Cytologia 42: 347-356, 1977

Cytological Investigations on the Indian Compositae VI. Chromosomes and evolutionary phylogeny

P. N. Mehra

Department of Botany, Panjab University, Chandigarh,

Received December 2, 1975

Based on our studies, chiefly of meiotic chromosomes , of 223 species of Com positae belonging to 97 genera and dispersed among all the 13 tribes,1 I propose to discuss in this paper the probable evolutionary phylogeny of Compositae, the relationships of its various tribes and the mechanisms of its cytological evolution. This is the concluding paper of the present series on the cytological investigations of the Indian Compositae. As stated earlier Rendle (1952) estimated the number of species in the family to be nearly 14,000 in 800 genera, although a more recent estimate is of over 13,000 species in about 900 genera (Airy Shaw 1966). There has been no major change in its segregation into 13 different tribes since the masterly essay was written by Bentham on its classification, history and geographical distribution in 1873, ex cepting that the tribe Helenieae has been considered by various authors to be re presenting no clear cut grouping, its genera being closely related to some of those belonging to Heliantheae and hence the former tribe has been merged into the latter (Crounquist, cf. Airy Shaw 1966). There is no doubt that the family is the highest in the scale of evolution among the Angiosperms and is one of the four largest, the other three being Orchidaceae, Gramineae, and Leguminosae. The members of the family are world-wide in distribution but are best represent ed in the New World, excepting the two small tribes, Calenduleae and Arctotideae, which are confined almost exclusively to S. Africa. In the Indian sub-continent it is represented by nearly 120 genera and more than 600 species (Hooker 1882). The family is largely temperate, rare in tropics. There are scarely any aquatic marshy or epiphytic species, or climbers, but a few members are met with in highly arid environments and show succulent habit resembling that of many cacti. The earliest remains of the family are from mid-Tertiary in Oligocene, 36 mil lion years back, mainly in the form of fruits resembling the ones belonging to some of the extant genera. A modest estimate, therefore, is that the family must have had its origin some 40 million years back and during this span of time has diversified and evolved to a truly remarkable extent.

Origin of Compositae Before the origin of the family can be discussed satisfactorily it is imperative to highlight its pertinent features. The habit is predominantly herbaceous, tree

1 Heliantheae 34, Helenieae 5, 32, Anthemideae 22, Cynareae 18, Mutiseae 4, Calen duleae 3, Vernonieae 9, Eupatorieae 5, Senecioneae 16, 44, Cichorieae 29 and Arctotideae 2. 348 P. N. Mehra Cytologia 42 element being only to the extent of 11/2%and that too more or less confined to the oceanic islands. The leaves may be alternate, opposite or radicle but always ex stipulate. The inflorescence is characteristic, a capitulum, which basically is a raceme with the axis condensed and telescoped, yet there are some forms like Rudbeckia, Spilanthes and Galingsoga which represent a transitional phase in the form of an abbreviated spike. The involucre which undoubtedly represents the outer (origi nally lower) bracts on the condensed axis, mostly without flowers in their axils, is foliaceous, chaffy or spiny, yet in some forms a flower still arises in the axil of a bract. The receptacle or the telescoped axis bears the flowers; in Heliantheae each floret arises in the axil of a receptacular scale-like bract or palea, in many of the other tribes this feature is either completely lost or at least is not a consistent feature of their constituent genera. The florets in a capitulum may be all regular and actinomorphic- obviously a primitive condition (Vernonieae, Eupatorieae), or they may be zygomorphic and all bilabiate or the ray florets may be bilabiate whereas the inner or disc florets are regular and actinomorphic (Mutiseae), or the ray florets are ligulate and the disc florets regular actimorphic (most of the Helian theae, Astereae, Anthemideae, Inuleae), or all the florets in the capitulum may be zygomorphic and strap-shaped (Cichoreae) representing a most highly evolved con dition. The calyx may be formed of 5 small scales or reduced to bristles or hairs which may branch, or may form a pappus loosing all semblance to a calyx. The petals are 5 and so are the stamens arising on them. By far the most consistent is the syngenesious condition, the anthers forming a tube around the style with introrse dehiscence and yet there are exceptions as in Xanthium and other Ambro sineae (sub-tribe of Heliantheae) where they are free or loosely united, thus revealing the original or the ancestral condition. The mechanism of pollination is highly characteristic. The florets at one point of time are functionally male and at another female so as to bring about cross pollination employing a variety of insects, Le pidoptera, bees, flies and beetles, but in case of failure yet retaining the capacity of self-pollination by recurving of stigmas to present their inner receptive faces to the mass of pollen outside. The mechanism of pollination is so strikingly characteristic that one has to take a serious notice of it, in case the like of it is visible elsewhere, while determining the phyletic affinity. The carpels are two, syncarpus, with a basal anatropous ovule in the single loculus. Anatomically, only the tribe Cichoreae possesses laticiferous vessels, generally in the phloem tissue, the others are charac terised by the presence of oil canals. However, some members of Arctotideae do possess laticiferous vessels too in the phloem region. We believe the Compositae is strictly monophyletic in origin. By this concept is meant that the origin is not necessarily from a single or species but from a plexus of basically similar forms with, broadly speaking, similar gene potential. (In contrast polyphyletic origin is considered to be from entirely diverse groups with different genetic outfits as a result of homoplastic evolution, often in response to similar environmental factors). There have been two main contestants in the field in the matter of ancestory of Compositae. Majority of the systematists believe in the Campanulacean ancestory (Delpino 1871, Eichler 1875, Kirchner 1897, Warming 1913, Hallier 1905, Wett 1977 Cytological Investigations on the Indian Compositae VI 349 stein 1901, Wernham 1912, Small 1919, Bensen 1957 and Hutchinson 1959). There are others who uphold Rubialean origin (Bentham 1873, Candolle 1873, Cronquist 1955, 1965). The close affinity of the family with Campanulaceae seems not much in doubt. Campanulaceae are generally herbs, rarely shrubs and only exceptionally trees, like in the Compositae. The leaves are extipulate. Articulated laticiferous tubes are present generally in the inner phloem region. Although flowers are in racemes, spikes or heads, in some forms like Jasione and Hedraeanthus bracts do form an involucre as in Compositae. Strikingly, the method of pollination by insects, the exposition of the male and female stages of flowers, the brush mechanism of the style and the recurving of stigmas to touch the stylar brush for effecting self-pol lination, in case cross pollination fails, closely simulate the Compositae. In the sub-family Lobeloideae, the anthers are joined laterally to form a tube (syngenesious condition) like in the Compositae. Lobeloideae do possess a tendency to bilabiate condition such as is exhibited in the tribe Mutiseae of Compositae. In contrast Rubiaceae belongs to the class Arboreae of Hutchinson with pre dominantly tree or shrubby habit, are tropical in distribution, possess stipulate leaves which is their very consistent feature, in strong contrast to the Compositae. The inflorescence in Rubiaceae is typically cymose, again in contrast to the racemose organisation of the capitulum in Compositae. Although the flowers, chiefly of the genera inhabiting tropics, are pollinated by bees and Lepidoptera, there is no simi larity with the highly specialised mechanism exhibited by the Compositae or Cam panulaceae. This pattern originally achieved in the Campanulaceae seems to have been carried forward in the Compositae in the course of its evolutionary phylogeny.

Phyletic relationship of tribes Heliantheae has been regarded as the most primitive tribe by many of the mor phologists, mainly because of 3 reasons: disc florets arise in the axil of a scale-like bract or palea, calyx is not reduced to hairs or pappus but still retains its normal form of 5 members though of a very dimunitive type, and the involucral bracts are foliaceous, in several series, not membranous or scarious at the margins. On the other hand, the capitulum is in most cases differentiated into ray florets which are ligulate strap-shaped-an advanced feature, while the disc florets retain the primitive actinomorphic symmetry. Cytologically it is a most unstable tribe in the matter of consistency of basic chromosome number. In fact no single number could be considered basic, since a wide variety of them are discernible in the various members that have been hith erto investigated. Helenieae is closely related to Heliantheae. In fact, as already stated, the vari ous genera included in it show such unmistakable affinity with some of the Helian theae that it has been considered advisable to merge this tribe in the Heliantheae as it does not represent any distinct entity of its own. Recently, on an electron microscopic study of pollen, Skvarla and Turner (1966) noticed a close resemblance of the pollen walls of Heliantheae and Helenieae suggesting a new evidence strength ening this relationship. 350 P. N. Mehra Cytologia 42

From a purely morphological point of view the tribes Eupatorieae, Vernonieae, and Senecioneae (at least some genera) need consideration in that the flowers in a head are all actinomorphic and regular which indeed is a primitive condition. But in all of them the pappus is most unlike a calyx. It is setose and copious in Ver nonieae, of 5-oo bristles in Eupatorieae, and hairy in Senecioneae. Also the florets on the receptacle do not arise in the axil of a receptacular bract or palea. In Sene cioineae the involucral bracts, which may be in one or a few series, are often more or less united representing an advanced condition. The cytological picture of these 3 tribes is highly interesting and meaningful. The basic chromosome number is 5, although most of the members have been stabi lized at 10-a multiple of this number. Eupolyploidy is observed in a large number of cases. It must not, however, be understood that there is no deviation from this, for aneuploidy is not unoften observed in Eupatorieae (n=17) and Vernonieae. (n=1l, 17). Arano (1965), who has studied the karyotypes of a large number of Japanese species of the 6 tribes, Senecioneae, Anthemideae, Astereae, Cynareae, Mutiseae and Inuleae, is of the view that the basic karyotype of Senecio (x=10) is the most primitive because of its highly symmetrical nature with median centro meres and large size of chromosomes. The Inuleae include members in which all the florets or the disc florets only are regular representing a combination of primitive and advanced condition. The most dominant base numbers here are x=10 (obviously a polyploid derivative from 5, in Odontospermum, Buphthalmum, Tessaria, Pluchea, Pulicaria and many species of Inula), and x=7 (an aneuploid derivative from 5, in Gnaphalum, Anaphalis, Filago, Antennaria and species of Helipterum and Helichrysum, although the latter two genera possess representatives with other aneuploid members too). In Leontopodium, Ammobium and Evax yet a third, though less dominant number x=13 is visible which undoubtedly is a drop from the tetraploid condition based on x=7. Like Inuleae, Astereae too possess either all or only disc florets regular. The tribe is world-wide in distribution but almost two third of the genera are met with in the New World. The base number x=9 is the dominant. Of the 31 species of Indian members belonging to 12 genera, all were found to possess the haploid chro mosome number 9 or its multiple, with the sole exception of Cyathocline lyrata. Solbrig et al. (1964, 1969) whose contributions are the maximum have likewise sug gested 9 as the dominant base number for the tribe. However, in Aster and Haplo pappus chromosome numbers other than 9 are also reported in a number of species. While discussing the base number of the tribe Mehra and Remanandan (1974) arrived at the conclusion, in consonance with the views of Turner et al. (1961) and Arano (1965), that x=9 is of ancient polyploid origin from the ancestral base number x=5. Anthemideae which is also world-wide in distribution is close to Heliantheae in that involucral bracts may be in several series but they possess scarious or membra nous margin. In some members at least the disc florets may arise in the axil of a scale or palea on the receptacle as in Heliantheae. But here the basic chromosome number as in Astereae, is stabilised at x=9, since it is observed in a large majority of members. 1977 Cytological Investigations on the Indian Compositae VI 351

Mutiseae represents a condition more akin to Lobeloideae of Campanulaceae. Here the ray florets, when present, are bilabiate (rarely strap-shaped) and the disc florets may be bilabiate or regular. The cytological condition of this tribe is as un stable as that of Heliantheae or Cynareae in respect of the basic chromosome numbers of the constituent genera. In the latter tribe the involucre is in many series, often thorny, and the receptacle is covered by numerous bristles or spines. They re present the thistles. Undoubtedly the Cichoreae is the advanced tribe. All the florets in a capitulum are ligulate strap-shaped. Another advanced feature is the presence of laticiferous vessels in the phloem which it shares with some members of Artotideae, and in the ancestral family Campanulaceae. Here too the basic number is referable to x=9 although deviations and aneuploid reductions are obvious in many members as in Astereae or Anthemideae. It is futile to arrange the various tribes in a serial order, for in a modern family like Compositae which at the present time is at its zenith of evolutionary diversity, one can only arrange them in the order of their affinity, which in turn represent not the numerical position of the chromosomes alone but primarily the kind of gene blocks that have become stabilised in their genomes giving expression to the charac teristic reproductive features illustrated by their capitula and florets. The phyletic picture as visualised here, is presented in Fig. 1. In this picture the numbers given below a tribe represent the basic numbers, the ones underlined being the most domi nant. Those included within bracket are the presumed base numbers although not represented in any of the living members at the present state of our knowledge. It is obvious that four conditions are met with: In Eupatorieae, Vernonieae and Sene cioneae the predominant basic number is 10 which in all probability is a derivative of the ancestral number x=5. That this was the situation has been discussed in our earlier papers (Mehra et al. 1965, Mehra and Remenandan 1975). The same conclusion was arrived at by Turner and Lewis (1965) and confirmed by Arano (1965) on the basis of a comparative study of the karyotypes of 6 tribes of Japanese Compositae. The second condition is in Inuleae in which the predominant base numbers are 7 and 10. These could be interpreted as aneuploid and polyploid derivatives from 5. The third important condition is noticeable in Astereae, Anthe midea and Cichoreae, all the three of which are advanced and possess the predomi nant base number x=9. The last condition is manifested in Heliantheae (including Helenieae), Cynareae and Arctotideae which exhibit fluidity in regard to the base number. It may be stated in conclusion that no single tribe in Compositae can be consid ered primitive in all respects. Heliantheae is primitive in many morphological features like the retention of abbreviated inflorescence axis in some of its members, occurrence of receptacular bracts in the axils of which florets arise and a calyx like pappus but has ligulate ray florets and regular disc florets and highly fluid basic chromosome number. Senecioneae (mostly), Eupatoreae or Vernonieae have the primitively uniform regular corolla of all the florets in a capitulum together with 5 or 10 as the more or less con sistent base number but the receptacular bracts are absent and the pappus is unlike a calyx. Mutiseae retains the bilabiate condition seen in Lobeloideae of Cam 352 P. N. Mehra Cytologia 42 1977 Cytological Investigations on the Indian Compositae VI 353 panulaceae either uniformly in all the florets of a capitulum or the ray florets are bilabiate and the disc florets regular, with a highly plastic basic chromosome number of the constituent genera. It appears, therefore, that a plexus of forms grouped under Campanulaceae probably evolved into Compositae. These ancestors possessing basically similar genomic potential deviated, broadly speaking, in an identical fashion, suggesting a sort of an orthogenetic trend, to give rise to members now classed among the Compositae, yet retaining some of their own individualistic traits. Cichoreae, with all the flowers uniformly zygomorphic ligulate, and a pappus most unlike a calyx, with laticiferous vessels in the phloem region, undoubtedly is the most complex of the composites.

Cytogenetical evolutionary mechanisms Almost all the mechanisms of cytogenetical evolution known in the king dom are operative in Compositae too. Homoploidy is practically absent. Neither is there any consistency in basic chromosome number at the family level, such as is observed in some of the arboreal families like Magnoliaceae, Aceraceae, Rubiaceae, Fagaceae, Lauraceae, Juglandaceae or coniferous families like Pinaceae, Taxo diaceae, Cupressaceae and Araucariaceae. This is perhaps because of 1) herbaceous habit involving rapid turn over of generations, 2) predominantly outbreeding re productive behaviour and 3) an intrinsic potentiality of throwing out chromosomal mutations. There are evidences of gene mutations, structural chromosomal alterations, euploidy, aneuploidy, compounding of chromosome numbers, apomixis, and the occurrence of B-chromosomes with whatever effect the latter may have on pheno typic variability or reproductive behaviour. These are illustrated below citing examples mainly from the Indian Compositae. Structural chromosomal alterations are manifest in the aberrations at meiosis in a small or large percentage of mother cells in the form of inversion bridges and fragments (Tridax procumbens, Blumea mollis), sticky bridges and laggards (Inula cuspidata, Carduus nutans), interlocking of bivalents (Scorzonera divaricata) and manifestation of structural hybridity (Chrysanthemum sagetum, C. carinatum and C. coronarium) resulting in loss of pollen fertility to a greater or lesser extent. Euploidy is a common phenomenon in the Indian Compositae as elsewhere. Cytological races have been found in Inula cappa, Siegesbeckia orientalis, Gynura angulosa, Chrysanthemum leucanthemum, Aster thomsonii, Artemesia parviflora, Ageratum conyzoides (in all these cases 2x, 4x); Achillea millifolium (2x, 4x, 6x); Artemesia vulgaris (2x, 4x, 5x, 6x); Erigeron bonariensis (2x, 6x) and Anaphalis margariatacea (4x, 6x, 8x). In other instances aneuploid cytotypes have been discovered as in Lactuca macrorhiza (n=8, 9), Blainvillea rhomboidea (n=17, 39), Senecio rufinervis (n=20, 18), Erigeron niveus (n=14, 11) and Saussurea candicans (n=17, 16). These aneuploid changes have involved either addition or deletion of one or more chromosomes. In these races, while there may be minor quantitative alterations in the phenotypic characters of the species, the variations do not transcend the specific boundry. Whereas in euploids there is the balanced 354 P. N. Mehra Cytologia 42 summation of the total gene content, in aneuploids it is the partial accentuation with its attendant variation in the particular characters affected by the presence of the particular chromosome/s in excess. But aneuploidy is not restricted to intraspecific level. If accompanied by gene mutations and structural chromosomal alterations, it transcends the specific boundry. Eupatorium (x=10, 17) of the Eupatorieae; Leontopodium (x=7, 13) of Inuleae; Cnicus and Arctium (x=16, 18) of Cynareae; Ligularia (x=24, 29, 30), Petasites (x=26, 29, 30) of Senecioneae are some of the examples. Aneuploidy may be responsible for evolution of genera, groups of genera within a tribe, or even different tribes. Such is probably the case in Cyathocline with n=11 belonging to Astereae where the general rule is evolution on the base number x=9, Adenostyles (x=19) and Mikania (x=19) of the Eupatorieae, probably representing a drop from the tetraploid number 20; or the tribe Inuleae where, while the predominant base number is x=7, there are genera which possess x=9 (Vicoa, Pulicaria), 10 (Laggera, Inula, Sphaeranthus, Carpesium), 11 (Blumea) or 13 (Ammobium). This feature is much more emphatically expressed in Heliantheae-Helenieae where no consistent base number is observed in the different genera which on the basis of morphological characters alone find there grouping in this tribe. Aneuploidy at the tribal level is also to be seen in Compositae. In all proba bility the original basic number of the ancestors was x=5 which became stabilised in many of the tribes at the tetraploid level with x=10 but there are others where the stabilisation has been achieved at the aneuploid level (x=9) as in Astereae, Anthemedieae and Cichorieae, coupled undoubtedly with major gene mutations and perhaps structural chromosomal alterations.

Apomixis Among the taxa investigated, Erigeron mucronatus (tetraploid, 2n=36) and E. annus (triploid, 2n=27) which, on the basis of highly irregular meiosis leading to 40-50% pollen sterility coupled with the formation of 70% of embryo containing achenes in a head, were suspected to be apomicts, have been confirmed to be so on embryological investigations (Mehra and Gill 1972). The former is parthenogenetic. The other suspected cases on the grounds of high degree of meiotic aberrations but good seed set are Eupatorium glandulosum (2n-51), E. odoratum (2n=51) and Hieraceum crocatum (2n=27). All the three are triploids. Both the genera are known in the literature to possess apomictic species. The sixth apomict in the area is 1araxacum officinale. It is widely distributed, being met with in the Himalayas, the Nilgiris and the Pulney hills. Four cytotypes have so far been discovered by us with 2n=24, 32, 27 and 40. They exhibit wide variation in morphological charac ters and altitudinal distribution. Of these the triploid (2n=24) is the commonest. Meiotic irregularities in the nature of univalents and multivalents at diakinesis and unequal distribution of chromosomes at A, and A2 were frequent leading to high percentage of pollen sterility. Only 25-35% pollen were stainable, the rest being shrivelled. Whereas trivalents were observed in the triploid cytotype, quadrivalents were hardly noticed in the tetraploid. Takemoto (1956) reported two races with 2n=24, 26 from Japan, whereas Furnkranz (1960) recorded cytotypes with 2n=16, 1977 Cytological Investigations on the Indian Compositae VI 355

18, 24, 32, 34, 36, 37. It is well known that apomicts are opportunists that exploit the local conditions to which they are adapted to their best advantage. They have no evolutionary potential if they are of obligate type, since there is no recombination of characters due to loss of sexuality. The only source of variability in them are the mutations at the genic or chromosomal level. However, if the apomicts are facultative, they combine the advantages of sexuality as well as apomixis in their progeny which lead them to a high degree of variability as well as to environmental adaptability. The categorisation of the variant populations of apomicts is, however, problematic. In our opinion, these should at best be regarded at the level of microspecies. To sum up, with its predominantly herbaceous habit, which in all probability was the ancestral condition, coupled with an efficient outbreeding mechanism, the Compositae have not stayed conservative in the matter of variability at the genic level, or stability of the chromosome numbers or the karyotype but have made rapid advances in all directions leading to a highly successful diversification.

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