Proc. Wash. Acad. Sci., 9: 159-178 (July, 1907)

ORIGIN AND EVOLUTION OF ANGIOSPERMS THROUGH APOSPORY
O. F. COOK

THE phylogeny of the coniferous plants or gymnosperms has been traced through the ferns and the Cycadofilices, an extinct intermediate group. Evidence of this alliance of the gymnosperms has increased rapidly in recent years, but has not been accompanied by any equally convincing indications that the angiosperms or true seed-bearing plants shared the same pteridophytic ancestry. Morphologists may be willing, therefore, to consider an alternative possibility, that the origin of the angiosperms should be sought more directly in some such primitive condition as the thallose liverworts, without the need of following back through the stages of development represented by the ferns and other "vascular cryptogams."

This briefer course of evolution would be opened if we were to consider the female reproductive apparatus of the angiosperms as analogous to the fern-prothallia which are sometimes produced directly from the parent plant, without the intervention of spores, that is, by aposporous growth from cells of the parent fronds. In this method of development the aposporous prothallus serves as means of attachment for the young plant during its embryonic stages, and can supply it with food-materials drawn from the parent.

A reason why this rather obvious analogy has failed to receive adequate consideration in the past may be found in the fact that apospory is usually associated with apogamy or other absence of normal fertilization, and is commonly thought of as a method of asexual propagation. It can be shown, however, that this implication is not necessary, and that apospory need not interfere with the formation of sex-cells, nor with the continuation of truly sexual methods of reproduction. The elimination of the spores does not require that the fusion of chromatin (mitapsis) which must precede the formation of new sex-cells, shall also be omitted; it may be merely deferred and passed along to later generations of cells. If instead of occurring in the body of the parent plant, mitapsis were carried over into an aposporous female prothallus and thus approximated in time to the formation of the sex-cells we would have a condition similar in all important respects to the reproductive system of the angiosperms.

The whole group of the archegoniate plants affords a conspicuous instance of such deferment of mitapsis into later and later cell-generations, instead of taking place in the fertilized egg-cell as in the lower algae. Unless mitapsis had been deferred the larger "sporophytes" and increasingly abundant sporogenous tissues which characterize the various families of archegoniates could not have developed. A still further postponement of mitapsis, combined with apospory, is therefore entirely in accord with the general course of evolution already followed by the group from which the primitive angiosperms are now commonly believed to have arisen.

THE VEGETATIVE CAPSULE OF ANTHOCEROS.

Anthoceros is a thallose liverwort which has been accepted by some as representing a primitive ancestor of the ferns, but which may be used with greater propriety to illustrate a stage in the development of the angiosperms.

Until fruiting begins, a plant of Anthoceros consists merely of a thallus, or plate of slightly differentiated cells, lying flat on the surface of moist soil. The fruiting part of the plant is an upright, cylindrical, two-valved capsule. The outer walls of the capsule consist of fleshy, green tissues, like those of the thallus, and similarly endowed with the power of vegetative growth. This vegetative capsule is even provided with specialized breathing-pores, though the thallus is without stomata. Finally, the growth of the capsule is persistent and indeterminate. New tissue continues to form at the base and to push up from below long after the terminal portion has ripened its spores and shriveled away.

A first step toward the derivation of angiosperms from Anthoceros would be taken if the two-valved vegetative capsule should acquire the power to pass through a resting stage and renew its growth, after the death of the parent thallus. Some of the species of Anthoceros are perennial, even in very dry regions, either by the survival of the tip of the thallus, or by specialized tubers. The capsule continues to grow as long as the thallus lives, and, as Campbell well says: "All that is needed to make the sporophyte entirely independent is a root connecting it with the earth." Most of the liverworts, both thallose and foliose, are able to survive long periods of drought, as are also the moss "fruits" and the fern-fronds which correspond to the capsule of Anthoceros.

ANTHOCEROS NOT REPRESENTATIVE OF ANCESTRAL PTERIDOPHYTE.

1The diversity of liverwort capsules in these respects is shown by a recent paper by Lang.
"When we look for sporogonia resembling that of Cyathodium probably the closest comparison as regards the relation between capsule and foot is presented by Sphaerocarpus and Riella. The mode of segmentation of the embryo in these genera has much in common with the Marchantiaceae, the comparison between Sphaerocarpus and C. cavernarum being particularly close. In both Riella and Sphaerocarpus the mature sporogonium consists of a small capsule connected by a narrow stalk with a small bulbous foot. In some species of Riella the stalk consists of a single row of cells, as in C. cavernarum, and the bulbous foot, which in Riella is composed of more numerous cells, shows a tendency to form absorbent processes. In all the Merchantiaceae and the Jungermanniaceae, with these exceptions, the foot and seta of the mature capsule appear to be relatively bulky. On the other hand, in the Ricciaceae the sporogonium shows no trace of a foot." See Lang, William H., 1905. On the Morphology of Cyathodium, Annals of Botany, Vol. 19, p. 424.

It has been customary to utilize Anthoceros as the best living analogy for an archetypal pteridophyte, but the sporangia or capsules of ferns are much more similar to those of some of the more primitive members of other orders of liverworts, such as the Marchantiaceae and Ricciaceae. It is only in the mosses and in the Anthocerotaceae that the walls of the sporogonia or capsules have become thickened and adapted to vegetative functions. The fronds of ferns may be said to correspond to the thickened capsule-bases of the Marchantiaceae and Jungermanniaceae. The delicate stalked capsules themselves are still very much in evidence in the ferns and have not assumed any vegetative functions.1

Likewise, it is only in the capsules of mosses and of Anthoceros that we find a columnella or central pith of sterile cells serving as a supporting axis. An internal framework is quite as important as chlorophyllose external walls, if a capsule is to be transformed into a vegetative structure. Ferns of the family Hymenophyllaceae have their capsules clustered on the ends of percurrent veins and surrounded by cup-like expansions of the margins of the fronds, thus giving a striking superficial resemblance to the columellate capsules of mosses. But this apparent columella of the Hymenophyllaceae bears many capsules, instead of being enclosed in a capsule, as in the mosses and in Anthoceros. Instead, therefore, of representing an ancestral condition from which the fern phylum might have developed, Anthoceros appears to be farther advanced than the ferns in the direction of the angiosperms.

The prothalli of ferns may be taken as the best indication of the nature of their bryophyte ancestors. Fern prothalli viewed as liverworts represent very primitive types. Their habit of bearing archegonia on the under side may explain why a fern sporangium, instead of developing merely a nursing-foot for more efficient connection with its parent prothallus, found means to get into communication with the ground. The development of the capsule base of vegetative cells was then no longer limited by the supplies of water and nutrient substances which the prothallus could provide, and the way was open for the evolution of a new plant structure.

It is often assumed that the fern prothallus has degenerated, since the sporophyte has so greatly surpassed it in size and vegetative activity, but there is no very good reason for supposing that the prothallus is any smaller or less important now than before. The theory of the reduced prothallus has been applied to the ferns in order to reconcile us in advance to the assumption that a much more extensive reduction has taken place in the angiosperms. Apospory affords a suggestion of a method by which the independent vegetative prothallus of the ancestors of the angiosperms may have been directly eliminated instead of being gradually reduced to a non-functional status.

VEGETATIVE CAPSULES OF MOSSES AND FERNS.

When once a capsule like that of Anthoceros had taken on the vegetative functions of the thallus there would be nothing unreasonable in expecting that it might also be able to pass a resting stage in the dried condition, revive again on the recurrence of favorable weather, and send out fresh root-hairs to draw moisture from the soil, just as the young fern-plant does. The capsules of mosses sometimes give rise to delicate protonema-like filaments, as though attempting to produce roots and thus to maintain an existence independent of the parent leafy axis. This possibility is quite within their reach, as far as powers of assimilation are concerned, for the vegetative tissues of moss-capsules are highly differentiated and even provided with breathing-pores, which the leafy part of the plant does not have. In the moss genus Buxbaumia the leaves are reduced to mere rudiments deficient in chlorophyll, showing that the assimilatory and vegetative functions have been definitely transferred to the large, hollow-walled capsule.

The independent existence of the vegetative Anthoceros capsule would afford a plant like a seedling angiosperm with its two cotyledons, but bearing spores on the inner faces of the cotyledons. No steps are required which have not been closely paralleled in the evolution of one or another of the archegoniate plants.

ACROGENOUS VEGETATIVE PROPAGATION.

1Mr. A. J. Pieters informs me that in several species of Plantago pieces of the cotyledons have the power of producing new plumules and root-hairs from the cut surface, and that perfectly normal plants have grown to maturity from such new-formed plumules.

The further stages of progress toward angiospermy are equally supported by precedents in the vegetable world. An intercalary lengthening of the periods of vegetative growth and propagation marks the histories of many groups of higher plants. The simplest thallose liverworts, the Ricciaceae, are annuals, but the Marchantiaceae are perennial, one thallus growing out of the tip of another in indefinite succession. The primitive mosses like Archidium are also annual and each plant is normally fertile, but among the higher mosses fruiting is often deferred till a considerable number of plants, often a whole tuft, has been formed by vegetative propagation. The same is true among the ferns, and in many different families of the flowering plants. It is accordingly not unreasonable to think of the cotyledons as multiplying, after vegetative growth has commenced, to form a poly-cotyledonary, leafy axis, with the spore-bearing functions restricted to the upper members of the series, just as many ferns produce spores only on a few small specialized fronds. The formation of a compound plant by adding units one above another is simpler and more direct than the budding out of lateral shoots from lower down, like those which form roots and rootstocks. The successive members of the series have the same relations to each other as the original basal unit might have had to its parent plant, or as the vegetative capsules of Anthoceros and of the mosses still have. The jointed internodal structure which characterizes the stems of angiosperms is itself a distinct intimation that the plant-body in this group has been made up in a manner essentially different from that of the comparatively jointless stems of higher pteridophytes and conifers. That the plumule may be viewed as an outgrowth from the cotyledons, instead of being a predetermined structure to which the cotyledons are accessory, is indicated by the fact that in some plants there is more than one plumule, and that in others, such as the cotton plant, buds many arise in the axils of the cotyledons, and in others still, small pieces of the cotyledons can produce plumules.1

It is also noteworthy that other internodes, like the cotyledons, grow by intercalation, or at the base, instead of at the apex, the terminal bud having been laid down in advance, like the plumule, before the expansion of the internode begins. This principle of intercalary growth is illustrated most strikingly, perhaps, in the palms, in which not only the internodes themselves, but their leaves and inflorescences are definitely constructed from the apex downward. The terminal portions of the leaves and inflorescences may be pushed out as finished products while their basal tissues are still in a rudimentary and delicately protoplasmic condition.

The development of a series of capsules or cotyledon-individuals by apical budding or plumule-formation is certainly no more remarkable than that new moss-plants should arise from cells of the stem of a moss-capsule, or even from the lid. Nor is it an any more improbable phenomenon than the development of adventitious buds as a result of injuries to parts which normally do not produce buds at all, as for example, in a piece of cotyledon of Plantago or in the embryo of Sechium, which produces new roots and new plumules if the originals fail of their purpose.

APOSPORY WITH DEFERRED MITAPSIS.

The final step in the present suggestion of a course of evolution toward angiospermy is that the primitive cotyledon-like plant becomes aposporous, so that it can produce prothalli instead of spores, the fusion and reduction of the number of the chromosomes (mitapsis) being deferred until the egg-cells are to be formed. Apospory, with the retention of the double number of chromosomes has been ascertained to exist in ferns of the genus Nephrodium.

1While the article was in the hands of the printer this supposition has been confirmed. See Farmer, J. Bretland, and Digby, L., 1907, Studies in Apospory and Apogamy in Ferns, in Annals of Botany 21 161-199, Pls. 16-20, Apr. 1907.
2Digby, L., 1905. On the Cytology of Apogamy and Apospory, Proc. Royal Soc. London, 76: 463.

"The prothalli of the two apogamous varieties, Nephrodium pseudo-mas Rich. var. polydactyla Wills, and Nephrodium pseudo-mas Rich. var. cristata apospora Druery, exhibit two striking differences. Whereas in the former nearly all the prothalli, except very young ones, have a strand of vascular tissue extending throughout the greater part of their length, in the latter only two cases of feebly-developed tracheides have been seen. Again, in Nephrodium pseudo-mas var. polydactyla, migrating nuclei, some of which have been seen to fuse, are a characteristic feature. Out of a large number of prothalli it was found that about 73 per cent. of the young ones exhibit phases of nuclei passing from one cell to another. As this fern produces fertile spores, it is almost certain (it is hoped shortly to settle this point) that there is a true reduction during the division of the spore mother cells, the doubled number characterizing the sporophyte is apparently brought about by the migration and fusion of prothallial nuclei.1 In Nephrodium pseudo-mas var. cristata apospora, out of 80 prothalli examined, only two showed possible cases of nuclear migration, and these were open to doubt as regards their interpretations.
     The reason for the absence of fusion in other cases is obvious, for the prothalli of Nephrodium pseudo-mas var. cristata aposora, as we have seen, already possess the full complement of somatic chromosomes. Hence there is no need for the fusion of two nuclei which, by their union, double the number of chromosomes."2

Two varieties of the same fern show two very different systems of apospory, thus illustrating the range of choice of aposporous methods of reproduction which lay open to the ancestor of the angiosperms. In the one variety (cristata apospora) apospory is accomplished without a reducing-division and the resulting prothallus develops a new plant without fertilization. In the other variety (polydactyla) the development of the aposporous prothallus is initiated by the chromatin-fusion of a vegetative cell. Two vegetative cells of the prothallus afterward unite, and thus restore the double number of chromosomes, so that the new plant can be developed.

A less violent departure from normal methods of reproduction would place a primitive plant on the road toward evolution into an angiosperm. The type of apospory which the angiosperms appear to represent is somewhat intermediate between these two, and somewhat less abnormal than either. Apospory, as illustrated in angiosperms as a group, does not involve that mitapsis be omitted altogether, as in one of the fern varieties; it is merely postponed to a later generation of cells. Neither is there an abandonment of fertilization by the male gamete as in the other fern variety. If the aposporous prothalli were to retain more of the functions of true prothalli, they would be able to produce young plants sexually, and these would then correspond completely, in their origin, with the embryo of a flowering plant. The parallel with one of the Nephrodium varieties is complete in the genus Bryophyllum where from certain points on the margins of the leaves young plants can arise, and not merely ovules which have to be fertilized, or pollen-grains to fertilize them. In the genus Begonia the tissues of the leaves retain still more of their cotyledonary functions and can produce aposporous new plants with almost as much facility as in Nephrodium.

The more complete form of apospory, shown in Nephrodium, Bryophyllum and Begonia, not only omits the spores, but also passes by the stage in which new conjugations can be undertaken. It becomes simply a method of vegetative propagation. As such it may have an environmental advantage, but it constitutes at the same time a grave evolutionary danger. Habitual vegetative propagation conduces to deterioration of sexual processes and final sterility. The more advantageous purely vegetative forms of aposporous propagation might become, the more certain would be the extinction of the species.

In proportion as plants rely upon vegetative propagation the power of sexual reproduction declines. Many domesticated and wild plants might be cited as representing stages in this process of deterioration. That there are no wild angiosperms in which the power of sexual reproduction is entirely lacking, may be taken to indicate that organisms of this stage of development can not long survive the discontinuance of sexual reproduction.

It would appear, then, that the form of apospory which could open the way to the evolution of angiosperms must have been radical enough to eliminate the macrospores and attach the aposporous prothallus to the parent plant, but not great enough to exclude the formation of egg-cells and the continuation of sexual reproduction.

ANTICIPATION INSTEAD OF RECAPITULATION.

The currently accepted doctrine or "biogenetic law" of recapitulation tends to conceal the possibility of such evolutionary changes as apospory. Recapitulation affords an idea and method of expression often very convenient for describing in a general way the facts of developmental history, but evidently does not represent a universal or causal principle or a necessary sequence in evolutionary progress.

In the archegoniate plants there are numerous independent instances of what might be called syncopation or anticipation, rather than recapitulation, for instead of merely following over the ancestral lines of development in gradually shorter and less accentuated form, various pieces of the life-history appear to have dropped out, suddenly and completely. Thus in apospory a cell which might normally give rise to spores, produces, instead, a prothallus, such as might grow from the spores, which are then entirely omitted from the program. In a similar manner, the conjugation of two of the unspecialized cells of the prothallus may result in the growth of a sporophyte, the formation of specialized archegonia, antheridia and gametes being entirely omitted. Nor do these instances show the limits of anticipatory abbreviation of the life-histories of the archegoniate plants.

Instead of merely producing prothallia by apospory, many ferns produce young plants by direct growth from the cells of the leaves. Likewise in Isoetes, young plants may replace the sporangia, in the axils of the leaves, though it is possible that the thread or column of cells on which these aposporous plantlets are borne may represent the prothallus. Indeed, it may be that Isoetes, rather than the terrestrial heterosporous archegoniates, represents the nearest pteridophytic analogue of the flowering plants. Many of the smallest and least specialized angiosperms are aquatic types, like the Lemnaceae and the Podostemonaceae, and some of them have little more differentiation of tissues than Anthoceros itself.

Podostemon and its aquatic allies may never have had the acrogenous internodal structure of the higher angiosperms, and may illustrate a different method by which angiosperms could arise from an Anthoceros-like ancestor. The so-called leaves of the Podostemonaceae appear much more analogous to the fronds of ferns and algae than to the leaves of other angiosperms, and appear to be mere thalloid outgrowths of the primitive capsule-base, like the fronds of ferns, instead of developing as an acrogenous series of vegetative capsule-units.

1The only obvious difference yet detected between these Palaeozoic fossils and the modern Podostemonaceae lies in the fact that the capsules of the latter are many-seeded, while the supposed seeds of the fossils are single, and much larger. Such diversities in the numbers and sizes of seeds inside the same family are very frequent, of course, among the flowering plants. The habits of life of the Podostemonaceae would render many small seeds preferable to fewer large ones, so that a reduction in size and an increase in numbers might naturally be expected as a result of a long evolutionary opportunity such as any extant descendants of these paleozoic plants would have had. They are aquatic plants, living in tropical water-courses, but the rocks over which they creep are often completely exposed for long periods in the dry season. The seeds have the primitive function of carrying the species through the annual period of drought.

Systems of botanical classification usually treat the Podostemonaceae as degenerate representatives of one or another of the terrestrial families, but the justification for this is not obvious. That the family may prove to have historical significance as a primitive group of angiosperms is suggested by some Paleozoic fossils to which my attention has been called by Mr. David White. These remains have been looked upon hitherto as ferns, but Mr. White has ascertained that they produce quadrivalvate capsules each apparently containing a single seed-like body. The resemblance to some of the recent Podostemonaceae is very striking throughout. Indeed, it is not now possible to specify any differences by which they can be excluded from that group, though Mr. White assures me that paleontologists will be very reluctant to admit the existence of even very primitive angiosperms in an epoch so remote.1

ELIMINATION OF MACROSPORES BY APOSPORY.

If the present view can be justified, it will not be necessary to think of the egg-cell or of the egg-apparatus as representing a macrospore which remains attached to the parent plant and germinates, instead of falling off as macrospores should. The attachment of the young plant to its parent is adequately explained by apospory, and can be viewed as entirely parallel with the attachment of a fern-capsule to its parent plant or of the very young fern-frond to the female prothallus from which it springs. The egg-apparatus can be looked upon as the archegonium of an aposporous prothallus, the only essential difference being that mitapsis has been postponed until shortly before the formation of the egg-cells.

The divisions of the pollen nucleus may be homologous with the subdivision of a microspore to form a prothallus, but the fact that some of these nuclei may enter into conjugation renders them also homologous with the antherozoids to which the moss-plant or the fern-prothallus eventually gives rise. In a similar way, the egg-cell and its immediate predecessors may be compared directly to those of the archegoniates, but they need not be supposed to have the double homologies enjoyed by the pollen nuclei. The complete female homologue of the pollen-grain or microspore would, in this system, no longer exist, the female prothallus being supplied by aposporous development before mitapsis takes place. The aposporous prothallus anticipates and supplies the period of life-history previously attained by the independent development of the detached macrospore.

A prothallus which arose by apospory, by maintaining an intimate contact with the parent plant, would be able to nourish and protect its progeny much better than the prothallus developed from a detached macrospore. The relation of the young plant to its prothallial parent would be quite the same as that of a moss-plant to its capsule or a fern plant to its prothallus, as already stated. The difference lies in the special relation of the aposporous prothallus to its vegetative parent.

ASSOCIATION OF TWO GENERATIONS BY APOSPORY.

Under the doctrine of alternation of generations it is often said that the moss-capsule develops as a parasite on the parent plant. In the angiosperms there would be, by parity of reasoning, a double parasitism, the embryo is a parasite on the nucellus, and the nucellus upon the parent plant. Parasitism is, however, hardly the correct word, for the moss-capsule, the fern-frond and the angiosperm-embryo are all developments from fertilized eggcells. The difference is merely that of the stage at which the gametes or their products shall part company with their parent organisms. By continuing to assist the fertilized egg-cell, and allowing it to develop into a capsule, the moss-plant is able to produce thousands of spores from a single archegonium, instead of four only, or merely a few. The plants have simply followed the same course as the animals, in extending the periods of family relations. The capsule is the offspring of the moss plant, the prothallus the parent of the fern. The angiosperms add another member to the series of prolonged family contacts. The young embryo might be said to be nourished not only by a mother, but also by a grand-mother. The archegoniate plants usually bring only the members or phases of one generation or life-cycle into definite supporting relations, but the aposporous ferns and the flowering plants are able to connect in this way two entirely distinct generations. Unless apospory takes place, mitapsis concludes each generation with the formation and scattering of separate spores, from which the next generation must be independently built up. But by means of apospory and delayed mitapsis two previously separated generations can be brought into effective contact. It would seem, then, that it is apospory through which the evolution of the angiosperms has become so nearly parallel to that of the mammals that both have actually been described as placentate organisms.

ORDER OF CHANGES NOT ESSENTIAL.

It is not necessary to hold that the changes involved in such an evolution of angiosperms from aposporous archegoniates took place in the particular order in which they have been mentioned. There is no objection to supposing that any or all of them might have been in progress during the same period, while the plants were still too small and the tissues still too soft to favor the preservation of fossil remains. The extension of the primary capsule-base or nursing foot into a leafy axis by vegetative growth may have come about after the aposporous seed-producing condition had been reached, rather than before. In Streptocarpus we have plants in which the cotyledons are the only vegetative organs, the plumule consisting only of flower-buds and in Welwitschia (Tumboa) there are at most but four true leaves.

If the habit of apospory were adopted far enough back it would have greatly facilitated the other changes, if it did not actually bring them about. By enabling the plant to elide that part of its life-history in which the delicate spore and prothallus must find continuous moisture, it would deliver the primitive angiosperms from the disabilities suffered by most of the ferns and enable them to advance into the open sunlight.

Young angiosperm seedlings are already of very large size in comparison with fern spores, and are to that extent the better able to establish themselves rapidly in exposed situations, and send their roots down promptly into the permanently moist subsoil, instead of remaining dependent upon the precarious surface conditions which still restrict most of the pteridophytes to humid, sheltered places.

The origin of angiosperms through apospory requires, as already intimated, a less violent deviation from the normal and primitive methods of sexual reproduction than that which is definitely known to exist in Pellaea, Bryophyllum and Begonia, so that no objection can be made to it on the ground of feasibility.

INTERNODAL METAMERISM OF ANGIOSPERMS.

There are several morphological advantages in recognizing this more simple and direct route of evolution. The first and most general is that it would explain the internodal structure of angiosperms, by establishing on a natural basis the complete homology of all the vegetative parts and floral envelopes, the cotyledons, leaves, sepals, petals, carpels and stamens. All alike correspond to the same primitive structures, the capsule-valves of the Anthoceros-like ancestor.

The internodes of the angiosperms have an individuality of the same kind as that of the fronds of ferns. The cotyledons may be considered as members of the series of internodes or joints of which each compound plant individual is composed. The cotyledons are usually less different from the succeeding vegetative internodes than these are from the internodes of the flowers and fruits, to which the vegetative internodes finally give rise. In some plants, such as Persea and Pachira, the internodes which immediately succeed the cotyledons are specialized. In others, like Eucalyptus, young plants may continue for a long time to produce leaves which are very different from those of the adults. That there is no essential distinction between the vegetative and the floral internodes, has long been recognized. The flower leaves may take on at times the green color and firmer texture of the vegetative organs, as often happens in roses and trilliums, or the carpels themselves may function as green expanded leaves after opening to scatter their seeds, as in Sterculia, or they may take on functions of the cotyledons or of the endosperm by storing nourishment for the use of the young plant of the next generation, as in the long-persistent pericarps of Sechium and Melocanna.

The individual angiosperm, like the individual worm or centiped, is a doubly composite organism. It is not merely a colony or complex of cells, but also a combination of a number of theoretically equal and equivalent body-parts or metamers, such as the internodes of the plants and the segments of the animals. The cells are associated into metamers, and the metamers are combined into the complete organism, just as the individual ants or bees join to make the still higher social unit or colony.

In the internodal metamerism of the angiosperms only one metamer is formed in the egg or embryo and the others are added by subsequent vegetative propagation. In the segmental metamerism of arthropods the association is more complete, in that numerous metamers are formed in the egg and usually few are added afterward, or none at all. Thus among the millipeds and centipeds where metamerism is very highly developed the larvae of some groups are hatched with only three leg-bearing segments and the others supplied by intercalation at subsequent periods of moulting. But in other families, including those which have the largest number of joints, the young leave the egg with the full complement of segments. In the suborder Geophiloidea the number of segments ranges between 31 and 173, far exceeding the number of internodal joints of many plants.

In many of these lower types of animals a relative equality of the body metamers has been preserved, but in the higher groups the metamers become specialized and unequal. Similar inequalities exist in plants, even among vegetative metamers. Thus in numerous plants such as coffee, cacao, cotton and the Central American rubber tree (Castilla) there are two kinds of branches. The metamers composing one type of branches are in all respects the equivalents of those of the primary stem or trunk, while the others are distinctly inferior and unable to produce or regenerate primary branches.

STRUCTURE OF VEGETATIVE METAMERS.

The ideal of a vegetative metamer of an angiospermous plant individual includes three kinds of parts: (1) the internode proper, forming a section of the stem of the plant, (2) an expanded assimilatory plate or leaf, usually adapted for exposure to light, and (3) a terete absorptive organ, or root, which usually buries itself in the ground and there produces root-hairs.

Internodes are generally simple, but the coffee shrub might be said to have compound internodes, since each primary internode produces two branches from extra-axillary buds. The number of leaves borne by each internode is usually only one or two, but some plants have whorls of several leaves, though this condition may be reached by the shortening of some of the joints. In most plants only the lower internodes produce roots, but there are also many species, as among the aroids and figs, where all the internodes bear roots freely, and in a very large number of plants they have the power of doing so under special conditions.

The more primitive types of leaves consist of two parts, a cylindrical basal sheath surrounding the next internode, and an expanded terminal blade. From the basal sheath stipules have been derived like those of Rosaceae and Ranunculaceae, and bud-scales like those of Ficus and Castilla. In Inodes, Thrinax and other fan-palms the sheath has been prolonged into a petiole, which ends in a ligule. On the other hand, Desmoncus and related genera of cocoid palms have ligules in the same position as the grasses, as direct extensions of the sheath, above the insertion of the blade. Evidence is thus afforded that in the Cocaceae, at least, the petiole is not a part of the sheath, but a prolonged naked base of the midrib of the blade. Similar differences in the homologies of the petioles are doubtless to be found in the leaves of other angiosperms.

The leaf may be considered the most primitive element, and is in most cases also the most essential part of the plant metamer. The joints are often reduced to mere rudiments, and the roots entirely lacking. Sometimes internodes of special stems (rootstocks) are devoted to the production of roots. Sometimes roots produce buds and give rise to new stems or new plant individuals. Thus the many seedless varieties of the breadfruit are propagated from pieces of roots. In Sechium the primary metamer has no internode-like basal joint (hypocotyl), but many roots grow out independently from the united bases of the cotyledons. Root-hairs grow out in a similar manner from basal cells of the embryos of Podostemonaceae. The cotyledons of Plantago and the leaves of Begonia and Bryophyllum also produce roots.

1Safford, W. E., 1905. The Useful Plants of the Island of Guam. Contrib. U. S. National Herbarium, 9: 69. These spine roots of Dioscorea protect the edible starch-filled tubers.

In addition to their absorptive functions, roots often serve as organs of aeration. Even subterranean roots may send branches upward into the open air for this purpose. This occurs not only in the mangroves and other swamp plants, but in cotton and other dry land types. Roots may also be specialized as haustoria in parasites, and as hold-fasts in climbers, or even as spines to afford a protective armature, notably in certain species of yams1 and in the palm genus Acanthorhiza. Although the spines of Acanthorhiza are often large and compound like those of Gleditschia, it is apparent that they are roots, not only because there is a complete series of transitions, but also because of the large deciduous root-caps.

1Professor Edward L. Greene has pointed out to me that the spine-clusters of Mammillaria are similar and perhaps analogous with those of certain of the species of Mesembryanthemum, which represent marginal spines of the reduced blade of the leaf, while the conical prominence upon which the cluster or compound spine is seated may represent the petiole or base of the leaf. The flowers and fruits of Mammillaria do not emerge, as in Opuntia, from the same point as the spines, but from the axils of the fleshy prominences which bear the spines. But Professor Greene considers the assignment of Mammillaria to the same family with Opuntia an artificial arrangement, so that an analogy between Mammillaria and Mesembryanthemum would not necessarily interfere with the recognition of the capped Opuntia spines as roots. That the spines of Opuntia and Cereus are not to be interpreted as equivalents of marginal projections of a reduced leaf-blade, seems to be proven by a fact observed by Dr. J. N. Rose, that in these genera new spines may be added one after another, even in very old clusters. Nor is it likely that new leaves would be pushed out in this manner, which is much more appropriate for branches or for roots. That the thorns of some of the cacti secrete nectar, as shown by Ganong, does not exclude the possibility that they are roots. Exposed root-tips often produce secretions, and my son Robert informs me that the secretion of the aerial roots of the corn plant has a sweet taste.

It is not impossible that even the spines of cacti may prove to be modified roots, instead of leaves. The spines of many species are capped, and their number, position and arrangement are at least as favorable to their being roots as to the usually accepted theory that they represent leaves. The modification that roots would require to become spines is much less than in the case of leaves. Not only in the genus Peireskia, but in many species of Opuntia, true leaves are developed, and it is in the axils of the leaves that the spines arise, just below the point from which the new growth appears, whether of flowers or branches or of true functional roots. A cluster of spine-like leaves or branches in this position would need to represent a rudimentary branch or series of branches. The arrangement of these would be spiral or concentric, which is evidently not true of the spines.1

APOSPORY AND ALTERNATION OF GENERATIONS.

In comparison with the current application to the higher plants of the doctrine of alternation of generations, the present suggestion may also claim merits of simplicity and directness. It is no longer necessary to imagine that two generations originally alike have become specialized, nor that one generation is borne parasitically on the other except in the manner in which the aposporous fern prothallus is borne.

The evolutionary history of the angiosperms can be thought of as a definite progressive sequence, without the need of supposing that one "generation" has deteriorated while another has expanded. The macrospores and the vegetative prothalli, having been completely eliminated from the life-history of the primitive angiosperms, did not have to be gradually reduced from a functional to a rudimentary condition.

The so-called endosperm of the true seed plants need not be supposed any longer to correspond to the prothallial endosperm of the cycads and coniferae. It is not built up before fertilization takes place, but afterward. It does not arise from a germinating spore, but as a result of the conjugation of two nuclei, comparable, perhaps, to the conjugations of adjoining cells which occur in the prothallia of certain ferns and give rise to the new double-celled structural phase by apogamy without the production of antheridia and archegonia, as though the ancestral form had all the liberty of alternatives possessed by the ferns and had ended by combining them into the complex and hitherto altogether mysterious reproductive processes of angiosperms. The part of the angiosperm which, in the present view, might correspond to the prothallus itself, is the nucellus. And even this relation would not be direct, for the nucellus of the angiosperms might not be homologous with the nucellus of the conifers and cycads, which, if current interpretations are correct, is more analogous to the placenta of the mammal than to an aposporous prothallus.

The obviously very great and fundamental difference between the angiosperms and gymnosperms would be adequately accounted for. The homologies which have been alleged hitherto appear very artificial, and leave us with a problem as difficult as that which they are intended to solve, namely, how structures derived from those of ferns or of gymnosperms could have become so completely different in the angiosperms.

VEGETATIVE PARTS REPRESENT STERILIZED REPRODUCTIVE TISSUES.

1Cook, O. F., and Swingle, W. T., 1905, Evolution of Cellular Structures, Bul. 81, Bureau of Plant Industry, U. S. Department of Agriculture.

The deduction based by Bower on his studies of fern-structures would remain thoroughly applicable to the angiosperms, since their vegetative parts would still represent sterilized reproductive tissues. Indeed, this proposition becomes a mere truism after the essentially sexual nature of the double-celled structures of the higher plants has been realized. The growth of the whole plant body has been intercalated into the sexual process. It is built up during conjugation and not after conjugation has been completed.1

FUNCTIONS OF THE APOSPOROUS PROTHALLUS.

The gymnosperms may be supposed to have the ovules and seeds naked because they are still borne in an endosperm which corresponds to the primitive, vegetatively functional prothallus, though it now remains attached to the much more highly developed double-celled structure which corresponds, in turn, to the capsule of the liverwort and the moss, the frond of the fern and the leafy axis of the club-moss. The ovule and seed of the angiosperm are borne, not on the original vegetative prothallus, but on a structure which, if it arose by apospory, would never have had independent vegetative functions. It need never have been very large, and could have been reduced very readily in becoming more specialized. There was no occasion to assume protective or nutritive duties, since there was always an enclosing capsule or carpel.

The fern and the flowering plant are alike in that their ancestors can be traced back to the capsules of simple thallose plants like Anthoceros, but there appears to have been, at some very remote point, a divergence of procedure, the group which gave rise to the ferns and gymnosperms retaining for a much longer period a functional prothallus which the adoption of apospory enabled the ancestors of the angiosperms to completely eliminate.

Lastly, a certain presumption of probability may be claimed for a suggestion which enables the peculiarities of such plants as Nephrolepis, Begonia and Bryophyllum to be associated with other phenomena of apospory and thus to find places in normal evolutionary history, instead of remaining mere meaningless "freaks of nature," because they may have appeared to lie far outside the pale of former interpretations.