The Colours of Animals


The Colours of Animals is a zoology book written in 1890 by Sir Edward Bagnall Poulton. It was the first substantial textbook to argue the case for Darwinian selection applying to all aspects of animal coloration. The book also pioneered the concept of frequency-dependent selection and introduced the term "aposematism".
The book begins with a brief account of the physical causes of animal coloration. The second chapter gives an overview of the book, describing the various uses of colour in terms of the advantages it can bring through natural selection. The next seven chapters describe camouflage, both in predators and in prey. Methods of camouflage covered include background matching, resemblance to specific objects such as bird droppings, self-decoration with materials from the environment, and the seasonal colour change of arctic animals. Two chapters cover warning colours, including both Batesian mimicry, where the mimic is edible, and Müllerian mimicry, where distasteful species mimic each other. A chapter then looks at how animals combine multiple methods of defence, for instance in the puss moth. Two chapters examine coloration related to sexual selection. Finally Poulton summarizes the subject with a fold-out table including a set of Greek derived words that he invented, of which "aposematic" and "cryptic" survive in biological usage.
The Colours of Animals was well received on its publication, although the book's support for sexual selection was criticised by Alfred Russel Wallace, and its Darwinism and critique of Lamarckism were attacked by Edward Drinker Cope. Wallace liked Poulton's experimental work but was critical of his opinions on sexual selection. The Neo-Lamarckian Cope criticised Poulton's support for Darwin but liked the book's many observations of animal coloration. Modern biologists respect Poulton's advocacy of natural selection and sexual selection, despite the lack at the time of an adequate theory of heredity, and his recognition of frequency-dependent selection.

Book

Approach

; Evidence for natural selection
Poulton explains in his Preface that
; Evidence for sexual selection
File:ArgusDisplayLyd4.png|thumb|right|Male argus pheasant displaying to a female, from Richard Lydekker's Royal Natural History, 1895.
Poulton strongly supports Darwin both on the general theme of natural selection, and on the power of sexual selection in species which are sexually dimorphic :
Poulton knew his view was controversial, but believed he was winning the argument:
; Frequency-dependent selection
In The Colours of Animals, Poulton introduced the concept of frequency-dependent selection in the context of a polymorphism which he argued would otherwise soon vanish:
; Mimicry and aposematism
The basic concept of warning coloration is approached very simply:
In the next paragraph Poulton ties aposematism to mimicry as follows:
Poulton introduced the term aposematism with the words:

Contents

The book's structure emphasises the extent to which Poulton, like Darwin, relied on a mass of evidence, mainly from insects, to make his case:
Chapter 1 The Physical Cause of Animal Colours.
Chapter 2 The Uses of Colour.
Chapter 3 Protective Resemblances in Lepidoptera.
Chapter 4 Protective Resemblances in Lepidoptera, Dimorphism, Etc.
Chapter 5 Protective Resemblances In Vertebrata, Etc.
Chapter 6 Aggressive Resemblances — Adventitious Protection.
Chapter 7 Variable Protective Resemblance in Vertebrata, Etc.
Chapter 8 Variable Protective Resemblance In Insects.
Chapter 9 Protective Resemblances in Lepidoptera .
Chapter 10 Warning Colours.
Chapter 11 Warning Colours .
Chapter 12 Protective Mimicry.
Chapter 13 Protective and Aggressive Mimicry.
Chapter 14 The Combination of Many Methods of Defence.
Chapter 15 Colours Produced by Courtship.
Chapter 16 Other Theories of Sexual Colouring.
Chapter 17 Summary And Classification.

Reception

On first publication in 1890

Wallace in ''Nature''

The co-discoverer of natural selection Alfred Russel Wallace, reviewing Poulton in Nature, was interested by Poulton's observations on thin films producing iridescence: "In some cases dried insects lose some of their metallic colours, but these reappear when the specimen is dipped in water." However, Wallace objected to Poulton's suggestion that arctic birds and mammals are white to reduce heat loss by radiation, for which he argued there was no evidence in favour, while a thicker "covering, such as actually occurs in all arctic animals" would reduce heat loss effectively, and could be observed to do so.
Wallace was enthusiastic about Poulton's experimental work on how butterfly larvae vary their coloration according to the background, admiring "a number of ingenious experiments" in which Poulton illuminated the insects in light of one colour or another, causing reliable colour changes which could not be direct, like photography, but had to be mediated by the animal's nervous system:
In some cases even the cocoons spun by the larvæ are modified by the surrounding colours; and still more curious changes are effected in the larva itself when... the same species feeds on several plants having differently-coloured leaves. Even the presence of numerous dark twigs has been shown to cause a corresponding change of colour in the larva of the peppered moth."

Wallace's main criticism, occupying half his lengthy review, was of Poulton's acceptance of sexual selection. He begins by stating "Mr. Poulton fully accepts Darwin's theory of female choice as the source of the greater part of the brilliant colour, delicate patterns, and ornamental appendages that exist among animals, and especially among birds and insects." Wallace then cites Poulton on the courtship behaviour of spiders:
"'The female always watches the antics of the male intently, but often refuses him in the end, 'even after dancing before her for a long time.' Such observations strongly point towards the existence of female preference based on æsthetic considerations'"

at once objecting "To the last four words we demur, as being altogether unproved. Why æsthetic considerations?" Wallace then spends a whole page attacking Poulton on "the possession of an 'æsthetic sense' by those creatures in which sexual ornament occurs". Wallace objects that Poulton asserts the reality of sexual selection with no proof other than mentioning that insects can perceive colour, and that "a few birds collect bright objects, as in the case of the bower-birds".
Wallace gives a detailed counter-example to refute Poulton's argument, arguing that "really beautiful combinations of colour and marking" are found on the sea shells of molluscs "where sexual selection has certainly not come into play". To make the point, Wallace lists
"the cones, cowries, olives, harps, volutes, pectens, and innumerable other molluscan shells; while many of the sea-anemones, and considerable numbers of the caterpillars with warning colours, are equally beautiful."

And that was not all. Wallace continued:
"Still more doubtful and more opposed to reasonable probability is the statement that 'our standards of beauty are largely derived from the contemplation of the numerous examples around us, which... have been created by the æsthetic preferences of the insect world'--alluding... to the colours and structures of flowers as being due to the need of attracting insects to fertilize them."

There was, Wallace insisted, "not a particle of evidence" of aesthetic preferences in "an insect's very limited mentality". The mention of the term aesthetic was "not scientific".
After so many "preceding remarks" against "the theory of sexual selection", Wallace concludes that "The book is well illustrated by numerous excellent woodcuts and a coloured plate", congratulates Poulton on "having produced so readable and suggestive a volume", and on having "contributed so largely" by "his own researches" into animal coloration.

''New York Times''

An anonymous reviewer in the New York Times wrote that "Mr Poulton wishes first of all to put himself right with regard to his attitude to Darwinism", mentioning that in 1888 he had been cited in the Edinburgh Review as attacking Darwinism. The reviewer hastens to agree that Poulton is in fact "ready to combat Wallace, his master, on points wherein that great fellow-laborer with Charles Darwin dissents from the latter's views."
As an example of this, the reviewer mentions Poulton's argument that Wallace must be wrong that "the coloring whereby the sexes often differ one from the other in a startling way is occasioned by a surplus vitality" because "sexual colors are only developed in species which court by day or twilight" and then only on parts of the body which the female "would oftenest and best see them".
The New York Times reviewer argued that the title should have been less general "for readers are sure to demand too much from so comprehensive a term", given that Poulton refers mainly to insects rather than "wild beasts", but in the end he agreed "that Mr. Poulton has written a very suggestive treatise, well fitted for the general reader".

E.D. Cope in ''American Naturalist''

The Neo-Lamarckian Edward Drinker Cope, reviewing the book for the American Naturalist, wrote that "Mr. Poulton supports his own theory of the direct physiological value of the uses of colour to animals by a large amount of experimental evidence brought together from many sources". Cope is attracted by "a detail of great interest" in a caterpillar's camouflage "by the semblance of a small hole to indicate piercing by insect larvae", and is impressed by Poulton's observations of "perhaps the most perfect concealment attained by any butterfly" in the dead leaf butterfly Kallima, first described by Alfred Russel Wallace.
While admiring of Poulton's detailed observations, Cope was critical of his support for Darwin, arguing that Poulton failed to explain how the variability that natural selection needs to work on actually arises.
Cope also objected to Poulton's critique of Lamarckism, where in a footnote he cites S.B.J. Skertchly as writing that "other butterflies noticed this immunity copied it, to which Cope replies as that "even the American Neo-Lamarckians do not follow their founder so far as to believe that the volition of an animal could account for all the details of mimetic resemblance."