Book excerpt from The Wisdom of Birds
In Chapter 9, “Darwin in Denial,” author Tim Birkhead explains how Darwin’s failure to recognize avian female promiscuity resulted in a century of misconceptions about sexual selection
On a small area of waste ground outside the Andalusian town of Gaudix half a dozen middle-aged men are preparing for a contest that will determine their social status for weeks to come. Five of the men each carry a male pigeon bearing a colourful design painted on its wings. The sixth man holds a female pigeon decorated, incongruously, by the addition of three long pink feathers to her tail. At a given signal the female is placed on the ground and the men release their males in front of her. The effect of the female upon the males is electric: they launch themselves into a frenzy of courtship, strutting, tail-sweeping and bowing and cooing for all they are worth.
1 This extraordinary pigeon behaviour became a popular sport in Italy during the Middle Ages. The contests were called triganieri and involved two or more groups of pigeons flying around together until summoned back to their lofts by their owners’ flags or whistles, when any strangers were then taken captive. Friendly contests saw the captured pigeons returned or ransomed; in less friendly events, the captives were killed.
The Moors brought triganieri birds to Spain during the Middle Ages, where they became known as palomas ladronas, or ‘thief pigeons’. The birds were deliberately bred and trained to lure members of the opposite sex back to their home loft. Not everyone appreciated them, and one eleventh-century law from Seville stated, ‘The sale of thief pigeons will be absolutely prohibited, a custom used exclusively by people without religion…’2
The behaviour of the thief pigeons and their ‘victims’ is absolutely remarkable. Male thief pigeons excel in attracting and accumulating females, copulating with them and abandoning them to rear the offspring alone. An exceptional male can even induce an incubating female to abandon both her partner and her eggs—almost unheard of among wild birds—and return with him to his loft. The fact that females will desert their nest, eggs and partner for a male she deems more attractive flies in the face of just about everything we expect of birds, and certainly of pigeons, which were once considered models of monogamy.
Darwin was well aware of the existence of thief pigeons and also knew from observations of his own birds that female pigeons were occasionally unfaithful. But he was in denial: acknowledging that promiscuity among males was natural, he seems to have ignored the fact that it takes two to tango, and that females were also promiscuous.3
Perhaps he was seduced by the long-standing, popular belief in the fidelity of female doves, enunciated (somewhat contradictorily) since Pliny’s time:
Next to the partridge, it is in the pigeon that similar tendencies are to be seen in the same respect: but then, chastity is especially observed by it, and promiscuous intercourse is a thing quite unknown. Although inhabiting a domicile in common with others, they will none of them violate the laws of conjugal fidelity: not one will desert its nest, unless it is either widower or widow.4
Despite recognising the pigeon’s tendency to ‘stray’, Pliny and everyone else persisted in promoting the pigeon as a paragon of sexual fidelity. For Darwin, male promiscuity was the norm and an important part of his vision of sexual selection. Female promiscuity on the other hand was explicitly not part of sexual selection; in Darwin’s book females were coy, cautious and, above all, faithful:
It is shown by various facts, given hereafter, and by the results fairly attributable to sexual selection, that the female, though comparatively passive, generally exerts some choice and accepts one male in preference to the others.5
The strange thing about this statement is that Darwin knew it wasn’t true. He simply chose to ignore all the evidence that females could be promiscuous.
For example, Aristotle had commented on the fact that female fowl sometimes copulated with more than one male, and when they did the offspring resembled the second of the two males: ‘and the eggs previously fertilised by another breed of male change their nature to that of the male which copulates later’.6
William Harvey, in his Disputations on Generation in the 1600s, said:
There are some species of animals in which one male suffices for many females as in the case of hinds and does, and breeds of cattle. And again there are others in which the females are so passionate with desire that they are scarcely satisfied with many males, as the bitch and the shewolf, and for this reason prostitutes are called ‘she-wolves’ because they make their bodies public, and brothels ‘lupanaria’, in which they offer their wares for sale.7
Daniel Girton writing in 1765 warned pigeon-breeders that their strains might be ‘adulterated by a false tread’, which he said ‘an over salacious hen will frequently submit to…’ thereby providing clear evidence that doves at least occasionally engaged in extra-pair copulations.8
William Smellie wrote of the domestic fowl: ‘The dunghill cock and hen, in a natural state, pair. In a domestic state, however, the cock is a jealous tyrant, and the hen a prostitute.’9
Even more surprisingly, Darwin himself actually describes a case that exemplifies female promiscuity. The information came from William Darwin Fox, his cousin and chum from their Cambridge undergraduate days. Fox was a clergyman and, fascinated by natural history, kept a menagerie at his home in Cheshire. In 1868 he wrote to Charles to tell him about his geese, and the story subsequently appeared in Descent:
The Rev. W. D. Fox informs me that he possessed at the same time a pair of Chinese geese and a common gander with three geese. The two lots kept quite separate, until the Chinese gander seduced one of the common geese to live with him. Moreover, of the young birds hatched from the eggs of the common geese, only four were pure, the other eighteen proving hybrids; so that the Chinese gander seems to have had prepotent charms over the common gander.10
So why, in the face of so much evidence, did Darwin deny female promiscuity? There are several possibilities. The first is that he simply did not see it. Darwin’s purpose in recounting his cousin’s goose story was evidence for female choice, not promiscuity. It also suited Darwin to assume females to be monogamous. Victorian gentlemen did not discuss infidelity—at least, not openly. Assuming females to be monogamous also avoided any embarrassment at home. Darwin’s daughter Etty, then in her late twenties, was helping him correct the proofs of Descent and so he was extremely careful about what he wrote.11
Darwin wasn’t alone. Other natural history writers found it politically (or commercially) convenient to assume female fidelity. In some wonderfully florid prose, Buffon (probably disingenuously) extolled the pigeon’s social virtues:
They are fond of society, attached to their companions, and faithful to their mates; a neatness, and still more the art of acquiring the graces, bespeak the desire to please; those tender caresses, those gentle movements, those timid kisses which grow close and rapturous in the moment of bliss; that delicious moment soon renewed by the return of the same appetites, and by the gradual swell of the soothing melting passion; a flame always constant, and ardour continually durable; an undiminished vigour for enjoyment; no caprice, no disgust, no quarrel to disturb the domestic harmony, their whole time devoted to love and progeny; the laborious duties mutually shared; the male assisting his mate in hatching and guarding the young:—If man would copy, what models for imitation.12
William Smellie, on the other hand, while acknowledging female promiscuity excuses it as an artefact of domestication. He assumes logically that promiscuity in the domestic fowl is a consequence of their pampered life in captivity, drawing a parallel with those human cultures where abundant resources in the hands of a few powerful males results in them acquiring and jealously defending harems of submissive females.13
The idea that birds and other animals might provide appropriate models for human behaviour wasn’t new, but it led to a distortion of the facts and there was precious little consistency in whether a particular species exemplified virtue or vice. Pigeon-fancier John Moore, for example, proposed that we should emulate the English Pouter pigeon:
Separate the old ones, placing them in different coops, and feeding them high with hemp…then turning them together; and by being very hearty and salacious, they breed pigeons with very good properties; from whence we may observe, that would mankind be alike abstemious, their progeny might be more complete both in body and mind.14
In other words, Moore implies that sexual abstinence somehow results in better quality offspring.
The idea that birds provided moral guidance encouraged religious societies to foster bird-keeping and ornithology, and explains why Anglican organisations like the Society for the Promotion of Christian Knowledge (SPCK) and the Religious Tract Society published so many books on natural history and bird-keeping during the Victorian period. These included Anne Pratt’s Our Native Songsters and Our Domestic Fowls and Song Birds by William Linnaeus Martin who wrote: ‘In the creation of animals, whether quadrupeds or birds, expressly serviceable to man, and so highly conducive to his prosperity, and, at the same time, so easily subjugated or tamed, we cannot but see the wisdom and goodness of Divine Providence.’15 God’s creatures also provided role models for human behaviour and the British ornithologist the Reverend Frederick Morris advocated (mistakenly, as we’ll see) that his parishioners emulate the dunnock:
Unobtrusive, quiet, and retiring, without being shy, humble and homely in its deportment and habits, sober and unpretending in its dress, while still neat and graceful, the Dunnock exhibits a pattern which many of a higher grade might imitate, with advantage to themselves and benefit to others through an improved example.16
Darwin’s influence on biology was such that his statement about female fidelity resulted in a century of mistaken belief about their sexual behaviour. Even in the 1950s and 1960s, when field studies of the behaviour of individually marked birds were just starting to yield rich returns, ornithologists were still in denial. When they saw extra-pair matings in species thought to be monogamous, they simply discounted the possibility that females were in any way responsible, and sometimes even excused the males by suggesting they were sick or suffering from a hormone imbalance.17 In other words, as recently as fifty years ago infidelity among socially monogamous birds was considered a mistake.
The change occurred in the late 1960s, as ideas about the way evolution occurred were brought into sharper focus. Over the preceding years, biologists had allowed the idea of natural selection to drift away from Darwin’s original, ruthless process that cut down or promoted individuals, and instead—in certain quarters at least, and especially in the public’s eye—had become more benign and more concerned with preserving the species. With this mindset it is easy to see how ornithologists prior to the 1960s might have struggled to make sense of infidelity: what possible advantage could there be to the species of one male inseminating another’s partner?
Not everyone at that time thought of natural selection operating on species. David Lack for one did not. He and a handful of others stuck rigorously to Darwin’s original view that selection worked on individuals. Most influential of these was George Williams, then at Stony Brook University, New York, whose book Adaptation and Natural Selection was written to counter such species-centered evolution. It launched a new era in evolutionary thinking and in bird biology in particular.18
Two young biologists, Geoff Parker and Bob Trivers, neither of whom were strictly ornithologists, were keen advocates of Williams’ new way of thinking. Parker, an amateur breeder of exhibition poultry and a professional zoologist, studied the promiscuous mating behavior of dungflies. Bob Trivers, more interested in ideas than animals, was none the less inspired by the behaviour of the pigeons on his Harvard apartment windowsill:
What soon became clear in this monogamous species was that males were sexually much more insecure than were females, and males acted to deprive their mates of what they would be happy to indulge in themselves, that is, an extra-pair copulation…the group outside my window began with four pigeons—two mated couples. They slept next to each other in the gutter of the roof of the house next door…the two males, although they were the more aggressive sex, always sat next to each other with each one’s mate on the outside. By sitting next to each other, the males could ensure that each one was sitting between his mate and the other male.19
More or less independently, Trivers and Parker capitalised on individual selection to create a new vision of sexual selection. With an explicitly individual perspective reproduction was no longer the cosy, cooperative affair between male and female operating for the good of the species, but instead was a battleground in which members of each sex competed among themselves, attempting to exploit the other in a struggle for genetic representation. Sexual selection was about producing descendants and, from an evolutionary perspective, genetic descendants were all that mattered.
Thanks to Geoff Parker and Bob Trivers sexual selection was reborn in the late 1960s. What they said was what Darwin had meant all along, although, to be fair, he hadn’t always said it as clearly as he might have. Parker and Trivers picked up this new version of evolution and ran with it and so rich were the insights it provided that biologists have been running with it ever since.
By assuming females to be sexually monogamous Darwin automatically imposed the view that sexual selection came to an end once an individual of either sex had acquired a mating partner. What Parker recognised as he watched his female dungflies copulate with a succession of males was that sexual selection also continues after insemination and carries on, right up to the moment of fertilisation. Males compete for fertilisations, not females.20
By being promiscuous a female carries the sperm of several males simultaneously and those sperm then compete to fertilise her eggs. Sperm competition, as Parker called it, is a potent evolutionary force, for in an evolutionary sense it pays a male to protect his own paternity, but at the same time it also pays to steal paternity from other males. As Parker recognised, the conflict this inevitably creates in the evolutionary struggle for descendants drives males to outdo each other, through their behaviour, anatomy or physiology—in any way possible. For the time being, females were not considered.
Acknowledging the existence of sperm competition allowed other pieces of the reproductive puzzle to fall into place. For centuries, biologists and others had pondered the significance of unusual reproductive phenomena. This new view of sexual selection—it was called ‘postcopulatory’ to focus attention on the fact that the battle for paternity continued after copulation and insemination—provided answers to many questions, including one asked by John Ray in The Wisdom of God:
Why should there be implanted in each sex such a vehement and inexpugnable appetite of copulation?21
Here, Ray may have been thinking of the house sparrow, whose copulatory prowess was legendary:
Its desire for coitus and reproduction is so compelling that it may copulate as many as twenty times an hour.22
In 1559 Dresden’s parson Daniel Greysser was commended for his Christian zeal in having ‘put under ban the sparrows, on account of their unceasing and extremely vexatious chatterings and scandalous unchastity during the sermon’.23
We now know the reason for their inexpugnable appetite: female promiscuity. If females are promiscuous a male’s best chance of being the true father of the chicks he helps to rear is to copulate repeatedly with his partner. House sparrows, for example, form season-long pair bonds, but infidelity is common and some 10 to 15 per cent of all chicks are the outcome of extra-pair copulations. The figure would be higher still if male partners did not copulate so frequently with their female. The rules are pretty much the same for other birds, too, and indeed elsewhere in the animal kingdom; frequent copulation is a paternity assurance device and therefore an evolutionary imperative. I cannot help feeling that, had this been explained to Ray, he would have seen its compelling logic.
Birkhead, Tim. The Wisdom of Birds: An Illustrated History of Ornithology. pp. 301-12. ©2008 (Bloomsbury). Reprinted by permission of Bloomsbury.
2. This law dates from the eleventh century: ‘Treatise of Ibn Abdun’, Seville. Article 141 (Levi-Provencal, 1947). The contest known as triganieri is clearly an ancient one; it continues to be popular in Scotland in Glasgow’s East End (Hansell, 1998; Birkhead, 2000). Darwin (1871) knew about thief pigeons and I find it remarkable that he never followed up on this for it was fabulous evidence for sexual selection; the fact that some males were more attractive than others, but that breeders could artificially select for this attractiveness, confirmed that it was heritable. Darwin was in denial twice over, failing to recognise that females could be promiscuous and that thief pigeons provided incontrovertible evidence for sexual selection.
3. Darwin (1871).
4. Pliny, Book X, chapter 52. In fact, like much else, this comes from Aristotle, who was also probably the first to comment on pigeon infidelity; ‘As a general rule these birds [pigeons] show…conjugal fidelity, but occasionally a female will cohabit with other than her mate’ (in Aristotle, History of Animals, Book IX).
5. Darwin (1871).
6. Aristotle, Generation of Animals, 757b2-3; see also Brock (2004). This statement has caused much discussion.
7. Harvey, cited in Whitteridge (1981: 178).
8. Girton (1765); Tegetmeier (1868) says that Girton was largely plagiarised from Moore (1735).
9. Smellie (1790).
10. Darwin (1871).
11. See Birkhead (2000) and Desmond & Moore (1991). John Murray, Darwin’s publisher, felt it was inappropriate to use the term ‘sex’ on the title page of ‘The Descent of Man and Selection in Relation to Sex’ (Browne, 2002), and when Darwin did have to refer something explicitly sexual—such as the colorful swellings of female monkeys’ ‘bottoms’ (in fact their genitalia)—he did so in Latin, presumably to minimise any embarrassment. Intriguingly, when Leeuwenhoek wrote to the Royal Society to tell them about his discovery of (his own) spermatozoa (see chapter 2), he also wrote in Latin—the only time he did so.
12. Buffon (1771).
13. Smellie (1790: 278). Smellie, who translated Buffon’s Histoire Naturelle, is paraphrasing Buffon here.
14. Moore (1735).
15. Pratt (1852); William Charles Linnaeus Martin’s book Our Domestic Fowls and Song Birds is undated, but was probably published about 1850. Linnaeus? What were his parents thinking?
16. Morris (1835).
17. See, for example, Marler (1956).
18. Williams (1966).
19. Trivers (2002: 58).
20. Sexual selection may even extend beyond fertilisation (see Birkhead and Moller, 1998).
21. Ray (1691: 115).
22. Albert the Great, as cited in Kitchell and Resnick (1999).
23. Evans (1906, 128).
March 19, 2011