The evolution of sex in plants

Front matter

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Prefatory Note

Permission has been obtained from the publishers of certain books by the author for the use of figures as follows:

From the American Book Company, for the use of Figs. 2-5, 8, 9, 11-14, 16-20, 22, 23, 28-32, 37, 39, 42, 44, 46, reproduced from A Textbook of Botany.

From D. Appleton & Co., for the use of Figs. 1, 6, 7, 10, 15, 24-27, 33-36, 38, 40, 41, 43, 45, reproduced from Elementary Studies in Botany.

CHAPTER

Chapter I

In any discussion of the evolution of sex it is necessary to consider asexual reproduction. The extent to which asexual reproduction occurs among plants is probably not fully appreciated. In many of the lower thallophytes sexual reproduction is unknown, and in all plants exhibiting it there are also asexual methods of reproduction. It is probably true, taking the plant kingdom as a whole, that the multiplication of individuals is greater by asexual than by sexual methods. It is obvious, therefore, that sex is not an essential feature of reproduction. Historically it was the last method of reproduction attained among plants, and when it appeared it did not replace the older methods, but was added to them.

The significance of sex, therefore, is not to secure reproduction, but to secure something in connection with reproduction that the other methods do not. It is necessary to keep this fact in mind in considering the origin and real function of sex. Our conceptions of sex have largely been determined by its place in the life histories of the higher animals, in which it has become the only method of reproduction. It is difficult, therefore, to think of it as having any function apart from reproduction; but among plants the sexual method has never become the only method of reproduction. Even among the flowering plants, which represent the culmination of the plant kingdom, and which would have eliminated asexual reproduction if it was eliminated at all among plants, reproduction by tubers, bulbs, and cuttings, as well as the universal occurrence of microspores (pollen grains) and megaspores, testify to the fact that asexual reproduction is not even a declining method.

It is also among plants that the origin of the sexual method is in evidence. It did not appear as an entirely new mechanism, detached from everything that preceded it, but arose as a gradual modification of one of the asexual methods; nor did it appear at first with all the significance it attained later. This seems obvious enough, even if the significance of sex in each step of its progress cannot be explained. If sexual reproduction has arisen from asexual reproduction, it is necessary to trace the evolution of the latter, at least to the point where sex appeared. In doing this no effort will be made to specify the plants that contribute the evidence. They are sufficiently known to botanists,- and would be meaningless names to those who are not botanists. The series of facts herewith presented, however, should be clear enough to all.

The use of the term “reproduction” in this discussion must be defined. Any cell that produces another one is performing the function of reproduction, but the result may be merely the growth of an individual, or the restoration of wasted tissue, or the healing of a wound. It is obvious that such results are not included in reproduction as currently understood. As ordinarily applied, and as it will be applied here, it means the production of new and independent individuals that become self-supporting.

J

The lowest members of the plant kingdom are individuals whose bodies consist of single cells. In these cases the individual and the cell are identical. For the benefit of those who are not biologists, it may be said that a cell is essentially an organized unit of protoplasm called a protoplast. The individual, therefore, in these low plants is a single protoplast whose structure is extremely complex and whose physiology is more so.

In this connection there is no need to outline what is known of the structure of a protoplast, and its physical and chemical activities could not even be outlined. The significant fact for this discussion, however, is that, among the activities of the protoplast, it has the power of self -division, by means of which it divides into two Fig. i— A one-ceUed plant new protoplasts, each like (pieurococcus), showing divisions the parent (Fig. i). The resulting^ 111 “w individuals.

visible machinery of this division has been described in great detail, and it indicates that an exact division of every constituent of the parent protoplast is provided for, so that each one of the daughter protoplasts is a duplicate of the parent in structure and soon it becomes a duplicate in size also.

I he forces which control this machinery, and which result in making any visible machinery at all, are much more important, but they are unknown. In fact, it is a fair question whether the so-called machinery is not made up of the visible results of an invisible process.

Whatever the mechanism of cell division may be, when the individual protoplast divides to form two new protoplasts, it performs the function of reproduction. A one-celled plant has in this way produced two new plants. It follows, therefore, that the fundamental reproductive mechanism is cell division, and there is really nothing more in the reproductive power than this phenomenon of cell division, whether it be sexual or asexual reproduction. If the essential machinery of reproduction is provided for in cell division, it follows that the cell fusion which precedes cell division, and which is often referred to as the sex act, must be regarded as an addition to the fundamental process of reproduction, an added preliminary process, not necessary to reproduction, but securing something in connection with it. In other words, reproduction is one of the functions of protoplasts, and when an individual is a single protoplast, cell division and reproduction are obviously the same.

A feature of most plant cells must be mentioned, since it is involved in the appearance of another form of asexual reproduction. In general, the protoplast is not naked, but invests itself with a firm but elastic wall or membrane. In any reproduction of one-celled plants, therefore, the wall as well as the active protoplast is divided, and new walls are formed between the two new protoplasts, thus completing the investment of the new cells. It must be remembered, however, that the wall is merely an incident in the division of the protoplast, and that wall division may be eliminated without affecting reproduction. What may be called the first stage in the evolution of asexual reproduction, therefore, is represented by those one-celled plants whose only method of reproduction is ordinary cell division, which is a function exercised by any protoplast under appropriate conditions.

When plants become many-celled, ordinary cell division does not result in new individuals; that is, ordinary cell division and reproduction are not synonymous. The result of cell division is not new individuals, but the growth of the same individual. In other words, cell division has become a feature of growth. In this situation, therefore, the most primitive form of reproduction has come to express itself in the growth of a single individual. This transition from cell division resulting in new individuals, to cell division resulting in growth, has established, or at least has become chiefly associated with, a new form of asexual reproduction.

Before describing this, however, attention should be called to the fact that in many-celled plants certain cells may appear to have lost the power of division, while other cells have retained it. This association of protoplasts in the individual, therefore, has not only modified the form of asexual reproduction, but has resulted apparently in the loss of the power of division by certain protoplasts. An analysis of the facts may modify this impression somewhat. As a rule, a meristematic cell, that is, one that divides, usually does so when it is young. If for any reason it becomes relatively old without dividing, it seems to have lost the power, and never divides, becoming a permanent cell, as contrasted with a meristematic one. With such facts under observation, it was natural to suggest that the power of division is a juvenile power of a protoplast, which is gradually lost as age increases. This would mean that the aging of a protoplast is accompanied by some definite physiological change; that it involves constitution as well as time. If this is true, the power of division has either disappeared or has been inhibited. That the latter alternative is the more likely is evident from the following facts. Whenever a cell becomes permanent it passes through its juvenile stage without dividing. This power, common to all young cells, has failed to express itself. Something, therefore, inhibits the division of young cells and determines that they shall become permanent, while their associates are not inhibited and continue to divide. It is also well known that in many cases a relatively old cell, fairly to be regarded as a permanent one, can regain the power of division under certain conditions. In this case an inhibition has apparently been removed from an old protoplast, just as it may be applied to a young protoplast. It becomes obvious, therefore, that the division of a protoplast is not a necessary function of its age, although it usually expresses itself in the juvenile stage. It is a power always present, which may be inhibited or may be permitted to express itself at any time in the life of an active cell. In any event, this shows that the power of reproduction is possible in any protoplast at any stage of its active life, and also that it may be inhibited at any stage.

As stated above, in many-cellcd plants cell division, which is the fundamental process of reproduction, results ordinarily in the growth of a single individual rather than in new individuals, and therefore does not result in reproduction as we have defined it. This situation necessitates a new form of asexual reproduction, not in essential features, but in details. So long as cells are held together by their walls, in the continuous framework of an individual, there can be no production of new individuals. There must be detachment from the parent stock sooner or later as a preliminary to the series of cell divisions that are to result in the new individual. Among the lower algae this is accomplished in a very simple way, and the separation from the parent stock takes place at the very beginning of the new individual. The protoplast detaches itself from the cell wall, which is a part of the permanent framework of the parent plant, and escapes into the surrounding medium (Fig. 2).

This escaped protoplast is the so- Fig. 2.— a spore of (Mocalled spore, which is nothing Sonium just escaped from more than a protoplast acting the °Id ceU waU' independently of its wall and of its parent plant. No new powers belong to the escaped protoplast; it begins a series of cell divisions, but, being free from the parent form, the divisions result in a new individual. The difference between such a spore, therefore, and any other protoplast belonging to the parent body is not a difference of power but of opportunity.

Ordinarily the spore-forming protoplast begins a series of divisions before it escapes, resulting in several spores, each one of which, continuing the divisions, forms a new individual. It is obvious that the series of cell divisions is responsible for reproduction, whether the protoplast divides before it escapes or escapes before it divides. The number of spores is a detail of secondary importance, and the relation of these spores to the medium (water or air) is also a secondary matter. If they escape into water they are likely to develop swimming appendages ( cilia ); if they escape into air they develop a protective wall. In this connection attention might be called to cases among the fungi in which the detachment of spores is secured, not by the discharge of protoplasts, but by the abstriction of walled cells from special branches. This pinching off a part of the body is merely a detail of separation. The essential fact is that a spore means a protoplast separated from one individual and capable of producing another individual.

The multitude of names applied to spores on the basis of secondary characters has obscured the fundamental idea that belongs to all of them. The ordinary definition of a spore is that it is a single cell, specially “set apart” to reproduce. It is not necessarily a single cell when it escapes, for any spore may begin its reproduction divisions before it escapes, nor is it specially “set apart” for this function in the sense that it is differentiated in structure and power from the other protoplasts. It is literally “set apart,” that is, detached from the parent stock, and that seems to be the only reason why it reproduces and the other protoplasts do not.

Although spore-formation is an effective method of producing new individuals asexually from many-celled individuals, it should not be understood that reproduction by spores is restricted to many-celled individuals. There are one-celled plants that also have spores, which means that for some reason the protoplast under certain conditions begins a series of divisions that do not involve the wall. It cannot be said, therefore, that spore-formation was developed in consequence of the multicellular habit of body, but that if it had not been developed, many-celled individuals could not have multiplied asexually except by fragmentation, which is simply body division that involves a group of cells.

It would be interesting to know what conditions determine the separation of a protoplast from its wall and its abandonment of a structure it had made and kept in condition. A possible suggestion may be obtained from the occasional behavior of protoplasts when protecting themselves against unfavorable conditions. Among the one-celled algae it is very common for the cell wall to become thicker in response to the influence of conditions unfavorable to vegetative activity. Upon the return of favorable conditions, the protoplast abandons the thick wall, made useless for an active cell, and forms a new wall. In other cases, as among the bacteria, in response to unfavorable conditions the protoplast becomes separated from its limiting membrane, rounds off, condenses, and passes into a dormant stage. These protected and dormant protoplasts of the bacteria are usually called ^spores,” but their significance is protection rather than reproduction, io and certainly they do not multiply individuals. They are the same individual in an inactive condition, no new individual being produced. In both of these cases the behavior of the protoplast is in response to conditions unfavorable to vegetative activity.

The same kind of response appears in ordinary spore-formation, in which the protoplasts become freed from the wall, round off, and are entirely detached from the general life of the individual producing them. In many algae and fungi it is entirely possible to control spore-formation experimentally. In other words, conditions can be supplied which inhibit spore-formation indefinitely, and other conditions can be supplied which stimulate abundant spore-formation. In general, whatever diminishes vegetative activity favors spore-formation, so that it is the physiological condition of the protoplast that determines whether it continues to do vegetative work or becomes a spore. It is well to emphasize this fact, because there is a general impression that spore-formation depends upon a certain amount of maturity in the plant, in other words, that plants produce spores “when the time of spore-formation comes.” It is true that the time of spore-formation is measurably uniform in the history of a given plant, but this simply means that the condition of spore-formation is measurably uniform in making its appearance. If it should appear earlier or later than the usual time, spore-formation will occur in spite of the time. The suspicion is that the favorable condition that induces spore-formation experimentally is represented in nature by the waning activity of the plant. Regular periods for spore-formation furnish abundant testimony to the

II remarkable uniformity of conditions in nature. It seems clear, therefore, that spore-formation is a response to relatively unfavorable conditions on the part of plants whose activity extends through a period long enough to encounter varying conditions.

One of the problems of reproduction, perhaps to be regarded as the most fundamental one, has been suggested by the previous discussion. When protoplasts are detached from a parent plant, whether it be a single protoplast called a spore, or a group of protoplasts, as in the case of a propagating bud, the whole structure of the parent is reproduced. Of course, the essential separation is physiological, which may take place although complete structural separation has not been effected. When one considers the reproductive power of any group of active cells isolated from the parent stock, such as gemmae, propagating branches, buds, tubers, bulbs, cuttings, isolated nodes, and even leaf fragments, it becomes evident that reproduction is a function of every active cell, and that it can express itself when certain conditions are supplied. The conspicuous condition seems to be detachment from the parent stock. It is really a restoration of lost parts, and therefore is a form of regeneration, differing from what is ordinarily called regeneration in degree but not in kind. Irom this point of view a spore is to be regarded, not so much as a specialized reproductive cell differing in power from other protoplasts, but as a single detached protoplast rather than a group of them, and therefore regenerating all the structures of the body. What induces these detached protoplasts, whether single or in groups, to produce a new individual, is no more clear than what induces a fertilized egg to produce a similar structure, but both seem to belong to the same category, and that is a series of divisions that result in a definite structure.

A second stage in the evolution of spore-formation is the differentiation of sporangia, which at first are

merely special spore-producing cells (Fig. 3). In the first stage of spore-formation described above, any active protoplast of the body is capable of becoming a spore or of dividing to form spores. In the second stage, apparently the power of spore-formation has been lost by most of the protoplasts,

Fig. 3. — A brown alga (Eclocarpus) : A, which Still retain the part of a filament showing a sporangium, power of cell division, and also an escaped spore; B, part of a ag expressed ill filament showing a gametangium, and also , . .

an escaped gamete. growth. This IS usu-

ally spoken of as a

differentiation of functions among the cells of the body, most of them retaining their vegetative activity and power of division, but losing their power of spore-formation; while comparatively few cells retain the power of spore-formation and are vegeta tivelv active only so far as it has to do with their own life. It is possible to arrange a series of algae, beginning with forms in which every protoplast is capable of spore-formation, and continuing through forms showing every degree in the restriction of this power, until finally forms are reached in which the sporangia are completely separated and distinct from the general vegetative body.

It should be remembered, however, that this differentiation of functions is still dependent upon a difference in conditions. In other words, even when there are distinct sporangia, this does not imply that spores are being formed under the same conditions that favor vegetative activity. In fact, during maximum vegetative activity, as a rule the sporangia are not formed. The conditions that favor spore-formation favor sporangium-formation. The sporangia are not formed as part of the body, awaiting appropriate conditions for spore-formation. When such conditions arise, sporangium-formation occurs whenever sporangia are distinct appendages of the body. When they are not, they are simply the vegetative cells selected to form spores. The fundamental difference, therefore, between plants without and with distinct sporangia is that in the former all protoplasts can respond to the conditions for spore-formation, while in the latter only a restricted number of protoplasts respond. What determines the selection is an important question which remains for physiology to answer.

It has been stated often that such a reproductive cell as a spore represents a cell with its primal powers, that is, powers that belonged to all cells originally; and that the other cells of the body, losing the power of reproduction through spore-formation, have become specialized cells. It is true that if specialization consists in losing a power, and lack of specialization means retaining it, then ordinary vegetative cells are specialized and spores are not, but the vegetative cells do retain the primal power of reproduction, in that they are able to divide. Spores represent another form of expression of the reproductive power; this form of reproduction is not primal, common historically to all cells, but is new in detail.

When the differentiation of sporangia takes place first, the vegetative cells have either lost the power of spore-formation, once common to all vegetative cells, or are inhibited from expressing it. Spore-formation by cells ordinarily vegetative occurs often enough to assure us that spore-formation is only inhibited in vegetative cells. It thus appears that vegetative cells, not acting in spore-formation, have become simpler in function. On the other hand, the sporangia, separated from the ordinary vegetative activity of the body, and nourished by the body in general, produce spores which are much more highly specialized cells than the ordinary cells of the body. Their increasing complexity in structure is visible in most cases, and there is no reason to doubt that their physiological specialization is equally marked. Certainly such a cell is more frequently equipped for reproducing a more or less complex body than an ordinary cell would be. It must be remembered, however, that the difference of equipment is a difference in degree and not in kind; a greater storing of the energies to be expressed in reproduction in the one case than in the other.

The claim, therefore, is that sporangia are not merely special organs, set apart from the rest of the body and detached from the ordinary activities, but that they are differentiated not only in their ability to respond to conditions favoring spore-formation, but also in the specialization of the spores they produce. For all ordinary cells, the primary reproductive power is retained only in cell division; reproductive power becomes more highly developed when special organs are set apart to produce reproductive cells. Spores to whose development a highly complex body contributes, and which are equipped to produce a complex body, must be regarded as highly specialized cells.

A summary of what may be called the three stages in the history of asexual reproduction, as given above, can be stated as follows. The first stage is represented by cell division, which belongs to cell activity in general; in other words, it is a process as natural to all protoplasts as any work. The second stage is represented by spore-formation, in which ordinary vegetative cells, under certain conditions, produce spores. In this case the activities of a cell are differentiated by varying conditions and are not differentiated permanently. The third stage is represented by the production of spores by special cells, which are differentiated in function permanently from the ordinary vegetative cells. This specialization of certain cells is accompanied by the inhibition of the spore-producing power of cells in general, and as a result the spores become more highly specialized. Through these three stages asexual reproduction had passed before sexual reproduction became established. This does not mean that sexual cells followed these three stages as a definite sequence, but that in connection with the evolution of spore-production the sexual cells appeared.

Before presenting the origin of sexual cells from spores, the further evolution of spore-production in connection with sexual reproduction may be considered. Among the vascular plants, a differentiation of spores occurs, related to the differentiation of sex. In the lower groups exhibiting sexual reproduction, the spores are all alike in appearance, usually producing individuals viduals, but no differentiation of Fig. 4— A megaspore the spores producing them is and microspore of a club observable. Among the vascular in relation to the differentiation of sex (Fig. 4). Spores begin to be distinguished as large and small ( megasporcs and micros pores), and apparently the only difference is that of size, although the constant difference in the product would indicate a more fundamental difference. The difference in size is due to the number of spores produced by the sporangium. In case only four spores are produced in one sporangium and hundreds are produced in another, the four spores are correspondingly larger. This great difference in size involves great difference in nutritive power, the microspores having that bear the two kinds of sexual cells. In other words, such an individual is bisexual. Not infrequently the individuals produced by such spores are differentiated sexually into male and female indimoss ( Selaginella ) drawn to same scale.

plants, however, the spores begin to differ in appearance, evidently very much less than the megaspores. The significant result of this differentiation is that the megaspores produce only female individuals and the microspores only male individuals. Among plants there is a very definite relation between high nutrition and the production of the female sex organ, so that it is impossible for so small a cell as a microspore to produce a female individual. This statement is not meant to imply that the difference between the two spores is merely one of nutrition, but that whatever the fundamental difference between “maleness” and “femaleness” may be, it is obvious that the latter cannot express itself except under conditions of high nutrition. This differentiation of spores, therefore, results in a definite differentiation of sexual individuals, so that plants become distinctly and permanently male and female. In this way the two methods of reproduction have reacted upon one another, a situation which will become much clearer when the differentiation of sex is described.

A final stage in the evolution of spore-production is attained when the two kinds of spores are produced by two kinds of individuals. This is illustrated by the familiar example of the willow or the chestnut, in which one individual produces microspores and another produces megaspores, or, in ordinary phraseology, one plant bears staminate flowers and another bears pistillate flowers.

A summary of all the stages in the evolution of spore-production is as follows:

(1) The production of spores by any active cell.

(2) The production of spores by a special cell or organ (sporangium).

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(3) The differentiation of spores in size, resulting in the production of male and female individuals.

(4) The differentiation of spore-producing individuals, so that the two kinds of spores are produced by different plants.

This emphasizes the fact that asexual reproduction by spores is a constant and conspicuous method throughout the plant kingdom, after plants became multicellular, and that when it came to be associated with sexual reproduction, the two reacted upon one another in the further evolution of both methods.

Chapter II

In discussing the origin of sex it must be understood that only the visible morphological structures are referred to. Even the morphology of the situation will have to be restricted to the gross aspect of the sexual cells {gametes). There are cytological features of gametes which cannot be accounted for historically as yet. It is also obvious that the pairing and fusing of gametes indicates a physiological situation that does not exist in spores. At the same time, the origin of the gamete as a whole seems obvious, both as to the structure from which it came and also as to the conditions under which the origin occurred. The cytological and physiological changes involved at the start are probably small as compared with those that developed later in connection with the so-called differentiation of sex. In any event, the origin of the gamete is the origin of sex, and the gross visible details of this origin will be presented.

If all plants were sexual, the origin of sex would be as obscure a problem as the origin of life. Fortunately, in the evolutionary sequence of plant groups the sexual cells appear for the first time far above the most primitive known plants, and therefore are as definitely related to previous structures as are any other features of evolutionary progress. It is evident that the gametes did not appear once for all, but that they arose independently in several plant groups, in response to similar conditions. For example, the beginnings of sexual cells are seen among both the green algae and the brown algae, in regions of the two groups that could by no chance be related; and the same fact is true in reference to several distinctly differentiated subdivisions of these two groups. Gametes, therefore have appeared as a natural response to certain conditions, and sexuality

is a product of plant evolution as natural and as distributed as is the production of spores.

One of the fresh-water algae ( Ulotlirix ) is commonly used to illustrate the origin of gametes, which means the origin of sex.

It is no better for this purpose than many other algae, but it is a common form and is an excellent example (Fig. 5). Its body consists of a single row of cells, forming a simple filament. All of the cells are vegetatively active so long as vegetative conditions are favorable, and all of them are meristematic, the cell divisions resulting in the elongation of the filament.

When the conditions become less favorable for vegetative activity, some of the protoplasts become detached from their walls and usually begin to divide. Such divisions naturally do not result in the growth of the body, but in spore-formation. The size of the spores depends upon the number of successive divisions, and in the