Prof: Welcome Orgo
survivors, and others.
I stuck this slide up,
sort of outside the framework
of the regular lecture,
and I did so just to indicate
that if you go through the
scientific literature,
you can probably find a neat
case of coevolution,
with some kind of beautiful
biology in it,
coming out every week.
 
This one came out last week.
 
This is a Proboscis fly that
lives in South Africa,
and it pollinates flowers.
 
And you can see that it has
evolved a very long proboscis,
and the flower has evolved a
very long nectary,
and it looks,
in fact, very much like
Darwin's orchid,
and that moth called Praedicta,
that Darwin predicted would
have a long proboscis.
But this is a fly.
 
This is not at all closely
related to moths,
and that flower is not at all
closely related to orchids.
So this is convergent evolution.
 
And I think you'll remember,
in reading the book,
that there was a neat
alternative hypothesis posed in
the book saying,
"Hey, it wasn't about the
coevolution of the flower and
the moth.
There's a spider that sits on
the orchid, and when the moth
flies in, the spider tries to
eat the moth;
and so the moth kind of evolved
a long proboscis so that it
wouldn't touch that flower with
anything but a ten-foot pole.
Okay?
 
So that was an alternative
hypothesis, and there's actually
some evidence for that in the
case of the orchid on
Madagascar.
 
But in the case of this
interaction,
which is in Cape Province in
South Africa,
with a fly and something that
is not at all an orchid,
the data indicate that,
in fact, a coevolutionary story
works just fine;
and that looks to be what's
going on.
 
The longer the nectary,
the more likely the
pollination;
the longer the proboscis,
the greater the energetic
reward--and the two things feed
back and forth to each other.
 
So this indicates actually that
Darwin's original idea was
probably correct.
 
And I would note that in the
case of the orchid on
Madagascar,
the fact that there's a spider
doesn't really mean that Darwin
was wrong in generating his
story,
it just means that there is
also something else going on.
 
Okay, so.
 
We spent the first part of the
course talking about
microevolution.
 
We spent the second part of the
course talking about
macroevolution.
 
And today and Monday,
we're going to talk about
coevolution and evolutionary
medicine as two areas in which
micro and macroevolution
interact in generating
explanations of things.
 
And I think that you'll
probably see,
if you think about it,
that in almost any reasonably
complicated or large-scale
biological pattern,
both things have been involved;
both micro and macroevolution.
There's been some things that
have been changing slowly and
some things that have been
changing quickly.
Now the tight genetic
definition of coevolution is
this.
 
In one species you have a
change in a gene,
and that--excuse me for missing
this;
I was doing proofreading this
morning;
there should be 't' there--it
stimulates an evolutionary
change in a gene in the other
species,
and that change in the other
species stimulates another
change in the first species;
so that you have kind of a gene
for gene succession in time.
 
One thing happens here;
that stimulates something here;
that stimulates something here.
 
That is the tight genetic
definition of coevolution.
If you could demonstrate that,
I think everybody would agree,
hey, you nailed it,
it's really there.
It's hard to do.
 
The reason it's hard to do is
that we don't normally know what
the genes are that involved.
 
We can see the phenotype,
but we have difficulty
inferring the genes.
 
There are some cases of this
that are well documented in
rusts, rust fungi inhabiting
wheat;
Ustilago hordii is one of them.
 
So, you know,
pathogens of crop plants are
things where this kind of
coevolution is well documented.
Another kind of coevolution is
phylogenetic.
So you use tree thinking to try
to infer what's been going on.
And you look at closely
interacting organisms--
pathogens, parasites,
pollinators,
things like that--
and you see if the trees can be
laid right on top of each other.
 
Or, if you have one group over
here--
so you have,
say, the pathogens over here
and you have the hosts over
here--
you see if the trees line up
and touch each other at the
tips.
 
That would indicate--without
any crosses,
so you don't see any lines kind
of crossing over when you line
them up--
that would mean that the trees
have exactly the same topology,
and that every time the host
speciated,
the pathogen speciated.
And if you see crossing lines,
it means that a pathogen has
jumped from one host to another.
 
So that kind of approach gives
you another definition of
coevolution, and another tool
for trying to infer it.
Now before I get into
coevolution proper,
I want to talk a little bit
about co-adaptation,
because co-adaptation actually
contains within it a message
that's of general significance
for coevolution.
Right at the beginning of life,
the first replicators had to
co-adapt in order to generate
say a well-functioning
hypercycle;
they had to co-adapt to each
other.
 
And at the level of the cell,
when you're looking at key
molecules in the cell,
all these interactions have
co-adapted to each other.
 
So, for example,
the ribosome here is in green,
and you've got the mRNA coming
into it like a ribbon,
and you've got--the transfer
RNA is pulling in the amino
acids out at their tips,
into the reaction center of the
ribosome.
 
And that brings the amino acids
into close juxtaposition where
an enzyme can operate on them to
join them,
and then clip them off of the
incoming tRNAs,
which then go on out,
back into the cell to do their
job again,
and the protein grows out here.
Well, this is a rough sketch of
the structure of the ribosome.
It's actually more complicated
than that, and it has really a
beautifully sculpted reaction
center in the middle of it.
And the message from this is
that every single important
biochemical step and
morphological structure inside
the cell is tightly co-adapted,
so that form matches function,
throughout the cell.
 
And the reason that's the case
is that these things are
processing reactions that happen
thousands of times a second,
and that therefore accumulate
to have big effects over the
lifetime of the organism.
 
If you've got something in you
that is going to happen say 50
billion times in your lifetime,
and you get a very,
very tiny, 1/1000^(th) of 1%
change in it,
that then accumulates 50
billion times,
you have a massive result at
the end of your life.
So that things that are
happening down at that level are
driven by high frequency
interactions.
And the frequency with which
things interact is one of the
key elements of coevolution,
in general.
If you look at a slightly
higher level in the cell,
you can find co-adaptation
going on again.
The axons that run into nerve
fibers have different lengths,
so that the signal coming from
the brain will arrive at things
that need to be coordinated at
the same time.
The muscles in electric eels
have been turned into storage
batteries,
and the axons that run from the
brain have had their lengths
modified,
so that they hit the different
cells in the storage battery at
exactly the same instance,
so that the electrical charge
goes out,
all at the same time.
A four- or five-foot electric
eel can kill a horse;
that's how much electricity
they can store up.
But they can only do it because
it's released exactly at the
same time.
 
If it dribbled out,
it wouldn't take the horse
down;
or the naturalist exploring the
shallow river in South America.
 
Right?
 
Same kind of thing in your
brain.
There's very tight
co-adaptation between your
retina and its projections into
the visual cortex at the back of
your brain.
 
So these connections have been
sculpted by evolution so that
the re-creation of the external
world, in your head,
is precise.
 
And this has gone on in every
organ of your body in one way or
another.
 
So the integration of the
organism is achieved by
co-adaptation of its parts.
 
That's not precisely the gene
for gene kind of interaction
between species,
that people think about in
coevolution,
but it is a gene for gene
interaction in the determination
of those organ systems.
A gene changes over here,
and another gene has to change
over there.
 
It's just that the process is
going on inside a single genome,
rather than in two different
genomes.
So that's not normally what
biologists mean by coevolution.
It usually refers to the mutual
adjustment of the genomes of
separate species.
 
And that's kind of arbitrary I
think,
and the reason I think it's
arbitrary is that we now
conceive of the organism as kind
of a babushka doll of nested
levels of hierarchies that have
been assembled over the course
of the evolution of life,
and that things that we now see
as being integrated organisms,
earlier, were independently
evolving systems,
and at that point the
coevolution, that we now see as
co-adaptation,
was actually coevolution sensu
strictu.
So I'm now going to talk about
some intercellular symbioses.
And the reason I picked
intercellular symbioses as the
first example of real
coevolution is that these things
are very intimate coevolutionary
interactions.
And you can see that in
mitochondria and chloroplasts of
course.
 
Then there's this wonderful and
interesting critter called
Wolbachia, that does lots of
things to arthropods.
The whole issue of the
symbiosis of algae in reef
building corals contains a lot
of beautiful biology,
and some interesting puzzles.
 
And in all of these cases the
interacting parts are really
closely connected.
 
Okay?
 
So there's been a lot of
evolution at the level of
intercellular metabolism.
 
And I think that these tight
symbioses are really major
transitions in the process of
being born.
So one of the issues in a major
transition is whether or not you
have a change in the pattern of
genetic transmission.
And in these cases independent
genomes are getting aligned,
and in the extreme case of
mitochondria or chloroplasts,
they actually have the same
pattern of transmission as the
maternal nuclear genomes,
of the host.
Okay?
 
So previously independent
things are being integrated.
Conflicts are being at least
partially resolved;
although there are traces of
these conflicts--as I told you
earlier, there are mitochondrial
cancers;
mitochondria do occasionally
get out of control.
And there are things like the
petite mutation in yeast,
which is a mitochondrial issue.
 
And then this new more or less
well integrated unit has a
performance.
 
That performance can vary among
units, and therefore natural
selection is starting to act on
the new unit.
So at the formation of the
eukaryotes,
when the mitochondria came in,
you had a new unit,
and then it was going to
perform with respect to other
such units,
depending on how well the
mitochondria were adapted to the
nuclear genome;
and that's a coevolutionary
process.
Okay, so with mitochondria
you've got all kinds of
communication and coordination
going on.
The cell membrane of the
previously independent purple
sulfur bacterium,
out here, now has within it an
inner membrane that has got all
kinds of biochemical machinery
on its surface.
 
And this is where the citric
acid cycle takes place,
where electrons go down the
electron transport chain,
making ATP, and in the process
letting a few protons leak out
into the cytoplasm,
which cause oxidative damage.
So if you are worried about
eating your blueberries and
drinking your pomegranate juice,
it is because mitochondria leak
protons and basically create
hydrogen peroxide in your
cytoplasm,
and hydrogen peroxide is highly
oxidative and can do damage in
the cell;
and there's lots of kinds of
repair machinery to deal with
that.
 
This process here of exporting
energy to the cell and getting
information and substrate into
the mitochondrion is a tightly
coordinated one,
and there have been lots of
modifications to the
mitochondrial membrane to make
it an appropriate filter for the
transport of goods,
in and out.
 
So it's been heavily modified
by coevolution.
Now, Wolbachia.
 
Wolbachia are very cool
bacteria.
They're cytoplasmic parasites.
 
They live in the cytoplasm of
arthropods.
So they occur in insects and
crustacea.
They sometimes occur in
nematodes.
They seem to be able to get
into things, generally speaking,
in that large chunk of the
tree, which is called the
ecdysozoa.
 
And if you just think about the
interests of the Wolbachia,
it can only get into the next
generation if it is in a female,
because it is transmitted,
like other cytoplasmic
organelles,
only through eggs and not
through sperm.
 
Now this creates some issues
for Wolbachia,
because if they end up in a
male, they're dead.
So they have evolved some
interesting ways out of that.
They can induce
parthenogenesis,
in some species.
 
So they will take that female
and they will make her asexual,
and then she makes only female
babies.
So they get into the eggs of
all of them.
They can feminize male hosts,
in pill bugs--
so Armadillidium,
the little pill bug that you
can find turning over logs--
it's an isopod and a
crustacean--and when Wolbachia
gets into Armadillidium,
basically it takes males,
and it has developed a method
of interfering with its sex
determination process and
development,
so that anything that's got a
Wolbachia in it will grow up to
be a female.
Now, as Wolbachia--and by the
way, this creates a huge
reproductive advantage for those
females, and they start to
spread through the population.
 
They're not suffering the
twofold cost of sex.
They're only making female
children.
They spread,
and they take over the
population.
 
And then, because there aren't
any males in the population,
and it's still a sexual
species, Armadillidium goes
locally extinct;
being driven to extinction by
the selfish cytoplasmic parasite
that it has.
And the response of some,
but not all,
Armadillidium populations has
been clever.
They have cut out the sex
determining part of the
bacterial chromosome and put it
into their nucleus and spliced
it onto one of their own
chromosomes,
so that there is now vertical
transmission of that selfish,
sex-determining element.
 
They don't really care very
much about the rest of the
bacterial genome that's been
causing all this problem.
The only thing that's really
critical is that they got the
sex determining part out,
and they spliced it into their
nuclear genome,
through a process that we don't
really understand.
 
All we can see is that we can
observe, in some populations,
that today that's the case.
 
This means that the conflict
has been removed,
at least for that
sex-determining element,
because now it's being
vertically transmitted through
both the male and female line,
because it's in a nucleus.
So the conflict disappears,
and a 50:50 sex ratio is
re-established;
well after awhile,
because now there's a new sex
chromosome.
Okay?
 
So now you have three sex
chromosomes, rather than two,
for awhile, and so there's a
bit of chaos in sex ratios.
And then that stabilizes;
you get back to 50:50 sex
ratios.
 
And then it gets infected by
Wolbachia, and the whole thing
starts over again.
 
And in some cases you can take
the genome of a Armadillidium
pill bug,
and sequence it,
and you can find four or five
fossilized,
sex determining chunks of DNA,
that have been stuck into it.
So there's an interesting
coevolutionary process going on
there.
 
In fruit flies and drosophila,
they cause reproductive
isolation, and they do that by
cytoplasmic incompatibility.
That means that a fruit fly is
only going to be able to have
offspring,
if it's mating with a Wolbachia
infested fruit fly,
if it's got the same Wolbachia
in it.
 
So Wolbachia are biochemical
geniuses and developmental
geniuses.
 
They have learned how to
manipulate the sex ratios and
mating success of their hosts,
and they really haven't been
domesticated.
 
And this is kind of interesting
if you go back to the whole
issue of well what happened when
mitochondria first started
getting into the eukaryotic
lineage?
Was there a period 15 hundred
million years when this kind of
stuff was going on?
 
Probably was.
 
It probably took some time to
resolve conflicts and really to
integrate the mitochondria into
the eukaryotic lineage.
So when we think about that
overall process of interacting
genomes, as I mentioned the
frequency of interaction is
really quite important.
 
You're not going to get tight
co-adaptation of two different
species unless they interact
with each other very frequently.
If they're only interacting
with each other occasionally,
then there's a lot of stuff
going on,
outside of the interaction,
that has costs and benefits,
that is going to be tweaking
the interaction traits in other
directions.
 
So it's got to be a very
consistent and persistent
process, to result in tight
co-adaptation.
So frequency is important.
 
And then, of course,
when they interact it must make
some difference to reproductive
success.
Then there's the issue of
relative evolutionary potential:
who's got the bigger population
size;
who has the shorter generation
time;
who has more genetic variation?
 
Those things are certainly
going to help determine the
outcome.
 
And then there's this issue of
the Red Queen,
which I will come to.
 
So there are some kinds of
interactions,
ecological interactions,
that favor strong coevolution
and specialization.
 
Parasite host interactions,
especially where the--this is
normally a case where the whole
live cycle is completed on a
single host;
plant/herbivore and
predator/prey interactions,
where you have got a fairly
narrow range of species that are
being eaten by the herbivore or
by the predator.
 
And there's one here--pandas
just eat bamboo,
and therefore that sixth
appendage,
the panda's thumb,
which is there for handling the
bamboo shoot,
has evolved.
Sage grouse basically just eat
sage--they're herbivores--and
sage has an awful lot of
upsetting biochemistry in it.
If you were to go out into the
American West and try to live
for a week on sage,
in the Great Basin,
you would become very sick.
 
Sage grouse do it just fine.
 
They've got all kinds of--it's
probably Cytochrome P450s that
are the enzymes that are
denaturing the plant products
that would make us sick.
 
But the one which is really
kind of sad and funny is the
aardwolf.
 
The aardwolf is a hyena that
has specialized on eating ants
and termites;
that's the only thing it eats,
as an adult.
 
Baby aardwolves grow up with
milk, from mom.
And my friend,
Tim Clutton-Brock,
has watched the weaning process
in an aardwolf,
where mother is trying to
convince baby to switch from
milk to ants.
 
>
 
And baby is not happy.
 
Those ants do not taste good.
 
And fortunately baby probably
doesn't realize that this is the
rest of life;
from here on out it's ants,
all the way through.
 
Okay?
 
So that's real specialization.
 
Another interaction that favors
specialization is mutualism,
where you have interactions
that are already positive,
or are becoming positive.
 
They have symmetrical impacts
on reproductive success,
and these things are living in
intimate contact for most or all
of their life cycle.
 
And mutualisms are very
interesting and they make
wonderful natural history,
but they also carry the message
that where it's a win-win
situation,
evolution is not always about
competition.
Evolution can be about both
sides profiting from the
interaction and doing better
because of it,
and that ends up in a
mutualistic relationship.
So the relative evolutionary
potential basically is
determined first by generation
time;
second by sexual mode.
 
Sexual partners can evolve more
rapidly than asexual partners,
and the partner that therefore
has more genetic variation,
for the interaction trait,
will evolve more rapidly.
So to some degree we kind of
predict how the coevolutionary
process will occur.
 
Now the Red Queen,
which comes from Through the
Looking Glass,
by Lewis Carroll--and I'll go
into that a little bit more--
is the idea that there is an
open-ended struggle that results
in no long-term reduction in
extinction probability.
 
Here's an example of a Red
Queen process;
there are many.
 
But this would be a
host/parasite interaction.
And what you see here is
generation time for things that
have about the same generation
time.
Okay?
 
So we have a host and a
parasite that have roughly the
same generation time.
 
This is the frequency of an
allele.
And these are interaction
alleles.
So these are genes that are
determining how well that
parasite will do on this host,
and how well this host will
resist that parasite.
 
And what's going on here is
that when a certain host allele
goes up to high frequency,
that turns out to be one that
this orange parasite allele can
attack very well.
And so the host has gone into a
state that's susceptible to
parasite attack;
therefore that parasite allele
increases in frequency.
 
But, because that parasite
allele is going up here,
it's killing a lot of hosts up
here, that host allele drops in
frequency.
 
As soon as that one drops in
frequency, it makes the host
less susceptible,
and the parasite allele drops
in frequency.
 
And you can see there's a lag,
there's a lag time between the
two.
 
Here it's sketched at about two
or three generations.
So this light rectangle here is
indicating where the host is not
having a problem,
and the grey rectangle is
indicating where the host is
having a problem.
So Leigh Van Valen is a
paleontologist at the University
of Chicago who came up with the
Red Queen hypothesis in 1973.
And he claimed that in fact
it's not just hosts and
parasites;
he claimed all life on earth is
in fact caught up in a
coevolutionary web of
interactions.
 
And his evidence for that is
that the long-term extinction
rate is constant.
 
If you look over the
Phanerozoic, if you look over
the last 550 million years,
the probability that a species
will go extinct,
within a given period of time,
has remained roughly constant.
 
There's some slight evidence
that maybe species have started
to live a little bit longer.
 
But, you know,
broad brush,
this claim is correct.
 
Things have not gotten better
at persisting,
over the last 500 million
years.
So in some sense I think
Leigh's claim is probably true.
Every time a species on earth
tries to get a leg up,
some other species compensates.
 
So this is where that term
comes from.
This is an illustration from
Through the Looking Glass
by Charles Dodgson (Lewis
Carroll).
This--Alice is a pawn on a
chessboard,
and Alice is supposed to,
in this mental game,
march down the chessboard and
get turned into a queen,
when she reaches the end.
 
And the Red Queen,
who is next to her,
says, "Alice,
this is a game in which you run
as fast as you can and you can
only stay in place."
So it's like one of those
nightmares that you have,
where you're running as fast as
you possibly can,
and you can't get away.
 
That's Leigh Van Valen's
metaphor for evolution:
everybody is running as hard as
they can and they're just
staying in place;
their fitness is not long-term
improving.
 
Now I'd like to give you a few
striking outcomes of
coevolution.
 
I'm going to do butterfly
mimics, reef-building corals,
leafcutter ants,
and rinderpest.
And each of these is making a
slightly different kind of
point, but each of them involves
some absolutely stunning natural
history.
 
So let's start with mimics and
models.
And these guys are,
by the way, all from the
Peabody Museum Collections.
 
So, you know,
if you love butterflies,
you can go over and talk to the
invertebrate curator at the
Peabody Collections,
and he can pull out tray after
tray after tray of thousands of
beautiful butterflies.
We had one of the great
butterfly biologists here,
Charles Remington.
 
And he was buddies with
Vladimir Nabokov,
who not only wrote
Lolita,
but was a lepidopterist,
and so we've got some Nabokov
butterflies in the collection as
well.
I don't know if any of these
are from Nabokov.
Okay?
 
So in Batesian mimicry you've
got an edible model that evolves
to resemble a warningly colored
noxious species.
Okay?
 
So actually what's going
on--I've actually misphrased
that a little bit.
 
The noxious one is going to be
the model, and the edible one is
going to be the mimic.
 
Sorry about that.
 
I'm going to go back and
correct that.
So the mimic is good to eat and
the model is bad to eat.
And on Madagascar there aren't
any models, and the male and the
female look the same in this
species.
But as you go out,
through Africa,
you find that in different
places in Africa there are
different nasty tasting models,
and the female turns into
something that looks very much
like them.
So this thing has evolved into
all of these other things,
depending upon where they are,
in Africa.
Now this is not simple.
 
It takes a lot of genes to turn
something like that into
something like that.
 
And when you go into a
neighboring race--it's still in
the same species;
the males are still looking
like that--you have to have a
whole bunch of coordinated
changes to make it into the
other one.
So what's happened is that
these genes have been pulled
together,
onto a chromosome,
and turned into a super-gene
complex,
which has been inverted so that
it doesn't recombine,
and they're inherited as a
package.
Now in Mullerian mimicry you
have a process whereby things
that all taste bad evolve to
look like each other.
Can anybody tell me why things
that all taste bad might evolve
to look like each other?
 
What's the advantage in that?
 
Yes?
 
Student: 
>
Prof: Right, exactly.
 
So basically what they're doing
is they're making it as easy as
possible for the predator's
learning process to figure out
that all things that look like
this taste bad.
They're reducing the mistake
rate, in the things that are
learning not to eat them.
 
So these are the Heliconia
butterflies of South America,
and they live all on passion
fruit vines.
So there's a big radiation of
different species of passion
fruit in South America,
and these butterflies all lay
their eggs on those different
species of passion fruit,
and where they overlap,
the different species have
evolved to look like each other.
 
So what we have here is
Mullerian mimicry going on here,
and here;
and we have Batesian going
on--excuse, me,
this is all Mullerian;
this is Batesian mimicry.
 
So Mullerian is everybody
distasteful.
This is a Batesian mimic of all
of these distasteful models.
This is a Batesian mimic of all
of these distasteful models;
and so forth.
 
So, those are pretty precise
adaptations.
I mean, if it gets to the point
where a good naturalist really
has to puzzle for awhile to
identify whether you're looking-
dealing with the model or with
the mimic,
and has to really know their
details of morphology,
it means that natural selection
has precisely adjusted virtually
every part of the body,
so that the mimic really looks
like the model.
 
Now a tight symbiotic
relationship is between- is the
one that's between
dinoflagellates,
that are called zooxanthellae,
and their corals.
And there are also--so here is
a coral.
And, by the way,
there are also zooxanthellae
living in the lip of this giant
clam.
So this giant clam and the
coral are both farming algae.
And the algae are
photosynthesizing and delivering
photosynthate,
to the host.
And you can see here the
chloroplast of one of these
algae, and its body is in here,
and it is producing
photosynthate;
and these are the starches that
it's accumulating.
 
Now the relationship goes
something like this.
The dynoflagellates,
which by the way look like this
when they're out in open water;
they're really quite lovely.
And remember,
these are some of the guys that
have so many membranes around
their chloroplasts,
because they're the result of
three or four ingestion events
over evolutionary time.
 
If they produce say 250 joules
of energy, through
photosynthesis,
they export 225 of it to the
corals;
and they only put about .2 into
growth and 25 into respiration.
 
So they've been almost
completely domesticated.
Pig farmers have been trying
for hundreds of years to get
pigs that would be this
efficient,
for humans, and these corals
have turned these
dinoflagellates into a energy
conversion machine that's just
incredibly efficient,
from their own point of view.
The corals, of course,
have tentacles,
and they will feed on
zooplankton and stuff which is
out there,
but they only get about
1/10^(th) of their energy from
feeding directly;
they get most of it from
photosynthesis.
And then what they do is they
put a little bit of it into
growth.
 
They put a lot of it into their
calcified skeleton--so basically
you're looking at where reefs
come from;
this is how a reef is
produced--and then they lose
quite a bit to respiration and
to the mucus that they produce
in their feeding.
 
So they're getting about ten
times the energy from their
symbiotic algae as they are from
direct feeding.
Now one of the implications of
this is this is why you do not
find reef-building corals deeper
than 20 meters.
It's because there's not enough
light for the algae,
any deeper than 20 meters.
 
Okay?
 
Now the crazy thing about this
system is that a baby coral has
to acquire the algae in each
generation, and the algae exist
as independent species.
 
So the algae are actually
incredibly phenotypically
plastic;
they have a free-living form,
and they have a domesticated
form, and they can reproduce
both ways.
 
And that's very interesting
because from the point of view
of the algae,
the free-living form is the
source and the domesticated form
is a sink;
and it's therefore puzzling to
see how it was that the corals
were able to engineer the algae.
 
There's got to be some kind of
coupling of the cycle so that
what goes on in the coral feeds
back into the free-living form;
otherwise you couldn't get this
tight adaptation.
They're re-domesticated in each
generation, in the coral.
Okay, now for a
macroevolutionary,
coevolutionary story.
 
How many of you have been in
the Tropics and have seen
leafcutting ants?
 
Four or five, six.
 
These guys are great,
and they form huge colonies.
The chamber that they can form
is the size of this dais up
here.
 
It will be three or four feet
high,
and if you're out in a
rainforest, the cutting
activities of the workers will
actually clear all the leaves
off the trees,
over the chamber,
right to the canopy;
so you kind of exist in a well
in the forest,
where the ants have essentially
punched right through,
200,250 feet up,
taking out all the leaves.
 
And they take them down,
into their underground chamber,
where they chew them up and
they feed them to a fungus.
And they domesticated this
fungus 50 million years ago.
Okay?
 
Humans figured out how to
domesticate wheat 10,000 years
ago.
 
The ants domesticated the
fungus 50 million years ago.
They're the first farmers;
well the corals probably did it
earlier.
 
Okay?
 
But this is another
domestication event.
So they cultivate this fungus
clonally.
The fungus can't reproduce
sexually, in the colony,
and it looks like it's been
asexual ever since it was
domesticated.
 
It's a monoculture.
 
Now in human agriculture,
a monoculture is incredibly
vulnerable to plant diseases.
 
Having a continent covered by a
single strain of wheat,
or a single strain of sorghum,
or a single strain of sugarcane
is a bad idea,
because pathogens will evolve
onto that particular monoculture
genotype,
and they can go through in an
epidemic and wipe the whole
thing out.
 
So having a mix of genotypes in
agriculture is a very good idea.
Well that's not what the
leafcutter ants did.
They have a pathogen that can
attack their own--okay?--and
it's also a fungus.
 
So there's another fungus that
can come into the colony and
take over their own fungus.
 
But to fight it,
they cultivate a bacterium,
and they use that bacterium as
a defense against the enemy
fungus.
 
And they have a- they've
evolved a special morphological
pouch in which they carry this
bacterium.
And you'll notice that because
it's a bacterium,
it has a short generation time.
 
So they have the coevolutionary
arms race matched up in terms of
timing.
 
They have a bacterium that can
evolve as fast,
or faster, than the fungus that
infects them.
So they have not only
domesticated their food supply,
they've also invented a health
delivery system to keep it
healthy;
they have a pharmacy.
Now if you look at the
macroevolution of this system,
what you see here basically is
the phylogeny of the ant,
the phylogeny of their fungus,
and the phylogeny of their
parasite,
over here.
And the thing that I want you
to notice is that although it's
not absolutely precise,
these things match up pretty
well.
 
So the parts that are in
blue--I mean,
sometimes you find a few more
parasites,
hitting a few more cultivars,
but roughly speaking if there's
a branch at a certain point in
the tree,
it is a branch for all three
things.
It's not precisely matched,
but it's pretty close.
This is an amazing system.
 
And when Ulrich Mueller,
who has worked on it--and this
is actually-- he's a co-author
on this paper.
He's a professor at the
University of Texas in Austin.
When he visited and gave a talk
on it, I asked Ulrich,
"How did you come to this
system?"
And he said,
"Well, about twenty-five
years ago I took an OTS course,
and we were sitting there in
Costa Rica,
and we played the 50 Questions
game,
and my question was about
leafcutter ants."
 
And that's his career.
 
Okay?
 
Questions have profound
influence.
Okay, rinderpest,
the final one in this series.
The point about rinderpest is
this.
I'm giving you this example to
show you what happens when
evolution has not occurred;
and that gives you a feel for
what has happened when evolution
has occurred.
Okay?
 
So this is the rinderpest
pathogen.
It's a virus,
and it attacks cattle,
buffalo, eland,
kudu, giraffe,
bushbuck, warthogs and bush
pigs;
those are all ungulates.
 
So it is attacking one clade on
the mammalian tree;
they're all things that have
two hooves.
And it evolved in Asia,
and it came into Europe through
human invasions,
repeatedly.
So things in Asia and Europe
had evolutionary experience of
rinderpest;
they'd been exposed to this
disease.
 
However, things in Africa had
not, and it got into Africa
probably either when the
Italians went into Somaliland,
or when General Gordon brought
in some Russian cattle when he
went to relieve Khartoum;
so in the 1880s rinderpest got
into Africa, and it came in
because Europeans were bringing
cattle in with them.
 
And by 1890,
it had crossed the Sahara,
and gotten into Southern
Africa.
So there were some direct
consequences.
It eliminated--in the 1890s it
took out most of the domestic
cattle and wild buffalo,
and many related bovids.
This caused enormous famine and
disruption in the humans who
were living in Africa and who
either had domestic cattle or
nomadic cattle.
 
So, you know,
the Masai really got hammered
by this.
 
Only one species went
extinct--it was a species of
antelope--
but the distributions of all of
the other wild ungulates in
Africa were altered,
and they remain altered to this
day.
They're springing back in some
areas, and there are now
vaccines for rinderpest that are
being used on domestic cattle in
places like South Africa.
 
So the distributions are
altering, but you can still see
the signature of the event.
 
People lost food supplies,
and there was an outbreak of
endemic smallpox,
while this was going on.
So it started causing a cascade
of effects, through the
ecosystem.
 
There were epizootics--an
epizootic is like an epidemic,
except it happens in
populations of wild animals.
So there were epizootics in
1917/18;
so right at the time of the
outbreak of the World Flu
Epidemic,
people in Africa were also
getting hammered by another
outbreak of rinderpest hitting
their animals.
 
1923; 1938 to '41.
 
This is the kind of habitat in
which rinderpest was spreading.
There were some interesting
indirect consequences.
So over a lot of the infected
area,
tsetse flies disappeared,
and the reason tsetse flies
disappeared is that they make
their living off of wild
ungulates.
 
So if there aren't any
wildebeest or giraffes around
for the tsetse flies to eat,
they will disappear from the
area.
 
Now they require trees and
bushes as their habitat,
and herbivores for their food.
 
Now when the herbivores
disappeared because of
rinderpest,
the tsetses lost their food,
but their habitat sprang up,
because there weren't ungulates
eating the bushes that the
tsetse flies would live in.
When things like wildebeest
disappeared, the lions got
hungry, and there were outbreaks
of man-eating lions.
So in the 1920s,
during a rinderpest epidemic,
there was one lion that killed
84 people.
When I first went to Queen
Elizabeth National Park,
in 1992, there were people
living in the park,
squatters living in the park,
and they would try to get to
the store at Park Headquarters,
on a bicycle,
and the lions had learned that
it was possible to separate that
blob on top of this funny
two-wheeled thing,
from what was moving so fast.
 
And so like pussycats chasing
balls of twine,
they had gotten into knocking
over bicycles and eating people,
and there had been thirteen
people who had been killed in
the two months before we
arrived,
in Queen Elizabeth National
Park.
That kind of thing still goes
on.
So the lions contributed to the
abandonment of big areas,
and thickets of brush grew up.
 
So the ungulates went down,
and the people pulled back,
and the bushes grew.
 
Now when the ungulates
developed some immunity to
rinderpest,
and they moved back into the
abandoned farming areas,
they then became hosts for
tsetse flies that could now live
in the new bushes.
Okay?
 
So you see rinderpest goes in,
and it changes a bunch of stuff
ecologically,
and it changes the geography of
Africa.
 
And the flies transmit sleeping
sickness;
so they do that,
by the way, both in the
ungulates and--sleeping sickness
is a real problem in domestic
cattle, as well as in people.
 
And so the humans really pulled
out of this area,
and they remained absent even
after the lions switched back to
eating the ungulates.
 
If you go into the Serengeti,
just west of Seronera,
there is a valley between
Seronera and Lake Victoria,
which is called The Valley of
Death,
and that's because of the
sleeping sickness that's endemic
in the valley;
and that's an example of what
happens in this process.
 
And by the way,
we call these areas now,
to a certain extent,
the National Parks of Africa.
So if you wonder why those
parks are where they are,
in part it's due to the history
that I just told you.
So rinderpest changed the
ecological structure of at least
half a continent,
for about a century.
The consequences were pretty
bad, and they were only kind of
predictable in retrospect.
 
Nobody had the knowledge,
when General Gordon relieved
Khartoum,
with a few Russian cattle in
his supply train,
that they were carrying a virus
that would do this to a whole
continent.
Okay?
 
I think that this is one of
those places where we have to be
extremely modest about how much
we understand about ecology and
evolution.
 
Bad shit can happen.
 
So the same thing happened in
the New World when Europeans,
who were relatively resistant
to smallpox and measles and
things like that,
brought with them their
diseases, and that is why they
were able to overthrow the Aztec
civilization.
 
If you ever ask yourself,
how the heck did a couple of
hundred Conquistadores wipe out
an Aztec army of 100,000,
the answer is the Aztecs were
all sick and dying,
and by the time the
Conquistadores got to Mexico
City,
from Vera Cruz,
the epidemic had spread ahead
of them;
and that happened all over the
New World and all over
Polynesia.
 
So the point of this basically
is we want to compare what
happened in Africa with what did
not happen in Asia and Europe.
The Eurasian ungulates have a
long evolutionary history with
rinderpest, and the ones that we
see there are the ones that are
not extinct;
they made it.
Okay?
 
And if we summarize coevolution
as a whole, there are lots of
things that coevolve.
 
It's not just species that are
coevolving with each other;
it happens at many scales.
 
And that means that other
living things are among the most
important elements of the
selected environment.
So you shouldn't think of
organisms as being faced only by
challenges of temperature and
rainfall and stuff like that.
Really, once life got going,
the different species on the
planet became each other's most
important interaction partners.
Part of this is running just as
fast as you can to stay in one
place;
and this Red Queen concept is
probably particularly
appropriate for the virulence
resistance paradigm,
and for the evolution of sex as
an adaptation against parasites.
 
And as the rinderpest example
shows us,
the extent of coevolution is
particularly strikingly revealed
when you see a foreign species
invade another continent after a
long period of isolation.
 
Okay.
 
