and their environments, we must keep them both capable of further change.
Thank you.
[59:40] [applause]
[59:42] Announcer: This lecture is part of the Arizona State University Darwin Distinguished
Lecture Series, and is sponsored by the ASU Office of the President, the College of Liberal Arts
and Sciences, the School of Life Sciences, the Center for Biology and Society, and is a
production of Grass Roots Studio.
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