SCIENCE AT THE SHINE DOME canberra 6 - 8 may 2009
Symposium: Evolution of the universe, the planets, life and thought
Friday, 8 May 2009
Professor Lindell Bromham
Centre for Macroevolution and Macroecology, Australian National University, Canberra
Lindell Bromham is a lecturer and researcher in evolutionary biology at the Australian National University. She takes a variety of approaches to studying macroevolutionary processes and patterns, which determine the diversity of species in space, time and between lineages. Most of her research focuses on investigating the record of evolutionary past and processes in the genome. She has applied DNA analysis to a range of fields including evolution, genetics, ecology, conservation, bioinformatics, development and virology. She has recently published an introduction to this topic called Reading the story in DNA: A beginner’s guide to molecular evolution.
Using DNA to uncover the evolution of life
Lindell Bromham: I have been asked to cover the evolution of life in 15 minutes; that is about 250 million years per minute, so I will have to speak fairly quickly. One way I could cover the evolution of life is to start at the beginning and work my way through to the end.
I might, for example, start with the primordial soup and talk about how inorganic molecules came together to form polymers capable of self-replication, which then increased information content to become something that we might call ‘genes’. These genes then banded together into cooperatives, called chromosomes. The chromosomes then built walls around themselves to separate themselves from the environment and they built specialised machinery to make replication more effective. These cells started cooperating together to reproduce as a whole to give rise to multicellular organisms, such as plants, animals and fungi. Then some of the individual animals within a species banded together in social groups, with a common reproductive purpose; and one of those social animals developed language and culture. This series of steps in the evolution of complexity is referred to as the ‘major transitions in evolution’.
But this is not how I am going to approach the evolution of life – and why not? There are two reasons. One is that I am slightly uncomfortable about this array: this familiar narrative we have of starting simple and getting increasingly more complex; this ladder-like progression. It is often referred to as the ‘great chain of being’, which is the very old idea – much older than evolution – that there is a scale of complexity.
On this depiction of the great chain of being you can see that plants are higher than inorganic things, animals are higher than plants, humans are better than animals, angels are above humans and so on. You might say, ‘Oh, we don’t believe in that any more.’ Yet, if you pick up any evolution textbook or even a popular science evolution book, you will often find something that looks very similar to this.
Many biology books start with single cells; then go on to simple multicellular algae; then plants; then animals and fungi. Animals with backbones are presumed more advanced than those without backbones; and furry animals with backbones rate higher than those with scales. The last chapter in the book will usually be on humans as if we were the pinnacle of evolution.
You might say, ‘Oh, well, this is just a way to present things; it doesn’t really matter,’ but it does actually influence our thinking. For example, there is an ad on ABC Radio at the moment for a program on hearing, on which there is a sound bite from an expert who says, ‘Insects have hairs on their body that detect air movement and this evolved into hearing in humans.’ We know that humans did not evolve from insects and yet that is the kind of error of thinking we find ourselves making, when we arrange this orthogenetic series. So this is one kind of objection to presenting the beginning-to-end model of evolution.
But there is a more practical reason: beginning-to-end is not how evolutionary biologists usually work. Most evolutionary biologists like me start with what we have here today, the evidence we have in the present, and we use that to work backwards: to go back through the history of life, to reconstruct the past and the processes that we cannot directly witness.
So what is this present evidence that we might use to reconstruct evolutionary past and processes? We might use fossils – and, remember, fossils are very, very rare matter that has survived through to the present day and that has been found. We might use the distribution of species on many different scales. We might use our understanding of the diversity of species and the relationships between lineages. But the form of evidence that I want to talk about today, which is playing an increasingly important role in evolutionary biology, is that of DNA evidence. DNA evidence in isolation will not answer all our questions and yet it is becoming an increasingly useful tool, when combined with these other sources of evidence.
Every living being on Earth has DNA in it – or RNA, which is very similar. So we could take any living biological material today and use that to trace backwards through the history of life. Since this backwards-with-DNA story could start with any biological sample, I thought I might as well start with the mysterious blob that washed up on a beach in Chile in 2003.
Other blobs just like this one have turned up on beaches and they have always mystified people. They are great for conspiracy theorists: is it a new species of giant octopus; is it a squid; is it a monster from the deep or an alien? These days, of course, we can answer that pretty much immediately. Scientists took a sample of material from this mysterious blob. They amplified the DNA from that material, sequenced the DNA; so they got the series of As, Cs, Ts and Gs that occur in that DNA molecule. They compared that sequence to the giant public databases that have all the DNA sequences that have ever been determined and looked for a match. They found that the DNA from that Chilean blob exactly matched the DNA from the sperm whale. So the mystery blob was nothing but blubber. So, as reported on unexplained-mysteries.com, ‘One of the myths of the sea has been skewered by gene researchers.’ (In this way, DNA has had quite an impact on cryptozoology).
But today I want to imagine taking that tiny little sample of mystery blob and, by comparing it to different DNA samples from different individuals and different species, see the way we can work backwards through the history of life and the kinds of processes and patterns that we can uncover by doing that.
As we have seen, we can take a DNA sample and identify species, and this has been very handy in identifying the whale species that turn up in markets. For example, biologists have gone to whale meat markets in Japan and Korea. They have bought whale meat products, taken them back to their hotel rooms and surreptitiously amplified the DNA. Again, they have sequenced it and compared it to these giant DNA sequence databases that we all have access to. By doing this, they have been able to show that the markets contain meat from species that could not be part of the scientific catch and that must have been caught outside of Japanese and Korean waters. In some cases, they have even managed to identify individual whales. For example, meat from a whale that was known to have been caught off Iceland in 1989 turned up in a market in Osaka in 1993. So, if you thought your whale meat was fresh, think again.
We can identify individuals, and the species from which they come, from DNA samples. Also, because each individual inherits its DNA from its parents, and they from their parents, and so on, you will find that relatives tend to have more similar DNA sequences than those who are more distantly related.
This is handy because it means that we can take DNA samples from groups and begin to say how they are related to each other. This is very useful for sperm whales because they have complex social behaviour that is very hard to observe. We are talking about animals that can dive to a depth of a kilometre and move over the entire globe. So little was known about their behaviour and their populations, until people started – as these brave biologists are doing – taking a DNA samples from whales. When you do that, you find that female sperm whales form matrilineal groups – groups of related females – that cooperate together. But the young males leave these groups and form roaming bachelor schools. Not only that, but DNA analysis has shown that females tend to stick to the ocean they were born in, whereas the males can roam over the whole globe. So, if you were to give me any bit of sperm whale tissue, even a skerrick of skin or a carved whale’s tooth, by sequencing DNA from that sample I would be able to tell you which ocean that whale had been born in.
You can extend this approach to whole populations. If you start taking DNA sequences from the global sperm whale population, you can begin to look at when they all last shared a common ancestor, and this helps to reconstruct the history of the population in a changing world. For example, scientists who have studied the DNA of the sperm whale population have suggested that there was a contraction of the population during the last ice age, as sperm whales had to retreat from the cooler polar waters into the tropics. This is a nice demonstration of the way that genetics can be used to look at the way populations change with a change in climate.
DNA analysis is also extremely valuable in reconstructing the origin of lineages. For example, the origins of the whale lineage, this fully aquatic mammal – so different from its terrestrial relatives – puzzled biologists. Darwin was famously puzzled by the origin of whales because he needed to be able to explain how you could get such a remarkably different animal from a series of small modifications, each of which would be beneficial. He did not know what the whale’s closest relatives were. For example, he hypothesised that they might have been changed from something like a bear. But now we can take the DNA from whales and compare it to other mammals to see which ones they are most similar to. The answer was quite surprising: whales are most closely related to hippos. This initially startling idea, which came to be known as the ‘whippo hypothesis’, was generated by DNA sequence analysis, but it has now been widely corroborated. I think Darwin would probably quite like this because it gives a picture of a possible semiaquatic stage between fully terrestrial mammals and the fully aquatic ones.
This adaption of whales to the aquatic niche was part of the great flowering of mammalian diversity that occurred after the final extinction of the dinosaurs. Dinosaurs last appear in the fossil record at the end of the Cretaceous. Mammals appear in the early Tertiary, and many of them look as though they are replacing the dinosaurs; in other words, they are filling those vacant niches. For example, some of the earliest fossil whales, such as Basilosaurus, look remarkably similar to the aquatic reptiles that they are apparently replacing, such as mosasaurs. We see the same thing when we look at dolphins that look remarkably similar, although they have completely different origins, to the reptilian icthyosaurs. So there has been this view of dinosaurs dominating all the ecosystems and then disappearing, with the mammals taking the stage and filling all of those roles that the dinosaurs previously occupied. When you look at the fossil record, this pattern is corroborated.
So, if we trace our sperm whale lineage back thought the fossil lineage, we find that the earliest whales appear in the early Tertiary, after the last disappearance of the dinosaurs. Indeed, if we take the artiodactyls, of which hippos are a part, or any other kind of modern animal, you see the same pattern: they are all appearing in the fossil record after the last extinction of the dinosaurs. This has been quite sensibly interpreted as an ‘explosive adaptive radiation’. Mammal fossils are known from the Cretaceous, but they are predominantly small, generalist, probably nocturnal little rug rats. Then suddenly their big competitors were removed and they could take over from where the dinosaurs left off. So this is a textbook example of an adaptive radiation into empty niche space.
But the DNA tells quite a different story. If we take DNA from our whale and compare it to DNA from a hippo, a bat, a mouse and so on, and look at the differences in their sequences and estimate how much change there has been between their genomes, and using our understanding of rates of molecular evolution try to estimate how long it would have been since those lineages split, we find that in the DNA sits a long hidden history: that these mammalian lineages began radiating long before the dinosaurs disappeared. This gives a very different view of mammalian diversification. Of course, what the DNA cannot tell us is what those earlier mammals were like – were they small rat-like things or were they large diurnal grazers? But it does suggest that our textbook picture of an adaptive radiation into empty niche space is perhaps simpler than the DNA would suggest and we may need to modify that.
A very similar story can be told if we use our sperm whale DNA to trace even further back to the origin of the different kinds of animals. The whales are part of the chordate lineage, as indeed we ourselves are. The chordates first appear in the fossil record in the early Cambrian, about half a billion years ago – as, indeed, do all the other different kinds of animals, such as arthropods, starfish, annelids, molluscs and so on. They all appear in the fossil record more or less simultaneously.
This puzzled Darwin because his theory suggested that all forms of animals should appear gradually by a series of slight modifications. How is it that all this diversity could all appear at once in one big jump? Many people have used this Cambrian explosion to suggest that Darwinian evolution must be missing something; there must be times when evolution leaps ahead by an unknown mechanism.
But, again, the DNA tells a different story from the fossils. So, if we compare our sperm whale DNA to snail or worm DNA, and count the differences and estimate how far back they must share a common ancestor, again we find that the DNA suggests a long hidden history that we cannot see from the fossil record. These results are controversial, but I present them to show you that DNA at least gives us an alternative narrative: another way of looking at history that will cause us to question some of the assumptions we have made about evolutionary patterns in the past.
Hopefully, this example of sperm whale DNA has shown you how we can work backwards through the history of life using DNA, identifying not only individuals but also the way families interact, the history of populations in a changing Earth, the way species arise into new ecological niches, the way that lineages diversify in adaptive radiations, the very origins of the different forms of animals and even allow us to question whether or not that happened by Darwinian or non-Darwinian mechanisms. Because every single living thing on this planet shares DNA as a genome, it provides a universal framework for us to ask these questions and possibly even to go back and look at our last common ancestor – which is not bad for something that you get out of a bit of blubber. Thank you very much.
Ross Crozier: We have time for some questions.
Question: You have shown a paradox between the animal fossil record and the clocks that you have calibrated. Isn’t that a paradox within a paradox because of the clocks calibrated with those fossil records?
Lindell Bromham: Yes. The trick is not to use the questionable parts of the fossil record to calibrate rates of molecular change. You need to calibrate rates based on areas of the fossil record that are quite good. So, if you have a continuous series of mollusc fossils, that is a part of the fossil record that you would be fairly sure you could look at for rates of change. However, if you get the very earliest mollusc, you do not know whether that was the first mollusc that ever existed or whether there were earlier ones further back in the past. This is why I say that DNA cannot possibly provide all of the answers. We cannot use it in isolation; we have to combine it with the other things that we know. Apart from anything else, we know that the DNA answers can be misleading, just as the fossil record can be misleading. So it is by combining the two together and playing those alternative narratives off against each other that we begin to ask more questions about that history.
Question: This is just a point about that same paradox. There is, of course, a substantial paleontological record in the so-called Ediacara and there are a lot of what are widely considered to be metazoan fossils in there. So there is another 50 to 100 million years of palaeontologically-recorded metazoan history in there as well. Maybe it is not much of a paradox.
Lindell Bromham: Indeed. When people started applying DNA to this question, you started with the palaeontologists saying, ‘Everything starts in the early Cambrian,’ and the molecular people saying, ‘It goes way back hundreds of millions of years beforehand.’ What we have seen is those answers coming closer together. The molecular dates have been refined upwards to some degree and the paleontological dates are now going back. So now it is reasonably uncommon to find palaeontologists who will insist that the early Cambrian is ‘the start’ of everything and many will accept that it does go back 150 million years. So, again, I think this reinforces the idea that these two things form a joint narrative: each of them informs the other and each of them causes us to ask questions about the other.
Question: Yes, I think that is good, but I beg to differ. I think that molecular biologists are catching up with palaeontologists. The history of the study of the Ediacaran fossils goes back to the 1920s.
Lindell Bromham: Yes; and the interpretation of the Ediacaran has gone back and forth with amazing rapidity. Even in the last 10 years, people have been saying, ‘Yes, they are metazoans,’ then it has become less fashionable to believe that they are metazoans and now it is becoming more fashionable again. Iconic fossils like Kimberella have been interpreted in many different ways. Noone is expecting this to be resolved any time soon, I think, so there are plenty of things to argue about still.