In this article we will discuss about the evolutionary trends among pollen grains based on palynotaxonomical works.
Primarily the aperture is proximal in position in all the taxa of plants, and a change from proximal to distal has been conditioned by physiological and ecological needs that arose in the wake of the origin of new plant taxa. The bryophytes and pteridophytes which are generally low growing are characterized by the proximal trilete or monolete apertures.
The apertural area is a weak part of the spore and its position toward the centre of the tetrad is considered to have been an adaptation to ensure protections of the protoplasm.
In primitive extinct gymnosperms like pteridosperms, pollen grains are called Pre-pollen which are characterized by proximal apertures (trilete: Lyginopterids, monolete: Medullosans) and presumed proximal germination rather than distal, equatorial or other typical apertures of seed plant pollen grains.
In all extant gymnosperms the aperture is distal and also have inaperturate forms in some members. Since the gymnosperms are mostly arboreal, they carry the male gametophytes (Pollen) high up in the air, preventing them from the effects of edaphic factors.
In angiosperm, there is an all round advancement in structural evolution of pollen, hence their male gametophytes are very well protected. So it hardly matters, whether or not the aperture is proximal, distal, zonal or global.
Although the global distribution of apertures increases the probability of pollen germination as any part of the pollen surface of pantoaperturate pollen adhere to stigmatic surface may accelerate pollen germination.
The most primitive trilete sporoforms are observed in mid Silurian – early Devonian vascular plants. In the extinct groups like Rhyniales, Zosterophyllales, Trimerophytales, Lepidodendrales, Sphenophyllales, Calamitales and Primofilicales, the spores are always triletous.
Pre-pollen in early gymnosperms like Pteridosperms, Cordiatales, Voltziales nearly always triletous. There are also transitional forms between the trilete and the monolete (monosulcate).
The Bennettitales particularly are monoletous (monosulcate), although the triletous forms are also present in some Cycadeoids. In the extant forms the spores/pollen are monolete in Psilotales and in some members of Filicales, inaperturate in Equisetales, monosulcate in Cycadales and Coniferales.
The new pollen-spore morphoforms that originated during the evolution of Pre-angiospermous vascular plants are given below:
A. Fundamental forms:
Trilete, non- perinous, non-saccate.
B. Derived forms:
a) Trilete, perinous, non-saccate
b) Trilete, saccate
c) Monolete, non-perinous, non-saccate
d) Monolete, perinous
e) Monolete (Monosulcate), saccate
f) Inaperturate
The perine and sacci developed later during the morphological evolution of spore and pollen. These facts indicate that the evolutionary process that underlines the origin of the monolete (=monosulcate) and inaperturate forms from the trilete, is one of reduction, and that of the perine and sacci, is one of the expansion (modification) of the basic structural organization.
The earliest record of angiosperm pollen is from Lower Cretaceous. The most primitive angiosperm pollen grain is boat-shaped monosulcate type.
These pollen grains were assigned to the dispersed pollen genera Clavatipollenites, Retimonocolpites and Liliacidites (Fig. 5.7) which might have had a common origin with the Mesozoic Bennettitales (Cycadeoidales).
This primitive condition is distributed among most gymnosperms like Cycas of Cycadales, Pinus, Abies, Cedrus of Coniferales, Ginkgo of Ginkgoales, and in the pollen grains of many primitive dicotyledonous angiosperms, for example, Magnolia, Degeneria.
This pollen type has been preserved in many monocotyledous, for example, among others in Arecaceae and also in some dicotyledons like Canellaceae. The distal sulcate aperture has given rise to a few other types like distal porate (ulcerate) aperture in some monocots, distal trichotomocolpate (=trichotomosulcate) aperture both in dicots and monocots, an equatorial ring-like aperture in Nymphaeaceae, inaperturate type having reduced thin exine and a thick intine.
The main trend of evolution of pollen aperture is the transformation of the distal monosulcus (monocolpate) into tricolpate condition. Takhtajan (1980) hypothesized that the tricolpate condition developed as a result of evolutionary deviation of the primitive stage of sporoderm development.
This arose de novo from the monocolpate condition. The tricolpate condition have given rise independently to polycolpate, polyrugate, triporate, pantoporate. The highest stage of evolution of pollen aperture is observed in many evolved families where compound apertures like tricolporate or tripororate etc., are evolved from simple tricolpate type (Fig. 5.8).
The most primitive pollen grains like Degeneria are atectate having columellaless exine structure which is amorphous and essentially homogenous. Such type of exine has given rise to the granular exine of Magnoliaceae and Annonaceae.
Further, incipient columellae are formed from granular layer. The well developed columellae are formed, either by enlargement and stabilization of intra-exinal cavities or by fusion of granules to form a basal foot layer and well marked columallae. According to Walker and Skvarla (1975) the columellate exine evolved independently a number of times.
The tectate columellate exine is rather primitive which ultimately gives rise to sub-tectate and intectate pollen via tectate perforate exine (Fig. 5.9). The most primitive pollen exine surface pattern are psilate or with foveolate (Pits) ornamentation (also found in earliest angiosperm pollen, “Clavatipollenites”), and generally devoid of external sculpturing. In advanced pollen grains external sculpturing of various types are noted.
The shape, type and symmetry of the early tetrad arrangement of pollen grains have provided valuable data in deciphering the distributional pattern of the apertures and the orientation of polarities. The tetragonal tetrads are more primitive than tetrahedral tetrads.
The pollen grains of the former are bilaterally symmetrical with distal apertures, and the latter are radially symmetrical with meridional apertures. With regard to polarity the isopolar grains with global and equational apertures are considered to be more evolved than the heteropolar monosulcate type.
The evolution of pollen grains from a primitive condition to an advanced one takes place with the change of position and polarity of aperture with the modification of apertural shapes. Pollen grains with a single sulcus (anasulcate) occur in Ranalian complex. The anasulcate apertures give rise to a number of parallel evolutionary trends in primitive dicotyledons and monocotyledons.
According to Chanda and Ghosh (1979) the main trends are:
A number of changes have taken place from monosulcate to non-aperturate condition that is, change in polarity (heteropolar to apolar), symmetry (bilateral to radial). Phylogenetically the non-aperturate stage is important as it is intermediate between primitive and advanced apertural conditions.
The evolutionary trends of non-aperturate condition to other forms are given below:
(a) Non-aperturate → Bisulculate [Caly- canthaceae (dicot) and Amaryllidaceae (monocot)] → Biporate [Trimeniaceae (Piptocalyx)] → Pantoporate (Trimeniaceae (‘Trimenia)].
(b) Non-aperturate → Tricolpate [Trocho- dendraceae, Tetracentraceae, Illiciaceae, Nelumbonaceae, etc., and other families at the base of higher dicots]
Chanda and Ghosh (1979) proposed a “genealogical tree” which reflects the evolutionary tendencies among the monocots and early dicots in terms of apertural evolution (Fig. 5.10).
The phylogeny of dicotyledons has been studied palynologically by many scientists. The order Tubiflorae (sensu Engler) is the largest order among sympetalous dicotyledons. The taxonomists differ on the pattern of division of Tubiflorae into several orders. Nevertheless, persistent irregularity prevails in the composition of this order.
The pollen morphological studies suggest that the Geraniales stock may have given rise to several types in a polyphyletic line, one to the tricolpate type of Convolvulaceae in Polemoniales along with Polemoniaceae.
The Geraniales Stock in another branch may have given rise to the order Boraginales. Pollen morphological data advocate the view that Lamiales could have been derived from Boraginaceae with Verbenaceae and Lamiaceae at the base of the order.
The pollen morphological characters also support the derivation of Bignoniales from the Polemoniales. The highly eurypalynous family Solanaceae bears affinity with Convolvulaceae which leads to the postulation that Solanaceae may have been derived from the Polemoniales, presumably through Convolvulaceae.
The other families of Scrophulariales have been derived from Scrophulariaceae, and Acanthaceae is probably the most advanced family in the Scrophulariales on the basis of the palynological data.
Chanda and Mukherjee (1978) proposed revision of the assemblage of families of the division Tubiflorae (sensu Engler) into five distinct smaller orders:
(1) Polemoniales (Convolvulaceae and Polemoniaceae),
(2) Boraginales (Hydrophyllaceae, Boraginaceae and Lennoaceae),
(3) Lamiales (Verbenaceae, Physopsidaceae, Lamiaceae, Avicenniaceae, Myoporaceae and Phryamataceae),
(4) Bignoniales (Bignoniaceae, Thunbergiaceae, Pedaliaceae and Myrtaniaceae) and
(5) Scrophulariales (Solanaceae, Nolanaceae, Scrophulariaceae, Orobanchaceae, Gesneria- ceae, Columelliaceae, Lentibulariaceae, Globulariacae, Selaginaceae and Acanthaceae).
Pollen morphology supports the segregation of Nolanaceae from Solanaceae, Avicenniaceae from Verbenaceae, Selaginaceae from Scrophulariacae, Thunbergiaceae from Acanthaceae and transfer of Trapella and Meyenia from Pedaliaceae and Acanthaceae, to Scrophulariaceae and Pedaliaceae respectively.
But the creation of Cobaeaceae from Polemoniaceae, Cuscutaceae from Convolvulaceae, Ehretiaceae from Boraginaceae, Stilbaceae and Chloanthaceae from Verbenaceae, the inclusion of Callitrichaceae as component of Lamiaceae, the transfer of Nyctanthes (Oleaceae) in Verbenaceae, are not in conformity with palynological results.
Palynological data supports that Geraniales stock gave rise to Polemoniales and Boraginales, almost parallel to each other. The Boraginales further gave rise to the Lamiales and Polemoniales to Scrophulariales and Bignoniales.
The monocotyledons are characterized by the dominance of monocolpate (=monosulcate) pollen grains followed by trichotomosulcate and colpate forms. In an analysis of the apertural forms in the families of monocots, Nair (1970) pointed out the occurrence of monocolpates in 31 out of 46 families, the trimorphous condition is most pronounced in the Liliflorae in general, and Liliaceae in particular.
Other apertural types include porate (mono- and pantoporate), inaperturate, tricolpate, trichotomocolpate, trizonocolpate and spiraperturate. The colporate forms of dicots are totally absent in the monocots.
With regard to the role of apertures in tracing the origin and evolution of the monocots, Chanda and Ghosh (1977) postulated a scheme on the basis of character and position of apertures as the most conservative approach. In monocots, the basic and most primitive apertural type happens to be monosulcate, derived from a pro-angiospermous stock (Fig. 5.10).
This apertural form also occurs in some primitive, dicot plants, which probably originated from a single apertural furrow as in the pro-angiospermous pollen grains, trichotomosulcate type has been placed at a slightly higher position than the basic monosulcate type.
The reason for placing trichotomosulcate type at a general lower level, in addition to the fossil evidence, is because this type occurs in a few extant but primitive monocot taxa. The trichotomosulcate type with a reduction in the central part of the aperture, probably led to the triporate type as in the pollen of Sclerosperma.
The position of Alismatineae in the beginning of Melchior’s revision of Engler’s classification with pantoporate and monosulcate pollen grains is questionable as neither Magnoliales nor Nymphaeales, from which the monocotyledons are presumed to have evolved, have pantoporate pollen grains.
The Liliales placed by Melchior (1964) nearly at the base of his system has palynological support as almost all the families of this order bear monosulcate pollen grains. A number of apertural types from monosulcate to spiraperturate and to ‘unipantocolpate’ types with some intermediate transitional forms are reported in the family Xanthorrhoeaceae. The proposed sequential lineage of Liliaceae, Xanthorrhoeaceae and Aphyllathaceae has pollen morphological support.
The Restionales and Eriocaulales originated after branching dichotomously from the Commelinales which in its turn originated from the Liliales. Commelinales mostly produce monosulcate grains, probably justifying its derivation from the Liliales, and in turn giving rise to ulcerate (Restionales) and spiraperturate (Eriocaulales) types. Morphologically, the evolution of the ulcerate pollen of Poales from the Restionales has been justified by Chanda (1966).
The derivation of Hydrocharitales, Potamogetonales and Triuridales from the Alismatales and Bromeliales; Iridales, Dioscoreales, Zingiberales, Orchidales and Cyperales from the Liliales appears to be justified as most of the derived orders have monoaperturate, sometimes non- aperturate types. A few other derived types possibly could be placed at a slightly higher level.
Chanda (1988) studied the pollen morphology of the order Alismatales (including Butomaceae, Limnocharitaceae and Alismata- ceae). They reported that pollen grains of monotypic Butomaceae are monosulcate and boat-shaped, those of Limnocharitaceae have 4 to 10 ill-defined, fimbriate globally distributed pores, and of Alismataceae are pantoporate and spheroidal, or rounded polyhedral.
However, Alisma oligococcum has unusual 2-porate, lens shaped pollen which indicates an isolated position in the family so far as apertures are concerned. Pollen morphological characters of this order have been analysed using cladistic methods and a hypothesis for pollen evolution in the Alismatales has been established. Monosulcate pollen is clearly primitive in the order, as amongst monocots in general, whilst derived pollen has a higher number of pores.
Fimbriate aperture margins, areas of circumporal ornamentation, and sunken apertures are also considered derived. Alismatales, therefore, are a relatively derived group of monocots, rather than the primitive group. The monosulcate pollen in Butomus represents the retention of a character primitive within the monocots and other seed plants. The other pollen types of the Alismatales may clearly be considered derived within the monocots.
There are a lot of controversy regarding the origin and evolution of pollen grains and spores. Considering the sporomorphs diversity of entire vascular plants the spore/pollen types can be categorized into three basic forms :
(1) The primitive triletous (proximal) apertures,
(2) The intermediate distal monoletous (monosulcate) aperture,
(3) The advanced meridional tricolpate and its derived forms like meridional tricolporate/tripororate, global pantoporate or polycolcate forms, etc.
Table 5.1 shows the evolution of various morphological characters in pollen and spores.
Conclusion:
The study of pollen morphology is of great significance to the disputed problems of higher plant taxonomy and phylogeny, since the pollen grains possess distinctly unique characters which are genetically labelled.
Palynologically plant families can be segregated into two groups:
(a) Stenopalynous, where the taxa of the family display more or less same type of pollen grains, e.g., Poaceae, Casuarinaceae, Chenopodiaceae, Amaranthaceae, etc., and
(b) Eurypalynous, where the taxa are characterized by an obvious difference in pollen types, e.g., Rubiaceae, Acanthaceae, Verbenaceae, Solanaceae, Convolvulaceae, Fabaceae, etc.
Based on stenopalyny or eurypalyny the inter- or intra- family affinity and phylogeny of taxa may be determined. The knowledge of pollen morphology has been to substantiate many taxonomic revisions sometimes even up to the formation of new taxa.
Segregation of Bombacaceae from Malvaceae, Trapaceae from Onagraceae, amalgamation of Cannaceae, Musaceae and Zingiberaceae into Scitamineae, and Moraceae and Cannabinaceae into Urticaceae, are a few examples of the contribution of the pollen morphology to taxonomy.
With evidences from other areas like anatomy, embryology, cytology, chemotaxonomy, the conclusions on the basis of palynology would become more trustworthy and resounding.