Theories about the Ancestors of Angiosperms

The following points highlight the top nine theories about ancestors of angiosperms. Some of the theories are: 1. The Isoetes – Monocotyledon Theory 2. The Coniferales-Amentiferae Theory 3. The Gnetaies’-Angiosperm Theory 4. The Anthostrobilus (Bennettitalean) Theory 5. The Caytonialean Theory 6. The Stachyospory-Phyllospermae Theory 7. The Pteridosperm Theory and Others.

1. The Isoetes – Monocotyledon Theory:

This theory was proposed by Campbell, and is essentially based on marked similarity between Isoetes and Monocots especially Najas flexilis.

He advocated that monocotyledons have been derived from Isoetes via Ophioglossaceae. Both eusporangiate and leptosporangiate ferns, and their allies like Lycopodiales, Isoetales, etc., have been shown to possess many common features with those of the monocotyledons.

Isoetes an aquatic or amphibious genera, is predominantly herbaceous and geophilous and like most of the Filicineae, it is found in the humid tropics, a habitat which is also characteristic of a large number of monocotyledons.

The marked similarity in habit and in the embryo and anatomy of the older sporophyte of Isoetes and some other lower aquatic monocotyledons, have also been pointed out by Campbell. He suggests that the herbaceous character in angiosperms is primitive, inherited from filicinean ancestors.

The probable origin of monocotyledons from various groups of Pteridophytes, through an intermediate and hypothetical group, the protangiosperms has also been postulated by Engler and his associates, according to whom due to the herbaceous nature of most of the members of this group, they are not represented in the fossils.

Engler also postulated the direct derivation of monocotyledons from Ophioglossaceae on the basis of similarities in their vascular bundles. However, this theory of Pteridophytes ancestry is highly unacceptable, as the monocotyledons are now considered as most advanced group of angiosperms and derived from dicotyledons.

2. The Coniferales- Amentiferae Theory:

This theory has been proposed by Eichler, Engler, Engler & Prantl , Rendle , Hagerup and Doyle. According to this theory, the Coniferales have been treated as the probable ancestors of angiosperms by several phylogenists including Engler and Rendle.

They pointed out several resemblances between angiosperms and conifers and proposed that the Coniferales might have given rise to primitive (hypothetical) group of angiosperms known as Amentiferae.

These similarities include:

1. Similarities between the inflorescences of the amentifers like Casuarinaceae, Salicaceae, Fagaceae, etc., consisting of simple and naked flowers, with those of the conifers.

2. Similarities in the stamens and bisporangiate microsporophyll’s of many conifers. Covered nature of seed in Agathis and Araucaria as found in angiosperms.

3. Similarities in the seed-scale complex of Juniperus with the gynoecia of Amentiferae.

4. Similarity in the fertilization process of certain conifers with that of angiosperms, where the pollen grains are deposited on the scale and only the pollen tube enters the micropyle.

In spite of these similarities, it is now very well documented that these resemblances are only superficial and due probably to parallelism. Further this theory is not acceptable because the Amentiferae group is now considered as an advanced group of angiosperms.

The advanced features in Amentiferae include:

5. The primitive angiosperm flower is bisexual whereas cones of conifers are uniformly unisexual.

6. The inflorescence of amentiferous families exhibit specialized structures. The flowers of these families are not primitively simple but are highly reduced.

7. The wood anatomical data suggest that Amentiferae are highly advanced. Some of the angiosperms like Trochodendron, Tetracentron and others, which lack vessels, have a structurally more primitive secondary xylem than conifers as well as amentifers.

8. The ovuliferous scales of conifers and carpels of angiosperms follow distinctly different lines of evolutionary specialization.

9. The carpels of angiosperms are modified leaves (phyllosporous), whereas the seed- bearing organs of conifers are never so and probably represent modified telome systems.

Thus, this theory, which proposes Coniferales as the ancestors of angiosperms and Amentiferae as primitive group of angiosperms is ruled out.

3. The Gnetaies’-Angiosperm Theory:

This theory was proposed by Richard von Wettstein and supported by Markgraf and Fagerlind.

According to this theory Gnetales, the transitional group between angiosperms and gymnosperms, are considered as the ancestors of angiosperms. Thus, among living plants, the gnetophytes (Ephedra, Gnetum, and Welwitschia, forming a monophyletic clade themselves), are believed to be most closely related to the flowering plants.

The gnetophytes, like the other extant (non- angiosperm) seed plants, had their greatest diversity in the past. However today, Gnetum forms a tropical moist-habitat plant, while Ephedra (containing about 30 species with a global distribution) and Welwitschia (represented by a single species that is restricted to some of the driest portions of the Namib Desert in Southwest Africa) are both, dry- climate or desert plants.

The Gnetales resemble angiosperms in many respects:

1. The leaves of Gnetum, have reticulate venation, resembling that of some dicot angiosperms. On the other hand Ephedra, in contrast to other conifers, whose leaves are vascularized by a single trace, produces highly reduced spike-like leaves, vascularized by a pair of traces that exit from the eustele and enter the leaf.

An even more bizarre leaf arrangement is found in Welwitschia, which produces a single pair of large, parallel-veined leaves that continue to grow throughout the life of the plants. This is a very derived condition that might best be interpreted as pro-genetic.

2. The Gnetales, like the flowering plants, possess vessels in their wood. However, the vessels in the Gnetales have a subtly different developmental origin and thus may not be strictly homologous with those of angiosperms.

3. All the three members of Gnetales have two cotyledons.

4. The stamens of all the three genera of Gnetales are apparently similar to those of angiosperms.

5. Unlike most gymnosperms, ovules of Gnetales have close resemblance with those of most angiosperms in possessing two integuments instead of only one.

These envelopes have been variously homologized with perianth or carpels of angiosperms:

a. In Gnetum the inflorescences are unisexual, which can be easily compared with the catkins of many amentiferous angiosperms. The strobili are arranged on axis with a conspicuous node-internode organization. Micro-sporangiate strobili have two fused bracts that form a cupule, and surrounds fertile shoots, each being composed of two fused bracteoles, which surround the microsporophyll.

In the megasporangiate strobilus, the cupule subtends a whorl of ovules, the outer integument of which are wrapped with two external envelopes, the tissue of which may be sclerified and fused to the integument to form a seed-coat-like structure, which makes the Gnetum seed appear like angiosperms.

b. Ephedra is dioecious, with mega- and microsporangiate strobili. The microsporangiate strobili consist of several pairs of bracts, from the axis of each of which arises a shoot bearing bracteoles (smaller bracts), each bracteole in turn surrounding a stalked microsporangiophyll bearing two or more pollen sacs (microsporangia).

The megasporangiate cone is also similarly arranged with pairs of bracts, the top two of which subtend an ovule, which appears to be surrounded by two integuments. However, according to most interpretations, the inner layer is the true integument, while the outer layer is a reduced bracteole similar to that surrounding the microsporangia.

c. The male flowers of Welwitschia are truly bisexual and show that they are derived by reduction of the female parts.

6. Gametophytes of Gnetum and Welwitschia are highly reduced like those of angiosperms.

7. In most angiosperms, in the process of double fertilization, two sperm are involved in fertilization, one of which unites with the egg cell to form a diploid zygote, while the other fuses with the two polar nuclei to form a triploid endosperm, which provide nutrition to the developing embryo. Ephedra and its sister taxon, Gnetum, undergoes a form of double fertilization, which is very much similar to that of angiosperms.

In Ephedra, two egg cells are produced, one of which is fertilized to become the embryo while, the other begins but does not complete development into an embryo, thus not providing nutrition to the developing embryo as does the endosperm of angiosperms.

The degenerate embryo is believed to be an intermediary step between the normal seed plant condition (where embryo is nourished by a larger gametophyte) and that of angiosperms (mega gametophyte so reduced as to not be effective for nourishing the embryo).

This can also be explained on the basis of reduction in the polyembryony as observed in many non-angiosperm seed plants, for example in some conifers, where several embryos form from fertilizations by several pollen grains, but ultimately, only one embryo per seed survives.

Unfortunately, in spite of these outward resemblances, the details of the vascular anatomy and developmental studies, strongly refutes the suggestion of the existence of any similarity between the two groups. Compared to that of some of the primitive angiosperms, the members of Gnetales have attained a higher evolutionary level in several respects.

For example:

1. They have vessels in the secondary wood, which are absent in the xylem of a few genera of angiosperms. Thompson has shown that the vessels of Gnetales originated in an entirely different way from those of angiosperms.

2. The scalariform pitted tracheids characteristic of primitive angiosperms, are eliminated from both the primary and secondary xylem in the Gnetales and replaced by circular bordered pits in the secondary xylem. This development of vessels is unique in type and is entirely different from that of vessels in angiosperms and certain vascular cryptogams.

3. The similarity between the strobilus of Gnetales and the aments of certain angiosperms, is now considered as superficial and due to some degree of convergence.

4. The ovules of Gnetales are naked, the nature of their envelopes is uncertain and they also differ in the general structure.

5. The similarity in the number of cotyledons between Gnetales and angiosperms also appears to be due to convergent evolution. Angiosperms might have been derived from poly-cotyledonous rather than dicotyledonous ancestors.

4. The Anthostrobilus (Bennettitalean) Theory:

The bennettitaleans, which first appeared in the Triassic and became extinct towards the end of the Cretaceous, were originally mistaken for cycads because of their cycad-like growth form. However, the reproductive structures of these plants and presence of syndetocheilic stomata, place them soundly in the anthophyte clade.

Two major groups of bennettitaleans have been recognized (Fig. 10.4):

1. Cycadeoidea:

They are with stout trunks and bisporangiate reproductive structures, and relatives of Williamsonia.

2. Williamsoniella:

They have slender, branching trunks and either bisporangiate or mono-sporangiate strobili. Both groups produced entire simple leaves or pinnate foliage and had woody stems that were heavily armored with persistent leaf bases, much like modern cycads. The groups only differ in the details of stomatal morphology.

The Bennettitalean theory was first proposed by Saporta and Marion (1885), followed by Arber and Parkin according to which, Bennettitales have been proposed as possible ancestors of angiosperms, on the basis of the resemblance in structure between the strobili of the Mesozoic genus Cycadeoidea and the flower of Magnolia.

Both these structures are:

i. Bisexual (Fig. 10.6-10.7), and

ii. Contain an elongated axis having protective bracts, microsporophyll’s and megasporophylls, arranged successively from below upwards.

However, in spite of these superficial resemblances, further studies have shown several differences, which are as follows:

1.In Magnolia, the microsporophyll’s (stamens) are free and are spirally arranged on the axis, whereas in Bennettitales they are whorled and mostly connate (Fig. 10.5).

2. In Bennettitales, the megasporophylls are greatly reduced, simplified stalk-like structures, each bearing a solitary terminal erect ovule. Between megasporophylls, there are sterile scales (inter-seminal scales), which are protective in function. No such structures are present in the flowers of Magnolia.

3. The micropylar tube formed in the ovules of Bennettitales are absent in the angiosperms and the pollen grains are shed on the stigma of the carpel (megasporophyll).

4. The seeds of Magnolia and other primitive angiosperms are with copious endosperm and small embryo while those of Bennettitales are non-endospermic with a large embryo.

5.In the bennettitalean stem there is a large pith, a thin vascular cylinder and a thick cortex, while the angiosperm stem has a small pith, a thick vascular cylinder and a thin cortex.

These differences indicate that Bennettitales cannot be considered as the ancestors of angiosperms. The similarities with angiosperms, most probably, might have resulted due to a common ancestry and parallel evolution. Arber and Parkin have postulated that the two groups did have a common origin from seed ferns and they might have diverged very early.

5. The Caytonialean Theory:

This theory was proposed by H. Hamshaw Thomas on the basis of comparative studies of modern flowering plants, with those of Caytoniales, which are certain fossil plants of the middle Jurassic. This theory was later supported by Stebbins.

Caytonia had a wide distribution and it has been described from Triassic to Cretaceous localities in most of today’s Northern Hemisphere. It is believed to have been a small tree, based on association of foliage with woody axis. Caytoniales, which seems to have a few angiosperm-like features, are looked upon as the possible ancestors of angiosperms.

These similarities include:

i. Leaves of Caytoniales exhibited reticulate venation as seen in angiosperms. The foliage of Caytonia (Sagenopteris) consisted of two to four palmately arranged lanceolate leaflets with a distinct mid-vein (Fig. 10.9). The epidermal structure of these leaflets shows some similarities to that of flowering plants.

ii. Caytoniales had angiosperm-like anthers produced in groups or singly on branching pinnate structures, which may be described as sporophylls. Such structures are comparable with the branched stamens found in such plants as Calothamnus, Hypericum and Ricinus.

The pollen-producing organ of Caytonia (iCaytonanthus), consisted of synangial units arranged along an axis, which probably represented a modified pinnate microsporophyll (Fig. 10.10). Each synangial unit had four fused, elongate microsporangia that showed some resemblance to the angiosperm anthers.

iii. In Caytoniales, the ovules were enclosed by a curved cup-like structure called cupule. The megasporophyll of Caytonia consisted of an axis bearing sub-opposite pairs of stalked, rounded cupules (Fig. 10.11). Each cupule was recurved, had a lip-like projection near the point of attachment, and contained several ovules arranged in a curved row with their micropyles facing the cupule opening.

The micropyles of the ovules were connected with the outer lip of the cupule via a canal. Proponents of caytoniales as the ancestor of the angiosperms point to the almost sealed cupule as suggestive of the way a carpel might have evolved.

According to Thomas, the carpel wall of angiosperms may represent a pair of concrescent cupules and he suggested that the possible origin of stigma should be considered in the light of these ancient forms.

iv. According to Gaussen and Stebbins, the ovule of angiosperms is homologous to the cupule of advanced pteridosperms, particularly Caytoniales, including both the Corystospermaceae (with uniovulate and indehiscent cupules) and the Caytoniaceae (with multi-ovulate and dehiscent cupules), where the position of the cupules relative to their stalks was strikingly similar to that of an anatropous ovule having a well developed funiculus, rather than to the unitegmic, orthotropous ovule of other seed plants.

However, the Caytoniales differed from the angiosperms in the following respects:

a. The caytonialian order was strongly pinnately veined, but the angiosperm carpel is palmate.

b. Presence of pollination drop and direct pollination.

c. Highly circularized winged pollen.

d. Absence of connective like structure in tetralocular synangia.

e. Presence of fleshy canals in the inner side of the curved cupules.

f. Caytoniale ovules had single integument while most angiospermic ovules have two integuments.

These dissimilarities strongly negate the theory of Caytonialean ancestry of angiosperms. Caytoniales, are now classified as Mesozoic remnants of the Pteridosperms as they have been shown to have relationships with the latter group.

The morphological studies on the nature of the carpel of angiosperms suggest that the ancestors of angiosperms must have had open megasporophylls with exposed ovules. Therefore, the ovary-like pouches of caytoniales cannot be taken to be the fore-runners of angiosperm carpel.

6. The Stachyospory- Phyllospermae Theory:

This theory was proposed by Sahni on the basis of supposed differences in ovule position borne on stem (Stachyospory) or on leaves (Phyllospermae), and it was later redefined and expanded by Lam.

According to this theory most of the dicotyledons were thought to have ovules enclosed in foliar carpels while the Monochlamydeae and most of the monocotyledons were considered to have mega sporangia protected by sterile organs. This theory was however considered valueless by Eames, as comparative morphology and anatomy show that all ovules are borne on appendages in angiosperms.

7. The Pteridosperm Theory:

Pteridosperms (seed ferns) have been considered as ancestors of angiosperms by a large number of phylogenists such as Andrew, Arnold, Cronquist , Long and Thomas.

This theory is based on the following characters, which are enough to bring seed ferns (Pteridosperms) closest to angiosperms:

i. Presence of features such as reticulate venation, monopodial branching and cambium.

ii. Origin of sepals from leaves and petals from sepals and stamens, and therefore, there is possibility of the evolution of a flower in angiosperms from cones or cone­ like structures of gymnosperms.

iii. The mega and microsporophyll’s are often borne on the same plant but they are not arranged in definite strobili.

iv. Similarities of seed structure and existence of one or several ovules subtended by a cupule. The angiosperm carpel is regarded as derived from a dorsoventral bivalved pteridosperm cupule by Long.

v. Similarity in the morphological nature of the mega sporangium or nucellus, as established by Hofmeister.

vi. Development of triploid endosperm and extreme reduction of female gametophyte.

vii. Some primitive angiosperms lack vessels in the secondary wood, a feature also found in seed ferns.

viii. The reproductive branch in Glossopteris (a pteridosperm) is somewhat comparable with that of the present-day angiosperm Dichapetalum.

Glossopterid leaves were abundantly and ubiquitously present in Pennsylvanian to Triassic rocks of Australia, Africa, South America, Antarctica, and the Indian peninsula, which lead geologists to the conclusion that these continents had once formed a continuous land-mass – the Gondwanaland.

The glossopteris are reconstructed (Fig. 10.12) as shrubs or large trees and the diversity of their reproductive structures suggests that they constituted a species-rich group, with a great number of species (over 200 described). Glossopteris leaves are tongue-shaped, commonly with an entire (smooth) margin. They have a distinct mid-rib and reticulate venation adjacent to the mid-rib.

Leaves are borne in spirals or whorls, probably on short shoots. Basically, both pollen and ovulate structures (Fig. 10.13) are borne separately on the adaxial side of a more or less modified Glossopteris leaf. In the case of ovulate fructifications, ovules are arranged on a dorsiventral structure that has been variously called capitulum, megasporophyll or cupule.

On the basis of this and other evidences, Melville has proposed a new theory regarding the origin of angiospermic flower known as the “Gonophyll theory“.

Advocates of the Glossopteris-ohgin theory propose the glossopteris vegetative leaf to be homologous with the angiosperms carpel, and the megasporophyll with the outer integument of an angiosperm seed, based on some peculiar specimens with abaxially borne seeds.

However, there are two serious objections to the theory of Pteridospermi ancestry of angiosperms, which include:

a. The absence of scalariform xylem elements in Pteridosperms, which occur in angiosperms.

b. No satisfactory explanation for cupule as an equivalent of capillary wall in case of multi-ovulate cupules.

In spite of these objections, the similarities found between the pteridosperms and angiosperms suggest that angiosperms have some very close connection with pteridosperms. Due to the absence of any direct evidence, there is a growing tendency among phylogenists to accept the pteridospermic ancestry of angiosperms, at least tentatively.

8. The Pentoxylales Theory:

Meeuse (1961) compared Pandanus, a monocot, with Pentoxylales, a group of fossil pteridophytes. Like Glossopteris foliages, Pentoxylon is also a Gondwanan taxon, which has been found in India, Australia and New Zealand.

It takes its name from the five wedges of wood that characterize its stem. Pentoxylon first appears in the later part of the Paleozoic, but its greatest diversity and abundance appears to be in the Jurassic, continuing into the Early Cretaceous

Pentoxylon has a distinct short-shoot-long-shoot morphology. Stems are eustelic with secondary wood developing in five or six wedges around a mesarch primary xylem strand. Foliage arises from short shoots, where leaf scars are commonly visible (Fig. 10.14A). Leaves are long and narrow with a prominent mid-rib, and secondary veins arise at right angles to it and continues, un-branched till the leaf margin.

Pentoxylon does not have bisexual reproductive structures like many other members of the anthophyte clade. Ovule-bearing structures are aggregated into strobili, which are attached to short shoots (Fig. 10.14B).

Individual cupules almost completely enclose a single ovule, the integument of which is composed of an inner sclerenchymitized layer and a fleshy outer layer (Fig. 10.14C). Pollen organs are also born in clusters on short shoots.

Meeuse (1961) listed a number of common features between Pandanus and Pentoxylon, which include:

a. Both the members are erect or sub-erect dioecious plants with slender cylindrical stems.

b. Both bear terminal tufts of strap-shaped leaves in spiral arrangement.

c. The inflorescences of both members are borne among the leaves or on short lateral branches in the axils of the scaly bracts.

d. In both cases, the peduncles of inflorescences contain tracheids with spiral thickenings and bordered pitting.

e. The seeds are enclosed in a fleshy layer called sarcotesta, and a seed coat consisting of two layers.

f. Both bear seeds with copius endosperm and with minute embryo.

Based on these similarities, Meeuse considered Pentoxylales as ancestors of angiosperms. He proposed that Pandanus “is a direct descendent of a group of plants practically identical” with Pentoxylales. However, in spite of these resemblances, authors like Pant and Kidwai hold that they could equally be the result of parallel evolution.

9. The Durian Theory:

Durio zibethinus, a member of Bombacaceae from Burmese and Malayan forests was considered by Corner (1949), as the only “surviving member of primitive angiosperms“. This theory is named after the name of the genus D. zibethinus is a cauliflorous tree with large, colored, loculicidal, spiny capsules and fleshy arillate seeds (Fig. 10.15).

According to Corner, arillate genera are found in about 45 families of angiosperms, mostly distributed in the tropics like Durio, and within these arillate families, a reduction series can be traced from genera with arillate fruits to genera having fruits of other types.

According to this theory, the primitive angiosperms are:

a. Mesophytic.

b. Tropical in distribution.

c. With cycad-like tree habit.

d. Have compound leaves.

e. Are probably monocarpic.

f. Have a large terminal cluster of arillate follicles.

The theory has however been strongly criticized by a number of morphologists including Fiji, Parkin, Metcalfe and Eames.