The Burgess Shale, Arthropods and Macroevolution - Professor Matthew Wills

The Director of the Milner Centre for Evolution, Professor Turi King, talks to Professor Matthew Wills about his career, his current research, and his passion for all things evolution.

Episode Transcript

(00:02):
Hello and welcome. You are listening to a podcast by the Milner Centre for Evolution,
at the University of Bath. I'm Professor Turi King, your host, and today I'm talking
to Matthew Wills, Deputy Director of the Milner Centre for Evolution. I'm going to be talking to
him about his career, his current research, and his passion for all things evolution.

(00:26):
Matthew, you're a professor of evolutionary paleobiology here at the University of Bath,
what got you into paleobiology?Well, I think in common with a lot of people,
as a kid, I was fascinated with dinosaurs. And I remember wondering where dinosaurs had
come from and indeed, where they gone, why were there none around today? And I think

(00:48):
probably at the age of about 5 or 6, my parents took me up to the natural history Museum. They
had loads of specimens on display. There were galleries full of trilobites and ammonites,
and there was a whole section of fossil fishes. And they had them organised chronologically. So,
through time you could see how groups had changed, through time.

(01:12):
And they also had a great deal of taxonomic information. So how groups of animals and
plants were structured into different groups because of their similarity. And you could see
that there was structure there. You could see the process of evolution, sort of, happening
on a grand scale. I think it was that sense of underpinning structure that really gripped me.

(01:36):
And the idea that there are patterns through time, I think, was what sort of hooked me in.
So, what did you do as your undergrad then?Well, I guess there were two choices. One was
to either pursue geology or to be a biologist or a zoologist. And I made the decision that I
didn't particularly want to be standing up Welsh mountainsides in the rain doing mapping. And

(01:58):
I wasn't so interested in mineralogy and volcanology and the hard rock stuff. So,
I did zoology, learning about the diversity of life. That was something which was,
you know, very much up my street. And I just thought, well, this is where I feel at home.
So, what did you do for your PhD then? Because you went on and studied this even further.

(02:18):
So, I was extremely fortunate, I was supervised by two people, Derek Briggs, who was in Bristol
at the time, now moved to Yale, and Richard Fortey, who worked at the Natural History Museum,
a trilobite expert. And they put me to work on a project on the Burgess Shale.

(02:38):
Now, the Burgess Shale is a site from British Columbia, from the Cambrian. These are rocks
around 508 million years old or thereabouts, a half a billion years old. And they're exceptional
because they show soft part preservation. Now, on the whole, fossils are of hard parts. They're

(03:00):
things like shells and bones that are heavily mineralised, and so they preserve relatively
easily. Now, lots of tissues are not like that, they’re soft parts, they're muscles, tissues, sinew,
skin and so forth. And even worse than that, there are things like little thin gill filaments,

(03:21):
and the animals of the Burgess Shale were buried very, very rapidly by a mudflow at
the bottom of a submarine cliff and buried at lots of different angles. And the sediment got
in between the limbs and the layers of tissue. So, it's possible to dissect through them,

(03:41):
almost like you're sort of opening up the leaves of a book. Now, this is not something I did. This
is something that people did writing monographs over 80 years or so. And those descriptions were
what I was working from in my PhD.And what were you looking at?
Well, the group I was particularly focusing on initially at least, were arthropods. And

(04:02):
arthropods are animals with jointed limbs and an exoskeleton. So, arthropods today include
things like insects, crustaceans, spiders, and millipedes. And virtually every arthropod
you pick up today fits nicely into one of those four groups. And they're classified, or you can

(04:26):
recognise which group they belong to, largely on the basis of the segmentation of the head.
So, arthropods are nice because they have bodies that are made of repeating segments. And those
segments typically each have a pair of legs. And the legs are specialised to do different jobs.
So that enormously successful, most animals are arthropods, most arthropods are insects,

(04:51):
most insects are beetles, but you can assign any living arthropod into one of these four groups.
Now, as you go back in time, and particularly as you get back to the Cambrian, you start to
encounter fossils that simply don't fit into any of those groups. And they have arrangements

(05:11):
of appendages and types of appendages that you don't find anywhere else. Now because the living
groups are classified according to their head structure, and because you find Cambrian things
that have entirely novel conformations of head structures, the argument went,

(05:34):
well these have to be groups of the same sort of importance and the same sort of rank, if you like,
as the living groups. And this set of whole, sort of, train of thought and a whole debate.
So, Stephen Jay Gould wrote a wonderful book called, Wonderful Life, that described the
discovery of the Burgess Shale by Charles Walcott. But he also accuses Walcott of a particular

(05:59):
worldview, and that Walcott was trying to shoehorn the Burgess Shale fossils into the groups that we
know about today. And some of them fit reasonably, others really don't. And so, it was understanding,
or trying to interpret the evolution of Burgess Shale arthropods that was the focus of my PhD.

(06:22):
Now, there are two ways that you can try to approach this. One way is that you can try to
produce a sort of evolutionary tree, a phylogeny of arthropods, including both living and fossil
forms. The other way is that you can try to quantify the morphological variety of arthropods,

(06:44):
both in the present day and in the Cambrian.Now, that second idea, trying to quantify
morphologic variety is something called disparity. And according to Gould, disparity in the Cambrian,
the variety of anatomic body plans was much, much greater than at any time since. In fact,

(07:08):
Gould talks about an inverted iconography of life.So classically we think of organisms having a
single origin. Groups have a single origin, there's one species and diversity or the
numbers of species, we envisage those sort of gradually increasing through time. And of course,

(07:30):
groups can also become less diverse and wax and wane. And ultimately, of course, they can go
extinct. But that's something quite distinct from disparity. Disparity is to do with how different
species are. And when you look at some of these Cambrian things, they look extremely disparate.

(07:51):
They look as though they are representatives of groups that are as distinct from one another as
the modern groups are distinct from one another.And so, the argument goes, a little bit like this.
We've got four major groups of arthropods today, and they're all distinguished on the
basis of their unique pattern of tagmosis and head segmentation. Therefore, we look back at

(08:12):
the Cambrian, and we've got 10 or 20 groups that have completely new sets of head appendages and
conformations of these, and so therefore they represent groups of equivalent sort of status.
Therefore, says Gould, we've got enormous Cambrian disparity, and much lower disparity today. So,

(08:32):
in terms of the natural sort of cone of increasing diversity, the traditional picture, Gould says,
we actually want to turn that on its head. And we've got much greater disparity in the Cambrian
than we have at any time since. So, my project was trying to sort of quantify, trying to put numbers
on how disparate really were Cambrian things.The answer is less astonishing than Gould

(09:00):
might have us believe. So, disparity in the Cambrian is about the same as it is today.
And when we produce a phylogenetic tree or an evolutionary tree, we find that on the whole,
the groups of living things are sort of interspersed, mixed up with many of the
Cambrian fossils. And some of the Cambrian things are a sort of assembling the body plans that we

(09:23):
see alive today. So many of these Cambrian fossils are transitionary forms on the way to
establishing the body plans of the modern groups.So, you finish your PhD, and I suppose you have to
think about what am I going to do now? I noticed you went and worked for the Smithsonian Museum,
which has got to be one of the coolest museums in the world. So, what took you there?

(09:44):
Yeah, again, a fantastic bit of luck. I was working with a chap called Doug Irwin, and he was
curator of, amongst other things, all the Burgess Shale fossils. So having worked from monographs,
during my PhD, I actually got to go and actually see these things, which was fantastic.
And so, it's there that I continued sort of thinking about the evolution of crustaceans,
worked a bit more on the priapulid worms from the Burgess Shale. So, these are a group that live

(10:08):
buried in the mud, and they sort of ambush things that wander by, and they have these
amazing eversible pharynxes, armed with all sorts of backward pointing spines and teeth,
and they're really rather rapacious predators. They're still around today, much less diverse,
and they occasionally pop up in films. So, there are gigantic ones in one of the remakes of King

(10:30):
Kong, and Andy Serkis gets eaten by one. I was the only person in the cinema going, it's a priapulid
worm, and my wife was going, please sit down dear.But yes, they're amazing. And again, it's the
same picture really, the priapulids from the Cambrian turn out to be about a disparate as
the ones from today. Now that sounds like, well, the explosion's much less big, and that's true,

(10:50):
but we're still left with this puzzle. How does all this disparity appear so quickly? And this is
something that kept Darwin awake at night, and he talks in The Origin of Species about his dilemma,
that this is a real challenge to his understanding of how evolution works.
What did he come up with in the end, in terms of explaining it?

(11:12):
Darwin thought it was possible there was a missing chunk of the fossil record,
so he thought that there was a tract of time that wasn't preserved. Other explanations have
been that maybe there's a period of cryptic evolution. So perhaps things are very small,
possibly, and they simply don't fossilise, or they don't have hard parts. So, the Cambrian

(11:32):
is not only the appearance of these modern phyla, it's also the evolution of hard parts,
it's the evolution of large size, it's the evolution of sensory systems. So,
predators and prey and teeth and jaws and all of these amazing devices. And you go back
before that and things don't have hard parts, so they don't tend to fossilise terribly well.

(11:54):
So that's one possible explanation. And there's a huge debate over exactly how much time we need to
fill and how long before the Cambrian things started to diversify. And this is mostly the
purview of molecular clock studies, that try to look at rates of molecular evolution and

(12:15):
then try to use fossil calibration points to extrapolate back and to work out when,
for example, things like jellyfishes diverged from vertebrates, and sort of right at the base
of the multicellular animal part of the tree.And estimates vary, but they're certainly 30
million years, possibly 300 million years, it depends who you believe,

(12:37):
to fill. But I think the gaps gradually closing, but there's still a lot to understand, I think.
So, you finish at the Smithsonian, and you then came here to Bath in 2000 as a researcher. And
clearly evolution is, it's in your blood. What's your research about now? I know you look at

(12:58):
macroevolutionary processes, but for those who don't know what that means, what is it?
Well, macroevolution is evolution on the sort of deep time, time timescale. So, it's evolution above
the level of speciation. And it's studying evolution over tens, hundreds of millions of
years. And often to see if there are any patterns.So, one of the patterns that people have studied

(13:23):
is looking at diversity through time. How many species are there? And when you plot
this out over the last half billion years or so, you can see that there are periods where
lots of diversity has been lost. Those are mass extinctions. And there are five of those events.
The best known is probably the one that wiped out the dinosaurs at the end of the Cretaceous.

(13:46):
But there's a much worse one, and that's the end of the Permian moving into the Triassic.
And that's often known as the Great Dying when something like 93% of species went extinct.
And the cause of the dinosaur extinction is almost certainly a large asteroid impact off
the coast of Yucatan. The Great Dying is almost certainly mass volcanism, but both

(14:12):
of those events have the effect of putting large volumes of greenhouse gases into the atmosphere.
So initially lots of dust, so a kind of nuclear winter effect. So,
everything gets very cold. And then subsequently global warming because of greenhouse gases. So,
you have big switches and shifts in the climate, similar to what we're doing today. Although of

(14:35):
course the mechanisms are different. The rate of change may be a bit slower, but we're also
shifting the climate and species are unable to adapt to that and therefore go extinct.
And we don't know how fast things are going extinct. We don't even know how many species
there are alive today. So, we're probably losing diversity that we've never even seen. We've never

(14:59):
even documented. So that's one aspect, is trying to understand whether we can learn
any lessons from the geological past, in order to understand the effects we're having today.
It may be, for example, that there's some selectivity. So, groups that are,
or species that have very precise niches, or require very stable environments. Those are

(15:22):
likely to do very badly as the environment changes rapidly. Those that are perhaps generalists,
those that borrow, for example, those that have a wide range of ecological niches and
things that they can do to earn a living, those tend to perhaps do a bit better. Being large
is bad news. Being endemic, not having a wide distribution is also very bad news.

(15:45):
One of the other things that interests me is the relationship, though, between disparity
and diversity. And it turns out that many groups have a high level of disparity, early on in their
evolution, even while the diversity is very low. So, for example, if you look at the echinoderms,

(16:06):
the group that includes the star fishes and the sea urchins and the sea cucumbers,
their diversity early on is quite modest, very few species. But the species which there are, all are
really different from one another. So, disparity seems to peak early, long before diversity peaks.

(16:26):
So, it's almost as though there's an evolutionary rule that says, and rule in inverted commas
because there are loads of exceptions to this. But you explore the ways you can do what you do
early in your evolution, and you sort of explore the morphological space, the multidimensional
morphological space that's available to you quite quickly and only subsequently do you riff on those

(16:49):
themes, do you produce higher diversity.And this is where we are now able to add
another layer of information, because I know you wrote this really interesting piece for
the conversation about how genetics is changing how we understand evolution. So, these days,
obviously we can look at genomes of organisms. We can see which ones are more closely related

(17:12):
to one another. And we know that mutations in the genome happen, kind of, at a particular rate. So,
we can kind of use it as like a molecular clock.So, tell me about how molecular analysis is
causing this really big shift in the field of studying evolution?
It's completely revolutionised everything. If you go back 40 years, there was only really one

(17:36):
way of working out how things were related, you had to do comparative anatomy. You had
to look at morphology and code up the shapes of bones, the positions of muscles and so on.
And molecular trees, now, some of them have supported what we kind of thought we knew before,
but some of them are completely at odds with our understanding. And perhaps the

(17:59):
best example is the evolution of mammals.So, 30 years ago, we had a picture of mammal
evolution that had been stable for rather a long time. There were a few controversies,
but broadly we thought we knew what the picture was. And the first molecular trees
of mammals completely overturned that picture.Now the early ones were based on single genes or 2

(18:22):
or 3 genes, but very quickly it became possible to concatenate data from tens or hundreds of
genes. And now the sort of gold standard is a phylogenomic analysis, where you have genes
spanning the entire genome, huge volumes of data. We can acquire that data more cheaply and more
quickly, and it's now a much more viable prospect.But the question arises, well, why were the

(18:48):
comparative morphological trees wrong? These were very clever people working for a very long time,
doing very detailed work. And in our paper, we compared molecular and morphological trees for
about 45 different groups of animals and plants. And of course, what do you use as the standard?

(19:09):
What do you measure the accuracy of these trees against? You can never know because we don't
have a time machine. You can never know where the truth lies. And many people have taken the
view that because our volumes of molecular data are much greater, and because the algorithms,
the models that we use to analyse those data are much more sophisticated, well, surely the

(19:33):
molecular trees must be correct, inasmuch as they disagree with the morphological ones.
So, what our paper did was to try to come up with an independent benchmark. Now for both Darwin and
Alfred Russel Wallace, one of the big clues, if you like, to understanding natural selection,
understanding the process of evolution, was that on their travels, they found that you have

(19:57):
different groups of organisms living in different places, centres of endemism and organism species
radiate out from those centres. But there's a biogeographical structure to where things are,
and that's an independent line of evidence for evolution. You don't find everything everywhere;
you find things living in particular regions. And it's also an independent sort of yardstick

(20:23):
by which we can sort of measure the congruence, the agreement with our different types of tree.
And it turns out when you do this, that more times than not, the molecular trees have a
pattern of branching that's more similar with the biogeographical distributions of species. So,

(20:43):
when we go back to the idea of mammals, now the major groups of mammals now have names that
reflect biogeographical regions. So there's a group called Afrotheria, and these comprise
things like aardvarks, elephants, tenrecs, which look a little bit like hedgehogs superficially,
organisms that were previously thought to be very dis… they were all mammals,

(21:07):
but they weren't thought to be closely related, but the molecular tree has pulled them together.
And these groups now reflect geographical regions, Afrotheria, Laurasiatheria and so on.
So, our understanding is completely changed, and this has happened for many groups,
but also because, as you mentioned, molecules often behave in a rather clock like way,

(21:28):
and it's a very imperfect clock. In some lineages the clock runs faster, in others
slower. And the rate of ticking correlates with a variety of things, generation time, body size,
rate of metabolism, and so forth. But if you can smooth those effects and if you can get really
good fossil calibration points, you can use the molecular clock to try and infer the divergence

(21:54):
dates of events that are much, much older.And this has become important in, for example,
trying to date the divergence of animal groups prior to the Cambrian or indeed to date, the
divergence of mammal groups relative to the K-Pg mass extinction that wiped out the dinosaurs. So,
there are sort of whole industry of papers trying to look at the timing

(22:17):
of radiations relative to major, sort of, climate shifts or Earth events and so on.
So obviously the study of evolution is something you've devoted your career to. So,
what is it that excites you about it? What is it that's getting you up in the morning?
I think evolution's the unifying theory in biology. It's the one thing that makes

(22:39):
sense of all of the other observations about life. It's the one thing that enables us to
make sense of the otherwise utterly bewildering biodiversity of animals, plants, fungi, microbes
that we see around us. And the idea that there's a single evolutionary tree of life and that we
can actually understand the structure of that. So, you and I are related, if we go back far enough,

(23:05):
and if we go back a bit further then we're related to chimpanzees, bit further still,
gorillas. But actually, you're related to the bacteria in your gut, and the trees outside,
and there is one overarching tree of life. And the idea we can know the structure of
that is really, really fascinating.But I think evolution as a science,
as a discipline, is also intimately linked with our study of biodiversity. The obvious question

(23:32):
is the evolution of what, and where, and how, and understanding biodiversity is incredibly
important. Paradoxically, the public understanding of the need to conserve
species has never been higher. But yet it's not something which is taught so much now in schools.

(23:52):
The A-level syllabus used to contain sections on the major phyla, body plans, the way that those
major groups were related, and it was certainly a conspicuous part of university syllabuses. And
that's no longer necessarily the case, there's a focus on reductionist approaches. There's a focus
on extremely vital things like biomedical sciences and human biology and so forth. But what we may

(24:18):
have lost, unfortunately, is an understanding of the big picture, the broad vista, kind of
approach. And that's something which is very unfortunate. And certainly, in our teaching here
in Bath, we still teach the diversity of life, and we feel that's vitally important for biologists to
know about that structure of the tree.So, what's next for you?

(24:40):
At the moment I'm interested in complexity and in the evolution of complexity. And trying to
quantify complexity is an even harder problem than trying to quantify morphological disparity.
And there's a relatively small literature on how to measure complexity and clearly the complexity,

(25:03):
or maximum complexity of living things has increased over time. We start off with single
celled organisms, and we now have a vast diversity of many complex organisms. But if you think about
the mean complexity, if you like, or the modal complexity, the most common level of complexity,
it's still very simple. So, there are still far more bacteria, far more micro-organisms than

(25:26):
there are multicellular organisms.And so, the question arises then,
is this a sort of passive process? Have more complex things become more complex as a sort
of drift or is there a kind of repeated tendency for things to evolve towards higher complexity,
what we would call a driven trend.And the only way to answer that question

(25:50):
is to look again at large phylogenetic trees, and to be able to map traits onto those trees.
Fossils again become vitally important because we need snapshots of the past. So even though
the information we get from them is often fragmentary, we often don't have soft parts,
we often only have part of the organism, nonetheless, they give us snapshots of what

(26:14):
was actually present in the past. These are not making inferences; this is actual data.
And we can use that data to map out the way in which traits have changed, the sequence
with which different complex body plans have been assembled. So, the classic example, I would say,

(26:34):
are the living archosaurs, so the ruling reptiles. Today we have crocodiles and alligators, and we
have birds. And those two groups are one another's closest living relatives. But they don't look
very similar, and they don't look very similar because they're separated by a huge tract of time

(26:56):
and a huge part of the evolutionary tree that's missing. So, dinosaurs, pterosaurs, phytosaurs,
aetosaurs, all these amazing extinct reptile groups are missing, they've all gone extinct.
The last of them died out at the K-Pg, and many of them died out before the end of the Triassic.
So, in order to make sense of that part of the tree, we really do need fossils to fill in these

(27:19):
gaps and to understand what it was possible for archosaurs to do. They were able to fly,
they evolved flight separately from the birds and the pterosaurs. And if you think about bird
evolution, the modern birds are just one group of eumaniraptora and theropod dinosaurs that
have evolved to fly. And now we're coming full circle and we're coming back to this

(27:41):
business about convergence. So, lots of groups of small, agile, lightly built insectivorous
dinosaurs evolved flight. Depends who you ask. might have been twice, might have been
three times, might have been four times.But you've got all the building blocks,
and you go from using feathers for insulation, for sexual signalling, for coloration, possibly for

(28:05):
catching prey and so on. So, they're fulfilling a variety of functions, feathers, but they're
not for flight. Then you tip over into flying.So, the fossil record allows you to test these
questions about repeated evolution of traits, and about the manner
in which complex body plans are assembled.Matthew, thank you so much for talking with me.

(28:29):
This was a podcast by the Milner Centre for Evolution at the University of Bath.
I'm Turi King and thank you for listening. If you have any thoughts or comments on this
or any other episodes, please contact us via our X channel @MilnerCentre.
For more information about the Milner Centre for Evolution, you can visit our website.