Origin of Alternation of Generations
Alternation of generations is a common component of all land plants, vascular and nonvascular; it does not express itself in the same manner in any other organisms. Given the
other overwhelming similarities in land plant biochemistry, photosynthetic pigments and
tissue organization, it seems that the easiest assumption is that they are derivatives of a
common ancestor.
The origin of alternation of generations is, however, unclear.
Considerable evidence suggests that the land plants (both vascular and non-vascular)
originated from a green algal ancestor that was haploid for most of its lifecycle, and only after
gametic fusion and fertilization was it briefly diploid. The resulting zygote was the only
diploid part of the life cycle, and it was immediately followed by meiosis. Thus, the zygote
directly gave rise to spores and the haploid generation was re-established. The gap from four
derivatives to more than four has already been bridged in some algal species by an intercalated
mitotic division. But the spore producing structure remains that of the former egg in a
unicellular organ. It could hardly be termed a sporangium, although it still had the same
function.
Was this early form simply a retained zygote, undergoing a chance mitotic division? If it
continued in its developmental program to become a spore there was no problem, but what if
it did not? If it were not to become a spore, what developmental program would be initiated?
What selection of developmental programs would be latent within these plants? Two
opposing theories for this phenomenon have been proposed. Unfortunately for students of
plant morphology, both theories are supported by data in the fossil record. It is far from clear
though to explain how both cases could have occurred during the origin of a common lineage
of land plants.
Transformation (homologous) theory. Simply stated, the transformation theory makes the
assumption that the mass of cells forming mitotically from the zygote may simply adopt the
developmental plan of the gametophyte, thereby forming a diploid sporophyte appearing
identical to the haploid gametophyte. Evidence for this very simple theory for the origin of
alternation of generations abounds among the algae, where there are examples of the
Chlorophyta, Phaeophyta and Rhodophyta that express isomorphic alternation of generations-all of which apparently arose independently during the course of evolution. In land plants, the
bryophyte Anthoceros, the hornwort, has a sporophyte generation that is photosynthetic and
therefore largely independent of the gametophyte generation on which it develops. Like a
gametophyte, it displays an extended lifespan.
Among vascular land plants, in Psilotum, which is possibly the most primitive extant vascular
land plant, the gametophyte is stem-like, persistent and independent in growth, and similar to
the sporophyte may produce tracheids within its thickest axes. In fact, it has been suggested
that stem emergences seen on the base of the rhyniophyte Aglaophyton (formerly Rhynia
gwynne-vaughnii) are examples of primitive archegonia. The figure to the right indicates a
reconstruction of such a body. This concept first engendered great excitement among
paleobotanists, since no sporangia had been seen on the aerial axes of this plant. It was even
theorized that Rhynia major was the sporophyte of this plant. However, since that time,
sporangia have been identified on axes of Aglaophyton. Therefore, although some specimens
might have been gametophytes, there is no compelling evidence that this must have been the
case. Also, there are no compelling examples of antheridia or embryos.
Interpolation (also called antithetic or heterologous) theory. The antithetic theory maintains
that the sporophyte and gametophyte generations are fundamentally dissimilar and that the
first mitotically dividing zygotes (embryos) entered into a substantially unique developmental
pattern, not copying the established developmental events of the gametophytes. This theory
suggests that the embryos were in a unique developmental relationship with the gametophyte
and therefore entered into an equally unique generation, eventuating in the production of
spores. Thus, the sporophyte generation was an innovation of critical significance.
A sequence that is likely to have initiated this process is occurrence of a cycle or two of
mitosis preceding the meiotic division of the brief diploid generation. Presumably, there was
not even a sporangium to start with, since all of the cells derived from the zygote underwent
meiosis. From this rudimentary condition, more spores, and ultimately a multicellular
sporophyte could be produced. Further retention of the sporophyte over the course of time
could eventually result in the formation of vegetative tissues to support the energetically
expensive process of producing numerous spores and organs with more complex forms of
dissemination. Once some of these land plants possessed the ability to produce and
effectively disseminate numerous spores, the development of a complex sporophyte presented
considerable evolutionary advantages in competing for the production of more haploid
offspring. Evolutionary pressure favoring the production of more spores, more protective
organs and the development sophisticated organs for spore production and dissemination
(sporangia) would
An illustration of the antithetic theory according to Bower. (A) Sporophyte consisting
principally of a sporangium producing spores (like Anthoceros does today) (B) Branching of
sporangium (C) Increased robustness of sporophyte (D) Independent Rhynia like sporophyte.
be expected and this would presumably occur swiftly as the early (pre-?)vascular plants
diversified to occupy the land environment. Bowers envisioned the sequence of events as
shown to the right.
Which model seems the best supported by currently available data? There is clearly data
supporting the origin of alternation of generations through both homologous and heterologous
origins. Certainly, there are strong examples of each in different groups. However, vascular
land plants appear to have originated through a heterologous method according to current
data. The rhyniophytes display such remarkable diversity that it is not difficult to imagine
them as an ancestral group to both the tracheophytes and bryophytes. The evidence of
"archegonia" in Aglaophyton is not entirely compelling because of the lack of embryos and
antheridia. At the current time, the interpolation theory seems more logically compelling as
an explanation for the origin of alternation of generations in land plants.
Why did sporophytes become dominant in vascular plants? For genetic reasons, it seems
likely that the diploid generation, with its greater resistance to the occurrence of lethal
recessive genes, which are expressed directly in haploids, would be favored. Diploids are
capable of masking such recessives, as long as the organism has only one copy of such a gene.
And as the complexity of the plants increased, the benefit of masking lethal recessives became
even more valuable. On the other hand, bryophytes appear to have diverged from this
strategy, adopting a cryptic life cycle and occupying environments that were occupied by
vascular plants only later in their evolution. The bryophytes appear to have adopted a reverse
strategy, although in many ways retaining much the same internal and external morphology.