GENETICS 12: 307-339. Jl 1927
Studies on the Genetics of Fragaria
A. J. Mangelsdorf and E. M. East
Harvard University, Bussey Institution, Forest Hills, Boston, Massachusetts
Received September 29, 1926


Few cases of anomalous inheritance are cited more frequently than the Fragaria hybrids of MILLARDET. In fact, it was the exceptional nature of his results that led to our re-examination of the behavior of species hybrids in this genus.

MILLARDET'S investigations, carried on at Bordeaux, where he occupied the botanical chair on the Faculté des Sciences, were begun in 1883 and extended over a period of eleven years. The thesis to which his observations led him is concisely stated in the introduction to his paper in the following words:

'Dans son important ouvrage sur l'hybridation des végétaux, Gärtner formule cette loi que "nous ne connaissons aucun cas où le type d'une des espèces composantes d'un hybride ait passé intégralement dans cc denier'. Tous les physiologistes qui se sont occupés d'hybridation, avant comme après lui, ont partagé cette même opinion. Mon intention, dans ce travail. est de démontrer que dans le genre Fraisier (Fragaria) les produits obtenus par l'hybridation de certaines espèces font exception à la règle générale qu'on vient de lire. Ils reproduisent intégralement le type spécifique du père ou celui de la mère, et ressemblent par conséquent exclusivement soit à l'un, soit a l'autre, sans réunir jamais à la fois aucun des caractères distinctifs des deux espéces composantes."

The results of the crosses upon which he bases his conclusions will be discussed in the order in which he presents them.

The first cross described is one in which "Fraisier des quatre saisons blanc" is used as the female parent and "Chili velu" is used as the male parent. The female parent, according to his description, is F. vesca, variety alba; the male parent is an hermaphroditic variety of F. chiloensis He obtained 4 hybrids, of which 1 resembled the female parent in every respect except that the fruit was red; the others resembled the male Parent "from which it was almost impossible to distinguish them."

The vesca group, to which the female parent belongs, has 7 pairs of chromosomes; F. chiloensis, the male parent, has 28 pairs. In our own progenies from crosses between these two groups there have appeared individuals which displayed a marked dominance in F1 of the 28-chromosome type over the 7-chromosome type. The dominance is not complete for every character, certain features such as flower form, for example, being intermediate between the two parents; but that MILLARDET should have seen in these three plants a "reproduction du type specifique paternel" is not surprising.

Even in the absence of other evidence, it is fairly safe to conclude from the partial sterility of these three plants that they are true hybrids.

"Les fleurs en sont grandes, hermaphrodites, mais a étamines assez peu dévelopées. Les anthères sont a peu près normales ainsi que le pollen. Toutes trois sont fertiles, mais médiocrement."

Our own hybrids between these two groups have thus far proved to be completely sterile. RICHARDSON (1918), however, obtained a slight degree of fertility in hybrids between F. vesca and F. virginiana, a cross involving the same chromosome numbers as the one under discussion.

The progenies of these 3 plants gave further evidence of the hybrid sterility which is to be expected in crosses between the 7-chromosome and the 28-chromosome group. Thus sowing "R" produced 2 plants "du type chiloensis pur. Ces plantes ont toujours été infertiles. Étamines et anthères peu développées. Pollen imparfait ou nul." MILLARDET stresses the fact that the plants are "paternal" in type, their sterility he evidently considers incidental and of no particular significance.

Several other sowings were made from these 3 plants, mostly from open pollinated seed. MILLARDET emphasizes the fact that in none of these progenies was there to be found the "slightest trace" of vesca characters. No conclusions can be drawn from these progenies since the pollen parents are unknown. If the pollen were supplied by one or more species of the 28-chromosome group, the vesca characters would again be covered up.

Let us return to the first of the 4 hybrids which MILLARDET describes as being "exactement semblable a la mère, sauf les fruits, qui sont rouges." The fact that this plant was red-fruited, while its mother was white-fruited does not trouble MILLARDET. In speaking of this family in another place, he says "dans l'exemple 1, sur quatre hybrides, tandis que trois reproduisalent le type du père, un reproduisait celui de la mère, avec cette variante sans importance que les fruits au lieu d'être blancs étaient rouges." (The italics are our own).

It will be recalled that fruit color in F. vesca depends upon the interaction of a single pair of factors, white being recessive to red. Red fruited individuals have the constitution RR or Rr, white-fruited, rr. The appearance of a white-fruited individual in the progeny of a red-fruited plant might be explained without much difficulty since the mother could have been heterozygous for the R factor; in such a case white-fruited offspring resulting from the parthenogenetic development of reduced eggs would have been at least a theoretical possibility. Even mutation as an explanation might have some plausibility if the change had been from red to white, for loss of color is rather common in plants; but there are few cases in the literature of white mutating to color. Apparently the reaction is not easily reversible.

Assuming that the plant is really of the parentage which MILLARDET assigns to it, only one explanation suggests itself for the red-fruit color (except the improbable one of mutation). Had it received the full complement of 28 chromosomes from its male parent, F. chiloensis, it would have shown the dominance of chiloensis characters, as did the other three members of the progeny. ICHIJIMA (1926) has found that at the reduction division of the hybrids between the 7-chromosome and 28-chromosome groups, 7 bivalents and 21 univalents can be distinguished. It appears that the 7 vesca chromosomes pair with 7 of the 28 chromosomes from the other parent, leaving 21 unpaired. It is conceivable that at the first division following the fusion of the male and female nuclei the unpaired chromosomes might be left behind, resulting in an individual with 7 pairs of chromosomes, like the female parent in appearance but having red fruit. That a plant receiving such a complement of chromosomes would appear vesca-like is purely an assumption, nor is there any evidence on the question as to whether the unpaired chromosomes might be left behind at the first division of the newly formed zygote, as postulated.

There is, however, a bit of evidence which might lend credence to the possibility. The F1 individuals resulting from species crosses of this type are extremely variable, ranging from vigorous plants entirely normal in appearance except for their sterility, to tiny dwarfs which can be kept alive only with difficulty. Varying degrees of chromosome elimination might conceivably bring about such results as those which MILLARDET obtained. But since no case has been found agreeing in every detail with that of the plant under discussion, the likelihood that the explanation suggested is the correct one appears to be very remote.

It seems much more probable that this red-fruited vesca plant is the result of one of several possible forms of contamination. The seed may have been present in the soil in which the sowing was made, F. vesca with the red fruits being the common wild strawberry of France. MILLARDET states that all sowings were made in "terre de bruyère" procured directly from the forest. This practice may have reduced the danger of contamination from foreign seed, but it certainly cannot have removed it entirely.

Another possible source of error comes from trespassing runners. Unless the plants are kept constantly under observation a runner from neighboring plant may, in a very short time, become established on the spot left vacant by the death of the original plant, and once the connection of the intruder with its parent is broken, as usually happens when the bed is cultivated, the evidence as to its origin is destroyed. A third and most probable source of contamination is that of wind-borne pollen. MILLARDET recognized the possibility of contamination from this source but apparently he did not regard it as serious. He describes the cages used to protect the plants as being "garnies de tulle, et quelquefois même de mousseline très fine, de manière a empêcher complètement non seulement l'accès des insectes, mais aussi, lorsqu'elles étaient couvertes de mousseline, la pénétration du pollen étranger qui aurait pu être apporté par le vent."

Certainly the cages which were covered with tulle offered practically no protection, and it is questionable whether those covered with muslin would exclude entirely pollen grams as small as those of Fragaria.

Most of the remaining crosses reported by MILLARDET present difficulties of interpretation similar to those just discussed. It is hardly desirable to consider each cross in detail. The results which he obtained will be briefly set down, however, as a matter of record.

"La plante est vigoureuse et fleurit abondamment. Les fleurs sont petites (de la grandeur des fleurs femelles de Virginiana et Clziloensis), a étamines atrophiées et a anthères de couleur sale, ne contenant pas de pollen. Comme la plante s'est toujours montrée stérile, on doit en inférer que ses ovules DC. sont pas en meilleur état que les anthères. Dans cet exemple, l'hybridation a reproduit le type spécifique paternel sans aucun mélange des caractères du type maternel, mais il y a impuissance complète tant des organes femelles que des mâles."

The plant is obviously a true hybrid with the characters of the 28-chromosome species dominant, as is usually the case in crosses between these two groups.

This plant, like the one in the preceding cross, is undoubtedly a true hybrid with dominance of the paternal characters.

Open pollinated seed from these hybrids gave, besides maternals, 2 plants of the 28-chromosome type, which presumably was due to the dominance of the characters transmitted through pollen from plants of that type. In addition 1 plant showing pure vesca characters appeared. Contamination in the seed pan or the trespassing of runners is the only explanation that can be offered for this plant. CORRENS (1901) comments on it thus:

"Ich weiss erst seit ein paar Wochen privatim, durch die Liebenswür- digkeit MILLARDET'S, dass sich hier ein Irrthum eingeschlichen hat.... Es waren mit der zur Cultur verwandten Haideerde Samen der wilden Fragaria vesca eingeschleppt worden. Herr Professor MILLARDET hat mir gütigst erlaubt, dies zu veröffentlichen."

One may sum up MILLARDET'S results as follows: He made many crosses between different species of Fragaria using methods of control which are satisfactory for most plants, but which we have found unsatisfactory for Fragaria where the pollen is extremely small. He dealt with general resemblances in species which differ from each other by rather vague quantitative characters, and was not impressed with minor, individual characters, with dwarfness, or with sterility, as genetic evidence. Many of his populations came from open-pollinated plants. Some of the aberrant plants which appeared, therefore, almost certainly resulted from pollen, seed, or runner contamination.

In addition, there are two phenomena to be explained. In the first place, many plants appeared which were of the type of the female parent. These maternal plants may have resulted either from accidental pollination with pollen of the same general type, or from pseudogamy. We are not prepared at present to accept either alternative to the exclusion of the other, but it cannot be denied that on general grounds pseudogamy is a possibility. In addition, there are four cases where individuals were obtained which resembled the male parent, excluding two instances of open pollination where the male parent was unknown. In two of these cases, F. vesca X Globe and F. vesca X Ananas (7-chromosome type X 28-chromosome type), the exceptional individuals, two in number, showed their hybrid nature by being completely sterile. The other two cases were F. vesca X F. chiloensis (7-chromosome type X 28-chromosome type) and F. elatior X Globe (21-chromosome type X 28-chromosome type). In each instance these plants showed their hybrid nature by greatly reduced fertility. They did indeed yield a few F2 progeny from open-pollinated seed, which were somewhat variable, but which in general resembled the plants of the F1 generation. These results, therefore, show only the dominance of the type with the higher chromosome number which is usually to be expected when plants are crossed which have markedly different chromosome numbers, and the unequal distribution of characters which naturally occurs under such circumstances. On the other hand, the case where the 28-chromosome type dominates the 21-chromosome type is in direct opposition to our own results. In our experience, the characters of the 21-chromosome type dominate the characters of the 28-chromosome type as well as the characters of the 7-chromosome type; but this is contrary to the experience of investigators on other genera with crosses showing analogous chromosome differences.

The results obtained by SOLMS-LAUBACH (1907) have been cited more than once as confirming the conclusions of MILLARDET. Indeed, it appears that SOLMS-LAUBACH himself believed that such was the case. He speaks of his findings as being "in schönster Uebereinstimmung mit den Ergebnissen jenes Autors."

SOLMS-LAUBACH made several crosses between a pistillate form of F. Virginiana as the female parent and F. elatior as the male parent. The heavy pubescence, the shape of the leaves, their light, slightly greyish green color, their deeply impressed venation and the general growth habit of F. elatior have proved in our own crosses to be almost completely dominant over the corresponding characters in F. virginiana. SOLMS-LAUBACH obtained a similar result, his experience being therefore different from that of MILLARDET.

"Aus den Samen der F. virginiana war also hier fast ganz reine elatior (moschata) auf gegangen, es war 'fécondation sans croisement' in schonster Form eingetreten."

The plants which result from crosses between these two species are completely or almost completely sterile; SOLMS-LAUBACH observed the fact but appears to have attached no significance to it.

It is obvious that here again we are dealing with true hybrids showing a dominance of the paternal type and displaying the sterility characteristic of hybrids between species differing in their chromosome numbers.

GIARD (1903) interprets the patroclinous hybrids of MILLARDET as having a basis similar to that of the development of spermatozoa in enucleated sea urchin eggs as observed by BOVERI (1895) and DELAGE (1899). This hypothesis is almost certainly incorrect. ICHIJIMA (loc. cit.) has made chromosome counts on several of such patroclinous hybrids and finds that they contain the sum of the haploid numbers of the parental species, indicating that the nuclei of both hybrids participated in the formation of the zygotic numbers.

The matroclinous plants which constituted a large part of most of MILLARDET'S progenies GIARD believes have resulted from a parthenogenetic development of the egg, induced by stimulus from the foreign pollen tube. They may have originated in this way, but it must be kept in mind that they may also have resulted from accidental selfing. In our own crosses between different species, diploid individuals of the maternal type have appeared from time to time. Furthermore, apogamy is a regular occurrence in other Rosacee, notably in Rosa (TACKHOLM, 1922 and LIDFORRS, 1914). It seems significant, however, that with the adoption of more rigorous measures to prevent contamination, such individuals have appeared less and less frequently in our cultures.

The most recent reference to the work of MILLARDET is that of LONGLEY (1926). He describes the results of a cytological study of various Fragaria forms, among them one matroclinous and one patroclinous hybrid, which he apparently believes afford further evidence in favor of MILLARDET'S assumption that a unique form of inheritance obtains in Fragaria.

The matroclinous plant appeared in the progeny of a cross between F. vesca (7-chromosome group) and F. chiloensis (28-chromosome group). This plant was found by LONGLEY to contain 7 bivalent chromosomes the same number as in the female parent. This observation, however, throws no light on the question as to whether such plants have resulted from parthenogenesis or from accidental selfing.

The second plant appeared in the progeny of a cross between F. vesca var. alba (7-chromosome group) and the cultivated variety Aroma (28-chromosome group). It resembles the male parent morphologically, and was found by LONGLEY to have the same chromosome number. Neither of these facts is particularly significant in establishing whether the plant is actually the product of the cross from which it is supposed to have originated. Here again the question arises as to whether the sowing was made in sterile soil, and whether the plant was kept constantly under observation from the seedling stage until maturity. Nevertheless, the possibility that the chromosomes of the female may somehow be lost at the fusion of the two gametes, resulting in an individual which duplicates the male parent, is certainly not to be excluded. The Tripsacum-Euchlaena hybrid of COLLINS and KEMPTON (1916) which, both in appearance and in three generations of breeding, showed no trace of any of the characters of the female, appears to furnish an example of some such phenomenon.


Fragaria species having the same number of chromosomes cross freely, yielding perfectly fertile hybrids in which segregation takes place in the normal manner. Typical segregation in sex manifestations was observed in crosses between 28-chromosome species, while normal segregation of two independent pairs of allelomorphs, pink flowers and white flowers and red fruit and white fruit, was observed on fairly large populations in crosses between 7-chromosome species.

Crosses in which F. elatior, the 21-chromosome species, was used as the female and 7-chromosome species as the male, resulted in failure. In the reciprocal crosses, fruit set readily; but the seeds showed only about 0.7 percent germination, and the few seedlings obtained died within two weeks.

Crosses in which the various 28-chromosome species were used as the female and the various 7-chromosome species as the male also failed; but reciprocal crosses were made without difficulty. Many of the achenes were poorly developed and germination was low. Three types of plants appeared in the F1 generation; vigorous hybrids showing a more or less complete dominance of the 28-chromosome type, dwarfs which did not flower, and maternals. The hybrids were completely sterile.

A pistillate individual of the 28-chromosome group set fruit readily with pollen from F. elatior (21-chromosomes). The seeds germinated well (90 percent). The plants were variable in vigor, but showed a striking dominance of the F. elatior characters. They were completely sterile. Maternals were also obtained.

The flowers of 7-chromosome species set fruit readily with pollen from Duchesnea indica (42 chromosomes). From 500 seeds, 30 plants were obtained. Of these 24 were small, weak hybrids; the remainder were maternals.

Two seedlings were also obtained from F. vesca (7 chromosomes) flowers fertilized with the pollen of Potentilla nepalensis.

Though rare cases of parthenocarpy were observed, pseudogamy was not induced by treatments given, unless the maternal individuals appearing in the crosses between species differing in chromosome number are such. These maternals have the diploid number of chromosomes characteristic of the species involved, and may result either from induced parthenogenesis (haploid development) with a doubling of the chromosomes during early development, or from induced apogamy (diploid development). But since the pollen in all the Fragaria species is extremely small and easily carried by wind currents, we are not prepared to maintain that these plants did not result from accidental selfing.

MILLARDET'S plants of maternal type must have been, like our own, the result either of pseudogamy or of selfing. His plants of paternal type were all obtained by crossing species with a lower chromosome number with species with a higher chromosome number, and were, we believe, merely hybrids showing general dominance of the type with the higher chromosome number. There is no evidence, therefore, that inheritance in Fragaria is of a new or unusual kind as has been so often maintained.