Popular Science Monthly/Volume 62/February 1903/The Evolution of Sex in Plants
| THE EVOLUTION OF SEX IN PLANTS. |
By Professor BRADLEY MOORE DAVIS,
UNIVERSITY OF CHICAGO.
IN a former paper published in The Popular Science Monthly[1] we considered the origin of sex in plants, describing the progenitors of the sexual elements or gametes and some of the conditions under which these cells assume sexual characters. No attempt was made to trace the later history of these primitive gametes as they become differentiated into the two extremes of sexual cells, the egg and sperm. This is a subject quite independent of the origin of sex and deserves the separate treatment that we are now to present.
Primitive gametes are sexual cells so similar in size, form and internal structure that they cannot be distinguished as male or female. They are found in a number of 
Fig. 1. Gametes and Gametangia of (a) Cladophora, (b) Ulva. the lower groups of algae and have the general appearance and same mode of formation as the zoospores from which they have been derived. Excellent illustrations are presented by Ulothrix, Cladophora, Hydrodictyon, Ulva and Ectocarpus. In these types the gametes are small motile cells, generally formed numerously C) in the mother cell or gametangium discharged into the water where they conjugate in pairs. The principal events of their formation and behavior are illustrated for Cladophora and Ulva in Fig. 1. In my former paper I described and figured the conditions for Ulothrix and Hydrodictyon. (Popular Science Monthly, November, 1901, pp. 70-73, figs. 2 and 3.)
Any one familiar with the examples mentioned above will note immediately that they are representatives of diverse groups which are not closely related to one another. On the contrary, most of the forms are associated with very clearly marked divergent lines of development. This is important, for it shows that sex did not arise at one period only and at a certain level of the plant kingdom, but, on the contrary, at a number of totally distinct times and in connection with as many independent lines of ascent. We can see no reason why zoospores might not at any time take on the attributes of sex, for the latter conditions are controlled and probably in large measure developed by the chemical and physical environment of the plant. Although sex has arisen a great many times in the plant kingdom and in groups independent of one another, the steps in the process and the structure of the primitive gametes are essentially the same in all cases. There are good reasons for believing that even now certain groups of the algae are developing sexuality, and that this process may be expected to continue wherever the lower algae have the habit of reproducing by zoospores.
With the origin of sex in any group of plants there is immediately presented the possibility of such further evolution as will give the differentiated and highly specialized sexual cells, the eggs and sperms. This evolutionary history is briefly expressed as the development of heterogamy from isogamy or the oosporic type of reproduction from the zygosporic.
Isogamy is the term applied to conditions in which the sexual cells are similar in form, morphologically identical. Heterogamy is the condition in which the female gamete is a motionless cell without cilia and the male gamete generally a ciliated sperm frequently highly specialized in form. Our problem is to understand the steps in the evolution of heterogamy from isogamy and, as far as possible, the factors influential in the process.
Isogamy is a condition very generally distributed among the various groups of algae. We may find it in almost all lines of ascent above the unicellular forms and it is not uncommon among these. Heterogamy always appears at higher levels of development than isogamy and in connection with general advances in vegetative complexity.
It customary to speak of the forms expressing the highest development of evolutionary lines as climax types. Climax types among the algae are almost all heterogamous. There are a few lines in which this level of sexual evolution has not been attained, as for example, the pond scums (Conjugates), the Hydrodictyaceae, Ulvaceae and several smaller groups of the lower algae. On the other hand, there are several heterogamous types standing quite by themselves as the final expression of certain lines of evolution that we can only conjecture because the lower representatives have become extinct. Notable illustrations of this character are the stoneworts (Charales) and the Oedogoniaceae.
Among the remaining groups of algae, and containing by far the greatest portion of this class, are a number of orders and families comprising isogamous and heterogamous forms clearly related in various ways to one another, by vegetative structure and similar life-histories, but offering a wide range of variation in the form and habits of the sexual cells. And it is among these algae that we may find material upon which to base general conclusions on the sexual evolution of plants. These processes are illustrated more or less completely by stages in several groups, but especially so in three lines of development which we shall use as the illustrative basis of this paper. They are the Volvocaceae, certain groups of the brown algae (Phaeophyceae) and the region of the green algae comprising the Ulothricaceae, Chaetophoraceae and Coleochaetaceae.
These three lines are very far removed from one another and must have become separated at an exceedingly early period of development, probably before the origin of sex and certainly before any extended sexual evolution. The Volvocaceae is an extreme side line, by which we mean that its higher members are very far removed from the theoretical main line of accent that runs through the algae to the next higher group of plants, the Bryophytes. The groups of the Phaeophyceae form a system of side lines very much more highly organized vegetatively than the Volvocaceae. The Ulothricaceae, Chaetophoraceae and Coleochaetaceae are the nearest of all algae to the theoretical main line of ascent, and some of their representatives are very close to this chain of extinct forms; it is, of course, too much to expect that any living alga should be actually one of the links. Each of these three series tells the same story of the general events of sexual evolution as do all other lines of ascent among the algae, fragmentary though some of them are.
We shall take up the Volvocaceae first. This is a peculiar family of plants, remarkable for the fact that the vegetative conditions are motile. Its highest member and a well-defined climax type is Volvox, one of the most highly specialized of the algae in its peculiar way. The lowest representatives of the Volvocaceae are unicellular (Chamydomonas, Sphaerella, etc.), and between these simple organisms and the complex Volvox there is a series of forms, all cell colonies (Gonium, Pandorina, Eudorina and Pleodorina), each more complex than the other as to the number, arrangement and degree of specialization of the cells. I know of no family of plants that illustrates so many important evolutionary principles as clearly as the Volvocaceae, and it might be made the subject of an interesting paper. But we are to consider now only the differentiation of the sexual cells.
The lower members of the Volvocaceae are mostly isogamous. In Sphaerella a large number of gametes (32-64) are formed in a mother cell. These sexual cells are quite similar in size and form, and when they conjugate no one could assert a difference in sex. Most species of Chlamydomonas resemble Sphaerella in having gametes essentially
similar (see Fig. 2, a), but there are forms in this genus presenting a marked advance. In Chlamydomonas Braunii[2] the gametes are of two sizes and the smaller always unite with the larger. However, both are ciliate and consequently motile, so that morphologically they are similar, although there can be no doubt of the sexual differentiation. It is not customary to call the female cell an egg until it has lost its free swimming possibilities and as a passive cell awaits the specialized motile sperm.
Pandorina, like Sphaerella, produces a large number of gametes, 16-32 in the mother cell, but here there is a considerable range of variation in the size of the sexual elements, although the form is always the same. Sometimes these gametes will pair, a small one with a larger (see Fig. 2, b), as in Chlamydomonas Braunii, thus showing the tendency towards sexual differentiation. However, there is no rule in this habit of Pandorina, for frequently gametes of equal size conjugate, and one can not assert that the larger cells are always destined to be female sought by smaller male elements. What determines the variation in size of the gametes in Chlamydomonas Braunii and Pandorina, and the consequent differentiation in sex? It. depends entirely on the number of gametes formed in the mother cells and on the size of the latter. The larger female gametes are formed less numerously and generally in larger mother cells and quently receive two to four times more protoplasma and food material than the smaller male gametes. This is an important distinction and fundamental to all sexual evolution. The differentiation of one of the gametes as the cell specialized to hold the greater part of the food supply marks the first step in the series of changes that follow.
Eudorina and Volvox are heterogamous. The eggs are large, the sperms highly specialized (see Fig. 2, c and d) and in all respects the differentiation of sex seems to be carried about as far as in any group of algae. The eggs are formed singly in the mother cell (oogonium), which means that all the protoplasm and all the food available is reserved for that gamete and this is a great advance over the lower types of the Volvocaceae. The sperms are produced abundantly in each antheridium, 64 in Eudorina and sometimes more than 200 in Volvox. Naturally one would expect the sperms to be minute and they are proportionally very many times smaller in relation to these eggs than the male gametes of Chlamydomonas are to the female.
The condition of heterogamy and its advance over isogamy is the result of several well-defined factors at work wherever sex is present. It is advantageous to specialize one gamete for the purpose of holding as much nourishment as possible, thereby providing well for the vegetative possibilities of the next generation. The most effective way to accomplish this end is to reduce the number of female gametes produced in each oogonium, and the best results will obtain when all the protoplasm from such a mother cell goes to a single female gamete. The absence of motility characteristic of eggs is an accompaniment of the increased food supply. It is a very natural condition and advantageous to the species. In the first place large cells can not move through the water as easily as small cells, and again most of the higher algae have the habit of retaining the eggs in oogonia, protecting them in that way for long periods and of course such eggs must naturally be quiescent. With respect to sperms the evolutionary tendencies are very easily understood. Relieve them of the responsibility of contributing much food material to the egg and it is obviously a great advantage to the organism that sperms be produced as numerously as possible, consistent with economy of energy. This demands the reduction in size of the sperm and also results in that high specialization of form so characteristic of motile male elements.
It is evident that all the factors work for the good of the species and are so vital in their bearings as to fall well within the sphere of natural selection. There are doubtless physiological principles taking part in the developmental processes of gamete formation, and at the higher levels of sexual differentiation important factors of heredity. But these have not been very clearly separated, except that the egg is commonly considered as lacking certain energy which is supplied by the protoplasm (kinoplasm) of the male cell. The sperm, on the other hand, while replete with energy, is ill supplied with nutritive protoplasm (trophoplasm) characteristic of the egg. The phenomenon of parthenogenesis and the recent work on artificial parthenogenesis in animal types show that the energy in the egg may be liberated and the wheels of development set in motion by the proper chemical and physical environment without the intervention of the sperm. But generally the sperm is required to start the egg into activity, and complete and normal development in most organisms probably requires fertilization.
Although most of the stages of sexual evolution are presented in the Volvocaceae, one important stage is there lacking which is especially well illustrated among the brown algae and in the Chaetophoraceae. This is the period of transition from the large free-swimming female gamete to the motionless egg, and covers that evolutionary forward step when the female gamete gives up its motility and the independence of its ancestor the zoospore and becomes the passive receptive egg.
The brown algae (Phaeophyceae) probably developed as an offshoot from the green algae (Chlorophyceae) at a level considerably above the unicellular forms. The lower members of this group are generally well developed filamentous types or more elaborately organized fronds of considerable thickness. Isogamy is general among the lower forms and heterogamy is characteristic of the highest groups (Fucales and Dictyotales). The sexual conditions among the lower groups are especially well exemplified in the genus Ectocarpus, whose species present a remarkable series of stages illustrating sexual evolution. The gametes are biciliate cells produced in peculiar types of gametangia which are modified branches whose cells become divided into an immense number of cubical compartments, each of which develops a single gamete. This type of structure is peculiar to the brown algae and is called the plurilocular sporangium or gametangium. It is one of the most interesting organs in the whole group of the Thallophytes because its structure throws light on the difficult problem of the origin of the archegonium.
Some species of Ectocarpus have gametes so nearly the same size as to be indistinguishable, but the genus as a whole is remarkable for certain variations in this particular. The plurilocular sporangia are frequently of three distinct sizes, and the zoospores that come from them vary accordingly. It is not always necessary that these zoospores from plurilocular sporangia conjugate in order to grow. There is a great amount of parthenogenetic development depending on environmental conditions that are in part understood. Thus cool temperature and bright illumination tend to suppress sexuality in these zoospores, making them neutral. In other words, sex in Ectocarpus is at such a low level of differentiation that its characteristics are still under the potent influence of external factors, and zoospores that will be sexual under certain conditions, e. g., high temperature, will germinate parthenogenetically if this environment is not present. Ectocarpus is then another illustration with Ulothrix and Hydrodictyon of that primitive state, considered in my former paper, when the asexual zoospore became the gamete under the influence of external factors.
But when the zoospores of Ectocarpus have sexuality there is a decided tendency for the smaller gametes to seek the larger more slowly swimming elements and fuse with them. The small gametes have, therefore, male characteristics, which is further shown by the fact that they are unable to develop parthenogenetically or, if they do so, grow into small plants much weaker than the normal.
Fig. 3. a, Ectocarpus siliculous, Female Gamete Surrounded by Male, Stages in the Fusion of Gametes. b, Ectocarpus secundus, showing the two sizes of the gametes; c, Cutleria mullifida, male and female gametes and gametangia. (a, after Berthold; b, Sauvageau; c Thuret.)
And now we may consider a habit peculiar to certain species of Ectocarpus which is of great interest as an important stage in the process of sexual evolution. It has been most thoroughly studied in Ectocarpus siliculosus. The female gametes of this species have a limited period of motility. They swim about slowly and shortly come to rest, attaching themselves. The male gametes are motile for a much longer time. While at rest the female gametes attract the males which hover around (see Fig. 3, a), with the result that one fuses with a motionless cell and fertilizes it. This is an exceedingly interesting condition and furnishes the last link in the chain of stages through which gametes pass in their sexual evolution. The gametes of Ectocarpus siliculosus are morphologically isogamous, i. e., both are biciliate cells similar in form when first set free from their respective gametangia. At the time of fusion, however, the condition is physiologically that of heterogamy, for the female cell is essentially a quiescent egg sought by motile sperms. There are species of Ectocarpus whose gametes have habits similar to siliculosus and which are also of two sizes (see Fig. 3, b), so that the resemblance to egg and sperm at the time of fertilization is very marked.
Another brown alga should be considered in connection with the forms noted above. Cutleria represents a family quite removed from the Ectocarpaceae and much more highly organized. The gametes differ greatly in size as do also the respective gametangia in appearance (see Fig. 3, c). The female gamete is exceptionally large and deeply colored, the male small and almost colorless. At certain seasons of the year (late summer and autumn on the coast of France and England) the female gametes germinate parthenogenetically. If sexual it moves about for a short time and then comes to rest, when it is fertilized as a quiescent cell. The conditions are then the same as in the species of Ectocarpus previously described.
Before leaving the brown algae, I am tempted to call attention to a very interesting condition in the group of the kelps (Laminariales). These forms are structurally very complex and are unequaled among the algae in size and luxuriance. But the zoospores of the kelps are never sexual, as far as is known, and the group is conspicuous as a wonderfully successful assemblage that has established itself in nature without the advantage of sexuality, which some biologists have supposed to be absolutely necessary for the high development of any group of organisms. The genus Caulerpa among the green algae presents a similar illustration.
We are now ready to examine certain groups of the green algae (Chlorophyceae). There are three families above the unicellular algae that are certainly nearer the main line of ascent than any other groups. They are related to one another and present an ascending scale in vegetative and sexual complexity. The Ulothricaceae, typified by Ulothrix, is the lowest group. They are isogamous and illustrate especially well the origin of sex as described in my former paper (Popular Science Monthly, November, 1901, pp. 70 and 71). The Chaetophoraceae are likewise isogamous, but sex is more firmly established in this group, and structurally its members (Drapanaldia, Chaetophora, Stigeoclonium, etc.) are much more elaborate than the forms of the Ulothricaceae. The Coleochaetaceae end the series with an heterogamous type of considerable complexity.
Among the Chaetophoraceae is the genus Aphanochaete (see Fig. 4), presenting one of the most interesting stages of sexual evolution and bridging over a very important gap. Aphanochaete develops its female gamete singly in a mother cell. It is discharged into the water surrounded by a delicate vesicle. The gamete, although very large, is ciliate. However, it moves about scarcely at all, and does not leave the vesicle. The sperms gather around the dissolving vesicle, and finally one pierces it and fuses with the female gamete. The fertilized egg immediately begins to turn on its axis and moves about in the water for a few moments and then settles down to rest. It is probable that the cilia remain on the egg for this short period of motility, but it is evident that the female gamete has entirely given up the free-swimming habit. But what is more important, the oogonium appears to deliver its gamete with reluctance, for it is not entirely freed from its investing membrane
until after fertilization. It would be but a small step for Aphanochaete to retain this female gamete in the oogonium as a motionless egg and thereby present the furthest extreme of heterogamy. Such a condition would place Aphanochaete very close to Coleochaete, which it strikingly resembles in some important respects.
The last form in this series of green algae is Coleochaete, the sole representative of the family Coleochaetaceae. Of all the algae this type probably stands the closest to the liverworts, not because its sexual organs are similar, but because it presents a sphorophyte generation resembling that of the lowest liverworts (Ricciales). Coleochaete is heterogamous, but its sexual organs can scarcely be compared with the archegonia and antheridia of the Bryophytes. These structures are to be related only with the greatest difficulty to the sexual organs of the algae, and probably not through any existing type of structure, unless it be the organ called the plurilocular sporangium.
There are several other groups of algae that confirm and illustrate in various particulars the principles of sexual evolution that we have traced in the three lines of development here described. The Siphonales duplicate the history in most of the stages. Isogamy with variation in the size of the gametes is found in several of the remaining groups. Heterogamy in its most extreme form is presented in such isolated types as the stoneworts (Charales), Oedogonium, Bulbochaete and Sphaeroplea. All these types stand as representatives of lines of extinct ancestry, whose sexual evolution must have passed through the stages that we have described.
The red algae (Rhodophyceae) do not enter into this discussion. They started with sexuality at an advanced stage of heterogamy.
Let us now briefly summarize with examples the steps in sexual evolution which we have discussed, beginning with isogamy, at the dawning of sex, and ending in heterogamy.
First Stage.—Isogamy with exactly similar gametes; the condition at the origin of sex. Exemplified by many of the lower algae, Hydrodictyon, Ulotlirix, Viva, Cladophora, etc., certain species of the lower brown algae and unicellular green.
Second Stage.—Isogamy with gametes similar in form but of different sizes, the female large and richly nourished, the male relatively small. Illustrated by species of Chlamydomonas and Ectocarpus, Bryopsis and the forms that also illustrate the third stage. An index to this condition is the differentiation of the gametangia with respect to the number of gametes developed. The female gametangium tends to reduce the number until a single egg takes all the material of the oogonium. The male gametangium increases the number of sexual products, becoming an antheridium that may develop numerous sperms.
Third Stage.—Isogamy in that peculiar form when the gametes are similar in form at the time of their discharge from the gametangia, but different at the time of fusion, because the female gamete becomes a motionless cell. Examples: Ectocarpus siliculosus and secundus and Cutleria multifida. This stage is the transition point between isogamy and heterogamy. Morphologically these gametes are isogamous; physiologically they are heterogamous.
Fourth Stage.—Heterogamy which has several grades in the degree of differentiation and specialization of the egg and sperm.
Fifth Stage.—The retention of the egg in the oogonium (female gametangium), a condition peculiar to but not at all universal among heterogamous higher algae. Illustrated by Oedogonium, Bulbochaete, Coleochaete, Sphaeroplea, Chara and Vaucheria. This stage would be developed quickly when once started, and a tendency in this direction is probably shown in Aphanochaete.