Preface

The organ Darwin chose

The eye has long held a special place in arguments about where complex organs come from.1 In Natural Theology, first published in 1802, William Paley opened the main application of his argument by comparing an eye with a telescope.2 Paley’s case was that an organ as complex as the vertebrate eye could only be explained by divine design.3 Darwin read Paley’s works as a student at Cambridge and admired them deeply.4 In 1859 he wrote that he had hardly ever admired a book more than Natural Theology.5

In the same year Darwin published On the Origin of Species, and in it he took on the eye directly, under the heading “Organs of extreme perfection and complication”.6 The passage, in the words of the first edition, reads:

To suppose that the eye, with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree. Yet reason tells me, that if numerous gradations from a perfect and complex eye to one very imperfect and simple, each grade being useful to its possessor, can be shown to exist; if further, the eye does vary ever so slightly, and the variations be inherited, which is certainly the case; and if any variation or modification in the organ be ever useful to an animal under changing conditions of life, then the difficulty of believing that a perfect and complex eye could be formed by natural selection, though insuperable by our imagination, can hardly be considered real.7

The first sentence is often quoted on its own, without the sentence that answers it.8 Darwin revised the passage in later editions, and by the sixth edition of 1872 its last clause said the difficulty should not be taken to undermine the theory.9 Two pages later he set his own test: the theory would fail if anyone found a complex organ that could not have been formed by many small, successive changes.10

In private the eye still troubled him. In February 1860 he wrote to Asa Gray that it gave him “a cold shudder”, though when he thought of the known gradations, his reason told him he should overcome it.11

What is known now

The evidence gathered since Darwin fills the rest of this book. A few headline facts show its scale.

Eyes are found in about a third of animal phyla, and those phyla contain more than 95% of all animal species.12 Animals form images in at least ten distinct ways, using pinholes, lenses, concave mirrors and several kinds of compound eye.13 Between them, eyes use nearly every optical principle known to physics.14 They range from less than a tenth of a millimetre across in some water fleas to close to 300 mm in giant squid and the extinct ichthyosaurs.15 The oldest fossil eyes date from the early Cambrian, about 530 million years ago.16

The light-sensitive protein at the heart of animal vision, opsin, evolved once, early in animal history, but focusing optics evolved independently many times.17 In 1977 Salvini-Plawen and Mayr estimated that eyes had evolved separately at least 40 and perhaps 65 or more times.18 The count is less clear-cut today. Complex eyes arose separately in different lineages, yet they share their opsins, their photoreceptor cells and some of the genes that guide their development, so the answer depends on what is being counted.19 What is clear is that many kinds of photoreceptor, eye and visual role evolved more than once, in a pattern set by the demands of the tasks each eye serves.20

Nilsson and Pelger (1994) calculated that a flat patch of light-sensitive cells could become a focused camera eye in under 364,000 generations, using deliberately pessimistic assumptions.21 Land and Nilsson remark that the result would have cured Darwin’s cold shudder.22

Eyes did not evolve from poor to perfect. Most are probably close to the best their owners can use, so the sequence runs from simple tasks done well to complex tasks done well.23 Nor is any eye perfect: every one carries trade-offs and traces of its history, such as the blind spot in the vertebrate retina and the limit on how sharply a compound eye can see.2425

Why “half an eye”

The title of this book borrows an old question: what use is half an eye? The question assumes that only a complete organ is useful, and it is among the most common objections to the evolution of complex organs.26 It is older than it looks. In 1871 St George Mivart argued that natural selection could not explain the first stages of useful structures, and he listed the eye among his examples.27 The chapters that follow answer the question with evidence, one stage at a time.

How this book is organised

The book reads in order, like a printed one. Part I, Foundations, explains what eyes do, the molecular toolkit they are built from and the physics that limits them. Part II, From light patch to image, follows the route from a light-sensitive patch to an image-forming eye, through the fossil record and the story of our own eyes. Part III, The diversity of eyes, surveys camera eyes, compound eyes, mirror eyes and colour vision. Part IV, Imperfection and trade-off, looks at what eyes cannot do and why.

Two reference sections sit alongside the chapters. The Atlas of Eyes gives one page to each animal, from a single-celled alga to the eagle. Claims and responses takes common claims that the eye could not have evolved and answers each one, linking back to the chapters that hold the evidence. The chapters themselves set out the science and leave the arguments to that section.

Every factual sentence carries a numbered note that leads to its source. The About page explains how the book was researched and checked, and how you may reuse it.