Some Assembly Required, by Neil Shubin (review)

by Paul Braterman

Some Assembly Required, Neil Shubin, Pantheon/Penguin Random House, March 2020, ISBN 978-1101871331, publisher’s price HB $26.95, £20.72

This book will be of interest to anyone who is interested in the way in which evolution actually proceeds, and the insights that we are now gaining into the genome, which controls the process. The author, Neil Shubin, has made major contributions to our understanding, using in turn the traditional methods of palaeontology and  comparative anatomy, and the newer methods of molecular biology that have emerged in the last few decades. He is writing about subject matter that he knows intimately, often describing the contributions of scientists that he knows personally. Like Shubin’s earlier writings, the book is a pleasure to read, and I was not surprised to learn here that Shubin was a teaching assistant in Stephen Jay Gould’s lectures on the history of life.

Shubin is among other things Professor of Organismal Biology and Anatomy at the University of Chicago. He first came to the attention of a wider public for the discovery of Tiktaalik, completing the bridge between lungfish and terrestrial tetrapods, and that work is described and placed in context in his earlier book, Your Inner Fish. The present volume is an overview, from his unique perspective, of our understanding of evolutionary change, from Darwin, through detailed palaeontological studies, and into the current era of molecular biology, a transition that, as he reminds us, parallels his own intellectual evolution.

Shubin3In addition to the underlying science narrative, we have a wealth of biographical detail regarding those involved in the discoveries being discussed, and the milieu in which they worked. These details are not mere embroidery, but an integral part of his exposition. For example, I was aware that Linus Pauling, with Emil Zuckerkandl, was a pioneer in the use of sequence differences as a molecular clock, but did not know how this related to Pauling’s interest in radiation damage to proteins, a topic that brought together his scientific and political concerns.

The exposition is clear enough to be followed by readers without background scientific training, but the range of topics discussed, the choice of illustrative details, and the historical and biographical background are such that I would expect even experts to find much in this book to inform and delight. The endnotes, as well as providing leading references and background material of interest to those who wish to dig deeper, add numerous interesting details worthy of the attention of any reader.

We start with a blackboard sketch from the author’s student days; a single arrow, reflecting what was known at the time, connecting a fish to an amphibian. But how could this possibly happen? There are so many things that have to change. Fins have to become legs, and breathing has to change from gills extracting oxygen from water, to lungs breathing air. But neither of these changes seems possible unless the other one has already taken place. Worse, we can understand that natural selection would refine the structures of legs and lungs, but what use would they be to a fish, and so how did they get started in the first place? To quote (as Shubin quotes) one of the strongest objections offered to Darwin’s theory when first presented, how can we get past “The incompetency of natural selection to account for the incipient stages of useful structures”?

Shubin4Darwin paid great attention to such criticisms, and even added a whole chapter (“Miscellaneous Objections to the Theory of Natural Selection”) to the sixth edition of On the Origin of Species. His answer to the problem of incipient stages is encapsulated within five words: “This subject is intimately connected with that of the gradation of the characters, often accompanied by a change in function.” For example, as shown clearly by embryological comparisons in 1895, the lungs of the lungfish and its terrestrial descendants, and the swim bladder used by other fish to control their density and position in the water, start out in exactly the same way, and we now know that their development is controlled by closely related genes. So the lungs first appeared, not in terrestrial vertebrates to which they are essential, but in fish that were already able to absorb oxygen from water through their gills. Likewise, we can regard tetrapod limbs as derived from fins, and as having had the early function of supporting part of the weight of the fish in shallow water.

Shubin quotes an observation made by the playwright Lillian Hellman, “Nothing, of course, begins at the time you think it did.” On inspection, the roots always live far deeper. To which I would add an observation of my own; nothing that is at the time essential can arise by evolution. For if it had been essential, the organism could not have survived to that stage without possessing it. Your backbone is essential to your survival; its Cambrian precursor tissue was not.

Now consider birds. As early as the 1860s, TH Huxley had seen these as related to dinosaurs and alligators. Archaeopteryx, described too late for the first edition of Origins but briefly mentioned in the fourth, was clearly in some sense intermediate between a modern bird and a reptile, but what kind of reptile?  We need to account for bipedalism, light bones, feathers, an active metabolism, and, I would add, the highly efficient respiratory system found in all birds, that uses one-way flow through the lungs, and  exhalation through air sacs. We now have evidence for all these things in dinosaurs, and the respiratory system  may have been relevant to the success of the dinosaurs in the relatively oxygen-poor atmosphere of the Triassic. Once again, the crucial steps do not involve the development of new features, but the repurposing1 of what is already in place.

Human embryo at 28 days showing gill arches

Repurposing also occurs during development. For example, the embryo gill arches, which in fish become, as their name suggests, gills and gill slits, develop in tetrapods to become the lower jaw and throat. To understand what is happening, we need to understand how development is controlled, and development is controlled, like so much else, by DNA. And it is this DNA that provides the theme of the final two thirds of the book.

Before DNA sequencing became available, Zuckerkandl and Pauling had realized2 that accumulated mutations would give rise to differences in the proteins found in different species, and that the degree of difference was a measure of the length of time that had passed since those species shared a common ancestor.

Protein sequencing has long since been superseded by DNA sequencing. Over the past two decades, DNA sequences have been obtained and published for numerous species, and used to construct, in greater detail, evolutionary family trees similar to those already known from the fossil record and comparative anatomy. One surprise is that only some 2% of the DNA directly codes for proteins. A lot of it must be junk, since there is no connection between the amount of DNA, and the complexity of the organism.3 One other interesting question also arises. How is it that a brain cell, a liver cell, and a skin cell develop in such extremely different ways, since they all contain exactly the same DNA?

It turns out that genes can be switched on and off depending on the environment that a cell finds itself in. In development, the switches are produced by genes which are themselves responsive to their environment, giving rise to complex causal networks. If that sounds complicated, that’s because it is. The molecular mechanisms of development, and how they themselves evolved, are among the most exciting areas of current research, and Shubin devotes considerable space to describing for us the current state of play.

Millipede (Harpaphe haydeniana)

Some features turn out to be common across the entire animal kingdom. Worms have segments, insects and other arthropods have segments, and at a very fundamental level our backbone is a series of segments. The control genes in worms, crabs and insects are directly related to the Hox genes of vertebrates, including fish, and the same Hox genes that are active in the development of toes are also active in the development of the terminal ends of fishes’ fins. Everywhere, we see the redeployment of similar subroutines.

Repurposing also takes place within the DNA itself, by means of duplication, as well as by transfer of genetic material between different species.  The existence of two separate subunits within the haemoglobin molecule is the result of an ancient duplication. Vertebrates show a fourfold repetition of their Hox genes, as the result of two episodes in each of which the entire genome was duplicated.  Colour vision is a much quoted example of the possibilities created by gene duplication. Old world monkeys and their close relatives (including us) have three-colour vision, unlike the two-colour vision of most mammals. This arose through duplication of the gene for green-sensitive visual pigment, allowing one copy, by a minor change in its protein sequence, to evolve sensitivity for red.

Sequencing shows that multiple repetition is so common as to make up two thirds of the entire human genome, and some fragments are “jumping genes”, which have replicated at multiple different sites. But replicating huge amounts of useless material must have a metabolic cost, and genomes must have a way of protecting themselves against parasitic duplicators, or else this duplication would be killing species in much the same way that unregulated duplication of cells kills cancer patients.

We can understand major changes in body form, even such major changes as those between fish and land animal, or between running dinosaur and bird, in terms of a sequence of small interlocking adaptations. The appearance of a new kind of cell, such as bone cells, presents a much more difficult problem, since it entails an entire new suite of proteins, so that it looks as if many different things would have had to happen at once. One way in which this can occur is by the incorporation of multiple copies of a sequence at different sites, as sometimes happens with jumping DNA derived ultimately from a virus. This has happened in the cells responsible for forming the mammalian placenta.

How predictable is evolution? Some generalisations arise from physical forces. Animals living in cold regions generally have smaller appendages (limbs, years, snouts, tails) than their relatives in more equitable climates, and tend to grow to larger size, all of which makes sense in terms of reducing heat loss in relation to body mass. But are there other propensities built into the evolutionary process itself?

Northern flying squirrel (Glaucomys sabrinus)

There are connections between evolutionary changes, and those that take place during development. This suggests that there is a certain repertoire of possible changes, so we can expect similar changes to occur independently in separate lines of descent, under the influence of similar environmental pressures. We can see such parallel evolution on a grand scale when we compare the marsupial mammals that made their way to Australia with the placental mammals that now dominate the other continents. Shubin mentions a marsupial flying squirrel, a marsupial mole, a marsupial ground cat, and among extinct species marsupial lions, wolves, and tigers.

Squirrel glider, not a squirrel at all but a marsupial related to the opposum

 Towards the end of the book, Shubin turns his attention to what he terms “Mergers and acquisitions”. The complex cells found in all plants, animals, and fungi are actually the result of a merger between two much simpler types, bacteria and archaea. This combined the energy-producing metabolism of bacteria (ultimate ancestors of our mitochondrial) with the ability to produce the large range of proteins required for complex life. The idea was highly controversial when advocated by Lynne Margulis in the 1960s, but DNA confirms the bacterial ancestry of mitochondria, and archaea as the ancestors of the nucleus. Green plants have undergone an additional merger, with their chloroplasts (where photosynthesis takes place) being derived from photosynthetic bacteria, known as cyanobacteria or, commonly but misleadingly, as blue green algae.

The individual cells of complex life forms are complex assemblages. The individual organisms are assemblages of such complex cells. But what is the origin of these higher level assemblages, which require a range of control genes, and specialized connective tissues?

Choanoflagellate rosette

Single-celled creatures known as choanoflagellates clump together under some circumstances, and their genome already shows the presence of genes that make collagen and sticky proteins. Here they are used to ward off predators, or to attach food particles. Once again, something absolutely essential at a later stage, the molecular scaffolding of complex organisms, had its origin in something much earlier.

Shubin concludes with one final example. A strange pattern was discovered in salt-loving bacteria, that had the effect of cutting up the nucleic acid of invading viruses. This system has now been refined into the molecular editing technique known as CRISPR, an extremely powerful tool for DNA editing, already in use in laboratories throughout the world. A system developed by one of the simplest of organisms to protect itself from an even simpler invader is now being used by the most complex organism on Earth to carry out feats of DNA modification that, in nature, would take millions of years. The ultimate in repurposing.

Disclosure: I have been guilty of piracy, albeit unintentionally. The copy of the book that I have been working from, which was obtained from an on line bookseller before publication date, turned out to be an uncorrected “not for sale” proof. This also means that I cannot comment on the index or illustrations, since my own copy lacks these.

1] The formal term is exaptation, but I prefer Shubin’s jargon-free replacement.

2] Evolutionary Divergence and Convergence in Proteins, Emile Zuckerkandl and Linus Pauling, Evolving Genes and Proteins, 1965, Pages 97-166, and earlier papers.

3] My favourite example (Gregory’s onion test, proposed by T. Ryan Gregory); an onion has five times as much DNA as a human. Gregory, T.R. (2007). The onion test. Genomicron, 25 April, 2007.

Shubin image from University of Chicago website. Tiktaalik image from The Field Museum, Chicago, via Wikipedia, under Creative Commons license. Human embryo image from Gray’s Anatomy (1918) via Wikipedia. Millipede (Harpaphe haydeniana) image by Walter Siegmund via Wikipedia under Creative Commons license. Flying squirrel and squirrel glider images, public domain. Choanoflagellate rosette image by Dzhanette, public domain, via Wikipedia.