The Evolution of the Human Head

Step into the National Portrait Gallery and look around. Heads are everywhere. Many portraits have shoulders, fewer have hands or torsos, but entire bodies are in a minority. All, though, have heads. Social interactions depend on heads, for recognising kin, friends and enemies, and inferring personality, emotions and background. Probably no other human body part merits its own museum. Hands barely merit a Los Angeles sidewalk, and a museum of famous footballers' feet would provide no insight into their feats. Heads, though, fill museums.

Heads also predominate in museums of archaeology, anthropology and anatomy. The vagaries of animal predation and fossilisation have left far more ancient human skulls than shinbones or ribs, and archaic human hands can be counted on one's fingers. Were there only thigh bones, then anatomical ingenuity would undoubtedly have worked out much. Give an anthropologist a skull, though, and they know almost everything that matters. Anthropologists may fantasise about complete, entire heads, but the soft stuff - skin, flesh, nerves, brain and gristle - is rarely preserved. It has, though, to hang on to the evolutionary palimpsests that are skull bones, leaving traces for the informed eye.

Daniel Lieberman has written a wonderful and inspiring book about the human head's evolution. It is the sort of book that governments, in Britain at least, find dangerous: there is no immediate economic impact; industry or business would not know what to do with it; its 700-plus pages are densely written, oozing scholarship; it fearlessly distinguishes paedomorphosis from peramorphosis, and klinorhynchy from airorhynchy, but lightens the load with diversions on head-binding, the sewers of Paris, and following chocolate trails around fields by sniffing.

One stands in awe at the work that has gone into it, the range of academic disciplines covered, the ability to take any feature of a head, however apparently trivial, and use measurement and comparison and theory and inference to extract so much. Such books are not produced in universities that ask professors each year whether they have earned their salary in teaching or research income, but in institutions that trust their scholars to produce work of the highest international quality. But Lieberman's university is Harvard, so enough said. Finding a parallel is hard, but I was reminded of D'Arcy Wentworth Thompson's masterpiece, published in 1919, On Growth and Form; of Julian Huxley's Evolution: The Modern Synthesis (1942); and J.Z. Young's The Life of Vertebrates (1950). Like them, this encyclopedic book is transformative.

Anatomy as a discipline - understanding the complex three-dimensional interrelations of the stuff that makes bodies - sank ever lower in the 20th century, as great 19th-century departments were absorbed into departments of applied molecular genetics. Dem dry, dry facts about dem dry, dry bones were seen as only relevant to surgeons or, increasingly, radiologists, whose ever more powerful scanners avoided any need to touch the soft, wet, pink and red stuff underpinning the ills that flesh is heir to. The morphological details in Lieberman's book make it a direct descendant of Gray's Anatomy, which Henry Gray published in 1858 just a year before Darwin's On the Origin of Species appeared. Lieberman's ruthless application of Darwinian principles to cranial anatomy makes his book thoroughly modern, each seemingly pointless detail of structure being shown, with a flourish, to be functional.

If a single word describes this book, it is integrative. The author integrates material from anatomy, physiology, physics, biomechanics, molecular and developmental biology, but brings all under the umbrella of evolutionary theory. What is became what is by changing what was, all the while surviving in an ever-changing environment. The many novel anatomical features make human heads unlike any other, even other great apes: a massive brain in a spherical vault, eyes below the frontal lobes, an external nose, a short mouth and tongue, a high larynx, omnivorous teeth with small canines, and eyebrows.

Each was a response to a changing environment and a changing ecological niche, as our ancestors evolved into a bipedal, social, diurnal omnivore, specialising in persistence hunts requiring aerobic endurance during the heat of the day, sweating to keep cool, collaborating to chase and exhaust prey and then safely dispatch them, and processing higher-energy foods needing less mastication and allowing earlier weaning of more frequent and larger offspring. All required massive changes in the head and left their marks. Only the chin, another human innovation, mystifies Lieberman, who wryly comments, "the chin may be an example of sexual selection. Testing this last hypothesis is especially difficult, but the reader is encouraged to think of appropriate experiments."

The mere how of evolutionary change and its functional adaptations is not the only challenge addressed. Change has to be realisable. Were a Mr Potato Head to be at an enormous selective advantage, with arms growing from the side of the head, such change could not be implemented, for evolution is the art of the possible. Evolution has to steer between, on one side, the Scylla of too much stability, in which organisms are reproducible from generation to generation but cannot change, and on the other, the Charybdis of too-great modifiability, where successful innovations are lost. (One thinks of the high mutation rate Haggunenons in Douglas Adams' Hitchhiker's Guide to the Galaxy, who found it easier to evolve a longer arm rather than reach for the sugar.)

Human engineering always suffers from excessive stability. To use Lieberman's example, gradually mutating a Porsche into a minivan, while functioning throughout, is barely conceivable. The missing ingredient is evolvability: the ability, presumably itself under evolutionary selection, to change effectively when change is necessary. Evolvability is a particular challenge for heads, which as Lieberman says are "like a Gordian knot of tissues, bones, organs and spaces".

Lieberman emphasises the process of head development. Bone is especially important, for it divides the head into abutting compartments; and bone is an intrinsically integrative tissue. It grows under stress, and resorbs under steady pressure. Deposition and resorption together allow bones to move, so that teeth, say, remain precisely aligned and chew effectively while children are growing. Development itself is a nexus of complex interactions. Genes make tissues grow, turning on and off during stages of development, while interacting epistatically with other genes, while tissues also interact, inducing or inhibiting other tissues.

Such processes allow what Lieberman, adopting Francois Jacob's term bricolage, calls "tinkering"; small changes in interactions between tissues or in the timing of gene action can produce large changes in the form of heads, while retaining functionality. In particular, the key insight is that evolvability requires much more than DNA.

The National Portrait Gallery in London does have one portrait without a head. Marc Quinn's portrait of Sir John Sulston, the Nobel prizewinning developmental biologist, consists entirely of Sir John's DNA. The gallery's website rather dubiously claims that "this portrait is an accurate display of Sulston's essential identity since it is composed of his own DNA" - but were Sir John an identical twin, that statement would definitely be wrong.

Lieberman's book reminds us that heads are determined by far more than DNA. The ontogeny of the Sulstonian head, from mere embryo through to adult form, with machinery for basic life support, complex intellectual machinations and generating the distinguished Sulstonian beard, all with its phylogenetic origins somewhere in Africa, are, as Lieberman eloquently shows, far richer, far more interesting and more complex than anything that base-pairs alone can tell us.

THE AUTHOR

Working on a project to estimate the brain size of an early human from a fragmented fossil found in Olduvai Gorge began Daniel Lieberman's fascination with the anatomy and biomechanics of the human head.

He was pursuing his undergraduate degree at Harvard University at the time. He is still at Harvard now, as professor of human evolutionary biology, in an office crowded with skulls - and running shoes.

Lieberman has long been an avid runner. Having completed several big events including the Bay State Marathon and the London Marathon, he is now training for the Boston Marathon this spring. A 2004 paper written with Dennis Bramble, "Endurance running and the evolution of Homo", sparked an interest in barefoot and minimal-shoe running, which he is very enthusiastic about.

He enjoys travelling and is fond of East Africa, where he has done much of his research since earning an MPhil in biological anthropology at the University of Cambridge in 1987. Six years later, he gained a Harvard PhD in the same subject.

Chloe Darracott-Cankovic