Finals week is upon me, and I should be working on piles of paper work right now, but I need a break … and I have to vent some frustration with the popular press coverage of an important scientific event this week, the publication of a draft of the platypus genome. Over and over again, the newspaper lead is that the platypus is “weird” or “odd” or worse, they imply that the animal is a chimera — “the egg-laying critter is a genetic potpourri — part bird, part reptile and part lactating mammal”. No, no, no, a thousand times no; this is the wrong message. The platypus is not part bird, as birds are an independent and (directly) unrelated lineage; you can say it is part reptile, but that is because it is a member of a great reptilian clade that includes prototherians, marsupials, birds, lizards and snakes, dinosaurs, and us eutherian mammals. We can say with equal justification that we are part reptile, too. What’s interesting about the platypus is that it belongs to a lineage that separated from ours approximately 166 million years ago, deep in the Mesozoic, and it has independently lost different elements of our last common ancestor, and by comparing bits, we can get a clearer picture of what the Jurassic mammals were like, and what we contemporary mammals have gained and lost genetically over the course of evolution.
We can see that the journalistic convention of emphasizing the platypus as an odd duck of a composite creature is missing the whole point if we just look at the title of the paper: “Genome analysis of the platypus reveals unique signatures of evolution.” This is work that is describing the evidence for evolution in a comparative analysis of the genomes of multiple organisms, with emphasis on the newly revealed data from the platypus.
Let’s start with the first figure from the paper, a cladogram illustrating the sequence of appearance of derived traits in the relevant lineages examined in this work. This is a fairly conventional picture of our evolutionary history, and I have to emphasize that this paper reinforces the evolutionary explanation for the illustrated relationships.
Note that the study includes genomic data from the chicken; it is not implying that monotremes are part bird. Birds are used as contemporary representatives of the sauropsid lineage, a group of reptiles that split off our family tree 315 million years ago. They are distant cousins. What’s useful about their comparison is that, for instance, if we find a feature in birds that is also present in monotremes, marsupials, or eutherians, it is likely that that feature was also present in our paleozoic common ancestor.
For instance, one of the unusual (for a mammal) features of the platypus is meroblastic cleavage. There is a famous telegram from 1884 sent from Australia to the British Association tersely announcing a dramatic discovery: “Monotremes oviparous, ovum meroblastic.” Those four words declare that the platypus and echidna are egg-layers (oviparous), and that the early stages of formation of the embryo resemble those of birds and reptiles, not mammals. We eutherians have eggs that go through holoblastic cleavage; the first cell divisions cut all the way through the ovum, producing multiple, separable daughter cells. In the meroblastic cleavage of the platypus and chicken, the large yolky egg would be inefficient to subdivide completely, so the early divisions are incomplete — they produce a sheet of cells on top of the large yolk that are cytoplasmically continuous with the yolk cytoplasm. This is a feature that is common in yolky eggs and is a consequence of physical constraints on cell division.
Now look at the cladogram. Birds (archosaurs) and lizards and snakes (lepidosaurs) exhibit meroblastic cleavage. Marsupials and eutherians divide holoblastically. To say that the platypus is part bird because of that is misleading; what we’d say instead is that meroblastic cleavage is likely to be a primitive character, one that was inherited from the last common ancestor of synapsids and sauropsids, over 300 million years ago. (Another possibility, of course, is that birds and monotremes evolved this feature independently, and it is an example of convergent evolution. Just the observation of one character is not sufficient to judge, and we have to look at multiple details of the process to determine whether something is a product of convergence vs. common descent.)
Every organism is going to be a mix of conserved, primitive characters and evolutionary novelties — a mouse is just as “weird” as a platypus from an evolutionary perspective, since each is the product of processes that promote divergence from a common ancestor, and each are equidistant from that ancestor. It’s just that we primates share more derived characters with a mouse than with a platypus, because we are more closely related, and the mix of characters in the mouse are more familiar to us.
OK, all clear on this? It’s just a peeve of mine; modern echidnas, elephants, and emus are all products of different evolutionary trajectories through history, and no one by itself is a representative of the ancestral condition. We derive the ancestral state by comparison of multiple lineages. And that is the virtue of this paper, that it adds another lineage to the data set, one that diverged from ours over 160 million years ago. It is a lens that helps us see what novelties arose in that 160 million year window … on both the eutherian and monotreme sides.
So what are the details that we’ve learned from the platypus?
One important message is the unity of life. The platypus has about 18,000 genes; humans have 18-20,000 genes. Roughly 82% of the platypus genes are shared between monotremes, marsupials, eutherians, birds, and reptiles. This is not at all surprising. All of these organisms are made of eukaryotic cells, and the basic eukaryotic machinery is going to be shared. We also share a lot of junk: about half the platypus genome consists of LINE and SINE-like sequences.
We do differ in the details. For instance, an obvious difference is that the platypus lays yolky eggs, while eutherians have yolkless eggs retained in the mother. As you might expect, the platypus has a gene that we lack, for vitellogenin, a crucial yolk protein.
Something that eutherians and monotremes have in common, but which is not shared with birds, is lactation (some birds can produce crop milk, but this is a different adaptation). In the ancestral state, lactation was probably the secretion of fluids and immune system proteins to keep eggs and newborns hydrated and protected, but in our history, parents who invested more effort in secreting additional nutritive components, like sugars, fats, proteins, and calcium, were more successful. The platypus secretes a true milk, loaded with all of those goodies. One of the predominant proteins in milk is a phosphoprotein called casein, which is thought to have originated by a duplication of a tooth enamel matrix protein gene, of all things. These tooth genes, enamelin and ameloblastin, are clustered with the casein genes in both platypus and the mouse, suggesting that the kind of sophisticated lactation abilities we share arose prior to the Jurassic.
One of the hotspots for adaptive change in all organisms is the immune system, since every organism has to face ongoing challenges from viruses and bacteria throughout its life. One of the advantages of being a placental mammal is that our embryos, which have poorly developed immune systems, can benefit from a prolonged period under the umbrella of the adult, maternal immune system, something an egg-layer lacks. The platypus genome has a large expansion of natural killer receptor proteins, certain antimicrobial peptides, and other components of the innate immune system.
An interesting specialization in the platypus is the evolution of venoms. The platypus has small, sharp spurs on its hindlimbs that it uses to inject defensive poisons into predators, a very unusual feature not found in other mammals. Where did these venoms come from? As it turns out, by duplication of genes that have other functions, with subsequent divergence, and many of these genes also come from the innate immune system. In particular, there are a set of proteins called the β-defensins, which we also have, as do plants, fungi, and invertebrates. These are small, cystein rich peptides that are rather like the bullets of the immune system; they can bind to viral coat proteins, they can punch holes in bacterial membranes, and we have many epithelial cells that secrete these onto our skins and the lining of our gut and respiratory tract to kill invaders. Cells of the immune system spew these onto foreign and phagocytized cells to kill them, too. The platypus has repurposed these genes, making copies that have been selected for more effective toxicity when injected into other animals.
One very cool observation is that these are also the same proteins used in venomous reptiles — snake venoms also contain novel forms of β-defensins. So, on our cladogram, two distant relatives, the lepidosaurs and the monotremes, all use β-defensin derived venoms. Does this imply that their last common ancestor also used these venoms?
No, and this is where the details are important. Venomous snakes and the platypus have different duplications of the β-defensin genes. So, while coopting these immune system proteins seems to be a common strategy for evolving venoms, the details of the duplications reveal that these are independently derived features, not primitive at all. This is clearly a case of convergent evolution.
The accompanying news article in Nature has a diagram that puts this work into context, showing the status of various ongoing genome projects. The first thing you should notice is that they are really heavily emphasizing mammalian genomes. I think this is justifiable; for puzzling out the significance of differences in the genomes, a good cluster of closely related species would have some real advantages in simplifying the problem. That the clade chosen happens to be mammalian is not quite as defensible on scientific grounds, but is a reasonable choice on economic and medical grounds, and also on the very important criterion of human vanity.
One virtue of the platypus is that it provides a relatively closely related outgroup to help tie together, and give perspective on, the various mammalian genome projects. It’s all part of the big picture in defining what a mammal is.
Of course, what we also need is an equally heavy investment in other diverse clades, like the molluscs (they aren’t on this figure at all!), the arthropods (only three species? Pathetic), protists, and bacteria (which are diverse enough to swallow everything else). Actually, we have to face the facts: what we really need are the complete genomes of every species on earth in a nice database where we can compare everything.
Brown S (2008) Top billing for platypus at end of evolution tree. Nature 453(7192): 138.
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