But. J . Linn. Suc., 6 6 : 127-141. With 4 plates and 1 figure
February 1973
The probable origin and relationships of the
garden cocltscomb
T. N. KHOSHOO AND M. PAL
National Botanic Gardens, Lucknow, india
Accepted f o r publication July 1 9 7 2
Cockscomb (Celosia cristata) was generally believed t o have arisen from the weedy C. argentea.
However, the former is 4 x while th e latter is 8x. Grant’s suggestion that the 4 x species gave rise
to the 8 x was rejected b y horticulturists and taxonomists, who felt that a grotesque cultigen
like cockscomb could not b e a parent of an old and widespread weed like C. argentea (Sx).With
the discovery in Central India of a wild 4 x form of C. argentea showing potentialities for
fasciation and perfect compatahility with cockscomb ( 4 ~ ) the
. origin of the latter is quite easily
understood.
CONTENTS
. . . . . . . . . . . . . . . . . . . . . .
Introduction
Material . . . . . . . . . . . . . . . . . . . . . . . .
Observations
. . . . . . . . . . . . . . . . . . . . . .
C. cristata . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . .
8x C. argentea
. . . . . . . . . . . . . . . . . . .
4x C. argentea
F , C. cristata var. plumosa x 4x C. argentea and F , C. cristata var. cristata x 4 x C.
argentea
. . . . . . . . . . . . . . . . . . . .
F, 8x C. argentea x 4x C.argentea
. . . . . . . . . . . . .
F , 8x C . argentea x 4x C. argentea
. . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . .
Discussion
. . . . . . . . . . . . . . .
Probable origin of cockscomb
. . . . . .
Origin of amphiploids and genesis of their bivalent pairing
. . . . . . . . . . . . . . .
Taxonomical considerations
. . . . . . . . . . . . . . . . . .
Summary and conclusions
. . . . . . . . . . . . . . . . . . . .
Acknowledgements
References
. . . . . . . . . . . . . . . . . . . . . .
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INTRODUCTION
Among the 3 5-60 species of the tropical-subtropical genus Celosia, C cristata
L. (= C. argentea var. cristata (L.) Kuntze), popularly called “cockscomb”, is
the only cultivated species well known for its ornamental inflorescences. The
species contains a most heterogeneous assemblage of forms with grotesque
fasciated inflorescences resolvable into two distinct types on the basis of
crested or plumose inflorescences. These have sometimes been accorded
127
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T. N. KHOSHOO AND M. PAL
taxonomic rank as varieties, namely C. cristata L. var. cristata and C. cristuta
var. plumosa Voss. Another species, C. argentea L., is a troublesome
pantropical weed. Among others, Grant (1954) found the former t o be
uniformly tetraploid (2n = 36) and the latter octoploid (2n = 72). What is more
important, he also observed a very low degree of crossing between the two, and
that the rare hexaploid hybrid is almost totally sterile. Furthermore, h e
concluded that the tetraploid cultivated species was one of the elemental taxa
involved in the origin of the octoploid weedy species. This is contrary to the
consistent conclusion of all taxonomists and the widely held opinion of all
horticulturists that the weedy octoploid C. argen tea represents morphologically
the ancestral condition from which the cultivated ornamental tetraploid C
cristata has arisen (Hooker, 1885; Kuntze, 1891; Schinz, 1893, 1934; Bailey,
1928; Standley & Steyermark, 1946; White, 1948; Backer, 1949; van Steenis,
1956; Haines, 1961; Aellen, 1961; Duke, 1961; Cavaco, 1962). This view
though tenable morphologically is not so cytogenetically because normally an
octoploid is not expected to give rise to a tetraploid. Grant’s conclusion
provoked van Steenis (1958) to write that “this would represent, I feel,
genetically a most unusual situation as it implies that cockscomb would have
been the ancestral species. I t is known only in cultivation. . .”. Furthermore,
he states “I expect that further chromosome counting must reveal diploid C.
argentea, my commonsense tells me that this must be the ancestral plant from
which a polyploid cockscomb arose as a sport and was saved by ancient man as
a curiosity”.
The present investigation on wild and cultivated Indian celosias reveals that
van Steenis’s prediction has come out to be substantially true. The discovery of
a tetraploid form of C. argentea from Central India (Madhya Pradesh) assumes
importance because this country is regarded by some as the centre of origin of
C cristata (Grant, 1954, 1962b) and King found “traces of very old cultivation
of cockscomb in Rajmahal Hills’’ (Hooker, 1885).
MATERIAL
The following taxa and hybrids were studied during the present study:
(i)
(ii)
(iii)
(iv)
(v)
(vi)
(vii)
4x C. cristata L. var. cristata
4x1 C. cristata L. var. plumosa Voss
8x C. argentea L. (including C huttonii Mart.)
4x C. argentea L. from Madhya Pradesh, India
4x C cristata var. plumosa Voss x 4x C argentea L.
4x C. cristata var. cristata Voss x 4x C argentea L.
8x C. argentea L. x 4x C argentea L.
As pointed out by earlier authors (see Grant, 1954), Celosia is extremely
difficult cytological material because, for some unknown reason, the chromosomes remain more or less clumped at metaphase I and prevent detailed
analysis. Therefore, the present study had to be limited to reliable preparations,
which were rather few in number.
ORIGIN OF T H E GARDEN COCKSCOMB
129
OBSERVATIONS
C. cris ta tu
A large collection of this species was available, which varies from 0.75 to
1.69 m in height, with bizarre inflorescence forms ranging from the typical
broad fasciated cristate cockscomb (Plate 1A) to plumose types (Plate l B ) ,
with colour variation in the inflorescence from the typical purple shades of red
to orange, and yellow to white, and leaves ranging from 13.5 to 20.8 cm in
length and 2.0 to 8.0 cm in breadth with all gradations between the two
extremes. In brief, the species contains a magnificent profusion of morphological types. This wide variation in the species stems partly from cross
pollination by bees. Compared with other species, there is considerable
reduction in reproductive capacity because seed formation is confined to the
flowers in the lower regions of the inflorescence. Although a number of other
specific and varietal names and a multitude of horticultural ones have been
used for different variants, a detailed study has shown that such a treatment
does not have a taxonomical basis. Only the typical cristate and plumose types
of inflorescences breed true to the type and have been elevated to varietal rank,
C cristata L. var. cristata and C. cristata var. plumosa Voss, respectively.
With such over-evolved inflorescence types and highly reduced reproductive
capacity, it is not unnatural to find that the species exists only in cultivation
and in this way seems to have been saved from extinction, because whenever it
escapes out of cultivation, it is soon wiped out. All the available phenotypic
variability was analysed cytologically in order to detect any chromosomal
variation, but all the material was unmistakably at homoploid level with 18
bivalents at meiosis (Plate 3A). While at diakinesis the number of chiasmata per
bivalent is one or two, at metaphase I most of the bivalents were rod-shaped
with only one chiasma. There were hardly any 2-3 ring bivalents. The
subsequent course of meiosis is perfectly regular and no variation was found
except that in C cristata var. plumosa some individuals were male-sterile. The
exact nature of male sterility has not been investigated so far. These
observations are in agreement with earlier authors (Wakakuwa, 193 1; Grant,
1954).
8x C. urgentca
This species is an annual summer weed of cultivation (Plate 1C) met with
throughout the tropics and subtropics of Asia, Africa and America. In India, it
is such a troublesome and dominant weed in the fields of Cajanus sativus that,
sometimes, it looks as if Celosia argentea is the crop and Cajanus a weed.
A large number of collections of this species together with what appears to
be a conspecific taxon, C huttonii Mart., were examined. Morphological
analysis of the entire collection has shown no qualitative variation, although
there is slight variability in quantitative characters. This is in strong contrast to
the cultivated C. cristata.
Parallel to the lack of variation in the morphological characters, the taxon is
uniformly octoploid with 36 bivalents with generally one and rarely two
10
130
T. N. KHOSHOO AND M. PAL
chiasmata per bivalent at metaphase I (Plate 3B). An extensive study showed a
total absence of multivalents. The subsequent course of meiosis is perfectly
regular with clean anaphase separation and normal pollen and seed fertility.
The species thus shows the typical alloploid behaviour. Again, these observations are in agreement with those of Wakakuwa (1931), Grant (1954) and
Sharma & Banik (1965).
4x C argentea
This is a new taxon raised from the seeds collected near Satna (Madhya
Pradesh), where it grows wild in rocky areas. While the different individuals
resemble one another very closely (Plate lD), they differ significantly from 8x
C argentea. Of interest are the differences in branching pattern and the leaf
shape. While in the octoploid the lateral branches are produced in the upper
half of the main stem, in the tetraploid these are spreading and arise right from
the ground level. The leaf shape in octoploid is ovate-lanceolate (Plate 1C>,
while in the tetraploid it is distinctive in being broader than long and abruptly
pointed at the top (Plate lD), a feature that led to its identification at Kew as a
form of C argentea “with unusually shaped leaves”. Other differences are
minor and relate to the tip of inflorescence’s being blunt in the octoploid but
pointed in the tetraploid (Plate 1C, D), the leafless stalk below the inflorescence’s being longer in the tetraploid than in the octoploid, and the rare
occurrence of primitive fasciated inflorescences (Plate 2D) and longer awns in
the tetraploid but not in the octoploid.
An examination of the herbarium sheets of C urgentea at Kew (K) and
Edinburgh ( E ) has shown that the tetraploid taxon, with its characteristic leaf
shape, had been collected earlier from the States of Orissa, Madras and
Bombay.
Like C cristata, this taxon possesses 18 bivalents (Plate 3C) with one or two
chiasmata at metaphase I, perfectly regular subsequent stages and normal
pollen fertility and seed set.
In a large population of this taxon, a few male-sterile individuals were
detected. The stamens are very minute with blackish anthers, and the
sporogenous tissue degenerates very early so that there is no pollen formation.
These plants, however, are fully female-fertile and bear abundant seed. While
the exact mechanism of male sterility is still under investigation, among the 27
plants raised from the outcrossed seed collected from male steriles, 1 3 were
male sterile and 14 male fertile. Whether the control is genetic or cytoplasmicgenetic cannot be answered at present.
F, C. cristata var. plumosa x 4x C argentea and
F, C cristata var. cristata x 4x C. argentea
These crosses were performed with a view to see the extent and nature of
cytogenetic differentiation between the two cultivated taxa of C cristata and
the wild tetraploid cytotype of C argentea. Since the inflorescence and flower
structure in these species of Celosia is such that the usual emasculation, bagging
and hand-pollination cannot be done, attempts were made to grow the taxa in
sufficient proximity t o take advantage of the natural cross-pollination. For this
ORIGIN OF T H E GARDEN COCKSCOMB
131
reason, the seeds collected from the true-breeding cultivated parents were
grown and, among the seedlings, those that were either like the male parent or
intermediate were segregated for study.
The F, plants in both cases lived longer than the cultivated parents, showed
marked luxuriance and possessed dominance of the wild tetraploid parent. This
is why it was easier to spot hybrids in the progeny of cultivated tetraploids
rather than in the reciprocal combination. Dominance was particularly evident
in general habit, branching pattern, unfasciated simple spikes and flower
structure, and even the colour was more or less like that of the wild parent. The
leaves were intermediate in shape. Rarely inflorescences were rather fasciated in
some branches in C. cristata var. cristata x 4x C argentea (Plate 2A). Vigorous
F2 progeny were raised from both F , hybrids and, while a detailed study is in
progress, it may be mentioned that there is a good deal of segregation in several
morphological characters. However, in the F2 from F, C. cristata var.
plumosa x 4x C argentea, neither the plumose inflorescence nor its gofden
yellow colour was recovered. On the other hand, some of the individuals in the
progeny of a hybrid involving C. cristata var. cristata as the female parent were
cristate.
In both F, hybrids there was perfectly regular meiosis with 18 bivalents
(Plate 3D, E) and clean anaphases with 18 : 18 segregation. Pollen fertility in
the first hybrid was 76%, while in the second it was 63%. The range of fertility
in the F2 was 58436%.
F, 8x C. argentea x 4x C. argentea
For a proper cytotaxonomic evaluation of the two cytotypes within C
argentea, it was imperative to find out the cytogenetic relationship between the
tetraploid and octoploid taxa. This became possible with the study of an
interploidal (6x) hybrid detected in a mixed population of the two taxa in the
experimental plot. When male sterile 4x C. argentea was grown together with
8x C. argentea, there was no seed formation in the former, indicating, as
generally is the case, that the 8x parent must have acted as the female parent in
the F 1 hexaploid hybrid. Crossability between the 4x and 8x plants is very low,
because, out of 150 individuals, only one proved to be a hybrid. The barrier
evidently is due t o the ploidal differences. A similar rarity of hexaploid hybrids
was noted by Wakakuwa (1931) and Grant (1954) between 4x C cristata and
8x C. argentea.
The hexaploid F, 8x x 4x C argeiztea resembled morphologically the
octoploid parent particularly in the branching pattern and inflorescence shape,
while in leaf shape it was nearer the tetraploid parent (compare Plate l C , D
with Plate 2B). In the flower structure it was nearly intermediate: the hybrids
could be spotted in a mixed population of the two cytotypes because of the
leaf shape and the sterility.
Pollen mother cells at diakinesis were not analysable. However, out of the 24
cells available for study at metaphase I (Table 1) nearly 54% contain 18
I1 + 18 I. The two extremes are 3 I11 + 17 I1 + 11 I (4.17%) and 17 I1 + 20 I
(12.5%, Plate 3F). The occurrence of 18 I1 + 18 I in more than half the cells
indicates that very likely 18 chromosomes from the tetraploid C argentea pair
with 18 out of the 36 from octoploid C argentea, leaving the other 18
T. N. KHOSHOO AND M. PAL
132
Table 1. Associations at metaphase I in the 6x F, hybrid
(8x C. argentea x 4x C. argentea)
Chromosome associations
Percentage cells
Trivalent
4.17
4.17
4.17
12.5
8.33
54.16
12.5
Average per cell
3
2
1
1
-
0.37i- 0 . 0 2
Bivalent
17
18
18
17
19
18
17
17.79
Univalent
_+
0.21
11
12
15
17
16
18
20
17.31 f 0.44
unpaired. Since there is total lack of quadrivalents in 8x C. argentea, the
possibility of the 18 bivalents being formed by 36 chromosomes contributed
by the 8x C. argentea may be ruled out. The bivalents had either one or two
chiasmata. The interesting feature, however, is the presence in some cells of 1-3
associations that apparently look like trivalents. Such associations may indicate
homology of some chromosomes forming bivalents with those of the unpaired
genome. The occurrence of more than 18 bivalents may be due to some
intragenomic pairing.
Anaphase I is highly irregular; while the bivalents separate normally and
reach their respective poles, the univalents are distributed at random. In one
cell at anaphase I a distribution of 23 : 3 1 was noted. Not all the univalents
reached one or other pole; some remained in the middle as laggards, and
Plate 4A shows such lagging univalents undergoing precocious division.
Anaphase I1 is also irregular and lagging univalents and chromatids are the usual
feature. Sometimes there are no clear-cut poles; and such cases result in the
formation of a monad, which perhaps is the source of some giant pollen grains
(73.8 pm) observed occasionally (Plate 4B). Quite often the second division
fails and diads are organized. Chromosomes which are not included in the
daughter nuclei at telophase I1 form micronuclei and result in polyads.
As expected from such a meiotic behaviour, there is high pollen sterility. The
stainable grains (2 1.1%) perhaps represent some unreduced pollen and other
balanced combinations with n = 18 and above. Few seeds were formed on
selfing, denoting some female fertility and viability of the stainable pollen.
Usually the size of the stainable pollen varies from 32.8 to 41.0 pm.
A similar meiotic behaviour has been found in the hexaploid interspecific
hybrid involving 8x C. urgetitea and 4x C. cristata reported earlier by
Wakakuwa (1931) and Grant (1954). This hybrid, like the present 6x
intraspecific hybrid within C. urgenteu, arose from a cross with the octoploid as
the female parent, exhibited dominance of the wild octoploid parent and was
almost totally sterile.
F, 8x C. argentea x 4x C. argentea
Twenty-one seeds were harvested from the bagged spikes of the F, hybrid,
which on sowing yielded a progeny of eight plants. These were numbered
ORIGIN OF THE GARDEN COCKSCOMB
133
Table 2. Meiosis in the six F, progeny plants
(8x C. argentea x 4x C. argentea)
Associations at metaphase I
Plant No.
I
2n=
No. of cells
Trivalent
Bivalent
Univalent
4 1 (4x+5)
2
-
18
17
20
7
1
1
1
I1
I11
IV-VI
4 0 (4x+4)
39 (4x+3)
108 (12x)
-
2
1
-
1
-
3
2
1
-
15
18
19
20
5
4
2
18.25 11+
4.5 I
18.75 11+
2.5 I
~
1
18
17
16
3
5
3
-
54
-
-
Average
association
0.17 III+
17.33 II+
3.83 I
54 I1
cells of each
I-VIII, and the first six analysed for their chromosome number and meiotic
behaviour. The data are summarized in Table 2.
Three of the plants (nos 1-111) were not healthy and possessed thin stems,
diffuse branching and narrow leaves. All the three were hypertetraploid
(2n = 39-41) with three, four or five extra chromosomes (Table 2). Most of the
chromosomes associated as bivalents (Plate 4C). The remaining three plants
(IV-VI) are morphologically almost identical and have been treated together.
They also have the same chromosome number (2n = l o g ) , i.e. they are 12x or
amphiploids between 8x and 4x parents.
The amphiploids are very vigorous and resemble tetrapIoid C. argentea in
habit and branching pattern (Plate 2C). The leaves are more like the tetraploid
parent but are thicker. The shape of the inflorescence resembles the octoploid
in having a blunt tip and being unfasciated. Except for the small quantitative
differences, the flowers of the amphiploids resemble the octoploid. The cell
size, as is clear from the dimensions of the stomata and pollen grains, is larger
than that of the parents and the increase is directly proportional to ploidy level
(unpubl. data).
All the three plants possess 54 bivalents with no multivalents whatsoever
(Plate 4D). The course of meiosis is perfectly normal, as is clear from the
54 : 54 segregation at anaphase I (Plate 4E) and no laggards were seen either at
this stage or at anaphase 11. Pollen fertility is about 91% (Plate 4F, compare
with Plate 4B) with normal seed set.
Amphiploids have been grown for seven generations and there has been
neither any evidence of impairment in fertility nor segregation in morphological characters. Vigour and high fertility have enabled the amphiploids to
colonize new areas near the Garden, to which they are well adapted.
Among the eight F, plants from the 6x F , hybrid 8x C. argentea x 4x C.
cristata, Grant (1954) found three to be 6x (2n = 54), one 9x (2n = 81) and
four were amphiploids, i.e. 12x (2n = 108). Two of the hexaploids possessed
18 I1 + 18 I, while the third appeared to have 27 11. The amphiploids had 54 11.
134
T. N. KHOSIIOO AND M. PAL
Of particular interest is the fact that he found most of the F2 plants,
particularly the amphiploids, to be meiotically irregular with lagging chromosomes at telophase 1 and 11, micronuclei, polyads and pollen abortion. This is in
total contrast to the present observations, particularly with regard to the
restoration of perfectly regular meiosis and normal fertility in amphiploids
from 6x F, C. argentca (8x) x C. argenfea (4x).
DISCUSSION
The foregoing observations throw new light on (i) the origin of the
ornamental cockscomb, (ii) taxonomic evaluation of the C. argentea complex
including the exclusively cultivated C. cristutu and the synthetic amphiploid C.
whitei, and (iii) the nature of polyploidy and the genesis of bivalent pairing in
all polyploids of this complex, particularly the synthetic amphiploids. 'These
may now be discussed in turn.
Probuhle origin of cockscomb
There is a general unanimity among taxonomists and horticulturists that the
cockscomb (C. cristatu) has arisen from C. urgentea, an annual often
troublesome weed of tropics with almost uniform morphology and ovate
cylindrical, unfasciated inflorescences (Hooker, 1885; Bailey, 1928; Van
Steenis, 1956; Li, 1959; Duke, 1961; Aellen, 1961; Cavaco, 1962). The two
species do not have any sharp differences except for the grotesque inflorescence in C. cristata. However, the work of Wakakuwa (193 1) and Grant
(1954) has shown that, while C. cristuta is uniformly tetraploid, C. argentea is
octoploid. This has been confirmed by the present authors. On this basis, Grant
(1954) argued that the above conclusion of a large number of authors that the
perfect alloploid 8x C. urgentcn was the species typicu from which 4x C.
cristatu could have arisen is untenable cytologically, because normally
tetraploid cannot arise from octoploid. Instead, he suggested that, cultivated C.
cristuta may have been involved in the origin of the wild pantropical octoploid
weed C. argenteu, which is apparently supported by the presence of 18 I1 + 18 I
in the hexaploid hybrid between the two species. The other possibility, that C.
urgentea may be a straight octoploid from C. cristatu, is untenable, as the
experimental 8x from C. cristutu raised by Kihara & Hishimoto (1938)
possessed a variable number of quadrivalents and was fasciated. Both these
features are totally absent in C. urgentea.
In spite of Grant's cytogenetic evidence, taxonomists have rejected the idea
that an exclusively cultivated taxon like C. cristutu could be the parent of a
widely distributed and successful weed C. argentea. Van Steenis (1958)
predicted that further cytogenetical work must reveal a wild tetraploid C.
argentca from which cockscomb arose. The present work on wild celosias has
fulfilled this prediction and a wild tetraploid cytotype of C argentea has been
discovered in Central India which differs from the widely distributed octoploid
in branching pattern, leaf shape and tip of the inflorescences.
In view of the regular meiosis and high fertility in the F 1 and F, hybrids
between C. cristatu vars. cristuta and plumosu on the one hand and the
tetraploid C. urgentea on the other, there is regular gene exchange and high
ORiGIN OF THE GARDEN COCKSCOMB
135
degree of genetic similarity between the two species, which are at the
ecospecific level of genetic differentiation. This is further borne out by their
identical behaviour with octoploid C. argentea. This is clear from the work of
Wakakuwa (1931) and Grant (1954) on 6x F , C. argentea (8x) x C. cristata
(4x) and that of the present authors on 6x F, C. argentea (8x) x C. argentea
( 4 ~ ) .In both hybrids the most common association during meiosis is
18 I1 + 18 I, which in both is accompanied by sterility. The only stable and
true-breeding progeny from both are the 12x amphiploids.
An analysis of the F, and F, progeny from hybrids between cultivated 4x C.
cristata var. cristata and var. plumosa, and the wild 4x C. argentea has shown
that the progeny is more akin t o the tetraploid C. argentea in being tall with a
similar branching pattern and the absence of fasciation. The dominance of the
wild parent is apparent and many important characters of C cristata could not
be recovered in F, , indicating thereby that the grotesque inflorescence
characters represent a recessive condition. This conclusion is also borne out
from the analysis of F, and F, generations of the hexaploid hybrid involving
C cristata and the 8x C argentea. There was almost total dominance of the 8x
parent except that one plant had minor fasciation which, however, did not
appear in its progeny (Grant, 196213).
The above facts, together with the opinion that India is probably the place
of origin of the cockscomb (Grant, 1954, 1962a) and the observation of King
(vide Hooker, 18SS), who found the existence of unmistakable signs of ancient
cultivation of the cockscomb in the Raj Mahal Hills (Bihar), indicate that the
tetraploid cytotype of C. argentea discovered in Central India by the authors
not only fulfils the prediction made by van Steenis (1958) but more or less also
conforms to the elemental taxon that could have given rise to the cultivated C.
cristata. This is further supported by the occasional occurrence of the primitive
type of fasciation in old plants, particularly in the male sterile form of this
taxon (Plate 2D).
The ancient Indians perhaps took an interest in this taxon because of
religious, magical or superstitious reasons (Grant, 1954, 1962a), and with
reduction of the breeding group and consequent inbreeding, recessives for
fasciation, colour, etc. began to appear and were selected. Some of these were
so grotesque and “over-evolved” that they, like maize, could be preserved only
in cultivation because of their low reproductive capacity. This is supported by
the fact that no true-breeding fasciated taxon exists in the wild Celosia or any
other genus (White, 1948).
De Roos (1968) has indicated south east Asia as the place of origin of the
cockscomb. Perhaps in view of the present discovery, it may be more pertinent
to assume that the cockscomb went to that area with the early migration of
Hindus and subsequently with that of Buddhists. Furthermore, because of
more cogenial conditions, this ornamental underwent a further and bigger cycle
of selection in that area.
Cockscomb, the oldest of the fasciated plants in the historical record (Grant,
1962b), is true breeding, and all diversity in this species is on the genic plane as
the species is homoploid. Mutations resulting in widening of the growing point
soon after normal seedling growth have been selected. These affect the length
of the main floral axis, which becomes fan-shaped, truncate and ribbed. The
genic control is complex and involves many genes.
136
T. N. KHOSHOO AND M. PAL
The process of selection for fasciated types or those in which number of
flowering stems is considerably increased (plumose types) has been aided by
the existence of such potentialities in 4x C. argeiztra. After their initial
unmasking, there was an accumulation through hybridization of a full
complement of recessive genes controlling heritable fasciation, which is not
modifiable by environment.
Origin ojamphiploids and geizesis oj’ their bivalent puiring
The results in Cefosia stand out on account of the fact that about 50%
progeny of the 6x F, hybrids contain amphiploids (12x) and, what is
important, there is almost immediate and complete isolation of the six
genomes, leading to restoration of near-normal fertility, imparting a truebreeding character and immediate establishment in nature to the new taxon.
Underlying such a precision must be some genetic properties or conditions
which may now be discussed.
Hexaploids arise very rarely, even when 8x C. argentea and 4x C. cristutu or
4x C. argentea are grown in sufficient proximity or even interplanted, which is
also clear from sporadic reports of such hybrids Erom a wide geographical area
ranging from Haiti, Nicaragua, Panama, Malaya and the Philippines t o India
(Grant, 1961, 1962a). ‘The minor differences between the hybrids are due to
the existence of such differences not in the octoploid parent but in the variable
tetraploid parent C. cuistata.
In the two experiments in which F, progeny was raised from the hexaploid
F, hybrid, it was noted that four (Grant, 1954) and three (present work)
plants out of eight and six respectively were dodecaploid, i.e. amphiploids. The
remaining four and three plants in both cases were either heteroploid with
hypertetraploid numbers like 2n = 39 (4x + 3 ) , 40 (4x + 4), 41 (4x + 5) or were
hexaploid (2n = 54) or 9-ploid ( 2 n = 81). This evidently shows that, due to
irregular segregation of univalents, gametes containing either 2x + 1-3 or 6x
numbers of chromosomes are functional. In view of the 50% 12x progeny, there is
a decided bias in favour of 6 x, i.e. unreduced gametes. Although the 4x C.
urgentea and 4x C. cristata are genetically extremely close, one parent (i.e. 8x
C. argentea) is common in the two types of amphiploids (12x) raised by Grant
(1954, 1962) and the present authors. The strong tendency to produce
unreduced sex cells and thereby amphidiploids, which is indicated but cannot
be categorically asserted, may be the result of a genotypical tendency of the
common parent. Such a high rate of doubling is also characteristic of species
like Gilia millefoliata, G. valdviensis and G. clilceyi and hybrids involving these
species, as one or both parents produce a high percentage of amphiploids (V.
Grant, 1965). Wherever these species were not involved, the hybrids failed to
produce amphidiploids. Furthermore, genic control of “chromosome doubling”
is known in Drosophila, Antirrhinum, Datura, Rumex, Triticum, etc. (Stein,
1942; Gloor & Staiger, 1954; Avery, Satina & Rietsema, 1959; Swietlinska,
1960; Wagenaar, 1968). I t is also clear that restitution during meiosis, leading
to unreduced cells, is not necessarily related to the lack of pairing (V. Grant,
1965), although this property is generally regarded as a prerequisite for their
origin. The critical stages of restitution are affected by genes irrespective of the
extent of pairing. The same applies to autogamy, which normally augments the
production of amphiploids once restitution has occurred.
ORIGIN OF THE GARDEN COCKSCOMB
137
The reasons for regular meiosis in the amphiploid from 6x F, C. argentea
(8x)x C. argentea (4x), as noted by the present authors, and the irregular
meiosis and sterility of the amphiploids from 6x F, C. argentea (8x)x C.
cristata (4x), as observed by Grant (1954), are not clear. Perhaps this
differential behaviour may be indicative of the difference between the male
parents (i.e. wild 4x C. argentea and cultivated 4x C. cristata) and the greater
degree of differentiation of 4x C. argentea in comparison with 4x C. cristata.
However, Grant (1961) subsequently noted that a natural amphiploid of the
same parentage from Malaya had, as in the present case, regular meiosis (54 11)
and normal fertility. According to him, the duplicated genomes cause irregular
meiosis in the raw amphiploid but once sufficient differentiation takes place
through natural selection, as perhaps is true of the Malayan plants, regularity
ensues.
The Drosera scheme (18 I1 + 18 I) shown by both 6x F, hybrids involving C.
argentea (8x), and C. argentea (4x) and C. cristata (4x) is not apparent from
the ensuing 12x amphiploids, which show 54 I1 and no trace of quadrivalents.
On the basis of pairing in the F , , the 12x should be auto-allododecaploid or
segmental-allododecaploid. Evidently, the 18 I1 in the 6x hybrid are the result
of homoeologous pairing and, in the 12x, bivalents are due to perfect
preferential pairing. However, the precision with which complete bivalent
pairing (therefore isolation of the six genomes), accompanied by total
restoration of fertility, has occurred in the amphiploids is perhaps indicative of
genotypic control of bivalent pairing. In genera1 it is believed that several
generations must elapse before normal fertility is restored by complete
differentiation of chromosomes. In actual practice, all these features have
accompanied the very origin of the 12x in the present amphiploid, with the
result that it is fertile, vigorous, true-breeding and has become established
immediately. All these properties have been accomplished in a single step here.
As stated above, on the basis of pairing in the 6x hybrid, the 12x amphiploid
should have been a segmental allo- or auto-allododecaploid, but actually the
above properties are strongly indicative of a successful genomic alloploid. This
could be accomplished only if we believe that bivalent pairing was instituted by
genetically controlled multivalent suppression, as has been actually demonstrated in hexaploid wheats (Riley & Chapman, 1958) and inferred in a variety
of polyploids like tobacco, cotton, etc. (Riley & Law, 1965). Evidently the
present amphiploids within the C. avgen tea complex offer additional examples
where bivalent pairing conceals the exact nature of polyploidy (see also
Khoshoo & Arora (1969) for 6x Verbena aubletia).
The present results have been summarized in Fig. 1. Allocation of genomic
formulae has been postponed till such time as more is known about the
cytogenetic architecture of the complex, because denoting genomes by
dissimilar symbols does not necessarily mean that they are genically as
dissimilar and vice versa (see Riley & Law, 1965; Khoshoo & Arora, 1969).
Taxonomic considerations
The complex is composed of the well-known ornamental cockscomb t o
which Linnaeus (1753) accorded specific rank as C. cristata, even though it is
exclusively a cultigen with relatively very low reproductive capacity. In fact it
138
T. N. KHOSHOO A N D M. PAL,
was recorded in botanical literature much earlier than the widespread weed C.
argentea L. (Grant, 1954, 1962a). There is no difference in the floral parts
between the two except for the occurrence of heritable fasciation in the.
former. On these accounts, Kuntze (1 891) degraded the former to varietal
rank, C. avgerzteu var. cristata, an evaluation which has been followed by most
taxonomists (Standley, 1917; van Steenis, 1956; Cavaco, 1962). However, on
account of the difference in level of ploidy, reproductive isolation (as
evidenced by the rarity of hybridization between the two), hybrid sterility and
morphological distinction based on fasciation, Grant (1954, 1962a) made out a
convincing case for the retention of the two species C. cristata and C. argentea.
The position requires reconsideration because of the discovery of a
tetraploid form of C. argentea, which differs from the more widespread
octoploid element of the species in its branching pattern, leaf shape and
inflorescence apex. Like 8x C. argentea, the 4x C. argentea resembles C. cristata
in floral structure and differs in being unfasciated; but, unlike the octoploid,
the tetraploid is not reproductively isolated, with the result that there is perfect
gene exchange with vigorous and fertile F, hybrid segregates. Furthermore,
12x amphiploids result from 6x F , hybrids between 8x and 4x C. argentea
(present work) and 8x C. argentea and 4x C. cristata (Grant, 1954). The
amphiploid from the latter combination was given specific rank as C. whitei by
Grant (1961). Both amphiploids are good species because of their fertility,
vigour and reproductive isolation from the parents, and they connect the
variation between parents (present work: Grant, 1962a). C. whitei is a
fasciated seedling from an unfasciated 6x F, hybrid between unfasciated 8x C.
argentra and fasciated 4x C. cristata. Grant (1962b) regards it as a mutant; but
in view of the 12x level it may be more plausible to regard the development of
fasciation as the result of rare intergenomal pairing involving recombination
between chromosomes containing fasciatedhormal (unfasciated) genes, in
which the dominant normal gene suppressing fasciated recessive was eliminated.
From Fig. 1, which summarizes the origin and interrelationships of the
various taxa, it appears that all the taxa together constitute a single
phylogenetic complex. This is particularly so after the discoveries of the 4x C.
argenteu and 12x C. whitei. ‘The various taxa represent different ploidal levels
and, following Love (1951), these need to be appropriately evaluated,
preferably to specific rank, particularly on account of the reproductive barrier
between the 4x, 8x and 12x taxa. From the genetic point of view the two
tetraploids (C. cristata and 4x C. argerztea) belong to the same species, while 8x
and 12x belong to separate species. However, recently Davis & Heywood
(1963), Mosquin (1966) and Khoshoo (1967) have advocated that, for a
utilitarian concept of the species, morphological distinctions are relatively more
important than genetic isolation. Following such considerations, the entire
complex would be more appropriately referable to C. argentea, in which the 8x
form would represent var. argentea (being typical of the species), folIowed by
var. cristata Voss for the cockscomb, var. orbiculata (?) for the wild cytotype
and var. whitei for the 12x cultivated cytotype.
The reason for such conflicting evaluation stems from the differential rates
of morphological and genetic evolution within the complex. While genetic
evolution of the taxa is complete, the commensurate morphological distinctions have yet to be achieved.
ORIGIN O F THE GARDEN COCKSCOMB
139
1 2 x 54II
Fe r t i10
cultivoted
1 2 x 54I.I
Fertile
I
Selection
Polyp1 oidy
FI
6.7 18II t I81
6 x BIS +I81
Sterile
Sterile
t
I
FI ondF2
4x
181I
Fertile
Po Iyp lo i dy
A
C.crisfoto
Celosio SP.
Fertile
unknown
Fertile
wild
and selection
Fertile
cult ivated
Figure 1. Diagram depicting interrelationships between different taxa in the C. argentea
complex.
SUMMARY A N D CONCLUSIONS
The general opinion of the taxonomists and horticulturists that C. argentea is
the ancestor of the cultivated cockscomb (C. cristata), was rejected by Grant
(1954) on the plea that the former is octoploid, while the latter is tetraploid
and, according to him, perhaps the cultivated form may have been one of the
parents of the 8x pantropical weed C. urgentea. A hitherto undiscovered
tetraploid cytotype of C. argentea, which species was so far known only as
octoploid, was discovered in Central India. This discovery fills the gap created
by the objection of Grant and fulfils the prediction made by van Steenis (1958)
that such a tetraploid form could be the ancestor of the cultivated cockscomb
C. cristata, which is also tetraploid. This view is further strengthened because of
the occurrence of fertile and vigorous F, and I;, hybrids involving the two
varieties of C. cristata and 4x C. argenteu. I t appears that the two species are
genetically similar and there are hardly any barriers between them. Furthermore, the behaviour of the 6x hybrids involving 8x C. argentea with 4x C.
argenteu and 4x C. cristata respectively is nearly similar. Both show 18 I1 + 18 I
and produce 12x (amphiploid) progeny in the F 2 . On the basis of meiosis
(18 I1 + 18 I) in the 6x F l hybrid, one could not have expected the regular
140
’I‘. N. KHOSHOO AND M. PAL
formation of 54 11, perfectly normal fertility and true breeding in the vigorous
amphiploid. That all these characteristics have been accomplished in a single
step shows that the perfect bivalent pairing in 12x is perhaps due to some
genetically controlled multivalent suppression which has isolated the six
genomes otherwise carrying different degree of homoeologies. The 12x type
emanating from one of the 6x hybrids (8x C. argentea x 4x C. cristuta) was
even given the specific name of C. whitei.
’The ecospecific relationship of the wild tetraploid form of C. urgentea and
cuItivated C. cristuta, together with the opinion that India is very likely the
place of origin of the latter, makes the origin of the cockscomb from 4x C.
argenteu quite plausible.
laxonomically the entire complex, namely the 4x and 8x cytotypes of C.
argentea, 4x C. cristatu, 12x C whitei and the 12x amphiploid from 4x and 8x
C. uvgenteu, constitutes a single phylogenetic entity. Except 4x C. urgenteu and
0’. cristatu, the different members of this complex are genetically strongly
isolated but do not possess commensurate morphological distinctions.
ACKNOWLEDGEMENTS
‘The authors thank Mr J . P. M. Brenan €or providing facilities to one of them
(T.N.K.) at the Herbarium, Royal Botanic Gardens, Kew, for surveying the
material of Celosia and to Mr T. K. Sharma for help with photographs
illustrating the paper.
REFERENCES
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Plate 1
0
T . N . KHOSHOO
AND
!VI. PAL
(Facing p . 140)
Bot. J. Linn. Soc., 66 (1973)
Plate 2
8
A
c
T. N. KHOSHOO
AND
M. PAL
Bot. J. Linn. Soc., 66 (1973)
Plate 3
c
.
' ••
D
,
E
T. N. KHOSHOO
AND
M. PAL
Bot. J. Linn. Soc., 66 (1973)
Plate 4
B
A
D
E
T. N. KHOSHOO
AND
M. PAL
F
ORIGIN OF THE GARDEN COCKSCOMB
141
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EXPLANATION OF PLATES
PLATE 1
Flowering shoots with !eaves: A, Celosia cristata var. cristata; B, C. cristata var. plumosa; C, C.
argentea (8x); D, C. argentea (4x).
PLATE 2
Flowering shoots with !eaves: A, F 1 hybrid C. cristata var. cristata x C. argentea (4x); B, 6x F 1
hybrid C. argentea (8x) x C. argentea (4x); C, amphiploid (12x) C. argentea (8x + 4x); D,
fasciation in C. argentea (4x).
PLATE 3
A, C. cristata var. cristata, metaphase I 18 II; B, C. argentea (8x), metaphase I 36 II; C, C.
argentea (4x) diakinesis 18 II; D, E, 4x F 1 hybrid C. cristata var. plumosa x C. cristata (4x),
diakinesis 18 II and metaphase 18 II respectively; F, 6x F 1 hybrid C. argentea (8x) x C.
argentea (4x), metaphase I 17 II + 20 I. All x1680.
PLATE 4
A, B, 6x F 1 hybrid C. argentea (8x) x C. argentea (4x), telophase I with precociously dividing,
lagging univalents and reduced (small and unstained) and unreduced (large and stained) pollen
grains; C, F 2 plant with 2n = 40 (20 II) from 6x F 1 hybrid; D-F, amphiploid (12x) C. argentea
(2n = 108); D, metaphase I 53 II + 2 I; E, anaphase I 54: 54; F, fertile pollen. A, C-E x1680;
B, F x190.