CHAPTER VII
THE CASE OF PAPILIO POLYTES
Many instances of mimicry are known to-day, but comparatively few of them have been studied in any detail. Yet a single carefully analysed case is worth dozens which are merely superficially recorded. In trying to arrive at some conception of the way in which the resemblance has come about we want to know the nature and extent of the likeness in the living as well as in the dead; the relative abundance of model and mimic; what are likely enemies and whether they could be supposed to select in the way required, whether the model is distasteful to them; whether intermediate forms occur among the mimics; how the various forms behave when bred together, etc., etc. Probably the form that from these many points of view has, up to the present, been studied with most care is that of the Swallow-tail, Papilio polytes. It is a common butterfly throughout the greater part of India and Ceylon, and closely allied forms, probably to be reckoned in the same species, reach eastwards through China as far as Hongkong. P. polytes is one of those species which exhibit polymorphism in the female sex. Three distinct forms of female are known, of which one is like the male, while the other two are very different. Indeed for many years they were regarded as distinct species, and given definite specific names. To Wallace belongs the credit of shewing that these three forms of female are all to be regarded as wives of the same type of male[1]. He shewed that there were no males corresponding to two of the females; also that the same one male form was always to be found wherever any of the females occurred. As the result of breeding experiments in more recent years Wallace's conclusions have been shewn to be perfectly sound.
The male of polytes (Pl. V, fig. 1) is a handsome blackish insect with a wing expanse of about four inches. With the exception of some yellowish-white spots along their outer margin the fore wings are entirely dark. Similar spots occur along the margin of the hind wing also, while across the middle runs a series of six yellowish-white patches producing the appearance of a broad light band. The thorax and abdomen are full black, though the black of the head is relieved by a few lighter yellowish scales. The under surface is much like the upper, the chief difference being a series of small and slightly reddish lunules running outside the light band near the margin of the hind wing (Pl. V, fig. 1 a). In some specimens these markings are almost absent. One form of female is almost exactly like the male (Pl. V, fig. 2), the one slight difference being that the lunules on the under surface of the hind wing are generally a trifle larger. For brevity she may be called the M form. The second form of female differs in many respects from the male and the M female. Instead of being quite dark, the fore wings are marked by darker ribbed lines on a lighter ground[2] (Pl. V, fig. 3). The hind wings shew several marked differences from those of the male. Of the series of six patches forming the cross band the outermost has nearly disappeared, and the innermost has become smaller and reddish. The middle four, on the other hand, have become deeper, reaching up towards the insertion of the wing, and are pure white. A series of red lunules occurs on the upper surface outside the white band, and the yellowish-white marginal markings tend to become red. These differences are equally well marked on the under surface (Pl. V, fig. 3 a). The colour of the body, however, remains as in the male. From the resemblance shewn by this form to another species of Swallow-tail, Papilio aristolochiae (Pl. V, fig. 5), we shall speak of it as the A form.
The third form of female is again very distinct from the other two. The fore wings are dark but are broken by an irregular white band running across the middle (Pl. V, fig. 4), and there is also an irregular white patch nearer the tips of the wing. The hind wings, on the other hand, are characterised by having only red markings. The yellowish-white band of the male is much reduced and is entirely red, while the red lunules are much larger than in the A form. The under surface (Pl. V, fig. 4 a) corresponds closely with the upper. The body remains black as in all the other forms. This type of female bears a resemblance to Papilio hector (Pl. V, fig. 6), and for that reason we shall speak of it as the H form. It should be added that these three forms of female are quite indistinguishable in the larval and chrysalis stages.
It was Wallace who first offered an explanation of this interesting case in terms of mimicry. According to this interpretation P. polytes is a palatable form. The larva, which feeds on citronaceous plants, and the chrysalis are both inconspicuous in their natural surroundings. They may be regarded as protectively coloured, and consequently edible and liable to persecution. The original coloration is that of the male and the M female. From this the other two forms of female have diverged in the direction of greater instead of less conspicuousness, although the presumed edibility of the insect might have led us to think that a less conspicuous coloration would have been more to its advantage. But these two females resemble the two species Papilio aristolochiae and Papilio hector, which, though placed in the same genus as P. polytes, belong to a very different section of it[3]. The larvae of these two species are conspicuously coloured black and red with spiny tubercles. They feed upon the poisonous Aristolochia plants. For these reasons and also from the fact that the butterflies themselves are both conspicuous and plentiful it is inferred that they are unpalatable. In short, they are the models upon which the two polytes females that are unlike the male have been built up by natural selection.
The suggestion of mimicry in this case is supported by the fact that there is a general correspondence between the areas of distribution of model and mimic. P. hector is not found outside India and Ceylon, and the H female of P. polytes is also confined to this area. P. aristolochiae, on the other hand, has a much wider range, almost as wide indeed as that of P. polytes itself. Generally speaking the A female accompanies P. aristolochiae wherever the latter species is found. Beyond the range of P. aristolochiae, in northern China, the M female alone is said to occur. On the other hand, as the matter comes to be more closely studied exceptions are beginning to turn up. The H female, for instance, is found on the lower slopes of the Himalayas, far north of the range of P. hector, and there are indications that a careful study of the distribution in China and Japan may prove of importance.
Moreover, the investigation of a smaller area may also bring to light points of difficulty. In Ceylon, for example, P. polytes is common up to several thousand feet, while P. hector is rare at half the height to which polytes ascends. Nevertheless the H form of female is relatively just as abundant up-country where hector is rarely found as it is low down where hector is plentiful[4]. On the other hand, P. aristolochiae may be exceedingly abundant at altitudes where hector is scarce. Yet the A form of polytes is no more relatively abundant here than elsewhere on the island. All over Ceylon, in fact, the relative proportions of the three forms of female appear to be the same, quite irrespective of the abundance or scarcity of either of the models. As, however, we shall have to return to this point later, we may leave it for the moment to consider other features of this case of P. polytes.
In collections of insects from India or Ceylon it is not unusual to find specimens of the A form of female of polytes placed with P. aristolochiae, and the H form with P. hector. When the insects are old and faded and pinned out on cork the mistake is a very natural one. But after all the enemies of polytes do not hunt it in corked cabinets, and any estimation of resemblance to be of use to us must be based upon the living insects. Are the resemblances of the mimics to the models when alive so close that they might be expected to deceive such enemies[5] as prey upon them and have no difficulty in distinguishing the male form of polytes from P. aristolochiae or P. hector?
To answer for a bird is a hazardous undertaking. We know so little of the bird's perceptive faculties whether of taste or sight. But on general grounds, from the specialization of their visual apparatus, it is probable that the sense of sight is keen, though whether the colour sense is the same as our own is doubtful[6]. On the other hand, the olfactory apparatus is relatively poorly developed in birds, and from this we can only argue that the senses of smell and taste are not especially acute. Really we can do little more than to describe how these mimetic resemblances appear to our own senses, and to infer that they do not appear very different to the bird. If there is any difference in keenness of perception we shall probably not be far wrong in presuming that the advantage rests with the bird. After all if there is any truth in the theory of mimicry the bird has to depend largely upon its keenness of sight in making its living, at any rate if that living is to be a palatable one. If natural selection can bring about these close resemblances among butterflies it must certainly be supposed to be capable of bringing the bird's powers of vision to a high pitch of excellence.
Returning now to the case of P. polytes, there is not the least doubt that to the ordinary man accustomed to use his eyes the A form of female is easily distinguishable from P. aristolochiae, as also is the H form from P. hector. The two models have a feature in common in which they both differ from their respective mimics. In both of them the body and head are largely of a brilliant scarlet, whereas neither of the mimics has a touch of red on the body. In the living insect when the body is swelled by its natural juices the effect is very striking[7]. It gives at once a "dangerous" look to the insect when settled, even at a distance of several yards, and this although one may be perfectly familiar with its harmless nature. The mimics on the other hand with their sombre-coloured bodies never look otherwise than the inoffensive creatures that they are. The "dangerous" look due to the brilliant scarlet of the body and head of hector and aristolochiae is reinforced by the quality of the red on the markings of the wings. In both models it is a strong clamorous red suggestive of a powerful aniline dye, whereas such red as occurs in the mimics is a softer and totally distinct colour. The difference in quality is even more marked on the under than on the upper surface (Pl. V, figs. 3 a—6 a), and the net result is that when settled, with wings either expanded or closed, there is no possibility of an ordinarily observant man mistaking mimic for model in either case, even at a distance of several yards.
It may, however, be argued that it is not when at rest but during flight that the mimetic resemblance protects the mimic from attack. Actually this can hardly be true, for the mode of flight constitutes one of the most striking differences between model and mimic. P. hector and P. aristolochiae fly much in the same way. They give one the impression of flying mainly with their fore wings, which vibrate rapidly, so that the course of the insect, though not swift, is on the whole sustained and even. The flight of all the different forms of polytes is similar and quite distinct from that of the models. It is a strong but rather heavy and lumbering up-and-down flight. One gets the impression that all the wing surface is being used instead of principally the fore wings as appears in P. hector and P. aristolochiae. The difference is difficult to put into words, but owing to these peculiarities of flight the eye has no difficulty in distinguishing between model and mimic even at a distance of 40 to 50 yards. Moreover, colour need not enter into the matter at all. It is even easier to distinguish model from mimic when flying against a bright background, as for instance when the insect is between the observer and a sunlit sky, than it is to do so by reflected light. I have myself spent many days in doing little else but chasing polytes at Trincomalee where it was flying in company with P. hector, but I was never once lured into chasing the model in mistake for the mimic. My experience was that whether at rest or flying the species are perfectly distinct, and I find it difficult to imagine that a bird whose living depended in part upon its ability to discriminate between the different forms would be likely to be misled. Certainly it would not be if its powers of discrimination were equal to those of an ordinary civilised man. If the bird were unable to distinguish between say the A form of female and P. aristolochiae I think that it would be still less likely to distinguish between the same A form and the male or the M form of female. For my experience was that at a little distance one could easily confuse the A form of polytes with the male. Except when one was quite close the red on the A form was apt to be lost, the white markings on the hind wing were readily confused with those of the male, and one had to depend entirely on the lighter fore wing. Unless the bird were keener sighted than the man the A form would be more likely to be taken in mistake for its unprotected relative than avoided for its resemblance to the presumably unpalatable model. On the other hand, if the bird were sufficiently keen sighted never to confuse the A female with the male form its sight would be too keen to be imposed upon by such resemblance as exists between the A female and P. aristolochiae.
These, however, are not the only criticisms of the theory of mimicry which the study of this species forces upon us. Papilio polytes is one of the few mimetic species that has been bred, and in no other case of polymorphism is the relation between the different forms so clearly understood. For this result we are indebted mainly to the careful experiments of Mr J. C. F. Fryer, who recently devoted the best part of two years to breeding the different forms of this butterfly in Ceylon[8]. Fryer came to the conclusion that an explanation of this curious case is possible on ordinary Mendelian lines. At first sight the breeding results appear complicated, for any one of the three forms of female can behave in several different ways. For the sake of simplicity we may for the moment class together the A and H females as the mimetic females, the non-mimetic being represented by the M or male-like females. The different kinds of families which each of the three females can produce may be tabulated as follows:—
- (α) The M form may give either:—
- (1) M only.
- (2) M and mimetics in about equal numbers.
- (3) Mimetics only.
- (β) The A form may give either:—
- (1) M and mimetics in about equal numbers.
- (2) M and mimetics in the ratio of about 1:3.
- (3) Mimetics only.
- (γ) The H form may give either:—
- (1) M and mimetics in about equal numbers.
- (2) M and mimetics in the ratio of about 1:3.
- (3) Mimetics only.
The males are in all cases alike to look at but it must nevertheless be supposed that they differ in their transmitting powers. In fact the evidence all points to there being three different kinds of male corresponding to the three different kinds of female. But they cannot shew any difference outwardly because there is always present in the male a factor which inhibits the production of the mimetic pattern even though the factor for that pattern be present.
Returning now to the records of the females it will be noticed that although the M form may breed true the mimetics never give the M form alone. Where they give the M form among their progeny they produce mimetics and non-mimetics either in the ratio 1:1 or of 3:1. This at once suggests that the non-mimetic is recessive to the mimetic forms—that the mimetics contain a factor which does not occur in the non-mimetics. If this factor, which may be called X, be added to the constitution of a non-mimetic female it turns it into a mimetic. If X be added to a male such an individual, though incapable of itself exhibiting the mimetic pattern owing to the inhibitory factor always present in that sex, becomes capable of transmitting the mimetic factor to its offspring. Expressed in the usual Mendelian way the formulae for these different butterflies are as follows:—
| M♀ | = | iixx | Iixx | = ♂ (1) |
| Mimetic | = | iiXX | IiXX | = ♂ (2) |
| ♀♀ | or iiXx | IiXx | = ♂ (3) |
where X stands for the mimetic factor and I for the factor which inhibits the action of X. All males are heterozygous for I, but during the segregation of characters at some stage in the formation of the families only the male-producing sperms come to contain the factor I. It is lacking in all the female-producing sperms formed by the male.
♂ (1) does not contain the factor for the mimetic condition and gives only daughters of the M form when mated with an M♀. ♂ (2) on the other hand is homozygous for the factor X, and consequently all of his germ cells contain it. This is the male that gives nothing but mimetic daughters with whatever form of female he is bred. ♂ (3) is heterozygous for X; that is to say, one half of his germ cells contain it, the other half not. With the M♀ he must give equal numbers of offspring with and without X, i.e. half of his daughters will be mimetic and the other half non-mimetic. With a heterozygous mimetic female (iiXx), which is also producing germ cells with and without X in equal numbers, he may be expected to give the usual result, viz. dominants and recessives in the ratio 3:1; or in other words mimetic and non-mimetic females in the ratio 3:1.
One of Fryer's experiments may be given here in illustration of the nature of the evidence upon which the above hypothesis depends.
Families were reared from the two wild H females of whom nothing was known either as to ancestry or husband. The first family contained 10 M and 7 H females. Hence the original wild mother was probably iiXx and had mated with a male of the constitution Iixx. The family from the second wild H female contained 26 H and 7 M females; i.e. the ratio in which these two forms appeared was not far from 3:1. Hence the wild female was probably iiXx and her husband IiXx. If this were so some of the 26 ♂♂ should receive the X factor from both parents and consequently be IiXX in constitution. This was almost certainly so in the case of the single male in this brood tested by mating with an M female from the other brood. All of his 12 daughters were of the H form, as should have been the case had his constitution been IiXX. Supposing this to be so, all his offspring, of both sexes, must be heterozygous for X. Consequently any pair mated together should give both H and M females in the ratio of three of the former to one of the latter. In Mr Fryer's experiment two males and two females chosen at random were mated together. In the one case six H and one M female were produced, in the other ten H and two M females. As was expected both classes of female appeared, and the looked-for ratio of three H to one M was, in view of the smallness of the numbers, not departed from widely in either instance.
In the experiments selected as an illustration, the mimetic females happen to be all of the H form. In other experiments, however, both the H form and the A form occurred. As the result of his experiments Mr Fryer came to the conclusion that here again the difference is one of a single hereditary factor. All mimetic females contain the X factor, but the H females contain in addition a factor which we may call Y. The function of the Y factor is to carry the change made by the X factor a step further, and to turn the A form of female into the H form. Y is a modifier of X, but unless X is present Y can produce no effect. All the different individuals which are to be found among P. polytes in Ceylon may be represented as follows:—
| ♂♂ | M♀♀ | A♀♀ | H♀♀ |
| IixxYY | iixxYY | — | — |
| IixxYy | iixxYy | — | — |
| Iixxyy | iixxyy | — | — |
| IiXxYY | — | — | iiXxYY |
| IiXxYy | — | — | iiXxYy |
| IiXxyy | — | iiXxyy | — |
| IiXXYY | — | — | iiXXYY |
| IiXXYy | — | — | iiXXYy |
| IiXXyy | — | iiXXyy | — |
In this way is offered a simple explanation in terms of three Mendelian factors which serves at once to explain the various results of the breeding experiments, and the fact that intermediates between the different forms of female are not found.
The only other experiments comparable with these on P. polytes are some made by Jacobsen on Papilio memnon in Java[9]. Here again there are three forms of female, one of which, laomedon, is something like the male, while the other two, agenor and achates, are quite distinct. Of these three achates, unlike the male and the other two females, is tailed, and resembles the species Papilio coon which belongs to the same presumably distasteful group as P. aristolochiae. These experiments of Jacobsen's are not so complete as the series on P. polytes, but Professor de Meijere and Mr Fryer have both pointed out that they are capable of being interpreted on the same simple lines.
Another instance of experimental breeding involving polymorphism and mimicry in the female sex is that of the African Papilio dardanus, but the case is here complicated by the greater number of female forms (cf. pp. 30-33). The data, too, are far more scanty than in the other two cases, but so far as they go there is nothing to preclude an explanation being eventually arrived at on similar lines[10].
And now we may consider briefly the bearing of these experiments on the theory of mimicry. Throughout the work no individuals intermediate between the three well-marked forms of polytes were met with. There is no difference in appearance between the heterozygous and the homozygous mimetic insects, whether they belong to the A or to the H form. The factor X, whether inherited from both parents, or from one only, produces its full effect, and the same is also true of the action of the factor Y. Now the most generally accepted hypothesis as to the formation of these mimetic resemblances supposes that they have been brought about through the gradual operation of natural selection accumulating slight variations. Professor Poulton, for example, a prominent exponent of this school, considers that the A form of female was first evolved gradually from the M form, and later on the H form came by degrees from the A form. If this be true we ought, by mingling the M germ plasm with the H germ plasm and by subsequently breeding from the insects produced, to get back our series of hypothetical intermediates, or at any rate some of them. We ought as it were to reverse the process by which the evolution of the different forms has taken place. But as is shewn by the experiment of Mr Fryer, which was quoted above, nothing of the sort happens.
From experiments with cultivated plants such as primulas and sweet peas, we have learnt that this discontinuous form of inheritance which occurs in P. polytes is the regular thing. Moreover, we have plenty of historical evidence that the new character which behaves in this way is one that has arisen suddenly without the formation of intermediate steps. The dwarf "Cupid" form of sweet pea, for instance, behaves in heredity towards the normal form as though the difference between them were a difference of a single factor. It is quite certain that the "Cupid" arose as a sudden sport from the normal without the intervention of anything in the way of intermediates. And there is every reason to suppose that the same is true for plenty of other characters involving colour and pattern as well as structure, both in the sweet pea, the primula, and other species. Since the forms of polytes female behave in breeding like the various forms of sweet pea and primula there is every reason to suppose that they arose in the same way, that is to say, as sudden sports or mutations and not by the gradual accumulation of slight differences.
But if we take this view, which is certainly most consonant with the evidence before us, we must assign to natural selection a different rôle from that which is generally ascribed to it. We cannot suppose that natural selection has played any part in the formation of a mimetic likeness. The likeness turned up suddenly as a sport quite independently of natural selection. But although natural selection may have had nothing to do with its production, it may nevertheless have come into play in connection with the conservation of the new form. If the new form possesses some advantage over the pre-existing one from which it sprang, is it not conceivable that natural selection will come into operation to render it the predominant form? To this question we shall try to find an answer in the next chapter.
- ↑ Trans. Linn. Soc. vol. 24, 1866.
- ↑ These darker ribs are also present in the male and M female but are obscured owing to the generally deeper colour.
- ↑ See Appendix II, p. 158.
- ↑ Spolia Zeylanica, 1910.
- ↑ We shall take it for the present that, from the point of view of mimicry, birds are the main enemies of butterflies (cf. Chap. IX).
- ↑ See later, p. 119.
- ↑ The specimens figured on Pl. V were dried in papers when taken. The body is consequently much compressed and the characteristic scarlet of P. hector and P. aristolochiae is largely hidden.
- ↑ Philosophical Transactions of the Royal Society, vol. 204, 1913.
- ↑ Tijdschr. voor Entomologie, vol. 53, 1909. A more accessible account is given by de Meijere, Zeit. f. indukt. Abstamm. u. Vererbungslehre, vol. 3, 1910.
- ↑ For further information see Poulton, Trans. Ent. Soc. Lond. 1909, and various notes in Proc. Ent. Soc. Lond. subsequent to this date.