Role Reversal, Sex Change and Intersexuality in Animals

David Lyon

Biologist. Government Service Officer
Gendys Conference, 1992

INTRODUCTION.

I wish to talk about sex in animals from a biologist's point of view and to run through some of the major groups which display some interesting features, say a few words about animal behaviour, and then finish with some animal/human interactions.

We have been discussing various aspects of "intersexuality", in its broadest sense, in humans. The existence of similar or analogous phenomena elsewhere in the animal kingdom has been well known since ancient times and has stimulated a variety of responses from institutions such as the church, to individuals from Aristotle to Darwin. More recently these phenomena have been the subject of much scientific research, not only because they are fascinating in themselves but also for the light they shed on matters such as the evolution of sex, the mechanisms that determine sex and, ultimately, human sexual problems.

This paper makes no claim to being an up-to-date, rigorous, scientific review of the subject; rather the aim is to show that the concept encapsulated in Genesis I:27, "Male and female created he them", certainly does not hold true in many parts of the animal world. Indeed, the concept of gender is meaningless in many of the lower animals, and nature displays a wonderful and diverse range of strategies when it comes to sex and reproduction.

Although the following account will concentrate on animals it should also be remembered that sex is also important in plants as well, and some may display unexpected features. Anyone who has wondered why the familiar common ash tree (Fraxinus excelsior L. Oleaceae) sometimes seems erratic in its fruiting habits will be intrigued by the following account in Alan Mitchell's book on European trees: Common Ash. Flowers and Fruit: Total sexual confusion: some trees all male, some all female, some male with one or more female branches, some vice versa, some branches male one year, female the next, some with perfect flowers (i.e. with flowers containing organs of both sexes, bisexual).

SEX - GENERAL.

Adam has been described as the first intersex, but since his day, man-made laws, while not defining male and female, have only allowed for the existence of one or the other, with no legal provision for any intersexual conditions, at least in humans.

From the biological point of view, the criteria used to define sex in the higher vertebrates, including humans, are:

1. Chromosomal sex (22 + 2 sex chromosomes; 46/XX or 46/XY in humans. We share about 98% of our genes with chimpanzees, there is only about 2% difference.)
2. Gonadal sex: ovaries or testes (histological structure determines)
3. Apparent sex: external genitalia and body form.
4. Psychological sex and sexual behaviour.

Hormones are not criteria as they are only a mechanism by which sexual characteristics are developed or influenced.

When one or more of these four crit eria is of a different sex to the rest then a state of intersex can be said to exist, at least by biologists.

There is little difference, at least from the cell biology point of view, between and an egg (ovum) and a sperm (spermatozoa). Eggs have a food supply to nourish the growing embryos and sperms have motility so that they can reach the egg to effect fertilisation. Otherwise, both eggs and sperm are simply the means of packaging and passing on genetic material (DNA).

It is impossible to speak of male or female in many of the lower animals, for example amoeba, the earthworm or the snail. The two latter are true hermaphrodites, containing both ovaries and testes, in contrast to most, but not quite all, higher vertebrates. Hermaphrodites may be self fertilizing or they may have behavioural mechanisms to ensure cross fertilization. Several hundred million years ago the early true vertebrates achieved a functional separation of the sexes which has persisted with some, but remarkably few, exceptions ever since.

Cross fertilization is the fundamental basis of sex in that it brings into being new genetic combinations upon which natural selection may act. The action is mediated by two kinds of gametes (sperm and ova) and in the course of evolution two kinds of soma (body forms) have developed as accessory phenomena. Sex is inseparable from reproduction only in vertebrates. In the lower animals sex, or the exchange of genetic material, may not lead to an increase in numbers (reproduction); this may be achieved by other means, such as simple fission, leading to clones. In mammals sex is determined genetically with the female being the homogametic sex (XX) and the male heterorogametic (XY). Abnormalities in these chromosome arrangements in humans (e.g. XO, XXY, XYY and so on), giving rise to such well known syndromes as Turner's, Klinefelter's etc. In birds, by way of contrast, it is the female that is heterogametic (ZW) and the male homogametic (ZZ). However, in many other groups of animals sex may not be controlled genetically, but by one or more of a range of environmental, population, behavioural or food factors. Also sex may not be constant throughout life, but may change; from male to female (protandric) or from female to male (protogynous), or may even alternate with the season or other factors. From the operational point of view phenotypic sex (sex of adult, or reproductive phase of the animal) is an effect, and genetic and environmental factors are causes. Knowledge of abnormal sex conditions in man is the result of being able to determine the genetic sex of an individual.

It has been said that modern man "cerebral, humorous, moral, religious and guilty animal that he is" finds particularly hard to stomach the fact that his reproductive and excretory systems are anatomically and functionally so closely linked.There are good reasons for this in the evolutionary history of the vertebrates. The original problem was how to get eggs and sperm from the interior body cavity, where they were produced, to the exterior. The problem was solved 400 million years ago by utilising some of the plumbing originally developed for excreting nitrogenous waste. Hence the juxtaposition of the two systems and the scope that exists for them to go wrong.

SEX IN INVERTEBRATES: MOLLUSCS

Molluscs include whelks and winkles, mussels and oysters, slugs and snails and the octopus. Many molluscs very familiar to us are hermaphrodite, for example the common garden slug. Some interesting research reported recently, has established that, for one species of slug, cross fertilization is the norm in the south of Britain, with self fertilization becoming more common as one travels north until it predominates in Scotland. Snails are also hermaphrodite, and cross fertilize. During courtship each shoots into the other a calcareous dart (telum amoris) which acts as a releaser stimulus for courtship behaviour. In one marine species (Limapontia) sperm is transferred through a hollow spine on the penis, which ruptures the body wall of the mate in a random way. This is known as hypodermic sperm injection.

The Slipper Limpet, which has a splendidly appropriate name (Crepidula fornicata) a pest of oyster beds, forms chains of individuals, ranging from tiny males at the summit, to old females at the base. As the animals age they change from male, through an hermaphroditic phase, to female in old age. This change can be modified by temperature, food, and the influence of association. Removal of a female will increase the rate of change of males to the female phase. This change from male to female (protandry) repre sents a deep seated tendency in molluscs. Sperm are less metabolically expensive than ova so are advantageously produced in young animals.

Copulating chains of hermaphroditic individuals are to be found in some marine molluscs, for example, the Sea Hare Aplysia. Here each animal acts as a male to the one in front and as a female to the one behind. If you have read any of the Marquis de Sade, you will remember this as one of his favourite fantasies.

In some parasitic molluscs, for example, Entocolax, a parasite of sea cucumbers, the male, termed a dwarf male, is reduced to little more than a testis living parasitically within the female. True parthenogenesis (virgin birth) is rare in molluscs, but males are unknown in at least two species. Self fertilization is common. In some species of oyster, individuals start life as males, but in the following and subsequent seasons, alternate sex phases between male and female. There is never a permanent change to female, always a reversion to male after egg shed.

FISH.

Of all the vertebrates the bony fish show the most divergent expressions of reproductive strategy, ranging from oviparity with external fertilization, through the laying of internal fertilized eggs, ovoviviparity, to true viviparity (livebearers). Care of the young may be exhibited by either parent, according to species, and is a well known feature of the sea horse (Hippocampus). Something of an icon for TV groups, it always, though, seemed to me to be more like an extreme example of the New Man, as defined by the Guardian Womens' Page. Here the genital opening of the female becomes distended with an intromittent organ which discharges the eggs into the male brood pouch where they are fertilized, protected and incubated. The walls of the brood pouch, like a true uterus, become richly supplied with blood vessels which give oxygen and nourishment to the embryos. Eventually, with a series of convulsive movements the father forces open the pouch and the babies are expelled, although they may return for shelter. In the related pipefishes, the female merely glues the eggs in ropes along the underside of the male body. In the midwife toad (Alytes), the eggs are wrapped around the male's legs.

Sexual dimorphism ranges from forms where the sexes cannot be distinguished to the extreme situation found in the deep sea angler fish, whose dorsal fin is modified to form a lure, with a phosphorescent organ at the tip. While the female may be up to 40" long, the male is about 4" and has roughly a thousandth of the female's body weight. It is parasitic, sinking its jaws into the female. Gradually the skin and blood vessels merge, until they become one. The male loses virtually all of its body parts and becomes little more than a testis.

Hermaphroditism in fish has been recognised since the days of Aristotle, Ovid and Pliny, but only recently has it been realised that hermaphrodite fish may be the exceptions that prove the rules for some of our most generally accepted concepts of vertebrate reproductive physiology.

A great range of hermaphrodite and intersexual states exist in fish, in some as part of the normal reproductive strategy, in others as abnormalities. In some species eggs and sperm develop simultaneously, in others the individual may first function as a male and later as a female (protandry) or vice versa (protogyny). There are many states of intersexuality, sex reversal and sex inversion described in the literature.

But there are costs to gender switching, which may normally be regarded as a special mechanism for ensuring repro ductive success. The costs include altering gonadal cell types, new enzymes to synthesise new hormones, colour mosaic changes, changes in behaviour, changes in body size, loss of reproductive time and increased risk of mortality, through predation of more conspicuous individuals, and from disease in temporarily weakened individuals.

Examples of protogyny include the red banded parrotfish, Sparisoma auro frenatum, in which the change from female to male involves a size increase. Normally 3-5 females share a territory with one male. A female, on changing sex, wanders off and establishes a new territory. In other species, for example Anthias squamipinnis, which may form large schools, removal of a male from the group induces a female, usually the largest one, to change sex, which can also result from the addition of more females. A similar situation is found in the wrasses, which may change from female to male, though one of the British wrasses changes, in middle age, from male to female. Protandry has also been shown in Amphiprion bicinctus, where in an experiment, a large number of females were removed from a group, and an almost equal number of males changed sex, but only when joined by sub-adult males.

In the swordtail, Xyphophorus, where the female changes to male, it has been said that "the mother becomes the father of her own granddaughter". In Thalassoma duperry (from Hawaii) a large female caged alone did not change sex, but if joined by a small female it did. A large female caged with a small, initial phase male (which is the same colour as a female), also changed sex, giving two males in the tank.

One hermaphrodite fish, Rivulus marmoratus (Mexico) is capable of self fertilization. This fish lives in rivers which dry up in summer, hence it is likely to find itself alone. In some species the male is not known to exist at all. In Poecilia formosa, a mollie, mating takes place with a male of a related species (P.latipinna, P.mexicana), whose sperm triggers development of the egg nucleus but doesn't fuse with it.

AMPHIBIANS AND REPTILES.

In amphibians (frogs, toads, salamanders), sex is determined genetically, but the interest in the group lies in the effects of hormones and they have become important experimental animals in hormone research. Androgenic steroids (e.g. testosterone) can cause sex reversal in female frogs. Some, sex reversed by this means, have been mated with normal females to produce 100 per cent female offspring. Paradoxically, in, for example, some of the salamanders, these same steroids can feminise males through pathogenic effects. Post steroid treatment, ovaries may develop in genetic males which, when mated with normal males, produce 100 per cent male offspring. High concentrations of estrogen may masculinise female frogs and in other species feminise males (e.g. Xenopus). In Xenopus, ripening of the eggs is controlled by a pituitary hormone, production of which is determined by external environmental factors, ensuring breeding is confined to the spring. Factors in the urine of pregnant women have a similar effect on Xenopus ovulation which was thus used as a pregnancy test. The extreme sensitivity of this species to hormones is illustrated by one of them, a frog, Rana sylvatica, in which complete masculinisation of females occurs with 1 part of androgen (testosterone proprionate) in 500 million parts of water. Activity has been demonstrated at one part per billion, which is the equivalent of five people in the whole world population.

In the snakes and lizards each egg possesses the potential to develop an embryo of either sex, and sexual differentiation is not completed until after hatching, although there is already a tendency towards either the male or the female. Intersexes are common in turtles and lizards, but rare in snakes and crocodiles. In crocodiles sex is determined by the temperature at which the eggs are incubated.

BIRDS.

Birds tend to show extreme sexual dimorphism, expressed in the plumage where the male is usually the more brilliantly coloured, and also in the so-called head furnishings (comb, wattles), which are more developed in the male. Birds therefore provide interesting opportunities for studying intersexuality. The importance of the domestic hen as a provider of eggs has stimulated much research, especially on avian hormones, aimed at developing methods of changing sex ratios in favour of egg laying females.

Sex differences in birds may be under genetic or hormonal control. Combs and wattles are usually controlled by male hormones. There may be no difference between the sexes in their plumage, as for example in the Seabright fowl, where both sexes have "henny" feathers. However removal of the gonads of either sex produces "cocky" feathers in both, indicating that both ovaries and testes produce hormones that suppress "cocky" feathers. In the second class of birds, plumage differences may only show up in the breeding season when males acquire a showy nuptial plumage. In species with permanent sexual dimorphism, plumage differences are usually under hormone control, with female hormones in the hen suppressing the development of male plumage. In the English sparrow, however, sex differences in the plumage are entirely under genetic control.

Birds show an almost unique asymmetry, or laterality in the development of both the male and the female reproductive systems, possibly associated with the very large size of eggs that are produced. This provides conditions which may result in varying degrees of intersexuality, particularly in the female. Generally both gonads in the female and the male have the potential to form testes, while the left gonad of both male and female (and to a lesser extent the right gonad of the female) can potentially form ovaries. Even after hatching, there remains potential testes forming tissue in the female bird's rudimentary gonad, and potential male ducts. Thus numerous cases of spontaneous intersexuality are found and this condition is not difficult to induce experimentally. Sometimes individual birds have been described as lacking gonads altogether. It has been suggested that this represents an avian version of Turner's syndrome (XO in neuter female humans, possibly ZO in these male birds)

The penis is not usually present in birds, although in most of the large flightless birds (ostriches, emus) and some of the ducks and geese it is.

Aristotle appears to have been the first to record intersexuality in birds, mention ing hens that began to behave and look like cocks as well as cocks showing female behaviour. Spontaneous masculinisation of hens is correlated with atrophy of the ovary for pathological reasons, with corresponding development of testicular tissue which may lead to complete functional sex reversal, including the adoption of male copulatory behaviour, although this is rare. In bred strains of fowl and pigeon there is a high proportion of hermaphroditism, as there is among hybrids, for example, between pigeons and doves. Also of interest are gynandromorphs, or mosaics, where the first case, reported in 1890, was a chaffinch. The left side of the bird had female plumage and an ovary while the right side showed male plumage and testis. Subsequently other examples in other species have been reported. In double yolked eggs where both are fertilized, and one is male and the other female the male may be somewhat feminised, a case analogous to the mammalian freemartin.

ROLE REVERSAL.

In courtship, typically, males compete for choosey females. This is thought to result from the fact that males invest far less parentally than females. But role reversal can occur when males do invest parentally. An Australian bush cricket (Orthoptera: Tettigoniidae) has recently been reported as displaying this change in role. Normally, during mating, the males not only transfer sperm to the female, but also a nutrient package that is consumed by the female. This increases the survival prospects of the offspring and both parents, therefore, invest in the eggs by nutrient provisioning. As food in the environment decreases, there is a change in the number of males able to provide this food for the female. Concomitant with this is an increase in female mating frequency and the operational sex ratio becomes skewed towards females, who now compete for the available males.

Desmond Morris has reported pseudo-homosexual behaviour in the ten-spined stickleback (1952), pseudofemale and pseudomale behaviour in the zebra finch (Pygosteus pungitius) (1954) and in the Green Acouchi (Myoprocta pratti), a small South American rodent related to guinea pigs (1962).

In ten-spined sticklebacks, where the male builds the nest, females are encouraged to enter the nest by an elaborate courtship dance by the male. On entering the nest, the female deposits her eggs. The male then enters and fertilizes them. Females who do not respond to the male advances are chased and bitten. In experimental conditions in fish tanks, not all the males could establish territories and build nests for reasons of available space. However these nestless males were highly motivated sexually, although frustrated and unable to express themselves in the presence of the dominant males. Homo sexual behaviour was displayed in the interaction of the restless males with the nest-owning males. When females were removed from the tank, nest-owners would perform the courtship dance to other males. Under certain circumstances, nestless males were observed to mimic courted female behaviour, entering the nest as if to lay eggs, even pushing females aside to do so. Morris suggests that this behaviour pattern is an outlet which relieves sexual frustration. He also suggests that the nervous behaviour pattern for females exists in the male, but is not normally used because the hormone balance favours the male pattern. Frustrated females were subsequently observed to behave in a male pattern (pseudomale behaviour).

While the reversal of sexual role in sticklebacks occurred in homosexual situations, that in the Zebra Finch was seen in heterosexual encounters between male and female birds. It invariably occurred when male courtship display, leading to mounting of the female, met with no response from the latter, so no copulation was effected. In these circum stances, the male would then display typical female courtship behaviour (involving tail quivering). Morris was convinced that this pseudofemale display resulted from thwarted male sexual behaviour. The point again is that a nervous pattern for female behaviour exists in the male bird, although it is only expressed in abnormal circumstances.

The long legs of the Green Acouchi provide a means for a considerable variety of behaviour patterns (in contrast to the short legs of the related guinea pig). Morris had, in a cage, a female Acouchi and her mate, together with a subordinate male (the lodger!). On one occasion, the subordinate male waited until the mate was asleep and then began to court the female himself. He was about to achieve success when, with his full attention on the female, he failed to notice that the other male had woken up. The latter approached the subordinate male without him noticing. When he realised his danger, he would, in normal circumstances have fled, but it was too late for this and, in a flash, he assumed the female sex crouch posture. This was produced from a combination of sexual motivation and fear. It had the advantage of reducing the aggression of the other male, whose sexual interest was immediately aroused, allowing the subordinate male to slip away and the dominant male to turn his attention to his mate. Again a demonstration of a nervous system in the male capable of producing female behaviour patterns.

HUMAN PERCEPTIONS OF ANIMAL INTERSEXUALITY.

Mention has already been made of Aristotle and Ovid among ancient Greek writers on animal intersexuality. Others who wrote on this in antiquity include Livy, Virgil, Cicero, Pliny and Martial. Aristotle, for example, wrote "with regard to sex, some animals are divided into male and female, but others are not so divided . . . . in quadrupeds the duality is universal, . . . . but among insects and fishes some cases are found wholly devoid of this duality of sex, for instance the eel is neither male nor female and can engender nothing." Eel reproductive biology has been a mystery until recently. They return to the sea to breed and it is not until they are fully grown adults and are ready to make the journey, that they develop as one sex or the other.

Pliny recorded that the Emperor Nero had a team of hermaphrodite horses harnessed to his chariot. Also, when his wife Poppea died, he castrated a lookalike slave, Sporus, and married him. Human intersexes were often thrown into the Aegean or the Tiber at that time.

Much later, St. Augustine was neither awed nor shocked; he included sex reversal among things more surprising than harmful, such as oxen speaking, infants crying certain words in the womb, serpents flying and hens and women changing into males.

But, by the Middle Ages, Christianity was in full flood and woe betide any wrong-doing pig or fowl (or any other creature). The Church had full power to exorcise, anathematise or excommunicate all animate and inanimate things. There were two processes:

Thierstrafen: execution of pigs, fowls, horses and other domestic animals for homicidal and other offences (compare the present-day trial and execution of pit bulls and rottweilers.

Thierprocesse: encompassed proceedings of exorcism or excommunication of plagues of locusts, slugs, fleas, weevils, mice, rats. Even swallows were excommunicated by Egbert, Bishop of Trier, for disturbing the devotions of the faithful by their chattering and chirping, and fouling his vestments with their droppings.

Against this background, it is not difficult to see that intersexed animals or sex changes might cause ecclesiastical offence. This particularly applied to chickens, which, being noisy birds tended to draw attention to themselves. Cocks and hens deviating from the norm suffered, with or without trial. It was widely believed that cocks that changed sex and laid eggs were possessed by Satan. Cock's eggs, when hatched, would produce a cockatrice or basilisk; part hen and part serpent, about four inches long. The glance of a basilisk could strike dead any living thing and its fiery breath could wither vegetation. Only cocks and weasels could live near basilisks. In 1474 a cock was tried in Basle for laying such an egg, and condemned, with its egg, to be burnt at the stake.

On the island of Espiritu Santo (part of what is now Vanuatu) in the Western Pacific and other nearby islands, a rather more positive view was taken of intersexuality, notably in pigs. Intersexual pigs were prized by the Sakuas above every commodity except women. In the local pig population, as a result, some 10-20 per cent were deformed or sterile. A man's progression up the social hierarchy into chieftainship depended on the number of intersexual pigs he could accumulate.

CONCLUSIONS.

A view of sex, gender and behaviour, based on what is said to be normal in humans, does not begin to encompass the vast range shown for these factors in the wider world of animals (and plants) where more or less every conceivable variation may be found in one species or another.

Nature does not put things in water tight taxonomic boxes, this is something humans do for convenience and as a way of coping with the continuous variability shown in Nature. There is a cost in that a degree of arbitrariness is necessary in any classification system.

Nature does not make moral judgements - its judgements are concerned with biological fitness and reproductive success; anything that contributes to these is likely to flourish. There is nothing biologically unusual about homosexual behavioural patterns, including pseudocopulatory activity - many species indulge this under a variety of circumstances.

In their behavioural patterns, many animals can lay latent properties belonging to the opposite sex. In the course of evolution, these can be brought to the front line if necessary, to deflect aggression or to relieve sexual frustration for example.

In conditions of overcrowding social structures in animals break down, and are destroyed, animals develop diseases, kill their young, fight viciously, mutilate themselves. Reproduction declines until numbers are reduced and breeding can be resumed.

The human population of the world at present stands at about 5 billion. By the year 2040 (within the lifetime of many of us alive today) it is expected to double to 10 billion before stabilising. India will need to increase its food production by 2.5-3 times to meet its expected population increase over the next 30 years. It is very hard at present to see how this will be achieved. This situation removes the former biologically-based criticism of non breeding minorities in human society, be they monks or nuns, long-term bachelors or spinsters, homosexuals or transexuals. These groups may continue to face social problems arising from their minority roles. Morris (1967) suggests that "Nevertheless, provided they are well adjusted and useful members of society outside the reproductive sphere, then they must now be considered valuable non-contributors to the population explosion."

FURTHER READING AND REFERENCES.

Most of the material in this paper originates from the following publications:

1. Armstrong C.N. and Marshall A.J. (eds), Intersexuality in Vertebrates Including Man. London (1964) (especially chapters by J. W. Atz (Fish), C. L. Foote (Amphibians), E. Taber (Birds) and J. Brunner-Lorand (Mammals).
2. Beach F. A. (ed), Sex and Behaviour. London 1965.
3. Morris D., The Naked Ape. London 1967
4. Morris D., Patterns of Reproductive Behaviour. London 1970
5. Morton J. E., Molluscs. London 1958
6. Potts L. W. and Wooton R. J. (eds), Fish Reproduction: Strategies and Tactics. London 1984