Australia’s egg-laying mammals provide clues to our earliest ancestor

I like the duck-billed platypus
Because it is anomalous.
I like the way it raises its family
Partly birdly, partly mammaly.
-OGDEN NASH

The platypus is famous for being one of the world’s strangest animals. When specimens were first shipped back from Australia, it was thought to be a taxidermic hoax. “Of all the Mammalia yet known”, wrote George Shaw in 1799, assistant keeper of the natural history department at the British Museum, “it seems the most extraordinary in its conformation; exhibiting the perfect resemblance of the beak of a duck engrafted on the head of a quadruped.”

Their strangeness is more than skin deep. From its webbed toes to the tip of its fat tail, the platypus (Ornithorhynchus anatinus) is packed with features that whisper of their ancient lineage, while their fossils and DNA leave us wondering if they are really so weird, or if it might be the rest of us who are the oddballs?

The platypus and its closest relative, the echidna, belong to an order of mammals called the monotremes (Monotremata). They are the only representatives of this group left, surviving among the marsupials of Australia, Tasmania and New Guinea. Like the marsupials and the largest mammal group alive today, the placental mammals, the monotremes are furry, warm-blooded, and produce milk. They also share skeletal mammal traits, such as a single bone in the lower jaw – the dentary – and three middle ear bones called the malleus, incus and stapes. But unlike other mammals alive today, they don’t gestate their young inside the womb, nor do they keep them in a pouch like the marsupials. Like our ancient reptilian cousins, they lay eggs.

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Monotreme means “single hole”, referring to the multi-purpose opening in their rear end used for both excretion and reproduction. This hole is called a cloaca, and is more commonly seen in reptiles, amphibians and birds than mammals (golden moles and tenrecs also have one, making them unique among placental mammals). When it comes to sex, monotremes party with a busy compliment of ten chromosomes – five X-chromosomes and five Y-chromosomes – and their X is more like the Z sex-chromosome of birds.

Reptilian and bird resemblances continue in the bones, as monotremes retain a complex pectoral girdle: bones around the chest and shoulders that provide a frame for muscle attachments. This, and the arrangement of their sturdy limbs, gives the platypus and echidna an ungainly lizard-like gait; swinging their sprawled limbs out to the side as they move, rather than bringing them directly under the body like other mammals.

You may be aware of the electro-sensory abilities of the platypus bill – the echidnas’ nose tip also retains this feature – but you may not know these little warriors have spurs on their heels. A male platypus can use these spurs to deliver painful venom to rival males or would-be attackers. We now know from genetic studies that the platypus has acquired its venom through alterations in the same genes as poisonous reptiles.

While the monotremes are indeed warm-blooded, they like to play it cool: five degrees cooler than us at a chilled out 32C. Although platypuses and echidnas feed their young on milk like other mammals, they don’t have nipples. Their milk oozes from special glands in the skin and is lapped up by their offspring. To compensate for this less sanitary delivery system, monotreme milk is packed with a record-breaking number of antibacterial proteins.

So what does this pick’n’mix of reptile, bird and mammal characteristics tell us about the very first mammals, our shared common ancestors? The ancestor of monotremes branched off from the rest of the mammals between 160 and 210 million years ago according to molecular studies. So which characteristics come from a common ancestor we both share, and which may have evolved in the millions of years since we diverged?

It turns out that many seemingly unique monotrematan traits may have been common in early mammals. The first mammals were almost certainly egg-layers - although direct fossil evidence of these fragile structures is yet to be found, and may never be. There’s a good chance they would therefore have possessed a cloaca. As for milk production, the first mammals had probably begun producing milk as suckling is linked to the evolution of deciduous dentition or “milk-teeth”; the pattern of tooth replacement that sees a first set of teeth being replaced by a permanent adult set. This deciduous dentition is one of the defining characteristics of mammals as a whole, also allowing for precise occlusion and complex food processing. The appearance of the nipple however, remains difficult to put your finger on.

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But what about the other traits of the monotreme: venom and low body temperature? There is evidence to suggest members of several different mammal groups had venomous spurs, or even venom in their bite. The spur of the platypus sits on a small bone called the os calcaris, and this bone has been found in multituberculates, an extinct order of mammals more closely related to the rest of Mammalia than to Monotremata. It has been suggested that poisonous spurs may even be one of the defining traits of all the first mammals, with later families losing their spurs.

Finding out the body temperature of early mammals is tricky, as this doesn’t preserve in the fossil record. It is thought that the mammal-like reptiles from which true mammals evolved had higher metabolic rates and body temperatures than their common ancestor with other reptiles. The first true mammals probably had a mix of warm-blooded, constant body temperature interspersed with daily, or even seasonal, torpor or hibernation. The echidna has been used as a modern example of this, as it can effectively turn off its inner thermostat to conserve energy during extremes of temperature.

The platypuses and echidna, animals we see as strange outliers among mammals today, are in many ways more akin to the original mammal blueprint than the rest of us. Had the luck of the evolutionary draw been different, and monotremes dominated mammal life on earth instead of us placentals, Dr. P. Latypus may have received a strange package from abroad with the first placental mammal specimen, and been flummoxed by this weird, spurless creature that can’t even lay eggs. She may even have thought it was a hoax.

References

Warren, W. C., Hillier, L. W., Marshall Graves, J. A., Birney, E., Ponting, C. P., Grützner, F., … Wilson, R. K. (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature, 453(7192), 175–183. http://doi.org/10.1038/nature06936

Whittington, C. M., Papenfuss, A. T., Bansal, P., Torres, A. M., Wong, E. S. W., Deakin, J. E., … Belov, K. (2008) Defensins and the convergent evolution of platypus and reptile venom genes. Genome Research, 18(6), 986–994. http://doi.org/10.1101/gr.7149808

Grigg, G., Beard, L., & Augee, M. (2004) The Evolution of Endothermy and Its Diversity in Mammals and Birds. Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches, 77(6), 982-997. http://www.jstor.org/stable/10.1086/425188

Lovegrove, B. G. (2012) The evolution of endothermy in Cenozoic mammals: a plesiomorphic‐apomorphic continuum. Biological Reviews, 87.1, 128-162. http://onlinelibrary.wiley.com/doi/10.1111/j.1469-185X.2011.00188.x/abstract?