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Insect Metamorphosis SMITHSONIAN MISCELLANEOUS COLLECTIONS VOLUME 122, NUMBER 9 INSECT METAMORPHOSIS BY R. E. SNODGRASS Collaborator of the Smithsonian Institution and of the U. S. Department of Agriculture (Publication 4144) CITY OF WASHINGTON PUBLISHED BY THE SMITHSONIAN INSTITUTION APRIL 1, 1954 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOLUME 122, NUMBER 9 INSECT METAMORPHOSIS BY R. E. SNODGRASS Collaborator of the Smithsonian Institution and of the U. S. Department of Agriculture ^<5« *z£>^ (Publication 4144) CITY OF WASHINGTON PUBLISHED BY THE SMITHSONIAN INSTITUTION APRIL 1, 1954 £#e Boti (§<xftimovt (pvtee BALTIMORE, MS., U. S. A. CONTENTS Page Introduction i I. Metamorphosis and classification : . 10 II. Hormones and metamorphosis 13 Secretory cells of the brain 14 The corpora cardiaca, or paracardiaca 14 The corpora allata 16 Pericardial glands 19 Ventral glands of the head 19 The prothoracic glands 20 The ring gland of cyclorrhaphous Diptera 21 The nature of hormonal action 23 III. Apterygota 24 IV. Plecoptera 26 V. Ephemeroptera 28 VI. Odonata 32 VII. Hemiptera 38 VIII. Thysanoptera 44 IX. Oligoneoptera, or typical Endopterygota : Neuroptera to Hymenop- tera 48 X. Larval heteromorphosis 61 Parasites with a planidial stage 62 Coleoptera 62 Neuroptera 66 Strepsiptera 66 Lepidoptera 70 Diptera 70 Hymenoptera 72 Parasites without a planidial stage 75 Diptera 75 Hymenoptera 77 XI. The pupal transformation 82 The epidermis 83 The appendages 86 The alimentary canal 87 The Malpighian tubules 93 The fat body 95 The oenocytes 96 The tracheal system 97 The dorsal blood vessel 98 The nervous system 99 The muscular system 101 XII. Muscle attachments and the nature of the pupa 107 References in INSECT METAMORPHOSIS By R. E. SNODGRASS Collaborator of the Smithsonian Institution and of the U. S. Department of Agriculture INTRODUCTION Ancient mythologies are replete with stories of the transformation of one creature into another, called metamorphosis. So the early stu- dents of natural history who first observed a caterpillar turn into a butterfly had a term ready made for the phenomenon they witnessed, and today in entomology we commonly think of metamorphosis as the transformation of a larval insect into the imago. In so doing, however, we overlook the fact, quite as extraordinary, that a caterpillar hatches from the egg of a butterfly. We might truly say, then, that the real metamorphosis in the life history of the species is that which has changed a young butterfly into a caterpillar, the subsequent change of the caterpillar into the butterfly being merely the return of the metamorphosed young to the form of its parents. The transforma- tion of the caterpillar into the butterfly is a visible event re-enacted with each generation ; the change of the young butterfly into a cater- pillar has been accomplished gradually through the past evolutionary history of the Lepidoptera. Today, there is not even any recapitula- tion of the butterfly stage in the ontogeny of the caterpillar ; the but- terfly's egg develops directly into the caterpillar form of its species. The idea that the caterpillar, because of its abdominal "legs," repre- sents a primitive stage in the ancestry of insects is quite out of har- mony with the modern structure of the caterpillar's head and with the fact that the caterpillar has wings developing beneath its cuticle. Both the caterpillar and the butterfly are modern end results of evolu- tion, but along different lines of development. In attaining their present distinctive forms, the butterfly has fol- lowed out the evolutionary path adopted by its adult ancestors, and therefore represents the adult line of descent ; the caterpillar, on the other hand, in its evolution has departed from the ancestral path and has become a new and distinct juvenile form of its species. Since the caterpillar leads an independent life in a very efficient manner as an SMITHSONIAN MISCELLANEOUS COLLECTIONS, VOL. 122, NO. 9 2 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 122 individual, it would seem that it might be capable of developing its reproductive organs to maturity and thus dispensing with the butter- fly stage entirely. The caterpillar, however, has limited powers of locomotion; the winged butterfly, therefore, retains the reproductive function because it can widely distribute the eggs for the next genera- tion of caterpillars and thus prevent overpopulation in any one place. The same principle applies to all winged insects, and it is easy to see the advantages insects have attained in acquiring wings, together with specialized types of feeding organs and organs for mating and egg laying. It is to be presumed then that the specialized forms and habits of many young insects also are of some advantage to the species as a whole. In short, we can readily perceive a reason for metamorphosis, but how the differences between young and adult have come about, and how two distinct creatures can develop from one egg are questions difficult to answer. Since there can be no doubt that the early insects lived on land and developed without metamorphic changes, the metamorphoses that we know among modern insects are of relatively late origin, and have no relation to the more primitive metamorphoses of the annelids and crustaceans. Even among the insects themselves metamorphosis has been independently developed in several groups, though the reason for it may be deduced from pretty much the same premises in all cases. Wherever a pronounced metamorphosis occurs in the life of an insect it is generally, but not always, true that the young and the adult lead different lives or inhabit different media, and are structurally modified in adaptation to their individual habitats or ways of feeding. Very probably the presence of functional wings only in the adult stage, or conversely, the flightless state of the young, was an impor- tant condition that led to structural differentiation between the juve- nile and imaginal stages. The winged adult insect has opportunities of extending its activities far beyond the range of the wingless young insect, and, as is amply shown in modern insects, various new ways of life are open to the winged insect if it is free to develop special structures, particularly feeding organs, that enable it to take advan- tage of them. Likewise, to the wingless young insect there are pre- sented in nature various possible habitats and sources of food, some of which might better its condition if it were free to make the ana- tomical adjustments that would accommodate it to a new way of liv- ing in some special environment. However, as long as the usual mechanism of inheritance makes it necessary that newly acquired adult characters be transmitted through the young, and that charac- NO. 9 INSECT METAMORPHOSIS—SNODGRASS 3 ters acquired in the juvenile stage must be passed on to the adult, neither the adult nor the young could be free to develop structures that would be detrimental to the other. Consider, for example, the plight of the caterpillar if it had to inherit the mouth parts of the butterfly, or that of a young mosquito equipped with blood-feeding organs but lacking wings. The adult flea, it is true, has mouth parts highly specialized for a blood diet, and still is wingless, but it has sub- stituted the power of jumping for that of flight. The Hemiptera are another exception to the rule that specialized adult mouth parts de- pend on wings, but here the mouth parts are just as practicable to the flightless young as to the adults. A prerequisite of metamorphic differentiation between the young and the adult, therefore, is the inhibition of some of the ordinary processes of heredity. The young insect can then vary to any extent by the development of adaptive structures for its own use so long as its new characters are suppressed at the change to the adult ; and the adult, on its part, can acquire special feeding organs that would be entirely impracticable to the wingless young. The individual, further- more, thus derives whatever advantages there may be in living a double life, or that may accrue from inhabiting successively two dif- ferent media. Moreover, the different specializations of the young and the adult may be mutually advantageous and therefore beneficial to the individual as a whole. The larva, for example, usually becomes the chief, and sometimes the only, feeding stage, thus giving the adult a large measure of freedom for the functions of mating and procreation. When the divergence becomes too great between the young insect and the adult, especially with regard to habitat, a liaison between the two must be established by compensating instincts in order to main- tain continuity of the individual life history. The adult female, for example, must know where to lay her eggs so that the emerging larva shall find its proper food, or be in its appropriate environment. The egg-laying instinct must be more and more precise as the habits of the larva become more restricted. The parent of an aquatic larva has only to deposit her eggs in some suitable place in the water, but the parent of a parasitic larva specific to some particular host must be able to insert her eggs into a member of this same host species. It has been shown by Thorpe (1938, 1939) that the egg-laying response of the adult may be a result of conditioning during the feeding of the larva. Likewise the larva, on its part, must be endowed with an instinct that brings it to undergo its transformation at some place ; 4 SMITHSONIAN MISCELLANEOUS COLLECTIONS VOL. 122 appropriate for the ecdysis of the winged adult. Most aquatic larvae come out of the water to pupate, some crawl up on rocks or plant stems, others travel inland ; the parasitic larva emerges from its host overwintering species find protection from the cold in concealed places or within the ground, and do not transform until the return of warm weather.
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