Popular Science Monthly/Volume 60/November 1901/The Origin of Sex in Plants
| THE ORIGIN OF SEX IN PLANTS. |
By Dr. BRADLEY MOORE DAVIS,
UNIVERSITY OF CHICAGO.
ZOOLOGISTS have held various views as to the origin of sex in animals, but the subject is confessedly speculative. They have very little data bearing upon the problem—the gap between the Protozoa and the Metazoa is so immense and characterized by such a paucity of intermediate types. We pass directly from relatively simple conjugation among unicellular forms to the complicated conditions in higher animals, where the sexual elements have reached a very high state of specialization.
Botany is very much more fortunate in this respect. It is not difficult to understand the evolution of multicellular plants from the unicellular, and we have a great deal of evidence that bears on the origin and differentiation of sex. Greater interest is added to this subject because we have reason to believe that sex has arisen in a number of divergent groups by identical processes but without relation to one another, so that similar complex results have been worked out independently.
We shall deal entirely with that large group of the lower plants known as the algae which includes all the plants below the liverworts and mosses with the exception of the fungi. One need study the algae but slightly to realize that they are a very diverse assemblage of forms comprising many lines of ascent, some of which are marked out clearly, but many of them mere fragments and remnants of former series that have been broken up by the extinction of ancestral types.
There are certain groups of algae well known to all students of botany that have no place in the present discussion. Such for example are the Conjugales comprising types such as Spirogyra, Zygnema, the desmids, and again, the diatoms. However valuable these forms may be for certain laboratory studies, they should never be cited as typical illustrations of sexual processes among the lower plants. They are rather extraordinarily specialized groups and have developed peculiarities of a high order. Again, there are numbers of groups complex in their organization, whose relationship to other forms is so remote that we must place them quite apart by themselves. Such for example are the stoneworts (Charales), the red algae (Rhodophyceae) and some forms of the brown algae (Phaeophyceae). These groups give us no data on the problems that we are to consider.
There is left for us a numerous and varied array of algae, representing several lines of ascent, all tending to diverge from one another. But these forms have some important points in common, particularly as concerns certain events in their life histories. There is immense variety in the form of the plant body which ranges from a single cell to structures with stalks and leaf-like organs. There are likewise exhibited many degrees of sexual development, from a few forms which actually appear to illustrate-the dawning of sex through various intermediate stages to many types in which the sexual elements have become highly specialized. The story of the differentiation of sex, that is, the evolution of the egg and sperm from the primitive sexual elements, is most interesting, but would require extended treatment. It must be left for some future paper. Our problem is to understand how the primitive sexual elements arose.
Almost all the algae in the groups referred to in the paragraph above have one phase in their life histories in common. They usually present a period, although sometimes very short, when the protoplasm of the cells is in the form of free-swimming elements. These are called zoospores or swarm-spores and they are commonly little pear shaped bodies, the pointed ends bearing 2 or perhaps 4 delicate hairlike organs, called cilia, whose vibrations give the zoospores their rapid movement. A glance at the illustrations will show the form of these motile cells.
Zoospores are likely to be produced in greatest quantity at certain seasons or under particular conditions of light or temperature, and their purpose is plainly the rapid 
Fig. 1. Stages in the Life history of chlamydomonas. a, vegetative cell. b, small Gamete. c, Conjugation of Gametes, d, Sexually formed spore, e, First division of Spore. f, Quiescent condition, Cells Multiplying by Division. (After Goroschankin.) propagation of the species. But there is a deep significance in their general conformity to a certain type of structure and their almost universal presence in the groups that we are considering. In a certain sense the zoospore represents a return on the part of these algae to primitive ancestral conditions.
There are many unicellular algae that pass a large part, perhaps the greater part, of their lives as motile cells with a structure essentially the same as zoospores. These lowly types of the Protococcales are certainly most nearly related to the parent forms of all the higher algae. The principal stages in the life history of such a type (Chlamydomonas) are illustrated in Figure 1. The free-swimming cell is shown in a and b. In c we have the conjugation of two individuals which gives a sexually formed spore such as appears in d. e and f present a quiescent condition when the cells multiply for a short time by fission.
The evolution of the algae has led for the most part to the development and long continuance of such phases of the life history as are stationary, and from these the filamentous, membranous and otherwise differentiated plant bodies have arisen. Finally the motile stage became so shortened as to be only a method of reproduction on the part of the plant and is passed over very quickly.
The zoospore then takes on new interest when one contemplates its relation to the past, realizing that it represents conditions of a remote period when the algae were much simpler than they are now and passed the greater part of their lives in a motile condition. It is not likely that the first algal types were motile, for the lowest group of all, the Cyanophyceae or blue-green algae, presents forms whose cells are always stationary, reproducing by simple fission.
But above the lower stretches of the algae, the zoospore appears with great regularity and usually conspicuously in the life history. There are certain types (unicellular Volvocaceae), whose life histories are mostly or entirely alternations of motile conditions and quiescent states when the cells come to rest, lose their cilia and remain motionless for many days. Such resting cells are well known to students of the lower algae, and it is an interesting fact that they may pass quickly and readily back to the motile form. Indeed there is every reason to believe that the one state or the other is largely determined by the physical environment of the organism. Recent studies by Livingston have shown for one type (Stigeoclonium) that zoospores immediately follow the transfer of cells in a resting condition from a certain solution of salts to a weaker solution, and this is an excellent illustration of the sort of factors that influence the alga.
In our discussion of the problem of the origin of sex we are to deal chiefly with forms whose motile conditions are so shortened as to be manifestly largely or wholly reproductive in their purposes. The plants are stationary, but at times and under certain conditions zoospores are produced in great numbers. These, after a brief existence as free-swimming cells, settle down and give rise to a new stationary plant body usually like the parent.
Zoospores or swarm spores are wonderfully alike in structure in the algae that are most closely related to one another. The prevailing type among the green algae (Chlorophyceae) is a pear-shaped cell with 2 or frequently 4 cilia at the pointed end. The illustrations show these and other characters clearly. A portion of the protoplasm is differentiated as a green body (chloroplast), which only partially fills the rounded end of the zoospore, leaving the rest of the cell quite clear. Sometimes the chloroplast contains a central body called the pyrenoid, which is associated with the starch-forming activities of the chloroplast. This structure must not be confused with the nucleus of the cell, the latter being almost always invisible in the living zoospore. Finally, one may always expect to find in the colorless pointed end, near the cilia, a small bright red body called the pigment spot. The pigment spot is generally believed to have a relation to the sensitiveness displayed by zoospores towards light, not in any sense, however, as an organ of vision, as might be judged by the unfortunate term 'eye-spot' that is sometimes applied to it.
Such is the structure of the zoospores. Now let us consider their habits. As we have said before, several are likely to be developed in a single cell, but there is no rule as to number. Sometimes the entire contents of a cell will slip out as a single zoospore, but more frequently 8, 16 or 32 will be formed, a variable number even in the same plant, and in certain cases the parent cell will give rise to hundreds. The zoospores escape from the mother cell or sporange usually through some opening in the wall and immediately swim off. They may be developed so numerously that the water is actually colored greenish and the field of the microscope shows hundreds of these organisms moving rapidly in various directions. Such appearances have given them the appropriate name of swarm-spores. The swarming of zoospores is best shown under certain conditions of illumination. The zoospores are very sensitive to light and usually arrange themselves with reference to its source so that the long axes are parallel with the incoming rays. If a vessel of water be placed so that the light rays come from one direction, as from a window, the zoospores will move in parallel lines towards or away from the source of the illumination. They will thus collect in clouds in various parts of the vessel, the exact position being somewhat modified by the currents of water that slowly circulate through every brightly illuminated vessel.
Generally speaking the swarm-spores that one is most likely to see will be asexual. Their activities cease after a few hours or perhaps minutes and they then attach themselves in some suitable position, germinate and develop young plants called sporelings. Sporelings of the alga, Ulothrix, are shown in Figure 2, d, they having developed from a zoospore like c.
But frequently and under conditions that have been in part determined swarm-spores will behave quite differently. They will swim at first very actively, approaching one another and then darting away, hut finally gathering in small groups and sorting themselves in pairs. The elements in such a pair begin to fuse together; the process is called conjugation and represents the simplest form of sexuality. The two sexual cells are called gametes, but they are nothing more than zoospores so constituted that they must fuse with one another in order to live.
The gametes show their relationship to zoospores in various ways and there is no doubt that they arose from the latter. In the first place they have the same general structure and are developed in the same sorts of cells on the mother plant. But the most important evidence of affinity is exhibited by certain gametes that are so much like zoospores that they will sometimes settle down and germinate without conjugation. This means that their sexual characters are not strongly enough developed to overcome the vegetative tendencies of their parents the asexual zoospores. However, the sporelings that come from these abortive or perhaps parthenogenetic gametes are weaker than the products of the ordinary or normal zoosopores and sometimes never reach full development. As may be guessed, this curious intermediate condition between the zoospore and gamete furnishes a most important clue to the fundamental distinctions that separate the one from the other. These differences are evidently physiological rather than morphological in character.
It is only recently that botanists have in part understood and attempted to define precisely the conditions that determine the development on the one hand of zoospores and on the other of gametes. In a general way it has been believed for a long time that the problem was a physiological one and that various environmental conditions of season, temperature or light were responsible for the results. But in the past ten years there have been numerous studies, on various types of the lower plants, attempting to establish as exactly as possible the chemical and physical factors at work. In this field of research the botanist, Klebs, has been especially active, and he, above all others, deserves the credit of developing certain experimental methods of attack. These have yielded important results and justify the belief that we may in the future obtain much precise knowledge.
Klebs treats the forms to as many well-defined conditions as he can devise, various as to the food, the osmotic properties of the water, the light and the temperature. The results have been very remarkable considering the difficulties of the problems. We can not do better than to follow his studies on one or two forms to illustrate the possibilities of investigations in this difficult field.
His studies on Ulothrix are interesting. This is a lowly type of unbranched filamentous alga common in both fresh and salt water. The zoospores (Figure 2, b) are formed in varying numbers, but usually 4 or 8 in a cell. They are relatively large structures with 4 cilia and have the appearance shown in Figure 2, c. These 4-ciliate zoospores are never sexual and they develop new Ulothrix filaments like their parent. This simple method of reproduction may be continued for
many months, but at times the conditions are such that another form of swarm-spore appears. These elements are much smaller than the usual zoospores, are developed more numerously in the mother cell and have 2 cilia as is shown in Figure 2, e, f. They are gametes and as a rule fuse readily with one another in pairs. The free-swimming gametes are shown in Figure 2, f, and two stages in the conjugation appear in g and h. If conjugation does not take place, the gametes settle down and in certain instances have been observed slowly germinating; but they develop feeble plants.
Now what are the causes that make the plant produce asexual zoospores on the one hand and gametes on the other? Are they deeply seated in the protoplasm of Ulothrix? In the first place there is no rule or rhythm in the appearance of zoospores or gametes, no time when conditions within the plant demand their development. And again, structurally, there is no hard and fast line between the zoospore and gamete; on the contrary, there are gradual transitions between these two forms of swarm spores. The problem thus resolves itself into an inquiry as to the precise environmental influences, the chemical and physical factors affecting the Ulothrix filament, whether they are actually able to make the plant form zoospores or not according to certain conditions. The habits of Ulothrix show us clearly that there are such factors, but the adjustments are so delicate that, apart from a very clear relation to temperature and the character of the salts in solution, it has not been possible to formulate them with exactness.
But other studies of Klebs, on forms that lend themselves more readily to cultivation than Ulothrix, have given some very definite results. Hydrodictyon, the water-net, is an alga that may be cultivated with great ease in the laboratory. This plant is a great cell colony, involving usually thousands of elements which are joined to one another to form a net of polygonal meshes. A portion of such a plant is shown in Figure 3, a. These cells after they have reached a certain age produce zoospores that may be either asexual or sexual (gametes). The gametes are smaller and are produced much more numerously than
the asexual elements. They escape from the mother-cell and after swarming in the water conjugate in pairs (see Figure 3, c, d, e). The asexual swarm-spores have the peculiarity of never leaving the mother cell. They swim around in the cavity bounded by the cell wall and shortly come to rest, arranging themselves to form a new net entirely within the parent cell. Thus by their habits one may readily distinguish the asexual zoospores and gametes of Hydrodictyon.
Now let us summarize the factors that will make Hydrodictyon form asexual zoospores at one time and gametes at another. The waternet grows luxuriantly in a culture solution containing a number of inorganic salts. If plants are removed from such a culture solution and placed in fresh water they will develop zoospores in 34 hours. The process takes place most rapidly if the temperature is slightly above the normal; indeed merely warming the water in which plants are living will frequently induce the production of zoospores. Plants refuse to form zoospores at a temperature as low as 8° C. but if such a culture be raised to the warmth of 16° or 20° the process is immediately resumed. Gametes are produced under very different conditions from those stated above. They demand organic food. Cultures of Hydrodictyon in a solution of cane sugar will almost certainly yield gametes after several days.
It frequently happens that the nets of Hydrodictyon will exhibit a well-defined tendency or preference to form either gametes or zoospores. Such a habit may be quite thoroughly broken by cultivating a plant under proper surroundings. Gamete-forming nets will shortly produce zoospores if grown in solution of inorganic salts and in bright sunlight. Nets with strong inclinations to form zoospores can be made to produce gametes by cultivating in a sugar solution in subdued light or darkness. Plants that have no special inclination to form either zoospores or gametes may be decided one way or the other by the illumination, bright light producing zoospores and darkness gametes. It is also fair to say that sometimes the tendency to form zoospores is so strong that a plant will not yield for several generations to the conditions that generally bring about the immediate production of gametes.
Let these studies on Hydrodictyon and Ulothrix stand as illustrations of the kind of evidence presented in varying degrees by many algae and fungi and constantly increasing as investigations in physiology proceed. The general trend seems unmistakable. We may feel sure that sexual elements, gametes, have arisen from asexual reproductive cells with an immediate relation to and probably because of certain environmental factors. In a general way these factors are known to be light, temperature, osmotic pressure and, most important of all, the chemical nature of the environment with especial reference to the kinds of foods.
What was the change that came over the asexual reproductive cell when it took on the stamp of sex? The differences are best measured in the possibilities of the two elements. The asexual zoospores may quickly and readily produce a new individual. The gamete, generally speaking, must fuse with its kind or else die. We have seen that primitive gametes may germinate without conjugation but the resulting plants in the cases best known are weaker than normal individuals. We also know that the lower stretches of the plant kingdom furnish abundant illustrations of parthenogenesis, that is, the power of an egg cell to develop without fertilization. These exceptions, however, strengthen the evidence that the essential differences between gametes and asexual zoospores are qualities lacking in the former, and especially the ability to continue and sustain the mechanism demanded by vital processes.
With conjugation all is changed, and the sexually formed spore has the qualities lacking in the two gametes from which it arose. The protoplasm is in a sense rejuvenated and with the stimulus comes sooner or later an expression frequently more vigorous than that of the asexual spore.
The most striking conjecture on the significance and origin of sex has been presented under the name 'autophagy.' It is a very simple hypothesis. However, its simplicity is its greatest danger and will probably be its complete undoing, for enough is known to indicate that the factors and conditions that produce the sexual act are immensely varied and complex. Autophagy explains the sexual act as a process by which sexual cells mutually devour one another. Each is fed to the other and by mutually contributing their substance both make possible the energy exhibited by the fusion cell.
Autophagy conceives the sexual cell (gamete) as one that lacks the energy of its progenitor, the asexual element. It is a cell reduced and starved. Ordinarily its vitality is at such a low ebb that further development is impossible. Sometimes it is not so far gone but that a favorable environment will induce parthenogenetic growth. The sexual cell may be brought back to virile activity with power to propagate the race, if supplied with the necessary energy. And the simplest method of attaining this end, according to autophagy, is the cooperative union of these weakened elements, a mutual feast, which revives the worn-out protoplasm and enables the fusion products to make a fresh start.
The hypothesis of autophagy may be attacked from several points, and becomes very unsatisfactory when so examined. It is crude and entirely insufficient to cover the subtle phenomena that it attempts to handle. The cause of the fusion of gametes involves problems of chemistry and physics which can only be investigated by methods of extreme delicacy and precision. One may see at a glance that conjugation is not the same as the actual feeding of one unicellular organism upon another. In such a case, which might be illustrated with many Protozoa, the captive form is destroyed and its dead substance is then worked over through elaborate changes into the protoplasm of the living cell. In the conjugation of sexual cells, the two masses of protoplasm fuse and mingle and perhaps the most significant feature of the process is the union of the two sexual nuclei.
As a matter of fact, sexual cells are, generally speaking, well nourished, and in all higher organisms the egg is specially provided with food, far above the amount ordinarily present in cells. The unfertilized egg does not lack food, but is unable to command the necessary energy or, if such be present, it is tied up in some form that cannot be used. The importance of the latter condition is indicated by the investigations of Dr. Loeb, who found that a slight increase in the density of sea-water will induce the immediate development of the unfertilized eggs of sea urchins, star fishes and a certain worm. In the earlier experiments, salts of magnesium and potassium were added to the sea-water, but later studies have shown that sugar induces similar parthenogenetic development. It is suggested that merely the withdrawal of water from the egg by osmosis is sufficient to cause its development without sexual intervention. And it may be supposed that normally the sperm brings to the egg substances that excite such conditions within the egg that water is given off. But we are far from understanding how such results are accomplished in nature or what other factors may be concerned.
It is certainly plain that the conditions surrounding sexual processes are immensely complex, and as yet we only know them in part and for a very few organisms. There is every reason to expect that investigation will so add to these that the subject will consist of very complicated problems in physics and chemistry. But it is something to know that important factors exist outside of the organism controlling in great part the sexual phase, and that some of them are so simple as light, temperature and osmotic pressure. Much is gained for biology in the understanding that sexual elements have arisen from asexual reproductive cells under the stress of environmental influences; that sexuality is not inherent in life although presented in almost all higher organisms, and that, however complicated the extreme conditions may be, they have arisen through a process of gradual evolution.
In another paper I shall hope to show the steps by which the highly differentiated egg and sperm in various groups of plants developed from the similar gametes presented at the dawning of sex. As stated in the beginning of this paper, the topic is a chapter in itself and well deserves separate treatment.