Cytology in its relation to taxonomy

T H E B O T A N I C A L R E V I E W VoI,. I I I JD'sY, 1937 No. 7

C Y T O L O G Y IN I T S R E L A T I O N T O T A X O N O M Y

EDGAR ANDERSON Missouri Botanical Garden, Washington University, St. Louis

Taxonomy and cytology study the same phenomena but from two very different angles. Cytology, or more properly karyology, con- cerns itself with the architecture of the germplasm ; taxonomy with the adult forms which result from germplasms. The relation between the two disciplines can be illustrated by means of a simple analogy. The two viewpoints are like the insight into a family of strangers gained from (1) meeting the members of the family on the street or (2) looking in their cellar windows. The analogy is quite precise; the first is essentially the method of taxonomy, the second that of cytology. There is a big element of chance in the additional information gained by means of the new approach. In the language of the analogy one sometimes learns nothing new about a family from looking in the cellar windows; on the other hand, one sometimes finds evidence which puts the family in an entirely new light and clears up points which had previously been mysteri- ous.

Continuing the analogy, it is sometimes difficult to see through the windows because they are small or dirty, as in the case of the I Iamamelidaceae where cytological examination is difficult (An- derson and Sax, 1935). In other cases, the windows are large and clear, as in the genus Tradescantia where the chromosomes are enormous and the reduction divisions are easy to find. In every case the two views supplement each other; the taxonomic observa- tions or the cytological data may be incomplete or partially in error, or one may be puzzled as to how the two sorts of information are to be reconciled, but there is no possible chance of real disagreement.

One of the simplest instances of the way in which cytological and taxonomic information supplement each other is provided by the American species of Tradescantia allied to T. virginiana (Ander-

335

336 T H E BOTANICAL REVIEW

son and Sax, 1936; Anderson and Woodson, 1935; Anderson, unpublished data). The basic sets of chromosomes in that group are practically indistinguishable from species to species by present cytological methods. Some of these tradescantias are diploids, that is, they have two sets of chromosomes ; other species are tetraploid, that is, they possess four sets; still other species have diploid and tetraploid races. These races are morphologically indistinguishable* but when separated by cytological means it is found that the tetraploids are, on the whole, a little larger, considerably stouter, a little longer-flowering, a little hardier, and a little easier to grow under varying conditions. That these differences operate in nature and are of taxonomic consequence is shown when the distribution of the diploids is compared wi th that of the tetraploids (fig. 1). The diploid species are of limited distribution arid even in those areas where they do occur are usually restricted to one particular

* And for that reason have been given no taxonomic designation.

FI6. 1. Relationship between polyploidy and geographical distribution in the American species of Traclescantia. Outer heavy line: maximum distribution of tetraploid species; inner heavy line: maximum distribution of diploid species; heavy cross-lined area: minimum distribution of diploid species. Centered about this same area are the known diploid areas of species elsewhere tetraploid: large dots, Tradescantia canaliculata; small dots, T. occidentalis; unbroken line, T. hirsutiflora; solid black area, T. ozarkana. The stippling and cross-hatching on the map itself are indicative of relative geological age. Data from Anderson and Woodson, Anderson and Sax, and Anderson (unpublished).

CYTOLOGY I N ITS R E L A T I O N TO T A X O N O M Y 337

habitat. By contrast, the tetraploid species and races have wide distributions and most of them have the ability to flourish under a variety of situations. By cytological methods, therefore, we can divide this group of closely related species into two categories, the diploid species and races, and the tetraploid species and races. Though they cannot be separated by orthodox morphological methods and, therefore, have been given no taxonomic designation, the diploids and tetraploids are so different physiologically that they fill somewhat different biological niches. The diploids are relatively invariable and most of them are extremely limited in distribution. The tetraploids are much more variable ; they occur under a greater variety of ecological conditions and have much wider distributions.

These same cytological facts may also be used in determining the center of distribution of this group of species. For simple genetical reasons, diploids may quite readily give rise to vigorous tetraploids but tetraploids seldom give rise to diploids and if these do occur they are prone to be weak. In those species which have both diploid and tetraploid races we therefore know that the tetraploids must have originated from the diptoids. Tradescantia occidentalis, to take a concrete example, is widely distributed throughout the Great Plains and eastern Rocky Mountains. I t is a tetraploid throughout most of its range, though there is a small area in central and eastern Texas where a diploid race is found. On cytological and genetical grounds we know that the ancestors of these diploids must have given rise to the tetraploids, which in comparatively recent times have greatly extended the range of the species. I t is, of course, con- eeivable that the diploids might since then have moved about considerably and the tetraploids did not actually spread out from this particular area. Such an argument is refuted by data from T. ozarkana, T. canaliculata and T. hirsutiflora, three other species which possess both tetraploid and diploid races. Tradescantia canaliculata forms the most effective comparison with T. oeciden- falls since the former reaches its southwestern limit in Texas while the latter is there at the southeastern extremity of its range. Never- theless, the diploid races of these two species occupy almost the same identical territory, suggesting that it was from this actual area that T. occidentalis tetraploids moved out over the Great Plains and T. canaliculata tetraploids, to the Mississippi Valley. This conclu- sion is strengthened when one finds that the two other species, T.

338 T H E BOTANICAL R E V I E W

hirsutiflora and T. ozarkana, exhibit the same tendency. Even more impressive is a comparison of this diploid area of species elsewhere tetraploid with the distribution of the species which are purely diploid (fig. 1). Using the method described by L. B. Smith (1934), the minimum area of the diploid species was determined. I t is a narrow belt running from the Edwards Plateau in central Texas to the southwestern edge of the Ozark plateau in northwest- ern Arkansas. The diploid races of the four species mentioned above are centered upon this area, which from geological evidence is known to have been continuously habitable for land plants since very ancient times. Cytology, therefore, brings a new kind of evidence to join with that from geology and from geographical distribution. The combination of all three suggests very strongly that this area in the southwest was the immediate center from which the American tradescantias have developed in comparatively recent times. In this particular group, cytology, though of no assistance in discriminating between species, has given useful and unique information. I t has shown that these species are made up of two physiologically different elements, the diploids and the tetraploids. It has, furthermore, given positive and independent evidence as to their center of distribution.

The case of these American tradescantias has been outlined in such detail because it is not an isolated instance but is certainly typical of very many genera of flowering plants. In a recent comprehensive survey of the phenomenon, Mfintzing (1936) sum- marizes fifty-eight instances in which races differing in the number of sets of chromosomes have been discovered within the same species. In all cases, the morphological differences between these races was slight; sometimes, as in the case of Tradescantia, too slight to merit taxonomic recognition; occasionally it was worthy of varietal or even sub-specific rank. In all these genera, however, the same sort of difference existed as in Tradescantia. Under controlle~t experimental conditions the races with multiple sets of chromosomes (hereinafter referred to as polyploids) were somewhat larger, thicker, darker green, slower growing, hardier, and had less conservative distributions.

From the standpoint of floristics the most interesting case which has yet been reported is that of BiscutelIa lae~gata, a European crucifer studied by Manton (1934). By cytological analysis carried

CYTOLOGY I N ITS RELATION TO TAXONOMY 339

on in collaboration with the most recent monographer of the genus (Machatschki-Laurich, 1926), Manton demonstrated that this species is made up of two very different elements: (1) the diploids, a series of rare, more or less isolated, pre-glacial or inter-glacial relicts along the river valleys of central Europe, and (2) vigorous, aggressive tetraploids, occurring mostly on floristically youthful territory which was covered by the Alpine ice sheet during the Gla- cial Period. Similar though less detailed reports have been given for American Cactaceae by Stockwell (1935), for Chrysanthemum by Shimotomai (1933), for Phleurn by Miintzing (1935), for Em- petrum by Hagerup (1928) and for Crepis and related genera by Babcock (1936).

In the cases reported above, the polyploids were the result of duplicating the same basic chromosome set, and they are accordingly known as auto-polyploids. Much more dramatic changes are brought about by the duplication of more or less unlike sets of chromosomes, a phenomenon known as allo-polyploidy. Though it is known to occur in nature, the clearest demonstration is provided by a cultivated house plant. Primula kewensis originated in England as a sterile hybrid between an Abyssinian species of Primula and one from the Himalayas. It was attractive and winter-flowering and so, in spite of its sexual sterility, was propagated vegetatively. Eventually on several different occasions plants of this sterile hybrid gave rise to vigorous fertile branches whose seed, in spite of the plant's hybrid origin, bred true to type. Cytological study provided a simple explanation of the phenomenon. Each of the parent species had nine pairs of chromosomes. The sterile hybrid, as we would expect, had eighteen chromosomes, nine from each species, but they were too unlike to pair and form fertile gametes. The fertile branches, however, had just twice the number of chromosomes, thirty-six per cell; they had originated when a nuclear division had not been followed by a cell division and from the resulting giant cell there had grown out an allo-polyploid branch with two full sets of chromosomes, that is, two of each of the parental species. It could, therefore, form germ cells in a substantially normal fashion and was fertile and true-breeding. Primula kewensis is only one of a very large number of cultivated plants which are now known to have originated through allo-polyploidy (Schiemann, 1932).

340 T H E B O T A N I C A L R E V I E W

The phenomenon is, however, not limited to cultivated plants. Miintzing (1936) has presented convincing morphological evidence to show that Galeopsis Tetrahit, a tetraploid European species, is an allo-polyploid derived from two other European species, both diploids. He has, furthermore, been able to prove his working hypothesis by actually synthesizing a duplicate of Galiopsis Tetrahit from the putative parental diploids.

Doubling of chromosome numbers in hybrids can take place quite as well when the parental stocks differ in their chromosome base number. To cover all such cases of fertile, true-breeding hybrids, resulting from doubling of the chromosome number, it is convenient to have a general term. While others have been suggested, the only one in general use is amphidiploid (Goodspeed, 1934).

One of the most interesting cases of amphidiploidy under natural conditions is that of Spartina Townsendii, a phenomenal inhabitant of north European estuaries and foreshores. Though it is known to have originated in modern times, it has within the last century not only spread widely but h~s produced a profound effect upon other coastal florae and faunae. Huskins (1931) has shown that its high chromosome number (126) is exactly what we would expect if Spartina Townsendii were an amphidiploid derived from the European Spartina stricta with fifty-six chromosomes and the American Spartina alterniflora with seventy. Since such an origin had previously been suggested from morphological evidence alone, the hypothesis, while, of course, still unproved, becomes increasingly probable.

Clausen (1933) and Keck (1932) have described an interesting case of amphidiploidy in Pent~temon, which will be even more sig- nificant when their combined taxonomic and cytogenetic study of that genus is published in full.

One of the most convincing cases of amphidiploidy is that of the American beardless irises, Iris versicolor, Iris setosa and Iris virginica. Anderson (1936) has shown that Iris versicolor has ~the chromosome number (108) which we would expect if it were an amphidiploid derivative of Iris setosa with thirty-eight chromosomes and Iris virginica with seventy. Iris versicolor is, furthermore, morphologically intermediate between the two putative parental species, though much closer to Iris virginica than to Iris setosa, as might have been predicted, since Iris virginica contributes nearly


twice as many chromosomes as Iris setosa and might, therefore, be expected to preponderate in the characters of the offspring. Iris virginica, furthermore, is centered upon a floristically ancient area in the southern United States and Iris setosa, the other supposed parent, has long been recognized as a typical glacial relict in the north (Femald, 1925). The theory harmonizes so many otherwise incoherent facts from cytology, genetics, morphology, geographical distribution and glacial geology that it is at least well-established as a working hypothesis.

Amphidiploidy has a number of effects of taxonomic consequence. One of the most important is its effect upon the phylogenetic (and hence the morphological) relationships between species. An attempt is made to demonstrate this point diagrammatically in figure 2 which shows the course of phylogenetic development in a genus with and without polyploidy, on the simplest possible assumptions. The course of evolution is shown in the lower part of the figure. The species, as we see them at the present time, are the separate strands which run across the top of the figure. In

7,,, :ii,il FIG. 2. Phylogenetic relationships with and without amphidiploidy.

Branched figures at the base represent hypothetical development from three original stocks. Short figures above represent existing species and varieties. Numbers refer to number of basic sets of chromosomes (2=diploid; 4 = tetraploid ; 8 = octoplo~d). Further explanation in text.

342 T H E BOTANICAL REVIEW

the absence of polyploidy it is possible from morphological analysis alone to recognize that there are three separate stocks involved, the globular, the crossbar and the pubescent. By a careful inspection of differences within these three stocks it would even be possible to construct a hypothetical phylogenetic tree which would be very close to the actual history presented in the diagram below. With polyploidy, however, the distinction between the three original stocks is broken down. The morphological resemblances and differences between the species as we see them at present are reticulate and an attempt to reconstruct the course of phylogeny on a simple den- dritic pattern would lead to gross error. For instance, were the difference between globular and oval species to be considered fundamental, one would have to hypothecate the parallel development, in both groups, of crossbarness and pubescence. If one, however, is provided with the chromosome numbers, as at the top of the diagram, it would be possible to reconstruct a substantially accurate phylogenetic diagram. The diploids would be recognized as fundamental and the tetraploids as derived from them, and the octoploid as originating from the tetraploids. In genera where there is no more amphidiploidy than in this diagram, it should be possible by a combined cytological and genetical attack to work out such phyloge- nies with a fair degree of accuracy. A number of such projects is already under way,, and preliminary reports have been made on a number of interesting cases (Babcock, 1936; Goodspeed, 1934; Skovsted, 1934).

The genera and families of the flowering plants will, therefore, differ greatly in their fundamental phylogenetic patterns according to the prevalence of amphidiploidy. There are whole families, such as the Cyperaceae, in which it has not been found, in spite of intensive search (Heilborn, 1924, 1932; Hicks, 1928; Hakansson, 1928). There are many genera in which it is wholly absent, or in which it is at least exceedingly rare, as for instance Rhododendron (Sax, 1930) and Ouercus (Sax, 1930). There are other genera in which it is about as common as in diagram 2, for example, Iris (Simonet, 1929, 1934). There are genera and families in which it is much more common. To this extreme group belong many of the Gramineae, the Solanaceae, the Labiatae, and above all the Malvaceae. Polyploid relationships reach such a complexity in many genera of that latter family, as in Sphaeralcea (Webber,


1936), that it is no wonder that taxonomists have been in puzzled disagreement as to generic and specific limitations and relationships. The interested reader is referred to the indices of Tischler (1935-36) and Gaiser (1930) where reports of chromosome numbers for the angiosperms are summarized by families and genera. I t is not possible from the mere report of chromosome number to know whether the polyploidy reported is auto-polyploidy or allo-polyploidy. Each, however, is an exceedingly common phenomenon. It is already safe to say that at least half the species and varieties of the flowering plants belong to polyploid series (Miintzing, 1936).

Chromosome number (or base number in the case of polyploid series) sometimes varies within the species, though such cases are rare. Occasionally, it is different in closely related species, as for instance in the genus Scirpus (H~kansson, 1928; Hicks, 1928). Much commoner is such a genus as Crepis or Viola in which the number varies within the genus but in which the related groups of species have the same chromosome number. Sometimes it is a character of even greater stability, as in the Pomoideae where only one base number (17) has been found in the entire sub-family (Sax, 1931). Chromosome number reaches its greatest stability in the gymnosperms (fig. 3) where the base numbers 10, 11, 12 and 13 are the only ones yet reported for the entire Coniferales, and the great majority of the genera belong either to a 12 series (Taxa- ceae and Abieteae) or an 11 series (Taxodieae and Cupresseae) (Sax & Sax, 1933).

The taxonomic usefulness of information about chromosome number and the purposes to which this information can be put will, therefore, depend upon its stability in the particular group which is being studied. Babcock (1936) has found it useful in clarifying the relationships of Crepis with related genera. One of the most interesting cases reported to date is Whitaker's work (1933) on the Magnoliales and their allies. It will be remembered that here are included such families as the Magnoliaceae, Winteraceae, Schi- zandraceae, Trochodendraceae and Cercidiphyllaceae. They form a more or less natural group with certain obvious interrelationships. They are certainly very ancient and include such curious missing links as Trochodendron and Tetracentron. Whitaker was able to show that the genera he studied in these families fall into two series, a 19 series and a 14 series. These two groups, though some-


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what different from the arrangements of previous students (no two of whom have ever been in complete agreement), were, neverthe- less, in accord with I. W. Bailey's unpublished evidence on nodal anatomy and with Wodehouse's (p. 331, 1935) pollen morphology. His evidence is particularly convincing, partly because the number 19 is so rare as a base number, and partly because Whitaker's grouping is in harmony with the known morphological facts.

CYTOLOGY IN ITS RELATION TO TAXONOMY 34S

Cytology sometimes gives decisive evidence on disputed taxonomic questions. Students of the Boraginaceae, for instance, have not been in agreement as to the proper disposition of Brunnera ~nacrophylla, some holding that it well merited generic recognition (Johnston, 1924), others believing that it belonged in the genus ,4nchusa. Smith's (1932) cytological study shows very clearly that Johnston and Stevan were right in recognizing Brunnera as a distinct genus. Cytology in this case not only demonstrates that the chromosomes of Brunnera are distinct from those of .4nchusa; the difference is of quite another order of magnitude than that found within the latter genus. Since S. G. Smith did not discuss

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Fxc. 4. Diagram of chromosome morphology in Anchusa and Brunnera, showing chromosome number, size, and position of attachment constrictions and satellites. Redrawn diagrammatically from Smith's published figures.

the evidence in detail and since Wright Smith (1933) has subse- quently questioned the weight of the cytological evidence, the original figures have been redrawn diagrammatically but to scale and are shown in figure 4. One set of chromosomes is shown for each of four species of Anchusa and for Brunnera macrophylla. It will be seen that there are three kinds of differences between Anchusa and Brunnera: (1) size; (2) number, Anchusa having eight as a base number, Brunnera having six; (3) morphology, Brunnera having two chromosomes with sub-terminal attachment constrictions (in addition to the chromosome with a satellite) while there are no such chromosomes in Anchusa, which also has two to three with median or sub-median constrictions though there is only


one in Brunnera. A triple difference of this magnitude within a genus would be extremely rare among the angiosperms. For the Boraginaceae, which are relatively conservative in such matters, a cytologist would confidently predict that Anchusa and Brunnera could not even be neighboring genera.

A similar instance is provided by McKelvey and Sax's (1933) discovery that Yucca and Agave with a few related genera have identical chromosome complements, an arrangement of five very large and twenty-five very smaU chromosomes, so distinctive that it is unthinkable that it could have arisen independently in both the Liliaceae and the Amaryllidaceae. Cytology, therefore, offers strong evidence in favor of Hutchinson's (1934) treatment of these genera as a distinct family, the Agavaceae. The cytological evidence might be carried even further to indicate relationships between the Agavaceae and other families of the monocots. Whitaker (1934) has already presented a preliminary discussion and further facts (though without comment) have been presented in such sum- maries as that of Matsuura and Suto (1935). Hutchinson's stimu- lating work has shown what radical changes may be necessary if we are to have a natural classification of the monocots. The time is ripe for some qualified investigator to undertake a comprehensive study of their generic and family relationships, utilizing the facts from morphology, geographical distribution and cytology.

It is difficult to set limits to the eventual usefulness of cytology in discriminating between species and genera. With advances in technique it has been possible to add such gross features of chromosome morphology as the satellites and the position of the attachment constrictions to the bare facts of chromosome number. In certain insects it is now possible, by means of the salivary gland technique, to examine the fine structure of the chromosomes. Bauer (1936) has shown how relationships in a whole family, the Chironomidae, may be studied by this technique and he has already made a begin- ning at assembling the necessary data. Dobzhansky (1937) has shown that not only can closely related species be effectively diag- nosed by this technique (Dobzhansky & Tan, 1936), but that morphologically indistinguishable races within the same species may be readily identified. He has even been able to plot the geographical distribution of races within the species and, what is even more important, to demonstrate beyond a reasonable doubt the developmen-

CYTOLOGY IN ITS RELATION TO TAXONOMY 347

tal sequence of these intra-specific races. With the rapid advances which are taking place in plant cytology it should not be long before similar studies will be possible in plant material.

Even with the relatively crude data already at hand there is a very large number of genera of the flowering plants where cytological data would be a useful guide to taxonomic relationships if carefully determined and used in conjunction with other evidence. Wright Smith (1933, p. 181) has discussed the cytological evidence obtained by Brunn (1932) for the genus Primula in the light of his own taxonomic studies in that genus. He concludes that in mono- graphic studies "the last word lies with the morphology. But I can record without hesitation my obligations to the cytologist. His con- tribution has been of the greatest interest and value. But only by marshalling all the data, morphological and cytological, can a final judgment be made."

With Wright, Smith's general position (see also Smith, 1936) that cytology merely contributes another bit to the sum total of morphological facts, the reviewer is in complete agreement, in so far as purely morphological contributions of cytology are concerned. Cytology is unique, however, in that it may indicate not only a difference between species or groups of species but may also demonstrate the way in which these differences came about. It is evidence as to the architecture of the very germplasm itself and is, therefore, of more fundamental importance than the mere architecture erected by that germplasm. Cytological evidence, therefore, can do more than discriminate between species ; it can illuminate species.

Any monographer who has had intensive experience with more than one or two families of plants knows that there are character- istic peculiarities of relationship in different families and genera. The sharpness of genera, the morphological relation of one species to another, the degree to which genera can be divided and sub- divided in clear-cut natural groups, are matters in which there are wide differences between certain of the families of the flowering plants, as for instance between the Cruciferae, the Liliaceae, the Malvaceae and the Orchidaceae. In other words, the very pattern of evolution differs from group to group. Cytology is of importance to taxonomy because it is already able to diagnose certain causes of these differences in the pattern of evolution. It is already able to discuss authoritatively such matters as reticulate phyloge-

348 TI3[E BOTANICAL REV~IW

tries, which had previously been perceived by only the most acute taxonomists and about which there is not yet any general agreement among taxonomists. Wi th the rapid advances in cytological technique which are taking place at the present time, it will not be long before cytology is able to play an even more important r61e in separating special, factors from general factors. The cyto-taxono- mist of the future, after a few routine examinations, will be able to estimate for a systematist, in advance of the morphological information, the probable evolutionary pattern in the genus or family he is about to monograph. He will, furthermore, supply the key to such puzzling problems as the Pomoideae, the Malvaceae, the genus Agropyron, or the genus Festuca. These are typical examples of many groups of flowering plants which in the opinion of the reviewer cannot be adequately monographed without correlated cytological and taxonomical research. Such pioneer work as Erlanson's on Rosa (1933) and Ruttle's on Mentha (1931) has demonstrated the absolute need of cytological information in the taxonomic inter- pretation of critical genera.

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Cytology in its relation to taxonomy